The diversity of microfungi in peatlands originated from the White Sea

Olga A Grum-Grzhimaylo1

White Sea Biological Station Faculty of BiologyLomonosov Moscow State University 1ndash12 Leninskie Gory119234 Moscow Russia and Faculty of BiologySt Petersburg State University 7ndash9 Universitetskaya nab199034 St Petersburg Russia

Alfons JM DebetsLaboratory of Genetics Plant Sciences Group WageningenUniversity Droevendaalsesteeg 1 6708PB Wageningenthe Netherlands

Elena N BilanenkoDepartment of Mycology and Phycology Faculty of BiologyLomonosov Moscow State University 1-12 Leninskie Gory119234 Moscow Russia

Abstract The diversity of culturable filamentousmicrofungi in peat and sediments of four peatlandsat the coastal zone of Kandalaksha Bay of the WhiteSea (Murmansk region Russia) was studied by culturemethods on standard and selective media Annually100 samples were collected from the bogs 2007ndash2010Based on morphological molecular markers and cul-tural features 211 taxa were identified Fungal com-munities observed at the peatlands were influencedmostly by their sea origin We discovered a large differ-ence between fungal communities from the peat andthe sediments of the peatlands In contrast to the sedi-ments the fungal community of the peat was found tobe consistent throughout sampling sites Fungi withspecific ecophysiology such as Sphagnum-decomposingspecies (Oidiodendron griseum O tenuissimum Penicil-lium spinulosum P thomii Talaromyces funiculosus)psychrotolerant and associated with insects species(Pseudogymnoascus pannorum Tolypocladium spp) typi-cal marine species (Acremonium spp) were found Inaddition different types of sterile mycelia were charac-teristic for the researched peatlands

Key words fungal diversity fungi decomposingSphagnum fungi in sediments molecular identifica-tion psychrotolerants

INTRODUCTION

Peatlands cover about 4 of the world more than10 of the territory of Russia and about 70ndash80 ofthe White Sea coastal territory (Yurkovskaya 2004)Peatlands accumulate peat partially decayed plantmaterial and play a significant role in the global carbon

cycle by virtue of their significant peat depositsthat contain 45ndash50 carbon (Thormann 2006b)The importance of peatlands for the global C cycle isillustrated by the fact that northern peatlands store180ndash277 Gt C (1 Gt5 16 109 metric tons) which con-stitutes approximately 10ndash16 of the total global terres-trial detrital C (Thormann et al 2001a)

Bogs are a dominant peatland type in the north ofRussia Coupled with spruce forest raised bogs prevailin the taiga zone in northeastern Europe Coastal raisedbogs predominate along the White Sea coast (Schulzeet al 2002 Yurkovskaya 2004) Raised bogs and aapafens (also called aapa mires) are the zonal mire com-plex types of boreal regions (Laitinen et al 2005)Raised bogs are ombrotrophic ecosystems that receivewater and nutrients solely from atmospheric precipita-tion They are commonly dominated by species ofSphagnum mosses Picea mariana and members of theEricaceae including species of Rhododendron spp Andro-meda spp and Vaccinium spp (Thormann et al 1999Thormann 2006a) Aapa fens are more minerotrophic(ie they receive their nutrients both from precipita-tion and the surrounding land because of their hydro-logical regime) These peatlands consist of a lakeelongated Sphagnum-formed hummocks and waterchannels (Keraumlnen and Kalpio 2001 Laitinen et al2005 2007) Aapa mire is a Finnish term for a largecomplex cold-climate wetland This is a mire-systemtype the central parts of which are characterized byminerotrophy and near to mire inherent influenceThese systems may receive supplementary nutrition totheir central parts in addition to marginal parts andbrook sides through meltwater from the surround‐ing area Aapa mires are morphologically variable(Laitinen et al 2007)

The annual accumulation of peat is caused by rela-tively slow organic decomposition by microorganismsbecause of extremely unfavorable conditions lack ofoxygen low temperatures high acidity and humiditythe presence of inhibitory complex phenolic compoundsfrom specific vegetation (mostly Sphagnum spp) andan inherent lack of microbial diversity to degrade themost complex polymers of peat (Untiedt and Muumlller1984 Tsuneda et al 2001 Thormann et al 2002Rice et al 2006 Andersen et al 2010)

In White Sea coastal raised bogs peat consists ofthe complex of plant material dominated by Sphagnumfuscum (Yurkovskaya 2004) Fungi together with het-erotrophic bacteria are the main decomposers ofthe organic matter in peat (Pankratov et al 2005Gilbert and Mitchell 2006 Thormann et al 2001a b

Submitted 19 Sep 2014 accepted for publication 20 Oct 20151 Corresponding author E-mail olgrgrwsbs-msuru

Mycologia 108(2) 2016 pp 233ndash254 DOI 10385214-346 2016 by The Mycological Society of America Lawrence KS 66044-8897Issued 19 April 2016

233

2006a b 2007 Andersen et al 2010) In the northernpeatlands fungal diversity estimates are 22ndash55 speciesper peatland Those species have a capacity for livingand physiological activity in peat (Nilsson and Ruumllcker1992 Czeczuga 1993 Thormann et al 2001b)

The respective role of fungi in litter decompositionand the multiple-factor peat-forming process in peat-lands is still poorly studied Most peatlands are in thenorthern hemisphere (Thormann et al 2007) how-ever little is known about fungal biodiversity of thenorthern peatlands Some data is available of peatlandfungi from western Siberian and central Russia(Golovchenko et al 2002 Kachalkin et al 2005Grum-Grzhimaylo and Bilanenko 2009 Filippova andThormann 2014) but almost no data is available forthe fungi from the peatlands in northwestern Russia

The peatlands at the Kandalaksha Bay of the WhiteSea have a unique origin They appear as a result of apart of the sea becoming isolated during rapid landuplift (05 cmy) followed by both demineralizationand the development of bogs (Shaporenko et al 2005Pantyulin and Krasnova 2011) In this process thesuccession of marine biota by freshwater takes placewhich is common for peatlands Fungi functioningas decomposers symbionts parasites and pathogensare associated with the evolution of the reservoirs thathave a sea origin (their number is evaluated from oneto several hundred at Kandalaksha Bay) but the dataon mycobiota of these systems are hardly discussed inthe literature

The aim of our research was to investigate fungaldiversity in the peatlands around the White Sea Biolog‐ical Station (WSBS) of Lomonosov Moscow State Uni-versity in northwestern Russia The fungi were isolatedfrom the peat and sediment samples taken from

four peatlands at different altitudes above sea level(15ndash87 m) representing different stages of bog forma-tion Fungi were identified with morphological andcultural features as well as DNA sequence data (ITSrDNA region along with SSU and LSU rDNA) Wecharacterized the composition abundance and spatialdistribution of species in fungal communities frompeatlands in connection with the age of the reservoirsand their contact with the sea

MATERIALS AND METHODS

Study areamdashIt is near the Karelian coast of Kandalaksha Bayof the White Sea (FIG 1) near the WSBS (66u349N 33u089E)Kindo Peninsula where the station is located is near the Arc-tic Circle The geographic position of lakes determines theclimatic conditions under which their hydrological regimeis formed In this case this is a long winter with an averagedaily temperature of minus11 C in Jan and a relatively shorthumid summer with a maximum precipitation in Aug and amean temperature of 14 C in Jul (Shaporenko et al 2005)Annual precipitation is 300ndash400 mm (Bubnova 2005) Geo-morphologically the region lies on the northern margin ofPribelomorskaya Lowland The maximum elevation of thearea is less than 100 m

Description of the investigated peatlandsmdashFour investigatedpeatlands are located ranging from the lowest to the highestpoint of the peninsula and represent almost all evolutionstages of bogs in this area of theWhite Sea coast (FIG 1 TABLE

I) Two of them represent raised bog-type peatlands (Verkh-nee Krugloe FIGS 2A 2B) the third is a transition aapa fen(Ershovskoe FIG 2C) and the fourth is a brackish lake detach-ing from the sea (Kislosladkoe FIG 2D) Kislosladkoe Lakehas both marine and continental features There is a combi-nation of typical littoral vegetation with bog plants dependingof coast parts in this peatland The characteristics of aapa fentypes were described in detail by Laitinen et al (2007)

FIG 1 Map of the Kindo Peninsula with four studied peatlands tagged A 5 Verkhnee Peatland B 5 Krugloe Peatland C 5Ershovskoe Peatland C(1) 5 Ershovskoe Verkhnee Lake C(2) 5 Ershovskoe Nizhnee Lake D 5 Kislosladkoe Peatland WSBS5 White Sea Biological Station

234 MYCOLOGIA

TABLEIDescriptio

nof

theinvestigated

peatlands

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

1Verkh

nee

8400

iexcl11

087

Raisedbo

g46

20

Peat

41

sedimen

ts60

minus20

Pinu

ssylvestris

Betula

nana

Cha

maeda

phne

calyculata

Calluna

vulgaris

Rubus

cham

aemorus

Oxycoccus

microcarpus

Ledum

palustre

Drosera

rotund

ifolia

D

anglica

Eriophorum

latifolium

Menyanthestrifolia

ta

Pleuroziu

mschreberi

Sphagnum

fuscum

Sphcapillifolium

Sphpapillosum

Sphmagellanicu

m

Sphmajus

Cladonia

rangiferin

aCl

alpestris

Clm

itis

Cetraria

islandica

Nephrom

asp

66u 32937

020

6Prime

33u595043

48Prime

2Krugloe

3970

iexcl40

275

Oligotroph

icaapa

24

14

Peat

41

sedimen

ts60ndash

65

minus10

Pinu

ssylvestris

Betula

nana

Calluna

vulgaris

Rubus

cham

aemorus

Oxycoccus

microcarpus

Vacciacutenium

sp

Drosera

rotund

ifolia

D

anglica

Baeothryon

caespitosum

Pleuroziu

mschreberi

Sphagnum

papillosumSph

fuscum

Sph

balticumSph

lindbergiiSph

subfulvum

Cladonia

rangiferin

aCladoniaspp

66u32932

841

6Prime

33u892245

92Prime

3Ershovskoe

810iexcl

4035

Transitio

naapa

-fen

18

18

Peat

55

sedimen

ts55ndash

80

minus5

Pinu

ssylvestris

Betula

nana

Rubus cham

aemorus

Oxycoccus

microcarpus

Vacciacutenium

sp

Eriophorum

polystachyon

Carexrostrata

Baeothryon

caespitosum

Menyanthestrifoliata

Utricularia

sp

Comarum

palustre

Descham

psiasp

Calamagrostissp

Spha

gnum

papillosumS

ph

subfulvu

m

Spha

gnum

spp

3_166u329

143874Prime33u39

357156Prime

3_266u

329279198Prime

33u3929628Prime

4Kislosladk

oemdash

15

Detaching

from

thesea

03

03

Peat

50-60

sedimen

ts50ndash

60

water

75ndash

92

minus5

Pinu

ssylvestris

Betula

pubescen

Betula

pubescens

6B

nana

Cornus

suecica

Em

petru

mhermaphroditu

Vacciniumvitis-

idaeaOxycoccus

palustris

Rubus

cham

aemorus

AstertripoliumT

riglochin

maritimaPhleu

malpinu

mFestuca

rubraJuncus

atrofuscusP

olygonum

viviparumB

lysmus

rufusEleocharis

uniglumis

Sphagnum

spp

66u329

525186Prime

33u898865Prime

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 235

SamplingmdashPeat samples (05-2 m deep) were taken every 50cm with a hand peat drill from each of the peatlands inSphagnum-covered sites (one series of samples from onecore of each peatland) Peat samples 50-10 cm deep plants(living and dead parts of Sphagnum spp) and soil sampleswere taken with a knife The tools were cleansed with waterand 96 alcohol after each extraction Twenty-two samplesof peat were taken from the Verkhnee Peatland 21 fromKrugloe 19 from Verkhnee Ershovskoe and nine from Kislo-sladkoe Peatland sediment samples were taken every 05 mat different depths by Scuba and free diving from both sur-face and from approximately 03 m below surface at eachsampling site Six sediment samples were taken from eachof the three peatlands the Verkhnee Krugloe and NizhneeErshovskoe four samples from the Verkhnee Ershovskoeand seven from the Kislosladkoe The collected sampleswere transferred to sterile Petri dishes and transported in acooler to the laboratory where they were stored at 5 C 1-2 dafter sampling The samples of different species of Sphagnumwere collected in sterile paper envelopes for identification

Fungal isolation and identificationmdashFrom the peat samplesSphagnum spp plant material and sediment dilutions wereprepared with 1 g in 10 mL sterile distilled water poundedby a mortar and further diluted 100-fold From this finaldilution 025 mL was pipetted on each of two Petri plates ofsix media malt agar (MA containing 17 g malt extract[Merck] and 20 g agar per liter) water agar (WA containing20 g agar per liter) citric-acid buffer agar (CA pH 4 contain-ing 800 mL citric-acid buffer (McIlvaine 1921) 17 g maltextract 30 g agar and 200 mL dH2O) Sphagnum extractagar (SEA containing 600 mL Sphagnum-extract (from 200 gSphagnum spp in 500 mL bog H2O) 20 g agar and 400 mLdH2O) alkaline buffer agar (AA pH 9 containing 12 gNa2CO3 6 g NaHCO3 17 g malt extract and 20 g agar)semi-saltwater agar (SWA containing 20 g agar per liter unfil-tered water from Kislosladkoe Lake) Petri dishes were incu-bated at room temperature in light until fungal coloniesappeared (5ndash30 d according to growth of fungi) the colonieswere subcultured onto MA as soon as they grew from thesamples Our isolation method did not yield yeasts or chytri-diomycetous fungi or lower fungi-like organisms such asOomycota Naturally our recovery output of fungi from theinvestigated habitats was affected by isolation and incubationbiases such as media type and incubation conditions Newlyisolated fungi were subcultured for identification accordingto the morphology and cultural features The cultures thatfailed to sporulate after incubation were considered sterileThe major part of the sterile mycelia and other species thatwere difficult to identify by morphology (Acremonium-likeCadophoraPhialophora-like Phoma-like isolates) were identi-fied by DNA sequence analysis of the ITS regions LSU andSSU of nuclear-encoded rDNA The same analysis was con-ducted for dominant fungal species to verify identificationby morphological features

Data analysismdashData on the total number of microscopicfungi were expressed in colony-forming units (CFU) per gdry peat For this purpose 1 g of every sample was placed inT

ABLEI

Con

tinue

d

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

Sorbus

aucuparia

Vaccinium

uliginosum

Ophioglossum

vulgatum

Prim

ula

nutansSalixsp

CarexsectT

emnelis

Trientaliseuropaea

Triglochinpalustris

Triglochin

maritima

Parnassia

palustris

Comarum

palustre

Listera

cordata

Comarum

palustre

Dactylorhiza

maculata

Eleocharispolystachion

236 MYCOLOGIA

a drying chamber at 120 C for 24 h to establish the water con-tent of each sample The spatial frequency () of every spe-cies was calculated as the number of sites of occurrence times100 divided by the total number of sites samples The abun-dance () of fungal divisions was calculated as the CFU ofthe genus 6100the total CFU of all genera from the peat-land Species diversity was determined by enumerating thenumber of species of the genus in the peatland Soslashrensenindex was used to compare fungal communities among thepeatlands (Zak et al 2004)

Molecular techniques and sequence analysismdashGenomicDNA was isolated from mycelium of the 152 fungal strainswith a chloroformisopropanol method (Karakousis et al2006) Before DNA isolation the fungi were grown on MAwith under cellophane membranep 3-5 d at 27 C The myce-lium was harvested frozen with liquid nitrogen and grindedtwice for 10 s with a bead-beater machine (beads 2 mm diam)added to the Eppendorf tube with mycelium Then 1 mLLETS buffer (01 M LiCl 10 mM EDTA pH 5 80 10 mMTris pH 5 80 05 SDS) was added mixed thoroughly(withvortex) and centrifuged 15 min at 13 000 rpm A totalof 700 mL supernatant was transferred into a fresh 2 mLEppendorf tube Five milliliters of proteinase K was addedand incubated 1 h at 37 C Subsequently 300 mL phenoland 300 mL SEVAG (isoamylalcoholchloroform 124) wereadded mixed thoroughly and centrifuged 15 min at 13 000rpm A total of 600 mL of the supernatant was transferred toa clean 15 mL Eppendorf tube 300 mL SEVAG was addedmixed thoroughly and centrifuged 15 min at 13 000 rpm Atotal of 500 mL supernatant was transferred to a clean Eppen-dorf tube 300 mL (066 volume) was added mixed andstored for 15 min at minus20 C or overnight at 4 C Then nucleicacids were centrifuged out of suspension in an Eppendorf cen-trifuge for 15 min at 13 000 rpm at 4 C The supernatant wasdiscarded with a micropipette the pellet was washed with100 mL ice-cold 70 ethanol and centrifuged 1 min at13 000 rpm at 4 C The supernatant was discarded with amicropipette the pellet was dried under vacuum and dissolvedovernight in 50 mL MQ water at 4 C Subsequently the solu-tion was mixed with a pipette and stored minus20 C The resultantDNA solution was used for subsequent PCR procedure

The primers ITS-1f and ITS4r (White et al 1990) wereused to amplify a portion of the nuclear ribosomal gene(rDNA) including the two internal transcribed spacerregions (ITS1 and ITS2) and the 58S rDNA The primersLR0R LR7 LR9 NS1 NS4 and NS8 (Vilgalys et al 1990httpwwwlutzonilabnetprimerspage244shtmL) wereused for amplification of part of the nuclear large and smallsubunits (LSU and SSU) of rDNA

PCR mixes (Promega Corp Madison Wisconsin) con-tained 05 mL 25 mM MgCl2 5 mL 56 PCR GoTag buffer 1mL 10 mM dNTP 1 mL 10 mM of each PCR primer 01 mLGoTag polymerase and 2 mL gDNA in 25 mL The amplifica-tion program included 35 cycles of 94 C for 1 min 52 C for 1min and 72 C for 1 min followed by final extension at 72 Cfor 7 min PCR products were purified with GenEluteTM

PCR Clean-Up Kit (Sigma) and sequenced in EurofinsMWG Operon (Ebersberg Germany) Sequences were com-pared with data from GenBank with a BLAST similarity

query If the ITS sequence similarity was more than 85we considered the isolate a member of kingdom Fungi

RESULTS

In total 501 fungal isolates were obtained from the 100samples of Sphagnum moss peat and sediments thatwere collected annually in summer (Jun-Jul) 2007ndash2010These isolates belong to 211 taxa representing 65 gen-era Of these taxa 113 (54) were Ascomycota 30(15) Basidiomycota seven (3) Zygomycota and 61were sterile unidentified morphotypes (including Fun-gus sp strain) (TABLE II) The number of viable fungalpropagules were 102ndash105 CFU per 1 g dry weightTaxonomic identification of all 211 taxa was based onmorphological characteristics and 98 of them alsowere identified by molecular genetics (ITS regionLSU SSU rDNA) including a major part of the sterilemycelia (93 of 153 isolates) other species difficult toidentify by morphology (13 taxa from Acremonium-like CadophoraPhialophora-like and Phoma-like groupsof fungi) and few frequent species (10 taxa) Newlygenerated sequences were deposited in the GenBankwith accession numbers provided (TABLE III) Due tothe lack of the GenBank data sequence identity forthe ITS in some cases was higher than for LSU (TABLE

III) On the whole 25 taxa were linked with known spe-cies and 73 remained undetermined The number oftaxa in the peatlands ranged from 44 (Krugloe Peat-land) to 84 (Ershovskoe Peatland) The number ofidentified taxa in the peat and sediments rangedfrom 30 (Krugloe Peatland) to 47 (Verkhnee andKislosladkoe peatlands) and from 18 (Krugloe) to 42(Ershovskoe Nizhnee) The overall frequency of fungaltaxa was low (20 and lower) The frequency of fungaltaxa in the peat and sediments of different bogs was34ndash321 and 34ndash179 respectively (TABLE II)

The dominance of fungi from the Ascomycota divi-sion was a common characteristic of the mycobiotafrom all reservoirs investigated due to the anamorphicspecies (FIG 3) The prevailing genus was PenicilliumLink with its Talaromyces CRBenj sexual stage (32species) predominantly from Monoverticillata andBiverticillata-Symmetrica sections (TABLE II) Only eightspecies (eg Talaromyces funiculosus P spinulosum Pthomii Cladosporium cladosporioides C herbarum Pseudo-gymnoascus pannorum Beauveria bassiana Tolypocladiuminflatum) were obtained from all peatlands and labeledtypical species for the investigated peatlands (TABLE II)The similarity of the fungal communities among thedifferent peatlands ranged from 020 (Ershovskoeand Kislosladkoe) to 032 (Verkhnee and Krugloe)(FIG 4)

Because the fungal communities of the peat andsediments of each of the four peatlands differed sub-stantially peat and sediments had to be analyzed

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 237

2006a b 2007 Andersen et al 2010) In the northernpeatlands fungal diversity estimates are 22ndash55 speciesper peatland Those species have a capacity for livingand physiological activity in peat (Nilsson and Ruumllcker1992 Czeczuga 1993 Thormann et al 2001b)

The respective role of fungi in litter decompositionand the multiple-factor peat-forming process in peat-lands is still poorly studied Most peatlands are in thenorthern hemisphere (Thormann et al 2007) how-ever little is known about fungal biodiversity of thenorthern peatlands Some data is available of peatlandfungi from western Siberian and central Russia(Golovchenko et al 2002 Kachalkin et al 2005Grum-Grzhimaylo and Bilanenko 2009 Filippova andThormann 2014) but almost no data is available forthe fungi from the peatlands in northwestern Russia

The peatlands at the Kandalaksha Bay of the WhiteSea have a unique origin They appear as a result of apart of the sea becoming isolated during rapid landuplift (05 cmy) followed by both demineralizationand the development of bogs (Shaporenko et al 2005Pantyulin and Krasnova 2011) In this process thesuccession of marine biota by freshwater takes placewhich is common for peatlands Fungi functioningas decomposers symbionts parasites and pathogensare associated with the evolution of the reservoirs thathave a sea origin (their number is evaluated from oneto several hundred at Kandalaksha Bay) but the dataon mycobiota of these systems are hardly discussed inthe literature

The aim of our research was to investigate fungaldiversity in the peatlands around the White Sea Biolog‐ical Station (WSBS) of Lomonosov Moscow State Uni-versity in northwestern Russia The fungi were isolatedfrom the peat and sediment samples taken from

four peatlands at different altitudes above sea level(15ndash87 m) representing different stages of bog forma-tion Fungi were identified with morphological andcultural features as well as DNA sequence data (ITSrDNA region along with SSU and LSU rDNA) Wecharacterized the composition abundance and spatialdistribution of species in fungal communities frompeatlands in connection with the age of the reservoirsand their contact with the sea

MATERIALS AND METHODS

Study areamdashIt is near the Karelian coast of Kandalaksha Bayof the White Sea (FIG 1) near the WSBS (66u349N 33u089E)Kindo Peninsula where the station is located is near the Arc-tic Circle The geographic position of lakes determines theclimatic conditions under which their hydrological regimeis formed In this case this is a long winter with an averagedaily temperature of minus11 C in Jan and a relatively shorthumid summer with a maximum precipitation in Aug and amean temperature of 14 C in Jul (Shaporenko et al 2005)Annual precipitation is 300ndash400 mm (Bubnova 2005) Geo-morphologically the region lies on the northern margin ofPribelomorskaya Lowland The maximum elevation of thearea is less than 100 m

Description of the investigated peatlandsmdashFour investigatedpeatlands are located ranging from the lowest to the highestpoint of the peninsula and represent almost all evolutionstages of bogs in this area of theWhite Sea coast (FIG 1 TABLE

I) Two of them represent raised bog-type peatlands (Verkh-nee Krugloe FIGS 2A 2B) the third is a transition aapa fen(Ershovskoe FIG 2C) and the fourth is a brackish lake detach-ing from the sea (Kislosladkoe FIG 2D) Kislosladkoe Lakehas both marine and continental features There is a combi-nation of typical littoral vegetation with bog plants dependingof coast parts in this peatland The characteristics of aapa fentypes were described in detail by Laitinen et al (2007)

FIG 1 Map of the Kindo Peninsula with four studied peatlands tagged A 5 Verkhnee Peatland B 5 Krugloe Peatland C 5Ershovskoe Peatland C(1) 5 Ershovskoe Verkhnee Lake C(2) 5 Ershovskoe Nizhnee Lake D 5 Kislosladkoe Peatland WSBS5 White Sea Biological Station

234 MYCOLOGIA

TABLEIDescriptio

nof

theinvestigated

peatlands

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

1Verkh

nee

8400

iexcl11

087

Raisedbo

g46

20

Peat

41

sedimen

ts60

minus20

Pinu

ssylvestris

Betula

nana

Cha

maeda

phne

calyculata

Calluna

vulgaris

Rubus

cham

aemorus

Oxycoccus

microcarpus

Ledum

palustre

Drosera

rotund

ifolia

D

anglica

Eriophorum

latifolium

Menyanthestrifolia

ta

Pleuroziu

mschreberi

Sphagnum

fuscum

Sphcapillifolium

Sphpapillosum

Sphmagellanicu

m

Sphmajus

Cladonia

rangiferin

aCl

alpestris

Clm

itis

Cetraria

islandica

Nephrom

asp

66u 32937

020

6Prime

33u595043

48Prime

2Krugloe

3970

iexcl40

275

Oligotroph

icaapa

24

14

Peat

41

sedimen

ts60ndash

65

minus10

Pinu

ssylvestris

Betula

nana

Calluna

vulgaris

Rubus

cham

aemorus

Oxycoccus

microcarpus

Vacciacutenium

sp

Drosera

rotund

ifolia

D

anglica

Baeothryon

caespitosum

Pleuroziu

mschreberi

Sphagnum

papillosumSph

fuscum

Sph

balticumSph

lindbergiiSph

subfulvum

Cladonia

rangiferin

aCladoniaspp

66u32932

841

6Prime

33u892245

92Prime

3Ershovskoe

810iexcl

4035

Transitio

naapa

-fen

18

18

Peat

55

sedimen

ts55ndash

80

minus5

Pinu

ssylvestris

Betula

nana

Rubus cham

aemorus

Oxycoccus

microcarpus

Vacciacutenium

sp

Eriophorum

polystachyon

Carexrostrata

Baeothryon

caespitosum

Menyanthestrifoliata

Utricularia

sp

Comarum

palustre

Descham

psiasp

Calamagrostissp

Spha

gnum

papillosumS

ph

subfulvu

m

Spha

gnum

spp

3_166u329

143874Prime33u39

357156Prime

3_266u

329279198Prime

33u3929628Prime

4Kislosladk

oemdash

15

Detaching

from

thesea

03

03

Peat

50-60

sedimen

ts50ndash

60

water

75ndash

92

minus5

Pinu

ssylvestris

Betula

pubescen

Betula

pubescens

6B

nana

Cornus

suecica

Em

petru

mhermaphroditu

Vacciniumvitis-

idaeaOxycoccus

palustris

Rubus

cham

aemorus

AstertripoliumT

riglochin

maritimaPhleu

malpinu

mFestuca

rubraJuncus

atrofuscusP

olygonum

viviparumB

lysmus

rufusEleocharis

uniglumis

Sphagnum

spp

66u329

525186Prime

33u898865Prime

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 235

SamplingmdashPeat samples (05-2 m deep) were taken every 50cm with a hand peat drill from each of the peatlands inSphagnum-covered sites (one series of samples from onecore of each peatland) Peat samples 50-10 cm deep plants(living and dead parts of Sphagnum spp) and soil sampleswere taken with a knife The tools were cleansed with waterand 96 alcohol after each extraction Twenty-two samplesof peat were taken from the Verkhnee Peatland 21 fromKrugloe 19 from Verkhnee Ershovskoe and nine from Kislo-sladkoe Peatland sediment samples were taken every 05 mat different depths by Scuba and free diving from both sur-face and from approximately 03 m below surface at eachsampling site Six sediment samples were taken from eachof the three peatlands the Verkhnee Krugloe and NizhneeErshovskoe four samples from the Verkhnee Ershovskoeand seven from the Kislosladkoe The collected sampleswere transferred to sterile Petri dishes and transported in acooler to the laboratory where they were stored at 5 C 1-2 dafter sampling The samples of different species of Sphagnumwere collected in sterile paper envelopes for identification

Fungal isolation and identificationmdashFrom the peat samplesSphagnum spp plant material and sediment dilutions wereprepared with 1 g in 10 mL sterile distilled water poundedby a mortar and further diluted 100-fold From this finaldilution 025 mL was pipetted on each of two Petri plates ofsix media malt agar (MA containing 17 g malt extract[Merck] and 20 g agar per liter) water agar (WA containing20 g agar per liter) citric-acid buffer agar (CA pH 4 contain-ing 800 mL citric-acid buffer (McIlvaine 1921) 17 g maltextract 30 g agar and 200 mL dH2O) Sphagnum extractagar (SEA containing 600 mL Sphagnum-extract (from 200 gSphagnum spp in 500 mL bog H2O) 20 g agar and 400 mLdH2O) alkaline buffer agar (AA pH 9 containing 12 gNa2CO3 6 g NaHCO3 17 g malt extract and 20 g agar)semi-saltwater agar (SWA containing 20 g agar per liter unfil-tered water from Kislosladkoe Lake) Petri dishes were incu-bated at room temperature in light until fungal coloniesappeared (5ndash30 d according to growth of fungi) the colonieswere subcultured onto MA as soon as they grew from thesamples Our isolation method did not yield yeasts or chytri-diomycetous fungi or lower fungi-like organisms such asOomycota Naturally our recovery output of fungi from theinvestigated habitats was affected by isolation and incubationbiases such as media type and incubation conditions Newlyisolated fungi were subcultured for identification accordingto the morphology and cultural features The cultures thatfailed to sporulate after incubation were considered sterileThe major part of the sterile mycelia and other species thatwere difficult to identify by morphology (Acremonium-likeCadophoraPhialophora-like Phoma-like isolates) were identi-fied by DNA sequence analysis of the ITS regions LSU andSSU of nuclear-encoded rDNA The same analysis was con-ducted for dominant fungal species to verify identificationby morphological features

Data analysismdashData on the total number of microscopicfungi were expressed in colony-forming units (CFU) per gdry peat For this purpose 1 g of every sample was placed inT

ABLEI

Con

tinue

d

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

Sorbus

aucuparia

Vaccinium

uliginosum

Ophioglossum

vulgatum

Prim

ula

nutansSalixsp

CarexsectT

emnelis

Trientaliseuropaea

Triglochinpalustris

Triglochin

maritima

Parnassia

palustris

Comarum

palustre

Listera

cordata

Comarum

palustre

Dactylorhiza

maculata

Eleocharispolystachion

236 MYCOLOGIA

a drying chamber at 120 C for 24 h to establish the water con-tent of each sample The spatial frequency () of every spe-cies was calculated as the number of sites of occurrence times100 divided by the total number of sites samples The abun-dance () of fungal divisions was calculated as the CFU ofthe genus 6100the total CFU of all genera from the peat-land Species diversity was determined by enumerating thenumber of species of the genus in the peatland Soslashrensenindex was used to compare fungal communities among thepeatlands (Zak et al 2004)

Molecular techniques and sequence analysismdashGenomicDNA was isolated from mycelium of the 152 fungal strainswith a chloroformisopropanol method (Karakousis et al2006) Before DNA isolation the fungi were grown on MAwith under cellophane membranep 3-5 d at 27 C The myce-lium was harvested frozen with liquid nitrogen and grindedtwice for 10 s with a bead-beater machine (beads 2 mm diam)added to the Eppendorf tube with mycelium Then 1 mLLETS buffer (01 M LiCl 10 mM EDTA pH 5 80 10 mMTris pH 5 80 05 SDS) was added mixed thoroughly(withvortex) and centrifuged 15 min at 13 000 rpm A totalof 700 mL supernatant was transferred into a fresh 2 mLEppendorf tube Five milliliters of proteinase K was addedand incubated 1 h at 37 C Subsequently 300 mL phenoland 300 mL SEVAG (isoamylalcoholchloroform 124) wereadded mixed thoroughly and centrifuged 15 min at 13 000rpm A total of 600 mL of the supernatant was transferred toa clean 15 mL Eppendorf tube 300 mL SEVAG was addedmixed thoroughly and centrifuged 15 min at 13 000 rpm Atotal of 500 mL supernatant was transferred to a clean Eppen-dorf tube 300 mL (066 volume) was added mixed andstored for 15 min at minus20 C or overnight at 4 C Then nucleicacids were centrifuged out of suspension in an Eppendorf cen-trifuge for 15 min at 13 000 rpm at 4 C The supernatant wasdiscarded with a micropipette the pellet was washed with100 mL ice-cold 70 ethanol and centrifuged 1 min at13 000 rpm at 4 C The supernatant was discarded with amicropipette the pellet was dried under vacuum and dissolvedovernight in 50 mL MQ water at 4 C Subsequently the solu-tion was mixed with a pipette and stored minus20 C The resultantDNA solution was used for subsequent PCR procedure

The primers ITS-1f and ITS4r (White et al 1990) wereused to amplify a portion of the nuclear ribosomal gene(rDNA) including the two internal transcribed spacerregions (ITS1 and ITS2) and the 58S rDNA The primersLR0R LR7 LR9 NS1 NS4 and NS8 (Vilgalys et al 1990httpwwwlutzonilabnetprimerspage244shtmL) wereused for amplification of part of the nuclear large and smallsubunits (LSU and SSU) of rDNA

PCR mixes (Promega Corp Madison Wisconsin) con-tained 05 mL 25 mM MgCl2 5 mL 56 PCR GoTag buffer 1mL 10 mM dNTP 1 mL 10 mM of each PCR primer 01 mLGoTag polymerase and 2 mL gDNA in 25 mL The amplifica-tion program included 35 cycles of 94 C for 1 min 52 C for 1min and 72 C for 1 min followed by final extension at 72 Cfor 7 min PCR products were purified with GenEluteTM

PCR Clean-Up Kit (Sigma) and sequenced in EurofinsMWG Operon (Ebersberg Germany) Sequences were com-pared with data from GenBank with a BLAST similarity

query If the ITS sequence similarity was more than 85we considered the isolate a member of kingdom Fungi

RESULTS

In total 501 fungal isolates were obtained from the 100samples of Sphagnum moss peat and sediments thatwere collected annually in summer (Jun-Jul) 2007ndash2010These isolates belong to 211 taxa representing 65 gen-era Of these taxa 113 (54) were Ascomycota 30(15) Basidiomycota seven (3) Zygomycota and 61were sterile unidentified morphotypes (including Fun-gus sp strain) (TABLE II) The number of viable fungalpropagules were 102ndash105 CFU per 1 g dry weightTaxonomic identification of all 211 taxa was based onmorphological characteristics and 98 of them alsowere identified by molecular genetics (ITS regionLSU SSU rDNA) including a major part of the sterilemycelia (93 of 153 isolates) other species difficult toidentify by morphology (13 taxa from Acremonium-like CadophoraPhialophora-like and Phoma-like groupsof fungi) and few frequent species (10 taxa) Newlygenerated sequences were deposited in the GenBankwith accession numbers provided (TABLE III) Due tothe lack of the GenBank data sequence identity forthe ITS in some cases was higher than for LSU (TABLE

III) On the whole 25 taxa were linked with known spe-cies and 73 remained undetermined The number oftaxa in the peatlands ranged from 44 (Krugloe Peat-land) to 84 (Ershovskoe Peatland) The number ofidentified taxa in the peat and sediments rangedfrom 30 (Krugloe Peatland) to 47 (Verkhnee andKislosladkoe peatlands) and from 18 (Krugloe) to 42(Ershovskoe Nizhnee) The overall frequency of fungaltaxa was low (20 and lower) The frequency of fungaltaxa in the peat and sediments of different bogs was34ndash321 and 34ndash179 respectively (TABLE II)

The dominance of fungi from the Ascomycota divi-sion was a common characteristic of the mycobiotafrom all reservoirs investigated due to the anamorphicspecies (FIG 3) The prevailing genus was PenicilliumLink with its Talaromyces CRBenj sexual stage (32species) predominantly from Monoverticillata andBiverticillata-Symmetrica sections (TABLE II) Only eightspecies (eg Talaromyces funiculosus P spinulosum Pthomii Cladosporium cladosporioides C herbarum Pseudo-gymnoascus pannorum Beauveria bassiana Tolypocladiuminflatum) were obtained from all peatlands and labeledtypical species for the investigated peatlands (TABLE II)The similarity of the fungal communities among thedifferent peatlands ranged from 020 (Ershovskoeand Kislosladkoe) to 032 (Verkhnee and Krugloe)(FIG 4)

Because the fungal communities of the peat andsediments of each of the four peatlands differed sub-stantially peat and sediments had to be analyzed

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 237

TABLEIDescriptio

nof

theinvestigated

peatlands

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

1Verkh

nee

8400

iexcl11

087

Raisedbo

g46

20

Peat

41

sedimen

ts60

minus20

Pinu

ssylvestris

Betula

nana

Cha

maeda

phne

calyculata

Calluna

vulgaris

Rubus

cham

aemorus

Oxycoccus

microcarpus

Ledum

palustre

Drosera

rotund

ifolia

D

anglica

Eriophorum

latifolium

Menyanthestrifolia

ta

Pleuroziu

mschreberi

Sphagnum

fuscum

Sphcapillifolium

Sphpapillosum

Sphmagellanicu

m

Sphmajus

Cladonia

rangiferin

aCl

alpestris

Clm

itis

Cetraria

islandica

Nephrom

asp

66u 32937

020

6Prime

33u595043

48Prime

2Krugloe

3970

iexcl40

275

Oligotroph

icaapa

24

14

Peat

41

sedimen

ts60ndash

65

minus10

Pinu

ssylvestris

Betula

nana

Calluna

vulgaris

Rubus

cham

aemorus

Oxycoccus

microcarpus

Vacciacutenium

sp

Drosera

rotund

ifolia

D

anglica

Baeothryon

caespitosum

Pleuroziu

mschreberi

Sphagnum

papillosumSph

fuscum

Sph

balticumSph

lindbergiiSph

subfulvum

Cladonia

rangiferin

aCladoniaspp

66u32932

841

6Prime

33u892245

92Prime

3Ershovskoe

810iexcl

4035

Transitio

naapa

-fen

18

18

Peat

55

sedimen

ts55ndash

80

minus5

Pinu

ssylvestris

Betula

nana

Rubus cham

aemorus

Oxycoccus

microcarpus

Vacciacutenium

sp

Eriophorum

polystachyon

Carexrostrata

Baeothryon

caespitosum

Menyanthestrifoliata

Utricularia

sp

Comarum

palustre

Descham

psiasp

Calamagrostissp

Spha

gnum

papillosumS

ph

subfulvu

m

Spha

gnum

spp

3_166u329

143874Prime33u39

357156Prime

3_266u

329279198Prime

33u3929628Prime

4Kislosladk

oemdash

15

Detaching

from

thesea

03

03

Peat

50-60

sedimen

ts50ndash

60

water

75ndash

92

minus5

Pinu

ssylvestris

Betula

pubescen

Betula

pubescens

6B

nana

Cornus

suecica

Em

petru

mhermaphroditu

Vacciniumvitis-

idaeaOxycoccus

palustris

Rubus

cham

aemorus

AstertripoliumT

riglochin

maritimaPhleu

malpinu

mFestuca

rubraJuncus

atrofuscusP

olygonum

viviparumB

lysmus

rufusEleocharis

uniglumis

Sphagnum

spp

66u329

525186Prime

33u898865Prime

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 235

SamplingmdashPeat samples (05-2 m deep) were taken every 50cm with a hand peat drill from each of the peatlands inSphagnum-covered sites (one series of samples from onecore of each peatland) Peat samples 50-10 cm deep plants(living and dead parts of Sphagnum spp) and soil sampleswere taken with a knife The tools were cleansed with waterand 96 alcohol after each extraction Twenty-two samplesof peat were taken from the Verkhnee Peatland 21 fromKrugloe 19 from Verkhnee Ershovskoe and nine from Kislo-sladkoe Peatland sediment samples were taken every 05 mat different depths by Scuba and free diving from both sur-face and from approximately 03 m below surface at eachsampling site Six sediment samples were taken from eachof the three peatlands the Verkhnee Krugloe and NizhneeErshovskoe four samples from the Verkhnee Ershovskoeand seven from the Kislosladkoe The collected sampleswere transferred to sterile Petri dishes and transported in acooler to the laboratory where they were stored at 5 C 1-2 dafter sampling The samples of different species of Sphagnumwere collected in sterile paper envelopes for identification

Fungal isolation and identificationmdashFrom the peat samplesSphagnum spp plant material and sediment dilutions wereprepared with 1 g in 10 mL sterile distilled water poundedby a mortar and further diluted 100-fold From this finaldilution 025 mL was pipetted on each of two Petri plates ofsix media malt agar (MA containing 17 g malt extract[Merck] and 20 g agar per liter) water agar (WA containing20 g agar per liter) citric-acid buffer agar (CA pH 4 contain-ing 800 mL citric-acid buffer (McIlvaine 1921) 17 g maltextract 30 g agar and 200 mL dH2O) Sphagnum extractagar (SEA containing 600 mL Sphagnum-extract (from 200 gSphagnum spp in 500 mL bog H2O) 20 g agar and 400 mLdH2O) alkaline buffer agar (AA pH 9 containing 12 gNa2CO3 6 g NaHCO3 17 g malt extract and 20 g agar)semi-saltwater agar (SWA containing 20 g agar per liter unfil-tered water from Kislosladkoe Lake) Petri dishes were incu-bated at room temperature in light until fungal coloniesappeared (5ndash30 d according to growth of fungi) the colonieswere subcultured onto MA as soon as they grew from thesamples Our isolation method did not yield yeasts or chytri-diomycetous fungi or lower fungi-like organisms such asOomycota Naturally our recovery output of fungi from theinvestigated habitats was affected by isolation and incubationbiases such as media type and incubation conditions Newlyisolated fungi were subcultured for identification accordingto the morphology and cultural features The cultures thatfailed to sporulate after incubation were considered sterileThe major part of the sterile mycelia and other species thatwere difficult to identify by morphology (Acremonium-likeCadophoraPhialophora-like Phoma-like isolates) were identi-fied by DNA sequence analysis of the ITS regions LSU andSSU of nuclear-encoded rDNA The same analysis was con-ducted for dominant fungal species to verify identificationby morphological features

Data analysismdashData on the total number of microscopicfungi were expressed in colony-forming units (CFU) per gdry peat For this purpose 1 g of every sample was placed inT

ABLEI

Con

tinue

d

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

Sorbus

aucuparia

Vaccinium

uliginosum

Ophioglossum

vulgatum

Prim

ula

nutansSalixsp

CarexsectT

emnelis

Trientaliseuropaea

Triglochinpalustris

Triglochin

maritima

Parnassia

palustris

Comarum

palustre

Listera

cordata

Comarum

palustre

Dactylorhiza

maculata

Eleocharispolystachion

236 MYCOLOGIA

a drying chamber at 120 C for 24 h to establish the water con-tent of each sample The spatial frequency () of every spe-cies was calculated as the number of sites of occurrence times100 divided by the total number of sites samples The abun-dance () of fungal divisions was calculated as the CFU ofthe genus 6100the total CFU of all genera from the peat-land Species diversity was determined by enumerating thenumber of species of the genus in the peatland Soslashrensenindex was used to compare fungal communities among thepeatlands (Zak et al 2004)

Molecular techniques and sequence analysismdashGenomicDNA was isolated from mycelium of the 152 fungal strainswith a chloroformisopropanol method (Karakousis et al2006) Before DNA isolation the fungi were grown on MAwith under cellophane membranep 3-5 d at 27 C The myce-lium was harvested frozen with liquid nitrogen and grindedtwice for 10 s with a bead-beater machine (beads 2 mm diam)added to the Eppendorf tube with mycelium Then 1 mLLETS buffer (01 M LiCl 10 mM EDTA pH 5 80 10 mMTris pH 5 80 05 SDS) was added mixed thoroughly(withvortex) and centrifuged 15 min at 13 000 rpm A totalof 700 mL supernatant was transferred into a fresh 2 mLEppendorf tube Five milliliters of proteinase K was addedand incubated 1 h at 37 C Subsequently 300 mL phenoland 300 mL SEVAG (isoamylalcoholchloroform 124) wereadded mixed thoroughly and centrifuged 15 min at 13 000rpm A total of 600 mL of the supernatant was transferred toa clean 15 mL Eppendorf tube 300 mL SEVAG was addedmixed thoroughly and centrifuged 15 min at 13 000 rpm Atotal of 500 mL supernatant was transferred to a clean Eppen-dorf tube 300 mL (066 volume) was added mixed andstored for 15 min at minus20 C or overnight at 4 C Then nucleicacids were centrifuged out of suspension in an Eppendorf cen-trifuge for 15 min at 13 000 rpm at 4 C The supernatant wasdiscarded with a micropipette the pellet was washed with100 mL ice-cold 70 ethanol and centrifuged 1 min at13 000 rpm at 4 C The supernatant was discarded with amicropipette the pellet was dried under vacuum and dissolvedovernight in 50 mL MQ water at 4 C Subsequently the solu-tion was mixed with a pipette and stored minus20 C The resultantDNA solution was used for subsequent PCR procedure

The primers ITS-1f and ITS4r (White et al 1990) wereused to amplify a portion of the nuclear ribosomal gene(rDNA) including the two internal transcribed spacerregions (ITS1 and ITS2) and the 58S rDNA The primersLR0R LR7 LR9 NS1 NS4 and NS8 (Vilgalys et al 1990httpwwwlutzonilabnetprimerspage244shtmL) wereused for amplification of part of the nuclear large and smallsubunits (LSU and SSU) of rDNA

PCR mixes (Promega Corp Madison Wisconsin) con-tained 05 mL 25 mM MgCl2 5 mL 56 PCR GoTag buffer 1mL 10 mM dNTP 1 mL 10 mM of each PCR primer 01 mLGoTag polymerase and 2 mL gDNA in 25 mL The amplifica-tion program included 35 cycles of 94 C for 1 min 52 C for 1min and 72 C for 1 min followed by final extension at 72 Cfor 7 min PCR products were purified with GenEluteTM

PCR Clean-Up Kit (Sigma) and sequenced in EurofinsMWG Operon (Ebersberg Germany) Sequences were com-pared with data from GenBank with a BLAST similarity

query If the ITS sequence similarity was more than 85we considered the isolate a member of kingdom Fungi

RESULTS

In total 501 fungal isolates were obtained from the 100samples of Sphagnum moss peat and sediments thatwere collected annually in summer (Jun-Jul) 2007ndash2010These isolates belong to 211 taxa representing 65 gen-era Of these taxa 113 (54) were Ascomycota 30(15) Basidiomycota seven (3) Zygomycota and 61were sterile unidentified morphotypes (including Fun-gus sp strain) (TABLE II) The number of viable fungalpropagules were 102ndash105 CFU per 1 g dry weightTaxonomic identification of all 211 taxa was based onmorphological characteristics and 98 of them alsowere identified by molecular genetics (ITS regionLSU SSU rDNA) including a major part of the sterilemycelia (93 of 153 isolates) other species difficult toidentify by morphology (13 taxa from Acremonium-like CadophoraPhialophora-like and Phoma-like groupsof fungi) and few frequent species (10 taxa) Newlygenerated sequences were deposited in the GenBankwith accession numbers provided (TABLE III) Due tothe lack of the GenBank data sequence identity forthe ITS in some cases was higher than for LSU (TABLE

III) On the whole 25 taxa were linked with known spe-cies and 73 remained undetermined The number oftaxa in the peatlands ranged from 44 (Krugloe Peat-land) to 84 (Ershovskoe Peatland) The number ofidentified taxa in the peat and sediments rangedfrom 30 (Krugloe Peatland) to 47 (Verkhnee andKislosladkoe peatlands) and from 18 (Krugloe) to 42(Ershovskoe Nizhnee) The overall frequency of fungaltaxa was low (20 and lower) The frequency of fungaltaxa in the peat and sediments of different bogs was34ndash321 and 34ndash179 respectively (TABLE II)

The dominance of fungi from the Ascomycota divi-sion was a common characteristic of the mycobiotafrom all reservoirs investigated due to the anamorphicspecies (FIG 3) The prevailing genus was PenicilliumLink with its Talaromyces CRBenj sexual stage (32species) predominantly from Monoverticillata andBiverticillata-Symmetrica sections (TABLE II) Only eightspecies (eg Talaromyces funiculosus P spinulosum Pthomii Cladosporium cladosporioides C herbarum Pseudo-gymnoascus pannorum Beauveria bassiana Tolypocladiuminflatum) were obtained from all peatlands and labeledtypical species for the investigated peatlands (TABLE II)The similarity of the fungal communities among thedifferent peatlands ranged from 020 (Ershovskoeand Kislosladkoe) to 032 (Verkhnee and Krugloe)(FIG 4)

Because the fungal communities of the peat andsediments of each of the four peatlands differed sub-stantially peat and sediments had to be analyzed

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 237

SamplingmdashPeat samples (05-2 m deep) were taken every 50cm with a hand peat drill from each of the peatlands inSphagnum-covered sites (one series of samples from onecore of each peatland) Peat samples 50-10 cm deep plants(living and dead parts of Sphagnum spp) and soil sampleswere taken with a knife The tools were cleansed with waterand 96 alcohol after each extraction Twenty-two samplesof peat were taken from the Verkhnee Peatland 21 fromKrugloe 19 from Verkhnee Ershovskoe and nine from Kislo-sladkoe Peatland sediment samples were taken every 05 mat different depths by Scuba and free diving from both sur-face and from approximately 03 m below surface at eachsampling site Six sediment samples were taken from eachof the three peatlands the Verkhnee Krugloe and NizhneeErshovskoe four samples from the Verkhnee Ershovskoeand seven from the Kislosladkoe The collected sampleswere transferred to sterile Petri dishes and transported in acooler to the laboratory where they were stored at 5 C 1-2 dafter sampling The samples of different species of Sphagnumwere collected in sterile paper envelopes for identification

Fungal isolation and identificationmdashFrom the peat samplesSphagnum spp plant material and sediment dilutions wereprepared with 1 g in 10 mL sterile distilled water poundedby a mortar and further diluted 100-fold From this finaldilution 025 mL was pipetted on each of two Petri plates ofsix media malt agar (MA containing 17 g malt extract[Merck] and 20 g agar per liter) water agar (WA containing20 g agar per liter) citric-acid buffer agar (CA pH 4 contain-ing 800 mL citric-acid buffer (McIlvaine 1921) 17 g maltextract 30 g agar and 200 mL dH2O) Sphagnum extractagar (SEA containing 600 mL Sphagnum-extract (from 200 gSphagnum spp in 500 mL bog H2O) 20 g agar and 400 mLdH2O) alkaline buffer agar (AA pH 9 containing 12 gNa2CO3 6 g NaHCO3 17 g malt extract and 20 g agar)semi-saltwater agar (SWA containing 20 g agar per liter unfil-tered water from Kislosladkoe Lake) Petri dishes were incu-bated at room temperature in light until fungal coloniesappeared (5ndash30 d according to growth of fungi) the colonieswere subcultured onto MA as soon as they grew from thesamples Our isolation method did not yield yeasts or chytri-diomycetous fungi or lower fungi-like organisms such asOomycota Naturally our recovery output of fungi from theinvestigated habitats was affected by isolation and incubationbiases such as media type and incubation conditions Newlyisolated fungi were subcultured for identification accordingto the morphology and cultural features The cultures thatfailed to sporulate after incubation were considered sterileThe major part of the sterile mycelia and other species thatwere difficult to identify by morphology (Acremonium-likeCadophoraPhialophora-like Phoma-like isolates) were identi-fied by DNA sequence analysis of the ITS regions LSU andSSU of nuclear-encoded rDNA The same analysis was con-ducted for dominant fungal species to verify identificationby morphological features

Data analysismdashData on the total number of microscopicfungi were expressed in colony-forming units (CFU) per gdry peat For this purpose 1 g of every sample was placed inT

ABLEI

Con

tinue

d

Peatland

Age

(year)

(Shilova

2011)

Alti-

tude

(m)

Typeof

peatland

Peat

depth

(m)

Max

depthof

sampling

(m)

pHof

samples

Water

levelin

sampling

places

(cm)

Dom

inan

tvege

tatio

nLatitu

de

longitude

(in

centers

oflake

s)No

Nam

eTrees

Shrubssub

shrubs

Herbs

Mosseslichen

s

Sorbus

aucuparia

Vaccinium

uliginosum

Ophioglossum

vulgatum

Prim

ula

nutansSalixsp

CarexsectT

emnelis

Trientaliseuropaea

Triglochinpalustris

Triglochin

maritima

Parnassia

palustris

Comarum

palustre

Listera

cordata

Comarum

palustre

Dactylorhiza

maculata

Eleocharispolystachion

236 MYCOLOGIA

a drying chamber at 120 C for 24 h to establish the water con-tent of each sample The spatial frequency () of every spe-cies was calculated as the number of sites of occurrence times100 divided by the total number of sites samples The abun-dance () of fungal divisions was calculated as the CFU ofthe genus 6100the total CFU of all genera from the peat-land Species diversity was determined by enumerating thenumber of species of the genus in the peatland Soslashrensenindex was used to compare fungal communities among thepeatlands (Zak et al 2004)

Molecular techniques and sequence analysismdashGenomicDNA was isolated from mycelium of the 152 fungal strainswith a chloroformisopropanol method (Karakousis et al2006) Before DNA isolation the fungi were grown on MAwith under cellophane membranep 3-5 d at 27 C The myce-lium was harvested frozen with liquid nitrogen and grindedtwice for 10 s with a bead-beater machine (beads 2 mm diam)added to the Eppendorf tube with mycelium Then 1 mLLETS buffer (01 M LiCl 10 mM EDTA pH 5 80 10 mMTris pH 5 80 05 SDS) was added mixed thoroughly(withvortex) and centrifuged 15 min at 13 000 rpm A totalof 700 mL supernatant was transferred into a fresh 2 mLEppendorf tube Five milliliters of proteinase K was addedand incubated 1 h at 37 C Subsequently 300 mL phenoland 300 mL SEVAG (isoamylalcoholchloroform 124) wereadded mixed thoroughly and centrifuged 15 min at 13 000rpm A total of 600 mL of the supernatant was transferred toa clean 15 mL Eppendorf tube 300 mL SEVAG was addedmixed thoroughly and centrifuged 15 min at 13 000 rpm Atotal of 500 mL supernatant was transferred to a clean Eppen-dorf tube 300 mL (066 volume) was added mixed andstored for 15 min at minus20 C or overnight at 4 C Then nucleicacids were centrifuged out of suspension in an Eppendorf cen-trifuge for 15 min at 13 000 rpm at 4 C The supernatant wasdiscarded with a micropipette the pellet was washed with100 mL ice-cold 70 ethanol and centrifuged 1 min at13 000 rpm at 4 C The supernatant was discarded with amicropipette the pellet was dried under vacuum and dissolvedovernight in 50 mL MQ water at 4 C Subsequently the solu-tion was mixed with a pipette and stored minus20 C The resultantDNA solution was used for subsequent PCR procedure

The primers ITS-1f and ITS4r (White et al 1990) wereused to amplify a portion of the nuclear ribosomal gene(rDNA) including the two internal transcribed spacerregions (ITS1 and ITS2) and the 58S rDNA The primersLR0R LR7 LR9 NS1 NS4 and NS8 (Vilgalys et al 1990httpwwwlutzonilabnetprimerspage244shtmL) wereused for amplification of part of the nuclear large and smallsubunits (LSU and SSU) of rDNA

PCR mixes (Promega Corp Madison Wisconsin) con-tained 05 mL 25 mM MgCl2 5 mL 56 PCR GoTag buffer 1mL 10 mM dNTP 1 mL 10 mM of each PCR primer 01 mLGoTag polymerase and 2 mL gDNA in 25 mL The amplifica-tion program included 35 cycles of 94 C for 1 min 52 C for 1min and 72 C for 1 min followed by final extension at 72 Cfor 7 min PCR products were purified with GenEluteTM

PCR Clean-Up Kit (Sigma) and sequenced in EurofinsMWG Operon (Ebersberg Germany) Sequences were com-pared with data from GenBank with a BLAST similarity

query If the ITS sequence similarity was more than 85we considered the isolate a member of kingdom Fungi

RESULTS

In total 501 fungal isolates were obtained from the 100samples of Sphagnum moss peat and sediments thatwere collected annually in summer (Jun-Jul) 2007ndash2010These isolates belong to 211 taxa representing 65 gen-era Of these taxa 113 (54) were Ascomycota 30(15) Basidiomycota seven (3) Zygomycota and 61were sterile unidentified morphotypes (including Fun-gus sp strain) (TABLE II) The number of viable fungalpropagules were 102ndash105 CFU per 1 g dry weightTaxonomic identification of all 211 taxa was based onmorphological characteristics and 98 of them alsowere identified by molecular genetics (ITS regionLSU SSU rDNA) including a major part of the sterilemycelia (93 of 153 isolates) other species difficult toidentify by morphology (13 taxa from Acremonium-like CadophoraPhialophora-like and Phoma-like groupsof fungi) and few frequent species (10 taxa) Newlygenerated sequences were deposited in the GenBankwith accession numbers provided (TABLE III) Due tothe lack of the GenBank data sequence identity forthe ITS in some cases was higher than for LSU (TABLE

III) On the whole 25 taxa were linked with known spe-cies and 73 remained undetermined The number oftaxa in the peatlands ranged from 44 (Krugloe Peat-land) to 84 (Ershovskoe Peatland) The number ofidentified taxa in the peat and sediments rangedfrom 30 (Krugloe Peatland) to 47 (Verkhnee andKislosladkoe peatlands) and from 18 (Krugloe) to 42(Ershovskoe Nizhnee) The overall frequency of fungaltaxa was low (20 and lower) The frequency of fungaltaxa in the peat and sediments of different bogs was34ndash321 and 34ndash179 respectively (TABLE II)

The dominance of fungi from the Ascomycota divi-sion was a common characteristic of the mycobiotafrom all reservoirs investigated due to the anamorphicspecies (FIG 3) The prevailing genus was PenicilliumLink with its Talaromyces CRBenj sexual stage (32species) predominantly from Monoverticillata andBiverticillata-Symmetrica sections (TABLE II) Only eightspecies (eg Talaromyces funiculosus P spinulosum Pthomii Cladosporium cladosporioides C herbarum Pseudo-gymnoascus pannorum Beauveria bassiana Tolypocladiuminflatum) were obtained from all peatlands and labeledtypical species for the investigated peatlands (TABLE II)The similarity of the fungal communities among thedifferent peatlands ranged from 020 (Ershovskoeand Kislosladkoe) to 032 (Verkhnee and Krugloe)(FIG 4)

Because the fungal communities of the peat andsediments of each of the four peatlands differed sub-stantially peat and sediments had to be analyzed

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 237

a drying chamber at 120 C for 24 h to establish the water con-tent of each sample The spatial frequency () of every spe-cies was calculated as the number of sites of occurrence times100 divided by the total number of sites samples The abun-dance () of fungal divisions was calculated as the CFU ofthe genus 6100the total CFU of all genera from the peat-land Species diversity was determined by enumerating thenumber of species of the genus in the peatland Soslashrensenindex was used to compare fungal communities among thepeatlands (Zak et al 2004)

Molecular techniques and sequence analysismdashGenomicDNA was isolated from mycelium of the 152 fungal strainswith a chloroformisopropanol method (Karakousis et al2006) Before DNA isolation the fungi were grown on MAwith under cellophane membranep 3-5 d at 27 C The myce-lium was harvested frozen with liquid nitrogen and grindedtwice for 10 s with a bead-beater machine (beads 2 mm diam)added to the Eppendorf tube with mycelium Then 1 mLLETS buffer (01 M LiCl 10 mM EDTA pH 5 80 10 mMTris pH 5 80 05 SDS) was added mixed thoroughly(withvortex) and centrifuged 15 min at 13 000 rpm A totalof 700 mL supernatant was transferred into a fresh 2 mLEppendorf tube Five milliliters of proteinase K was addedand incubated 1 h at 37 C Subsequently 300 mL phenoland 300 mL SEVAG (isoamylalcoholchloroform 124) wereadded mixed thoroughly and centrifuged 15 min at 13 000rpm A total of 600 mL of the supernatant was transferred toa clean 15 mL Eppendorf tube 300 mL SEVAG was addedmixed thoroughly and centrifuged 15 min at 13 000 rpm Atotal of 500 mL supernatant was transferred to a clean Eppen-dorf tube 300 mL (066 volume) was added mixed andstored for 15 min at minus20 C or overnight at 4 C Then nucleicacids were centrifuged out of suspension in an Eppendorf cen-trifuge for 15 min at 13 000 rpm at 4 C The supernatant wasdiscarded with a micropipette the pellet was washed with100 mL ice-cold 70 ethanol and centrifuged 1 min at13 000 rpm at 4 C The supernatant was discarded with amicropipette the pellet was dried under vacuum and dissolvedovernight in 50 mL MQ water at 4 C Subsequently the solu-tion was mixed with a pipette and stored minus20 C The resultantDNA solution was used for subsequent PCR procedure

The primers ITS-1f and ITS4r (White et al 1990) wereused to amplify a portion of the nuclear ribosomal gene(rDNA) including the two internal transcribed spacerregions (ITS1 and ITS2) and the 58S rDNA The primersLR0R LR7 LR9 NS1 NS4 and NS8 (Vilgalys et al 1990httpwwwlutzonilabnetprimerspage244shtmL) wereused for amplification of part of the nuclear large and smallsubunits (LSU and SSU) of rDNA

PCR mixes (Promega Corp Madison Wisconsin) con-tained 05 mL 25 mM MgCl2 5 mL 56 PCR GoTag buffer 1mL 10 mM dNTP 1 mL 10 mM of each PCR primer 01 mLGoTag polymerase and 2 mL gDNA in 25 mL The amplifica-tion program included 35 cycles of 94 C for 1 min 52 C for 1min and 72 C for 1 min followed by final extension at 72 Cfor 7 min PCR products were purified with GenEluteTM

PCR Clean-Up Kit (Sigma) and sequenced in EurofinsMWG Operon (Ebersberg Germany) Sequences were com-pared with data from GenBank with a BLAST similarity

query If the ITS sequence similarity was more than 85we considered the isolate a member of kingdom Fungi

RESULTS

In total 501 fungal isolates were obtained from the 100samples of Sphagnum moss peat and sediments thatwere collected annually in summer (Jun-Jul) 2007ndash2010These isolates belong to 211 taxa representing 65 gen-era Of these taxa 113 (54) were Ascomycota 30(15) Basidiomycota seven (3) Zygomycota and 61were sterile unidentified morphotypes (including Fun-gus sp strain) (TABLE II) The number of viable fungalpropagules were 102ndash105 CFU per 1 g dry weightTaxonomic identification of all 211 taxa was based onmorphological characteristics and 98 of them alsowere identified by molecular genetics (ITS regionLSU SSU rDNA) including a major part of the sterilemycelia (93 of 153 isolates) other species difficult toidentify by morphology (13 taxa from Acremonium-like CadophoraPhialophora-like and Phoma-like groupsof fungi) and few frequent species (10 taxa) Newlygenerated sequences were deposited in the GenBankwith accession numbers provided (TABLE III) Due tothe lack of the GenBank data sequence identity forthe ITS in some cases was higher than for LSU (TABLE

III) On the whole 25 taxa were linked with known spe-cies and 73 remained undetermined The number oftaxa in the peatlands ranged from 44 (Krugloe Peat-land) to 84 (Ershovskoe Peatland) The number ofidentified taxa in the peat and sediments rangedfrom 30 (Krugloe Peatland) to 47 (Verkhnee andKislosladkoe peatlands) and from 18 (Krugloe) to 42(Ershovskoe Nizhnee) The overall frequency of fungaltaxa was low (20 and lower) The frequency of fungaltaxa in the peat and sediments of different bogs was34ndash321 and 34ndash179 respectively (TABLE II)

The dominance of fungi from the Ascomycota divi-sion was a common characteristic of the mycobiotafrom all reservoirs investigated due to the anamorphicspecies (FIG 3) The prevailing genus was PenicilliumLink with its Talaromyces CRBenj sexual stage (32species) predominantly from Monoverticillata andBiverticillata-Symmetrica sections (TABLE II) Only eightspecies (eg Talaromyces funiculosus P spinulosum Pthomii Cladosporium cladosporioides C herbarum Pseudo-gymnoascus pannorum Beauveria bassiana Tolypocladiuminflatum) were obtained from all peatlands and labeledtypical species for the investigated peatlands (TABLE II)The similarity of the fungal communities among thedifferent peatlands ranged from 020 (Ershovskoeand Kislosladkoe) to 032 (Verkhnee and Krugloe)(FIG 4)

Because the fungal communities of the peat andsediments of each of the four peatlands differed sub-stantially peat and sediments had to be analyzed

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 237

FIG 2 Pictures and schemes of the investigated peatlands A Verchnee Peatland B Krugloe Peatland C ErshovskoePeatland D Kislosladkoe Peatland

238 MYCOLOGIA

independently An average specific abundance of thegenus Penicillium was 295 in peat and 115 in sedi-ments Common species in peat were Talaromyces funi-culosus Penicillium spinulosum P glabrum P thomiiCladosporium bruhnei C cladosporioides C herbarumBeauveria bassiana Oidiodendron griseum Tolypocladiuminflatum and Trichoderma harzianum We found 31 spe-cies that have not been observed before in Sphagnumpeat (TABLE II) (Thormann and Rice 2007) In the bot-tom sediments sterile mycelia Tolypocladium inflatumTrichoderma hamatum T polysporum Talaromyces funicu-losus Penicillium spinulosum Aureobasidium pullulansand Sistotrema brinkmannii were prevalent

In total 43 isolates of the Basidiomycota division werefound among them were species of genera PhlebiopsisJuumllich Sistotrema Fr Amylostereum Boidin Antrodia PKarst Ceriporiopsis Domański Gloeophyllum P KarstNeolentinus Redhead amp Ginns Phellinus Queacutel Pholiota(Fr) P Kumm Piptoporus P Karst Peniophora CookePolyporus P Micheli Resinicium Parmasto Stereum

Hill ex Pers Strobilurus Singer and unidentifiedBasidiomycota

The observed fungal diversity was affected by the iso-lation media (TABLE II) Many species were isolatedonly on one type of media Some versatile speciessuch as Penicillium spp Cladosporium spp Trichodermaspp and Sistotrema spp appeared on all types of media

We did not find distinct correlation between the spe-cies composition of the fungi and the depth at whichthe peat samples were taken The maximum speciesnumber of the micromycetes was isolated from theupper and the deepest peat horizons The number offungi isolated from the surface sediment was largerthan that obtained from the deep layer sediment

DISCUSSION

The composition of fungal species in the studied peat-lands is primarily associated with their origin Substan-tial parts of the coastal zone of the White Sea arerising As the result numerous bays armlets and coastalstraits separate from the sea which in turn leads to theformation of small lakes (Shaporenko et al 2005)Geological investigations and diatom analysis of thesediments indicated that all peatlands of the KindoPeninsula formerly were a part of the sea (Roma-nenko 2012) These isolated basins develop into peat-land lakes and evolve in different ways depending ondepth Those that are 5-6 m deep remain as meromic-tic lakes the shallower ones turn to fresh peatlandlakes or slack marshes (Pantulin and Krasnova 2011)

The maximum depth of the peatland lakes exploredwas 20ndash25 m (lakes Verkhnee Krugloe ErshovskoeVerkhnee) Based on this fact it can be assumed thatthese peatlands have a similar way of formation start-ing from their detachment from the sea and endingwith freshening and bogging (Olyunina 2008) The

FIG 3 Abundance () of fungal divisions in four peat-lands A Verkhnee B Krugloe C Ershovskoe D Kisloslad-koe

FIG 4 Similarity of fungal communities of the peatlands (Soslashrensen index) A Verkhnee Peatland B Krugloe PeatlandC Ershovskoe Peatland C(1) Ershovskoe Verkhnee Lake C(2) Ershovskoe Nizhnee Lake D Kislosladkoe Peatland

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 239

TABLE II The results of the molecular analysis of 152 taxa including accession numbers of DNA sequences and the closest matchfrom the GenBank database

GenBank accession No

Species ITS LSU SSU BLAST

Acremonium sp 1a JQ780657 JQ768402 Acremonium sp 499505 99 ITS FJ571421Acremonium strictum 13191337 98 LSU FJ176879

Acremonium sp 2 JX535092 JX535093 Acremonium sp 498505 99 ITS FJ571421Sarocladium ochraceum 800813 98 LSU HQ232070Acremonium strictum 12721299 98 LSU FJ176879

Acremonium sp 2 JX507654 JX507655 Acremonium sp 498505 99 ITS FJ571421Sarocladium ochraceum 800813 98 LSU HQ232070Acremonium strictum 12721299 98 LSU FJ176879

Acremonium sp 3 JX535076 JX535077 Acremonium potronii 443443 100 ITS DQ865091Emericellopsis maritima 13181321 99 LSU FJ176861

Agaricomycetes sp JQ780614 JQ768389 Sistotrema brinkmannii 560560 100 ITS JQ912675Antrodia gossypium 10101016 99 LSU EU232298Phanerochaete lamprocystidiata 898903 99 LSU GQ470648

Alternaria sp JX507701 Alternaria tenuissima 503503 100 ITS JX406554Alternaria brassicae 503503 100 ITS JX290140Alternaria alternata 503503 100 ITS JF802121

Alternaria sp JX535139 Alternaria tenuissima 503503 100 ITS JX406554Alternaria brassicae 503503 100 ITS JX290140Alternaria alternata 503503 100 ITS JF802121

Amylostereum areolatum JX507658 Amylostereum areolatum 525525 100 ITS JX049992Amylostereum areolatum 525525 100 ITS HQ864715

Antrodia xantha JX507636 JX507637 Antrodia xantha 531531 100 ITS EU232210Antrodia xantha 20872094 99 LSU AJ583430

Antrodia sp 1 JQ780622 JQ780623 JQ780624 Antrodia serialis 446560 98 ITS AJ345010Antrodia serialis10811092 99 LSU EU232293Antrodia variiformis 16631668 99 SSU AY336783

Antrodia sp 2 JX507729 JX507730 Antrodia sinuosa 587587 100 ITS GU991578Antrodia xantha 20152114 95 LSU AJ583430

Antrodiella romellii JQ780621 JQ768396 Antrodiella romellii 587587 100 ITS AF126902Antrodiella romellii 879879 100 LSU JN710520

Ascomycota sp 1 JX535148 JX535149 Helotiales sp 457464 98 ITS FN548161Articulospora tetracladia 19572051 95 LSU EU998928

Ascomycota sp 2 JX535116 Ascomycete sp 432450 96 ITS AY805600Ascomycota sp 3 JX507652 JX507653 Ascomycota sp 488510 96 ITS JN120374

Setomelanomma holmii 700701 99 LSU GQ387633Ascomycota sp 4 JX507689 Articulospora atra 459479 96 ITS FJ000402Ascomycota sp 5 JX507709 Hirsutella sp 489493 99 ITS EF029185

Ascomycete sp 448450 99 ITS AM084797Ascomycota sp 6 JX507650 JX507651 Lecythophora mutabilis 505505 100 ITS HQ637304

Hyalodendriella betulae 757779 97 LSU EU040232Basidiomycota sp 1 JQ780626 JQ780627 JQ780628 Basidiomycota sp 490492 99 ITS GU062230

Leptosporomyces galzinii 683692 99 LSU EU118642Athelia sp 9941005 99 SSU GU187619

Basidiomycota sp 2 JX507638 JX507639 Basidiomycota sp 642642 100 ITS FR682225Antrodia xantha 19682096 94 LSU AJ583430

240 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Basidiomycota sp 3 JX507646 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874

Basidiomycota sp 4 JX507631 JX507632 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874Multiclavula mucida 19832059 96 LSU EU909345

Botryotinia sp JX535121 Botryotinia fuckeliana 474474 100 ITS KC172064Botrytis elliptica 474474 100 ITS AY684918Botrytis sp 474474 100 ITS FR822791

Cadophora fastigiata JX535145 Cadophora fastigiata 521521 100 ITS JN689948Cadophora fastigiata 521521 100 ITS GU212371

Cadophora luteo-olivacea JX535088 Cadophora luteo-olivacea 563564 99 ITS JQ796751Cadophora luteo-olivacea 563564 99 ITS FJ486274

Cadophora luteo-olivacea JX535123 Cadophora luteo-olivacea 565565 100 ITS GU212374Cadophora luteo-olivacea 565565 100 ITS GU128589

Cadophora luteo-olivacea JX535125 Cadophora luteo-olivacea 563564 99 ITS AB725391Cadophora luteo-olivacea 563564 99 ITS GU212374

Cadophora luteo-olivacea JX535132 Cadophora luteo-olivacea 560560 100 ITS GU212374Cadophora luteo-olivacea JX535171 Cadophora luteo-olivacea 567568 99 ITS GU212374Cadophora luteo-olivacea JX535179 Cadophora luteo-olivacea 581581 100 ITS FJ430742Cadophora sp JX507647 Cadophora sp 555564 98 ITS JN859254Ceriporiopsissubvermispora

JX507705 JX507706 Ceriopsiopsis subvermispora 580580 100 ITS HQ659228

Ceriporiopsis subvermispora 840842 99 LSU FJ496707Cladosporiumcladosporioides

JX535079 Cladosporium cladosporioides 483483 100 ITS JQ768327

Cladosporiumcladosporioides

JX535084 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporiumcladosporioides

JX535135 Cladosporium cladosporioides 491491 100 ITS JQ768327

Cladosporiumcladosporioides

JX535166 Cladosporium cladosporioides 480480 100 ITS JQ768327

Cladosporiumcladosporioides

JX535173 Cladosporium cladosporioides 491491 100 ITS HQ380766

Cladosporiumcladosporioides

JQ780660 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporium herbarum JX535143 Cladosporium herbarum 494494 100 ITS AF455517Cladosporium herbarum JX535172 Cladosporium herbarum (Davidiella tassiana)

408408 100 ITSKC292373

Cladosporium langeronii JQ780666 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium langeronii JQ780667 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium sp 1 JQ780649 Cladosporium langeronii 501502 99 ITS DQ780380

Cladosporium cladosporioides 486490 99 ITS JN986780Cladosporium sp 2 JQ780629 Cladosporium cladosporioides 487488 99 ITS JN986780

Cladosporium sp 490491 99 ITS GU395509Cladosporium sp 3 JX535124 Cladosporium langeronii 463467 99 ITS JQ780667

Cladosporium cladosporioides 463467 99 ITS AF455525Clavulinaceae sp JX507640 JX507641 Clavulinaceae sp 608609 99 ITS FJ475570

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 241

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Clavulina sp 792829 96 LSU AY745694Clavulinaceae sp JX507727 JX507728 Clavulinaceae sp 610611 99 ITS FJ475570

Clavulina sp 812850 96 LSU AY745694Conichaeta sp JX507629 JX507630 Coniochaeta sp 489489 100 ITS HM595513

Coniochaeta sp 509509 100 LSU HM595603Crocicreas sp JQ780618 JQ768393 Crocicreas sp 477478 99 ITS FJ005100

Cyathicula microspora 13231339 99 LSU EU940088Crocicreas sp JX507682 Crocicreas sp 440442 99 ITS FJ005098

Crocicreas sp 438442 99 ITS FJ005099Dothideales sp JX535090 JX535091 Dothideales sp 510511 99 ITS HM240804

Dothideomycetes sp 503513 98 ITS GQ153228Dothideomycetes sp 763774 99 LSU GU323957Dothidea insculpta 764808 95 LSU NG027643

Dothideomycetes sp 1 JX535078 Paraconiothyrium sp 497515 97 ITS HM999948Paraphaeosphaeria sp 496515 96 ITS KC208020

Dothideomycetes sp 1 JX507635 Paraconiothyrium sp 494512 96 ITS HM999948Paraphaeosphaeria sp 493512 96 ITS KC208020

Dothideomycetes sp 2 JX535162 Mycosphaerella fragariae 472476 99 ITS GU214691Ramularia grevilleana 469475 99 ITS GU939181

Fungus sp JX507690 Hongkongmyces pedis 252285 88 ITS JQ435790Gloeophyllum sepiarium JX507712 JX507713 Gloeophyllum sepiarium 569570 99 ITS JQ358803

Gloeophyllum sepiarium 821821 100 LSU JN649344Gnomoniaceae sp JX507716 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Gnomoniaceae sp JX507717 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Helotiales sp 1 JQ780635 Lachnum sp 416435 97 ITS FJ378861Helotiales sp 2 JQ780665 Gremmeniella sp 450453 99 ITS FR715997

Helotiales sp 421423 99 ITS AY354243Helotiales sp 3 JQ780658 JQ780659 Godronia sp 439453 98 ITS EF672237

Godronia urceulos13201321 99 LSU EU754163Helotiales sp 4 JX535181 Varicosporium elodeae 489492 99 ITS GQ152148Helotiales sp 5 JX535100 JX535101 Helotiales sp 480490 98 ITS JN655578

Mollisia cinerea 801811 99 LSU DQ470942Helotiales sp 6 JX535046 JX535047 Hyaloscyphaceae sp 479488 98 ITS GU393951

Hyalodendriella betulae 727746 97 LSU EU040232Helotiales sp 7 JX535102 JX535103 Catenulifera brevicollaris 479507 94 ITS GU727561

Catenulifera brachyconia 784800 98 LSU GU727559Helotiales sp 8 JX507674 JX507675 Hymenoscyphus sp 472487 97 ITS GU479911

Hyaloscypha fuckelii 766780 98 LSU EU940154Helotiales sp 8 JX507670 JX507671 Hymenoscyphus sp 471486 97 ITS GU479911

Hyaloscypha fuckelii 806820 98 LSU EU940154Helotiales sp 9 JX507660 JX507661 Meliniomyces bicolor 480480 100 ITS HQ157926

Hyaloscypha hepaticola 829838 99 LSU EU940118Helotiales sp 9 JX507662 JX507663 Meliniomyces sp 500503 99 ITS JQ711936

Hyaloscypha hepaticola 830839 99 LSU EU940118

242 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Helotiales sp 10 JX507720 JX507721 Helotiales sp 488542 90 ITS FJ378857Neobulgaria sp 484542 89 ITS HQ211726Neobulgaria pura 752788 95 LSU DQ257365

Helotiales sp 11 JX507672 JX507673 Helotiales sp 492497 99 ITS JX852365Catenulifera brachyconia 766782 98 LSU GU727559

Helotiales sp 12 JX507664 JX507665 Acephala sp 478483 99 ITS JN655564Mollisia sp 771797 97 LSU EU107273

Helotiales sp 12 JX507666 JX507667 Acephala sp 479484 99 ITS JN655564Mollisia sp 737781 94 LSU EU107273

Helotiales sp 13 JX507676 JX507677 Cudoniella acicularis 435470 93 ITS DQ202512Varicosporium giganteum 737747 99 LSU GQ477344

Helotiales sp 14 JX507656 JX507657 Acephala sp 481489 98 ITS HQ889709Mollisia sp 737755 97 LSU EU107273

Helotiales sp 15 JX507693 Helotiales sp 531534 99 ITS GU934595Helotiales sp 16 JX535119 JX535120 Helotiales sp 424426 99 ITS AY354243

Godronia urceolus 831831 100 LSU EU754163Helotiales sp 17 JX507731 JX507732 Helotiales sp 491545 90 ITS FJ378857

Neobulgaria sp 487545 89 ITS HQ211726Neobulgaria pura 748783 96 LSU DQ257365

Helotiales sp 18 JX507688 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Helotiales sp 18 JX507714 JX507715 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076Neobulgaria lilacina 794821 97 LSU EU940141

Helotiales sp 19 JX507683 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Leotiomycetes sp 1 JQ780634 Leotiomycetes sp 471529 94 ITS HQ212354Leotiomycetes sp 2 JQ780630 JQ768398 Helotiaceae sp 463478 97 ITS GU997932

Helotiales sp 463478 97 ITS JN655588Hyaloscypha fuckelii 13241336 99 LSU EU940154

Leotiomycetes sp 3 JX507735 Dimorphospora sp 474479 99 ITS JX077075Ascocoryne sp 377382 100 ITS JX077076

Leotiomycetes sp 4 JX507684 JX507685 Leotiomycetes sp 521531 98 ITS HQ211767Hyaloscypha sp 810831 97 LSU EU940092

Leotiomycetes sp 5 JX507687 Dimorphospora sp 473478 99 ITS JX077075Ascocoryne sp 370377 100 ITS JX077076

Massarinaceae sp JQ780631 JQ780632 Saccharicola bicolor 491501 98 ITS AF455415Neottiosporina paspali 813822 99 LSU EU754172

Mollisia sp 1 JX507704 Mollisia minutella 488493 99 ITS FR837920Mollisia sp 2 JX507644 JX507645 Mollisia minutella 477484 99 ITS FR837920

Mollisia cinerea 732746 98 LSU DQ470942Mollisia sp 3 JX507668 JX507669 Mollisia minutella 483483 100 ITS FR837920

Mollisia cinerea 806819 98 LSU DQ470942Mortierella elongata JX535038 Mortierella elongata 468468 100 ITS KC018241Nectriaceae sp JX535175 Cylindrocarpon obtusisporum 475476 99 ITS GU726752

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 243

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

independently An average specific abundance of thegenus Penicillium was 295 in peat and 115 in sedi-ments Common species in peat were Talaromyces funi-culosus Penicillium spinulosum P glabrum P thomiiCladosporium bruhnei C cladosporioides C herbarumBeauveria bassiana Oidiodendron griseum Tolypocladiuminflatum and Trichoderma harzianum We found 31 spe-cies that have not been observed before in Sphagnumpeat (TABLE II) (Thormann and Rice 2007) In the bot-tom sediments sterile mycelia Tolypocladium inflatumTrichoderma hamatum T polysporum Talaromyces funicu-losus Penicillium spinulosum Aureobasidium pullulansand Sistotrema brinkmannii were prevalent

In total 43 isolates of the Basidiomycota division werefound among them were species of genera PhlebiopsisJuumllich Sistotrema Fr Amylostereum Boidin Antrodia PKarst Ceriporiopsis Domański Gloeophyllum P KarstNeolentinus Redhead amp Ginns Phellinus Queacutel Pholiota(Fr) P Kumm Piptoporus P Karst Peniophora CookePolyporus P Micheli Resinicium Parmasto Stereum

Hill ex Pers Strobilurus Singer and unidentifiedBasidiomycota

The observed fungal diversity was affected by the iso-lation media (TABLE II) Many species were isolatedonly on one type of media Some versatile speciessuch as Penicillium spp Cladosporium spp Trichodermaspp and Sistotrema spp appeared on all types of media

We did not find distinct correlation between the spe-cies composition of the fungi and the depth at whichthe peat samples were taken The maximum speciesnumber of the micromycetes was isolated from theupper and the deepest peat horizons The number offungi isolated from the surface sediment was largerthan that obtained from the deep layer sediment

DISCUSSION

The composition of fungal species in the studied peat-lands is primarily associated with their origin Substan-tial parts of the coastal zone of the White Sea arerising As the result numerous bays armlets and coastalstraits separate from the sea which in turn leads to theformation of small lakes (Shaporenko et al 2005)Geological investigations and diatom analysis of thesediments indicated that all peatlands of the KindoPeninsula formerly were a part of the sea (Roma-nenko 2012) These isolated basins develop into peat-land lakes and evolve in different ways depending ondepth Those that are 5-6 m deep remain as meromic-tic lakes the shallower ones turn to fresh peatlandlakes or slack marshes (Pantulin and Krasnova 2011)

The maximum depth of the peatland lakes exploredwas 20ndash25 m (lakes Verkhnee Krugloe ErshovskoeVerkhnee) Based on this fact it can be assumed thatthese peatlands have a similar way of formation start-ing from their detachment from the sea and endingwith freshening and bogging (Olyunina 2008) The

FIG 3 Abundance () of fungal divisions in four peat-lands A Verkhnee B Krugloe C Ershovskoe D Kisloslad-koe

FIG 4 Similarity of fungal communities of the peatlands (Soslashrensen index) A Verkhnee Peatland B Krugloe PeatlandC Ershovskoe Peatland C(1) Ershovskoe Verkhnee Lake C(2) Ershovskoe Nizhnee Lake D Kislosladkoe Peatland

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 239

TABLE II The results of the molecular analysis of 152 taxa including accession numbers of DNA sequences and the closest matchfrom the GenBank database

GenBank accession No

Species ITS LSU SSU BLAST

Acremonium sp 1a JQ780657 JQ768402 Acremonium sp 499505 99 ITS FJ571421Acremonium strictum 13191337 98 LSU FJ176879

Acremonium sp 2 JX535092 JX535093 Acremonium sp 498505 99 ITS FJ571421Sarocladium ochraceum 800813 98 LSU HQ232070Acremonium strictum 12721299 98 LSU FJ176879

Acremonium sp 2 JX507654 JX507655 Acremonium sp 498505 99 ITS FJ571421Sarocladium ochraceum 800813 98 LSU HQ232070Acremonium strictum 12721299 98 LSU FJ176879

Acremonium sp 3 JX535076 JX535077 Acremonium potronii 443443 100 ITS DQ865091Emericellopsis maritima 13181321 99 LSU FJ176861

Agaricomycetes sp JQ780614 JQ768389 Sistotrema brinkmannii 560560 100 ITS JQ912675Antrodia gossypium 10101016 99 LSU EU232298Phanerochaete lamprocystidiata 898903 99 LSU GQ470648

Alternaria sp JX507701 Alternaria tenuissima 503503 100 ITS JX406554Alternaria brassicae 503503 100 ITS JX290140Alternaria alternata 503503 100 ITS JF802121

Alternaria sp JX535139 Alternaria tenuissima 503503 100 ITS JX406554Alternaria brassicae 503503 100 ITS JX290140Alternaria alternata 503503 100 ITS JF802121

Amylostereum areolatum JX507658 Amylostereum areolatum 525525 100 ITS JX049992Amylostereum areolatum 525525 100 ITS HQ864715

Antrodia xantha JX507636 JX507637 Antrodia xantha 531531 100 ITS EU232210Antrodia xantha 20872094 99 LSU AJ583430

Antrodia sp 1 JQ780622 JQ780623 JQ780624 Antrodia serialis 446560 98 ITS AJ345010Antrodia serialis10811092 99 LSU EU232293Antrodia variiformis 16631668 99 SSU AY336783

Antrodia sp 2 JX507729 JX507730 Antrodia sinuosa 587587 100 ITS GU991578Antrodia xantha 20152114 95 LSU AJ583430

Antrodiella romellii JQ780621 JQ768396 Antrodiella romellii 587587 100 ITS AF126902Antrodiella romellii 879879 100 LSU JN710520

Ascomycota sp 1 JX535148 JX535149 Helotiales sp 457464 98 ITS FN548161Articulospora tetracladia 19572051 95 LSU EU998928

Ascomycota sp 2 JX535116 Ascomycete sp 432450 96 ITS AY805600Ascomycota sp 3 JX507652 JX507653 Ascomycota sp 488510 96 ITS JN120374

Setomelanomma holmii 700701 99 LSU GQ387633Ascomycota sp 4 JX507689 Articulospora atra 459479 96 ITS FJ000402Ascomycota sp 5 JX507709 Hirsutella sp 489493 99 ITS EF029185

Ascomycete sp 448450 99 ITS AM084797Ascomycota sp 6 JX507650 JX507651 Lecythophora mutabilis 505505 100 ITS HQ637304

Hyalodendriella betulae 757779 97 LSU EU040232Basidiomycota sp 1 JQ780626 JQ780627 JQ780628 Basidiomycota sp 490492 99 ITS GU062230

Leptosporomyces galzinii 683692 99 LSU EU118642Athelia sp 9941005 99 SSU GU187619

Basidiomycota sp 2 JX507638 JX507639 Basidiomycota sp 642642 100 ITS FR682225Antrodia xantha 19682096 94 LSU AJ583430

240 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Basidiomycota sp 3 JX507646 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874

Basidiomycota sp 4 JX507631 JX507632 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874Multiclavula mucida 19832059 96 LSU EU909345

Botryotinia sp JX535121 Botryotinia fuckeliana 474474 100 ITS KC172064Botrytis elliptica 474474 100 ITS AY684918Botrytis sp 474474 100 ITS FR822791

Cadophora fastigiata JX535145 Cadophora fastigiata 521521 100 ITS JN689948Cadophora fastigiata 521521 100 ITS GU212371

Cadophora luteo-olivacea JX535088 Cadophora luteo-olivacea 563564 99 ITS JQ796751Cadophora luteo-olivacea 563564 99 ITS FJ486274

Cadophora luteo-olivacea JX535123 Cadophora luteo-olivacea 565565 100 ITS GU212374Cadophora luteo-olivacea 565565 100 ITS GU128589

Cadophora luteo-olivacea JX535125 Cadophora luteo-olivacea 563564 99 ITS AB725391Cadophora luteo-olivacea 563564 99 ITS GU212374

Cadophora luteo-olivacea JX535132 Cadophora luteo-olivacea 560560 100 ITS GU212374Cadophora luteo-olivacea JX535171 Cadophora luteo-olivacea 567568 99 ITS GU212374Cadophora luteo-olivacea JX535179 Cadophora luteo-olivacea 581581 100 ITS FJ430742Cadophora sp JX507647 Cadophora sp 555564 98 ITS JN859254Ceriporiopsissubvermispora

JX507705 JX507706 Ceriopsiopsis subvermispora 580580 100 ITS HQ659228

Ceriporiopsis subvermispora 840842 99 LSU FJ496707Cladosporiumcladosporioides

JX535079 Cladosporium cladosporioides 483483 100 ITS JQ768327

Cladosporiumcladosporioides

JX535084 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporiumcladosporioides

JX535135 Cladosporium cladosporioides 491491 100 ITS JQ768327

Cladosporiumcladosporioides

JX535166 Cladosporium cladosporioides 480480 100 ITS JQ768327

Cladosporiumcladosporioides

JX535173 Cladosporium cladosporioides 491491 100 ITS HQ380766

Cladosporiumcladosporioides

JQ780660 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporium herbarum JX535143 Cladosporium herbarum 494494 100 ITS AF455517Cladosporium herbarum JX535172 Cladosporium herbarum (Davidiella tassiana)

408408 100 ITSKC292373

Cladosporium langeronii JQ780666 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium langeronii JQ780667 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium sp 1 JQ780649 Cladosporium langeronii 501502 99 ITS DQ780380

Cladosporium cladosporioides 486490 99 ITS JN986780Cladosporium sp 2 JQ780629 Cladosporium cladosporioides 487488 99 ITS JN986780

Cladosporium sp 490491 99 ITS GU395509Cladosporium sp 3 JX535124 Cladosporium langeronii 463467 99 ITS JQ780667

Cladosporium cladosporioides 463467 99 ITS AF455525Clavulinaceae sp JX507640 JX507641 Clavulinaceae sp 608609 99 ITS FJ475570

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 241

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Clavulina sp 792829 96 LSU AY745694Clavulinaceae sp JX507727 JX507728 Clavulinaceae sp 610611 99 ITS FJ475570

Clavulina sp 812850 96 LSU AY745694Conichaeta sp JX507629 JX507630 Coniochaeta sp 489489 100 ITS HM595513

Coniochaeta sp 509509 100 LSU HM595603Crocicreas sp JQ780618 JQ768393 Crocicreas sp 477478 99 ITS FJ005100

Cyathicula microspora 13231339 99 LSU EU940088Crocicreas sp JX507682 Crocicreas sp 440442 99 ITS FJ005098

Crocicreas sp 438442 99 ITS FJ005099Dothideales sp JX535090 JX535091 Dothideales sp 510511 99 ITS HM240804

Dothideomycetes sp 503513 98 ITS GQ153228Dothideomycetes sp 763774 99 LSU GU323957Dothidea insculpta 764808 95 LSU NG027643

Dothideomycetes sp 1 JX535078 Paraconiothyrium sp 497515 97 ITS HM999948Paraphaeosphaeria sp 496515 96 ITS KC208020

Dothideomycetes sp 1 JX507635 Paraconiothyrium sp 494512 96 ITS HM999948Paraphaeosphaeria sp 493512 96 ITS KC208020

Dothideomycetes sp 2 JX535162 Mycosphaerella fragariae 472476 99 ITS GU214691Ramularia grevilleana 469475 99 ITS GU939181

Fungus sp JX507690 Hongkongmyces pedis 252285 88 ITS JQ435790Gloeophyllum sepiarium JX507712 JX507713 Gloeophyllum sepiarium 569570 99 ITS JQ358803

Gloeophyllum sepiarium 821821 100 LSU JN649344Gnomoniaceae sp JX507716 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Gnomoniaceae sp JX507717 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Helotiales sp 1 JQ780635 Lachnum sp 416435 97 ITS FJ378861Helotiales sp 2 JQ780665 Gremmeniella sp 450453 99 ITS FR715997

Helotiales sp 421423 99 ITS AY354243Helotiales sp 3 JQ780658 JQ780659 Godronia sp 439453 98 ITS EF672237

Godronia urceulos13201321 99 LSU EU754163Helotiales sp 4 JX535181 Varicosporium elodeae 489492 99 ITS GQ152148Helotiales sp 5 JX535100 JX535101 Helotiales sp 480490 98 ITS JN655578

Mollisia cinerea 801811 99 LSU DQ470942Helotiales sp 6 JX535046 JX535047 Hyaloscyphaceae sp 479488 98 ITS GU393951

Hyalodendriella betulae 727746 97 LSU EU040232Helotiales sp 7 JX535102 JX535103 Catenulifera brevicollaris 479507 94 ITS GU727561

Catenulifera brachyconia 784800 98 LSU GU727559Helotiales sp 8 JX507674 JX507675 Hymenoscyphus sp 472487 97 ITS GU479911

Hyaloscypha fuckelii 766780 98 LSU EU940154Helotiales sp 8 JX507670 JX507671 Hymenoscyphus sp 471486 97 ITS GU479911

Hyaloscypha fuckelii 806820 98 LSU EU940154Helotiales sp 9 JX507660 JX507661 Meliniomyces bicolor 480480 100 ITS HQ157926

Hyaloscypha hepaticola 829838 99 LSU EU940118Helotiales sp 9 JX507662 JX507663 Meliniomyces sp 500503 99 ITS JQ711936

Hyaloscypha hepaticola 830839 99 LSU EU940118

242 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Helotiales sp 10 JX507720 JX507721 Helotiales sp 488542 90 ITS FJ378857Neobulgaria sp 484542 89 ITS HQ211726Neobulgaria pura 752788 95 LSU DQ257365

Helotiales sp 11 JX507672 JX507673 Helotiales sp 492497 99 ITS JX852365Catenulifera brachyconia 766782 98 LSU GU727559

Helotiales sp 12 JX507664 JX507665 Acephala sp 478483 99 ITS JN655564Mollisia sp 771797 97 LSU EU107273

Helotiales sp 12 JX507666 JX507667 Acephala sp 479484 99 ITS JN655564Mollisia sp 737781 94 LSU EU107273

Helotiales sp 13 JX507676 JX507677 Cudoniella acicularis 435470 93 ITS DQ202512Varicosporium giganteum 737747 99 LSU GQ477344

Helotiales sp 14 JX507656 JX507657 Acephala sp 481489 98 ITS HQ889709Mollisia sp 737755 97 LSU EU107273

Helotiales sp 15 JX507693 Helotiales sp 531534 99 ITS GU934595Helotiales sp 16 JX535119 JX535120 Helotiales sp 424426 99 ITS AY354243

Godronia urceolus 831831 100 LSU EU754163Helotiales sp 17 JX507731 JX507732 Helotiales sp 491545 90 ITS FJ378857

Neobulgaria sp 487545 89 ITS HQ211726Neobulgaria pura 748783 96 LSU DQ257365

Helotiales sp 18 JX507688 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Helotiales sp 18 JX507714 JX507715 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076Neobulgaria lilacina 794821 97 LSU EU940141

Helotiales sp 19 JX507683 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Leotiomycetes sp 1 JQ780634 Leotiomycetes sp 471529 94 ITS HQ212354Leotiomycetes sp 2 JQ780630 JQ768398 Helotiaceae sp 463478 97 ITS GU997932

Helotiales sp 463478 97 ITS JN655588Hyaloscypha fuckelii 13241336 99 LSU EU940154

Leotiomycetes sp 3 JX507735 Dimorphospora sp 474479 99 ITS JX077075Ascocoryne sp 377382 100 ITS JX077076

Leotiomycetes sp 4 JX507684 JX507685 Leotiomycetes sp 521531 98 ITS HQ211767Hyaloscypha sp 810831 97 LSU EU940092

Leotiomycetes sp 5 JX507687 Dimorphospora sp 473478 99 ITS JX077075Ascocoryne sp 370377 100 ITS JX077076

Massarinaceae sp JQ780631 JQ780632 Saccharicola bicolor 491501 98 ITS AF455415Neottiosporina paspali 813822 99 LSU EU754172

Mollisia sp 1 JX507704 Mollisia minutella 488493 99 ITS FR837920Mollisia sp 2 JX507644 JX507645 Mollisia minutella 477484 99 ITS FR837920

Mollisia cinerea 732746 98 LSU DQ470942Mollisia sp 3 JX507668 JX507669 Mollisia minutella 483483 100 ITS FR837920

Mollisia cinerea 806819 98 LSU DQ470942Mortierella elongata JX535038 Mortierella elongata 468468 100 ITS KC018241Nectriaceae sp JX535175 Cylindrocarpon obtusisporum 475476 99 ITS GU726752

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 243

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE II The results of the molecular analysis of 152 taxa including accession numbers of DNA sequences and the closest matchfrom the GenBank database

GenBank accession No

Species ITS LSU SSU BLAST

Acremonium sp 1a JQ780657 JQ768402 Acremonium sp 499505 99 ITS FJ571421Acremonium strictum 13191337 98 LSU FJ176879

Acremonium sp 2 JX535092 JX535093 Acremonium sp 498505 99 ITS FJ571421Sarocladium ochraceum 800813 98 LSU HQ232070Acremonium strictum 12721299 98 LSU FJ176879

Acremonium sp 2 JX507654 JX507655 Acremonium sp 498505 99 ITS FJ571421Sarocladium ochraceum 800813 98 LSU HQ232070Acremonium strictum 12721299 98 LSU FJ176879

Acremonium sp 3 JX535076 JX535077 Acremonium potronii 443443 100 ITS DQ865091Emericellopsis maritima 13181321 99 LSU FJ176861

Agaricomycetes sp JQ780614 JQ768389 Sistotrema brinkmannii 560560 100 ITS JQ912675Antrodia gossypium 10101016 99 LSU EU232298Phanerochaete lamprocystidiata 898903 99 LSU GQ470648

Alternaria sp JX507701 Alternaria tenuissima 503503 100 ITS JX406554Alternaria brassicae 503503 100 ITS JX290140Alternaria alternata 503503 100 ITS JF802121

Alternaria sp JX535139 Alternaria tenuissima 503503 100 ITS JX406554Alternaria brassicae 503503 100 ITS JX290140Alternaria alternata 503503 100 ITS JF802121

Amylostereum areolatum JX507658 Amylostereum areolatum 525525 100 ITS JX049992Amylostereum areolatum 525525 100 ITS HQ864715

Antrodia xantha JX507636 JX507637 Antrodia xantha 531531 100 ITS EU232210Antrodia xantha 20872094 99 LSU AJ583430

Antrodia sp 1 JQ780622 JQ780623 JQ780624 Antrodia serialis 446560 98 ITS AJ345010Antrodia serialis10811092 99 LSU EU232293Antrodia variiformis 16631668 99 SSU AY336783

Antrodia sp 2 JX507729 JX507730 Antrodia sinuosa 587587 100 ITS GU991578Antrodia xantha 20152114 95 LSU AJ583430

Antrodiella romellii JQ780621 JQ768396 Antrodiella romellii 587587 100 ITS AF126902Antrodiella romellii 879879 100 LSU JN710520

Ascomycota sp 1 JX535148 JX535149 Helotiales sp 457464 98 ITS FN548161Articulospora tetracladia 19572051 95 LSU EU998928

Ascomycota sp 2 JX535116 Ascomycete sp 432450 96 ITS AY805600Ascomycota sp 3 JX507652 JX507653 Ascomycota sp 488510 96 ITS JN120374

Setomelanomma holmii 700701 99 LSU GQ387633Ascomycota sp 4 JX507689 Articulospora atra 459479 96 ITS FJ000402Ascomycota sp 5 JX507709 Hirsutella sp 489493 99 ITS EF029185

Ascomycete sp 448450 99 ITS AM084797Ascomycota sp 6 JX507650 JX507651 Lecythophora mutabilis 505505 100 ITS HQ637304

Hyalodendriella betulae 757779 97 LSU EU040232Basidiomycota sp 1 JQ780626 JQ780627 JQ780628 Basidiomycota sp 490492 99 ITS GU062230

Leptosporomyces galzinii 683692 99 LSU EU118642Athelia sp 9941005 99 SSU GU187619

Basidiomycota sp 2 JX507638 JX507639 Basidiomycota sp 642642 100 ITS FR682225Antrodia xantha 19682096 94 LSU AJ583430

240 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Basidiomycota sp 3 JX507646 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874

Basidiomycota sp 4 JX507631 JX507632 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874Multiclavula mucida 19832059 96 LSU EU909345

Botryotinia sp JX535121 Botryotinia fuckeliana 474474 100 ITS KC172064Botrytis elliptica 474474 100 ITS AY684918Botrytis sp 474474 100 ITS FR822791

Cadophora fastigiata JX535145 Cadophora fastigiata 521521 100 ITS JN689948Cadophora fastigiata 521521 100 ITS GU212371

Cadophora luteo-olivacea JX535088 Cadophora luteo-olivacea 563564 99 ITS JQ796751Cadophora luteo-olivacea 563564 99 ITS FJ486274

Cadophora luteo-olivacea JX535123 Cadophora luteo-olivacea 565565 100 ITS GU212374Cadophora luteo-olivacea 565565 100 ITS GU128589

Cadophora luteo-olivacea JX535125 Cadophora luteo-olivacea 563564 99 ITS AB725391Cadophora luteo-olivacea 563564 99 ITS GU212374

Cadophora luteo-olivacea JX535132 Cadophora luteo-olivacea 560560 100 ITS GU212374Cadophora luteo-olivacea JX535171 Cadophora luteo-olivacea 567568 99 ITS GU212374Cadophora luteo-olivacea JX535179 Cadophora luteo-olivacea 581581 100 ITS FJ430742Cadophora sp JX507647 Cadophora sp 555564 98 ITS JN859254Ceriporiopsissubvermispora

JX507705 JX507706 Ceriopsiopsis subvermispora 580580 100 ITS HQ659228

Ceriporiopsis subvermispora 840842 99 LSU FJ496707Cladosporiumcladosporioides

JX535079 Cladosporium cladosporioides 483483 100 ITS JQ768327

Cladosporiumcladosporioides

JX535084 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporiumcladosporioides

JX535135 Cladosporium cladosporioides 491491 100 ITS JQ768327

Cladosporiumcladosporioides

JX535166 Cladosporium cladosporioides 480480 100 ITS JQ768327

Cladosporiumcladosporioides

JX535173 Cladosporium cladosporioides 491491 100 ITS HQ380766

Cladosporiumcladosporioides

JQ780660 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporium herbarum JX535143 Cladosporium herbarum 494494 100 ITS AF455517Cladosporium herbarum JX535172 Cladosporium herbarum (Davidiella tassiana)

408408 100 ITSKC292373

Cladosporium langeronii JQ780666 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium langeronii JQ780667 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium sp 1 JQ780649 Cladosporium langeronii 501502 99 ITS DQ780380

Cladosporium cladosporioides 486490 99 ITS JN986780Cladosporium sp 2 JQ780629 Cladosporium cladosporioides 487488 99 ITS JN986780

Cladosporium sp 490491 99 ITS GU395509Cladosporium sp 3 JX535124 Cladosporium langeronii 463467 99 ITS JQ780667

Cladosporium cladosporioides 463467 99 ITS AF455525Clavulinaceae sp JX507640 JX507641 Clavulinaceae sp 608609 99 ITS FJ475570

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 241

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Clavulina sp 792829 96 LSU AY745694Clavulinaceae sp JX507727 JX507728 Clavulinaceae sp 610611 99 ITS FJ475570

Clavulina sp 812850 96 LSU AY745694Conichaeta sp JX507629 JX507630 Coniochaeta sp 489489 100 ITS HM595513

Coniochaeta sp 509509 100 LSU HM595603Crocicreas sp JQ780618 JQ768393 Crocicreas sp 477478 99 ITS FJ005100

Cyathicula microspora 13231339 99 LSU EU940088Crocicreas sp JX507682 Crocicreas sp 440442 99 ITS FJ005098

Crocicreas sp 438442 99 ITS FJ005099Dothideales sp JX535090 JX535091 Dothideales sp 510511 99 ITS HM240804

Dothideomycetes sp 503513 98 ITS GQ153228Dothideomycetes sp 763774 99 LSU GU323957Dothidea insculpta 764808 95 LSU NG027643

Dothideomycetes sp 1 JX535078 Paraconiothyrium sp 497515 97 ITS HM999948Paraphaeosphaeria sp 496515 96 ITS KC208020

Dothideomycetes sp 1 JX507635 Paraconiothyrium sp 494512 96 ITS HM999948Paraphaeosphaeria sp 493512 96 ITS KC208020

Dothideomycetes sp 2 JX535162 Mycosphaerella fragariae 472476 99 ITS GU214691Ramularia grevilleana 469475 99 ITS GU939181

Fungus sp JX507690 Hongkongmyces pedis 252285 88 ITS JQ435790Gloeophyllum sepiarium JX507712 JX507713 Gloeophyllum sepiarium 569570 99 ITS JQ358803

Gloeophyllum sepiarium 821821 100 LSU JN649344Gnomoniaceae sp JX507716 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Gnomoniaceae sp JX507717 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Helotiales sp 1 JQ780635 Lachnum sp 416435 97 ITS FJ378861Helotiales sp 2 JQ780665 Gremmeniella sp 450453 99 ITS FR715997

Helotiales sp 421423 99 ITS AY354243Helotiales sp 3 JQ780658 JQ780659 Godronia sp 439453 98 ITS EF672237

Godronia urceulos13201321 99 LSU EU754163Helotiales sp 4 JX535181 Varicosporium elodeae 489492 99 ITS GQ152148Helotiales sp 5 JX535100 JX535101 Helotiales sp 480490 98 ITS JN655578

Mollisia cinerea 801811 99 LSU DQ470942Helotiales sp 6 JX535046 JX535047 Hyaloscyphaceae sp 479488 98 ITS GU393951

Hyalodendriella betulae 727746 97 LSU EU040232Helotiales sp 7 JX535102 JX535103 Catenulifera brevicollaris 479507 94 ITS GU727561

Catenulifera brachyconia 784800 98 LSU GU727559Helotiales sp 8 JX507674 JX507675 Hymenoscyphus sp 472487 97 ITS GU479911

Hyaloscypha fuckelii 766780 98 LSU EU940154Helotiales sp 8 JX507670 JX507671 Hymenoscyphus sp 471486 97 ITS GU479911

Hyaloscypha fuckelii 806820 98 LSU EU940154Helotiales sp 9 JX507660 JX507661 Meliniomyces bicolor 480480 100 ITS HQ157926

Hyaloscypha hepaticola 829838 99 LSU EU940118Helotiales sp 9 JX507662 JX507663 Meliniomyces sp 500503 99 ITS JQ711936

Hyaloscypha hepaticola 830839 99 LSU EU940118

242 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Helotiales sp 10 JX507720 JX507721 Helotiales sp 488542 90 ITS FJ378857Neobulgaria sp 484542 89 ITS HQ211726Neobulgaria pura 752788 95 LSU DQ257365

Helotiales sp 11 JX507672 JX507673 Helotiales sp 492497 99 ITS JX852365Catenulifera brachyconia 766782 98 LSU GU727559

Helotiales sp 12 JX507664 JX507665 Acephala sp 478483 99 ITS JN655564Mollisia sp 771797 97 LSU EU107273

Helotiales sp 12 JX507666 JX507667 Acephala sp 479484 99 ITS JN655564Mollisia sp 737781 94 LSU EU107273

Helotiales sp 13 JX507676 JX507677 Cudoniella acicularis 435470 93 ITS DQ202512Varicosporium giganteum 737747 99 LSU GQ477344

Helotiales sp 14 JX507656 JX507657 Acephala sp 481489 98 ITS HQ889709Mollisia sp 737755 97 LSU EU107273

Helotiales sp 15 JX507693 Helotiales sp 531534 99 ITS GU934595Helotiales sp 16 JX535119 JX535120 Helotiales sp 424426 99 ITS AY354243

Godronia urceolus 831831 100 LSU EU754163Helotiales sp 17 JX507731 JX507732 Helotiales sp 491545 90 ITS FJ378857

Neobulgaria sp 487545 89 ITS HQ211726Neobulgaria pura 748783 96 LSU DQ257365

Helotiales sp 18 JX507688 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Helotiales sp 18 JX507714 JX507715 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076Neobulgaria lilacina 794821 97 LSU EU940141

Helotiales sp 19 JX507683 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Leotiomycetes sp 1 JQ780634 Leotiomycetes sp 471529 94 ITS HQ212354Leotiomycetes sp 2 JQ780630 JQ768398 Helotiaceae sp 463478 97 ITS GU997932

Helotiales sp 463478 97 ITS JN655588Hyaloscypha fuckelii 13241336 99 LSU EU940154

Leotiomycetes sp 3 JX507735 Dimorphospora sp 474479 99 ITS JX077075Ascocoryne sp 377382 100 ITS JX077076

Leotiomycetes sp 4 JX507684 JX507685 Leotiomycetes sp 521531 98 ITS HQ211767Hyaloscypha sp 810831 97 LSU EU940092

Leotiomycetes sp 5 JX507687 Dimorphospora sp 473478 99 ITS JX077075Ascocoryne sp 370377 100 ITS JX077076

Massarinaceae sp JQ780631 JQ780632 Saccharicola bicolor 491501 98 ITS AF455415Neottiosporina paspali 813822 99 LSU EU754172

Mollisia sp 1 JX507704 Mollisia minutella 488493 99 ITS FR837920Mollisia sp 2 JX507644 JX507645 Mollisia minutella 477484 99 ITS FR837920

Mollisia cinerea 732746 98 LSU DQ470942Mollisia sp 3 JX507668 JX507669 Mollisia minutella 483483 100 ITS FR837920

Mollisia cinerea 806819 98 LSU DQ470942Mortierella elongata JX535038 Mortierella elongata 468468 100 ITS KC018241Nectriaceae sp JX535175 Cylindrocarpon obtusisporum 475476 99 ITS GU726752

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 243

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Basidiomycota sp 3 JX507646 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874

Basidiomycota sp 4 JX507631 JX507632 Armillaria novae-zelandiae 536592 91 ITS AF394919Coprinus sp 526590 89 ITS AY254874Multiclavula mucida 19832059 96 LSU EU909345

Botryotinia sp JX535121 Botryotinia fuckeliana 474474 100 ITS KC172064Botrytis elliptica 474474 100 ITS AY684918Botrytis sp 474474 100 ITS FR822791

Cadophora fastigiata JX535145 Cadophora fastigiata 521521 100 ITS JN689948Cadophora fastigiata 521521 100 ITS GU212371

Cadophora luteo-olivacea JX535088 Cadophora luteo-olivacea 563564 99 ITS JQ796751Cadophora luteo-olivacea 563564 99 ITS FJ486274

Cadophora luteo-olivacea JX535123 Cadophora luteo-olivacea 565565 100 ITS GU212374Cadophora luteo-olivacea 565565 100 ITS GU128589

Cadophora luteo-olivacea JX535125 Cadophora luteo-olivacea 563564 99 ITS AB725391Cadophora luteo-olivacea 563564 99 ITS GU212374

Cadophora luteo-olivacea JX535132 Cadophora luteo-olivacea 560560 100 ITS GU212374Cadophora luteo-olivacea JX535171 Cadophora luteo-olivacea 567568 99 ITS GU212374Cadophora luteo-olivacea JX535179 Cadophora luteo-olivacea 581581 100 ITS FJ430742Cadophora sp JX507647 Cadophora sp 555564 98 ITS JN859254Ceriporiopsissubvermispora

JX507705 JX507706 Ceriopsiopsis subvermispora 580580 100 ITS HQ659228

Ceriporiopsis subvermispora 840842 99 LSU FJ496707Cladosporiumcladosporioides

JX535079 Cladosporium cladosporioides 483483 100 ITS JQ768327

Cladosporiumcladosporioides

JX535084 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporiumcladosporioides

JX535135 Cladosporium cladosporioides 491491 100 ITS JQ768327

Cladosporiumcladosporioides

JX535166 Cladosporium cladosporioides 480480 100 ITS JQ768327

Cladosporiumcladosporioides

JX535173 Cladosporium cladosporioides 491491 100 ITS HQ380766

Cladosporiumcladosporioides

JQ780660 Cladosporium cladosporioides 481481 100 ITS JQ768327

Cladosporium herbarum JX535143 Cladosporium herbarum 494494 100 ITS AF455517Cladosporium herbarum JX535172 Cladosporium herbarum (Davidiella tassiana)

408408 100 ITSKC292373

Cladosporium langeronii JQ780666 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium langeronii JQ780667 Cladosporium langeronii 490490 100 ITS DQ780380Cladosporium sp 1 JQ780649 Cladosporium langeronii 501502 99 ITS DQ780380

Cladosporium cladosporioides 486490 99 ITS JN986780Cladosporium sp 2 JQ780629 Cladosporium cladosporioides 487488 99 ITS JN986780

Cladosporium sp 490491 99 ITS GU395509Cladosporium sp 3 JX535124 Cladosporium langeronii 463467 99 ITS JQ780667

Cladosporium cladosporioides 463467 99 ITS AF455525Clavulinaceae sp JX507640 JX507641 Clavulinaceae sp 608609 99 ITS FJ475570

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 241

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Clavulina sp 792829 96 LSU AY745694Clavulinaceae sp JX507727 JX507728 Clavulinaceae sp 610611 99 ITS FJ475570

Clavulina sp 812850 96 LSU AY745694Conichaeta sp JX507629 JX507630 Coniochaeta sp 489489 100 ITS HM595513

Coniochaeta sp 509509 100 LSU HM595603Crocicreas sp JQ780618 JQ768393 Crocicreas sp 477478 99 ITS FJ005100

Cyathicula microspora 13231339 99 LSU EU940088Crocicreas sp JX507682 Crocicreas sp 440442 99 ITS FJ005098

Crocicreas sp 438442 99 ITS FJ005099Dothideales sp JX535090 JX535091 Dothideales sp 510511 99 ITS HM240804

Dothideomycetes sp 503513 98 ITS GQ153228Dothideomycetes sp 763774 99 LSU GU323957Dothidea insculpta 764808 95 LSU NG027643

Dothideomycetes sp 1 JX535078 Paraconiothyrium sp 497515 97 ITS HM999948Paraphaeosphaeria sp 496515 96 ITS KC208020

Dothideomycetes sp 1 JX507635 Paraconiothyrium sp 494512 96 ITS HM999948Paraphaeosphaeria sp 493512 96 ITS KC208020

Dothideomycetes sp 2 JX535162 Mycosphaerella fragariae 472476 99 ITS GU214691Ramularia grevilleana 469475 99 ITS GU939181

Fungus sp JX507690 Hongkongmyces pedis 252285 88 ITS JQ435790Gloeophyllum sepiarium JX507712 JX507713 Gloeophyllum sepiarium 569570 99 ITS JQ358803

Gloeophyllum sepiarium 821821 100 LSU JN649344Gnomoniaceae sp JX507716 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Gnomoniaceae sp JX507717 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Helotiales sp 1 JQ780635 Lachnum sp 416435 97 ITS FJ378861Helotiales sp 2 JQ780665 Gremmeniella sp 450453 99 ITS FR715997

Helotiales sp 421423 99 ITS AY354243Helotiales sp 3 JQ780658 JQ780659 Godronia sp 439453 98 ITS EF672237

Godronia urceulos13201321 99 LSU EU754163Helotiales sp 4 JX535181 Varicosporium elodeae 489492 99 ITS GQ152148Helotiales sp 5 JX535100 JX535101 Helotiales sp 480490 98 ITS JN655578

Mollisia cinerea 801811 99 LSU DQ470942Helotiales sp 6 JX535046 JX535047 Hyaloscyphaceae sp 479488 98 ITS GU393951

Hyalodendriella betulae 727746 97 LSU EU040232Helotiales sp 7 JX535102 JX535103 Catenulifera brevicollaris 479507 94 ITS GU727561

Catenulifera brachyconia 784800 98 LSU GU727559Helotiales sp 8 JX507674 JX507675 Hymenoscyphus sp 472487 97 ITS GU479911

Hyaloscypha fuckelii 766780 98 LSU EU940154Helotiales sp 8 JX507670 JX507671 Hymenoscyphus sp 471486 97 ITS GU479911

Hyaloscypha fuckelii 806820 98 LSU EU940154Helotiales sp 9 JX507660 JX507661 Meliniomyces bicolor 480480 100 ITS HQ157926

Hyaloscypha hepaticola 829838 99 LSU EU940118Helotiales sp 9 JX507662 JX507663 Meliniomyces sp 500503 99 ITS JQ711936

Hyaloscypha hepaticola 830839 99 LSU EU940118

242 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Helotiales sp 10 JX507720 JX507721 Helotiales sp 488542 90 ITS FJ378857Neobulgaria sp 484542 89 ITS HQ211726Neobulgaria pura 752788 95 LSU DQ257365

Helotiales sp 11 JX507672 JX507673 Helotiales sp 492497 99 ITS JX852365Catenulifera brachyconia 766782 98 LSU GU727559

Helotiales sp 12 JX507664 JX507665 Acephala sp 478483 99 ITS JN655564Mollisia sp 771797 97 LSU EU107273

Helotiales sp 12 JX507666 JX507667 Acephala sp 479484 99 ITS JN655564Mollisia sp 737781 94 LSU EU107273

Helotiales sp 13 JX507676 JX507677 Cudoniella acicularis 435470 93 ITS DQ202512Varicosporium giganteum 737747 99 LSU GQ477344

Helotiales sp 14 JX507656 JX507657 Acephala sp 481489 98 ITS HQ889709Mollisia sp 737755 97 LSU EU107273

Helotiales sp 15 JX507693 Helotiales sp 531534 99 ITS GU934595Helotiales sp 16 JX535119 JX535120 Helotiales sp 424426 99 ITS AY354243

Godronia urceolus 831831 100 LSU EU754163Helotiales sp 17 JX507731 JX507732 Helotiales sp 491545 90 ITS FJ378857

Neobulgaria sp 487545 89 ITS HQ211726Neobulgaria pura 748783 96 LSU DQ257365

Helotiales sp 18 JX507688 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Helotiales sp 18 JX507714 JX507715 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076Neobulgaria lilacina 794821 97 LSU EU940141

Helotiales sp 19 JX507683 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Leotiomycetes sp 1 JQ780634 Leotiomycetes sp 471529 94 ITS HQ212354Leotiomycetes sp 2 JQ780630 JQ768398 Helotiaceae sp 463478 97 ITS GU997932

Helotiales sp 463478 97 ITS JN655588Hyaloscypha fuckelii 13241336 99 LSU EU940154

Leotiomycetes sp 3 JX507735 Dimorphospora sp 474479 99 ITS JX077075Ascocoryne sp 377382 100 ITS JX077076

Leotiomycetes sp 4 JX507684 JX507685 Leotiomycetes sp 521531 98 ITS HQ211767Hyaloscypha sp 810831 97 LSU EU940092

Leotiomycetes sp 5 JX507687 Dimorphospora sp 473478 99 ITS JX077075Ascocoryne sp 370377 100 ITS JX077076

Massarinaceae sp JQ780631 JQ780632 Saccharicola bicolor 491501 98 ITS AF455415Neottiosporina paspali 813822 99 LSU EU754172

Mollisia sp 1 JX507704 Mollisia minutella 488493 99 ITS FR837920Mollisia sp 2 JX507644 JX507645 Mollisia minutella 477484 99 ITS FR837920

Mollisia cinerea 732746 98 LSU DQ470942Mollisia sp 3 JX507668 JX507669 Mollisia minutella 483483 100 ITS FR837920

Mollisia cinerea 806819 98 LSU DQ470942Mortierella elongata JX535038 Mortierella elongata 468468 100 ITS KC018241Nectriaceae sp JX535175 Cylindrocarpon obtusisporum 475476 99 ITS GU726752

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 243

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Clavulina sp 792829 96 LSU AY745694Clavulinaceae sp JX507727 JX507728 Clavulinaceae sp 610611 99 ITS FJ475570

Clavulina sp 812850 96 LSU AY745694Conichaeta sp JX507629 JX507630 Coniochaeta sp 489489 100 ITS HM595513

Coniochaeta sp 509509 100 LSU HM595603Crocicreas sp JQ780618 JQ768393 Crocicreas sp 477478 99 ITS FJ005100

Cyathicula microspora 13231339 99 LSU EU940088Crocicreas sp JX507682 Crocicreas sp 440442 99 ITS FJ005098

Crocicreas sp 438442 99 ITS FJ005099Dothideales sp JX535090 JX535091 Dothideales sp 510511 99 ITS HM240804

Dothideomycetes sp 503513 98 ITS GQ153228Dothideomycetes sp 763774 99 LSU GU323957Dothidea insculpta 764808 95 LSU NG027643

Dothideomycetes sp 1 JX535078 Paraconiothyrium sp 497515 97 ITS HM999948Paraphaeosphaeria sp 496515 96 ITS KC208020

Dothideomycetes sp 1 JX507635 Paraconiothyrium sp 494512 96 ITS HM999948Paraphaeosphaeria sp 493512 96 ITS KC208020

Dothideomycetes sp 2 JX535162 Mycosphaerella fragariae 472476 99 ITS GU214691Ramularia grevilleana 469475 99 ITS GU939181

Fungus sp JX507690 Hongkongmyces pedis 252285 88 ITS JQ435790Gloeophyllum sepiarium JX507712 JX507713 Gloeophyllum sepiarium 569570 99 ITS JQ358803

Gloeophyllum sepiarium 821821 100 LSU JN649344Gnomoniaceae sp JX507716 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Gnomoniaceae sp JX507717 Gnomonia cf ischnostyla 475477 99 ITS EU254903

Ophiognomonia sp 474477 99 ITS JQ414264Helotiales sp 1 JQ780635 Lachnum sp 416435 97 ITS FJ378861Helotiales sp 2 JQ780665 Gremmeniella sp 450453 99 ITS FR715997

Helotiales sp 421423 99 ITS AY354243Helotiales sp 3 JQ780658 JQ780659 Godronia sp 439453 98 ITS EF672237

Godronia urceulos13201321 99 LSU EU754163Helotiales sp 4 JX535181 Varicosporium elodeae 489492 99 ITS GQ152148Helotiales sp 5 JX535100 JX535101 Helotiales sp 480490 98 ITS JN655578

Mollisia cinerea 801811 99 LSU DQ470942Helotiales sp 6 JX535046 JX535047 Hyaloscyphaceae sp 479488 98 ITS GU393951

Hyalodendriella betulae 727746 97 LSU EU040232Helotiales sp 7 JX535102 JX535103 Catenulifera brevicollaris 479507 94 ITS GU727561

Catenulifera brachyconia 784800 98 LSU GU727559Helotiales sp 8 JX507674 JX507675 Hymenoscyphus sp 472487 97 ITS GU479911

Hyaloscypha fuckelii 766780 98 LSU EU940154Helotiales sp 8 JX507670 JX507671 Hymenoscyphus sp 471486 97 ITS GU479911

Hyaloscypha fuckelii 806820 98 LSU EU940154Helotiales sp 9 JX507660 JX507661 Meliniomyces bicolor 480480 100 ITS HQ157926

Hyaloscypha hepaticola 829838 99 LSU EU940118Helotiales sp 9 JX507662 JX507663 Meliniomyces sp 500503 99 ITS JQ711936

Hyaloscypha hepaticola 830839 99 LSU EU940118

242 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Helotiales sp 10 JX507720 JX507721 Helotiales sp 488542 90 ITS FJ378857Neobulgaria sp 484542 89 ITS HQ211726Neobulgaria pura 752788 95 LSU DQ257365

Helotiales sp 11 JX507672 JX507673 Helotiales sp 492497 99 ITS JX852365Catenulifera brachyconia 766782 98 LSU GU727559

Helotiales sp 12 JX507664 JX507665 Acephala sp 478483 99 ITS JN655564Mollisia sp 771797 97 LSU EU107273

Helotiales sp 12 JX507666 JX507667 Acephala sp 479484 99 ITS JN655564Mollisia sp 737781 94 LSU EU107273

Helotiales sp 13 JX507676 JX507677 Cudoniella acicularis 435470 93 ITS DQ202512Varicosporium giganteum 737747 99 LSU GQ477344

Helotiales sp 14 JX507656 JX507657 Acephala sp 481489 98 ITS HQ889709Mollisia sp 737755 97 LSU EU107273

Helotiales sp 15 JX507693 Helotiales sp 531534 99 ITS GU934595Helotiales sp 16 JX535119 JX535120 Helotiales sp 424426 99 ITS AY354243

Godronia urceolus 831831 100 LSU EU754163Helotiales sp 17 JX507731 JX507732 Helotiales sp 491545 90 ITS FJ378857

Neobulgaria sp 487545 89 ITS HQ211726Neobulgaria pura 748783 96 LSU DQ257365

Helotiales sp 18 JX507688 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Helotiales sp 18 JX507714 JX507715 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076Neobulgaria lilacina 794821 97 LSU EU940141

Helotiales sp 19 JX507683 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Leotiomycetes sp 1 JQ780634 Leotiomycetes sp 471529 94 ITS HQ212354Leotiomycetes sp 2 JQ780630 JQ768398 Helotiaceae sp 463478 97 ITS GU997932

Helotiales sp 463478 97 ITS JN655588Hyaloscypha fuckelii 13241336 99 LSU EU940154

Leotiomycetes sp 3 JX507735 Dimorphospora sp 474479 99 ITS JX077075Ascocoryne sp 377382 100 ITS JX077076

Leotiomycetes sp 4 JX507684 JX507685 Leotiomycetes sp 521531 98 ITS HQ211767Hyaloscypha sp 810831 97 LSU EU940092

Leotiomycetes sp 5 JX507687 Dimorphospora sp 473478 99 ITS JX077075Ascocoryne sp 370377 100 ITS JX077076

Massarinaceae sp JQ780631 JQ780632 Saccharicola bicolor 491501 98 ITS AF455415Neottiosporina paspali 813822 99 LSU EU754172

Mollisia sp 1 JX507704 Mollisia minutella 488493 99 ITS FR837920Mollisia sp 2 JX507644 JX507645 Mollisia minutella 477484 99 ITS FR837920

Mollisia cinerea 732746 98 LSU DQ470942Mollisia sp 3 JX507668 JX507669 Mollisia minutella 483483 100 ITS FR837920

Mollisia cinerea 806819 98 LSU DQ470942Mortierella elongata JX535038 Mortierella elongata 468468 100 ITS KC018241Nectriaceae sp JX535175 Cylindrocarpon obtusisporum 475476 99 ITS GU726752

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 243

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Helotiales sp 10 JX507720 JX507721 Helotiales sp 488542 90 ITS FJ378857Neobulgaria sp 484542 89 ITS HQ211726Neobulgaria pura 752788 95 LSU DQ257365

Helotiales sp 11 JX507672 JX507673 Helotiales sp 492497 99 ITS JX852365Catenulifera brachyconia 766782 98 LSU GU727559

Helotiales sp 12 JX507664 JX507665 Acephala sp 478483 99 ITS JN655564Mollisia sp 771797 97 LSU EU107273

Helotiales sp 12 JX507666 JX507667 Acephala sp 479484 99 ITS JN655564Mollisia sp 737781 94 LSU EU107273

Helotiales sp 13 JX507676 JX507677 Cudoniella acicularis 435470 93 ITS DQ202512Varicosporium giganteum 737747 99 LSU GQ477344

Helotiales sp 14 JX507656 JX507657 Acephala sp 481489 98 ITS HQ889709Mollisia sp 737755 97 LSU EU107273

Helotiales sp 15 JX507693 Helotiales sp 531534 99 ITS GU934595Helotiales sp 16 JX535119 JX535120 Helotiales sp 424426 99 ITS AY354243

Godronia urceolus 831831 100 LSU EU754163Helotiales sp 17 JX507731 JX507732 Helotiales sp 491545 90 ITS FJ378857

Neobulgaria sp 487545 89 ITS HQ211726Neobulgaria pura 748783 96 LSU DQ257365

Helotiales sp 18 JX507688 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Helotiales sp 18 JX507714 JX507715 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076Neobulgaria lilacina 794821 97 LSU EU940141

Helotiales sp 19 JX507683 Dimorphospora sp 479479 100 ITS JX077075Ascocoryne sp 382382 100 ITS JX077076

Leotiomycetes sp 1 JQ780634 Leotiomycetes sp 471529 94 ITS HQ212354Leotiomycetes sp 2 JQ780630 JQ768398 Helotiaceae sp 463478 97 ITS GU997932

Helotiales sp 463478 97 ITS JN655588Hyaloscypha fuckelii 13241336 99 LSU EU940154

Leotiomycetes sp 3 JX507735 Dimorphospora sp 474479 99 ITS JX077075Ascocoryne sp 377382 100 ITS JX077076

Leotiomycetes sp 4 JX507684 JX507685 Leotiomycetes sp 521531 98 ITS HQ211767Hyaloscypha sp 810831 97 LSU EU940092

Leotiomycetes sp 5 JX507687 Dimorphospora sp 473478 99 ITS JX077075Ascocoryne sp 370377 100 ITS JX077076

Massarinaceae sp JQ780631 JQ780632 Saccharicola bicolor 491501 98 ITS AF455415Neottiosporina paspali 813822 99 LSU EU754172

Mollisia sp 1 JX507704 Mollisia minutella 488493 99 ITS FR837920Mollisia sp 2 JX507644 JX507645 Mollisia minutella 477484 99 ITS FR837920

Mollisia cinerea 732746 98 LSU DQ470942Mollisia sp 3 JX507668 JX507669 Mollisia minutella 483483 100 ITS FR837920

Mollisia cinerea 806819 98 LSU DQ470942Mortierella elongata JX535038 Mortierella elongata 468468 100 ITS KC018241Nectriaceae sp JX535175 Cylindrocarpon obtusisporum 475476 99 ITS GU726752

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 243

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Nectria lugdunensis 475477 99 ITS FJ000394Nectriaceae sp JX535186 Cylindrocarpon obtusisporum 480481 99 ITS GU726752

Nectria lugdunensis 482483 99 ITS FJ000394Nectriaceae sp JX535187 Cylindrocarpon obtusisporum 475477 99 ITS GU726752

Nectria lugdunensis 476477 99 ITS FJ000394Neolentinus sp JX507691 JX507692 Neolentinus lepideus 452455 99 ITS AB615456

Neolentinus lepideus 849856 99 LSU HM536077Penicillium spinulosuma JQ780638 Penicillium spinulosum 506507 99 ITS KC167850Penicillium spinulosum JQ780639 Penicillium spinulosum 510510 100 ITS DQ888735Peniophora piceae JX507718 JX507719 Peniophora piceae 545545 100 ITS AY781264

Peniophora sp 13521357 99 LSU DQ094783Peniophora sp 1 JX507724 JX507725 Peniophora pini 574576 99 ITS EU118651

Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Peniophora sp 2 JX535110 JX535111 Peniophora pini 569572 99 ITS EU118651Peniophora pini 13131331 99 LSU EU118651Peniophora cinerea 12901309 99 LSU DQ094786

Pezizomycotina sp 1 JQ780651 Ramularia eucalypti 451453 99 ITS EF394861Glomerella lagenaria 451453 99 ITS AJ301970

Pezizomycotina sp 2 JQ780663 Ramularia eucalypti 462465 99 ITS EF394861Phellinus sp JQ780625 JQ768397 Phellinus cinereus 554557 99 ITS AY340047

Phellinus igniarius 601604 99 ITS AM269797Phellinus cinereus 858859 99 LSU AF311027Phellinus igniarius 18381850 99 LSU AY839834

Phlebiopsis giganteaa JQ780612 Phlebiopsis gigantea 626626 100 ITS AF087487Phlebiopsis giganteaa JQ780617 JQ768392 Phlebiopsis gigantea 584584 100 ITS AF087487

Ceratobasidiaceae sp 12911335 97 LSU JF799768Phlebiopsis giganteaa JX507707 JX507708 Phlebiopsis gigantea 598598 100 ITS AF087487

Antrodiella romellii 19612058 95 LSU JQ768396Pholiota sp JX507628 Pholiota lenta 608608 100 ITS AY281022

Pholiota lubrica 602602 100 ITS JF908578Phoma poolensis JQ780633 JQ768399 Phoma novae-verbascicola 468468 100 ITS GU237753

Phoma novae-verbascicola 13231323 100 LSU GU238135Phoma poolensis JQ780648 JQ768403 Phoma novae-verbascicola 455455 100 ITS GU237753

Phoma novae-verbascicola 13191319 100 LSU GU238135Piptoporus betulinus JX507733 JX507734 Piptoporus betulinus 600600 100 ITS GU731570

Piptoporus betulinus 601602 99 LSU JQ700297Piptoporus betulinus 811843 96 LSU JQ700297

Pochonia bulbillosa JX535141 Pochonia bulbillosa 537539 99 ITS AB378551Pochonia bulbillosa JQ780661 JQ780662 Pochonia bulbillosa 534535 99 ITS AB378551

Pochonia bulbillosa 838840 99 LSU HQ232164Pochonia bulbillosa JX535180 Pochonia bulbillosa 538540 99 ITS AB378551Polyporus sp JX507702 JX507703 Polyporus lepideus 592593 ITS GU731572

Polyporus ciliatus 560567 99 ITS AB070883Polyporus arcularius 831840 99 LSU AF393067

Polyporales sp JX507648 JX507649 Oligoporus placentus 596597 99 ITS AJ416069

244 MYCOLOGIA

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Postia placenta 590597 99 ITS JQ700293Antrodia xantha 20392092 97 LSU AJ583430

Pseudogymnoascuspannorum

JQ768386 JQ768405 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Pseudogymnoascuspannorum

JQ780644 JQ768404 Pseudogymnoascus pannorum 487487 100 ITS HQ115661

Pseudogymnoascus pannorum 575576 99 LSU GU951694Resinicium bicolor JQ780611 JQ768387 Resinicium bicolor 518518 100 ITS DQ218310

Resinicium bicolor 12601266 99 LSU AY700183Resinicium bicolor JQ780619 JQ768394 Resinicium bicolor 495495 100 ITS DQ218310

Resinicium bicolor 12211226 99 LSU AY700183Resinicium sp JQ780620 JQ768395 Resinicium furfuraceum 609617 99 ITS DQ873648

Resinicium furfuraceum 13571364 99 LSU DQ873648Sistotrema brinkmannii JQ780616 JQ768391 Sistotrema brinkmannii 605605 100 ITS JQ912675

Sistotrema brinkmannii 12861303 99 LSU AF506473Sistotrema brinkmannii JX507642 JX507643 Sistotrema brinkmannii 577577 100 ITS JQ912675

Sistotrema brinkmannii 12751292 99 LSU AF506473Sistotrema brinkmannii JX535082 JX535083 Sistotrema brinkmannii 570571 99 ITS JQ912675

Sistotrema brinkmannii 12891306 99 LSU AF506473Sistotrema brinkmannii JX507686 Sistotrema brinkmannii 563563 100 ITS JQ912675Sistotrema brinkmannii JX535117 JX535118 Sistotrema brinkmannii 568569 99 ITS JQ912675

Sistotrema brinkmannii 12881305 99 LSU AF506473Sistotrema brinkmannii JX507710 JX507711 Sistotrema brinkmannii 570571 99 ITS AY089729

Sistotrema brinkmannii 12821300 99 LSU AF506473Sistotrema sp JQ780613 JQ768388 Sistotrema sp 530530 ITS 100 AY781271

Sistotrema brinkmannii 12821301 99 LSU AF506473Sistotrema coroniferum 12471277 98 LSU AM259215

Sistotrema sp JQ780615 JQ768390 Sistotrema sp 530530 ITS 100 AY781271Sistotrema brinkmannii 12841303 99 LSU AF506473Sistotrema coroniferum 12481278 98 LSU AM259215

Sistotrema sp JX507633 JX507634 Sistotrema sp 522522 100 ITS AY781271Sistotrema brinkmannii 12881307 99 LSU AF506473Sistotrema coroniferum 12521282 98 LSU AM259215

Sistotrema sp JX535108 JX535109 Sistotrema sp 530530 100 ITS AY781271Sistotrema brinkmannii 12851304 99 LSU AF506473Sistotrema coroniferum 12491279 98 LSU AM259215

Stereum sp JX535114 JX535115 Stereum hirsutum 470472 99 ITS JX501297Stereum annosum 565571 99 ITS DQ000294Stereum sp 789791 99 LSU EF600046

Strobilurus tenacellus JX507722 JX507723 Strobilurus tenacellus 686686 100 ITS GQ892812Strobilurus tenacellus 833833 100 LSU AM946470

Sydowia polyspora JQ780656 JQ768401 Sydowia polyspora 536537 99 ITS FR822985Sydowia polyspora 13051305 100 LSU DQ678058

Sydowia polyspora JX535167 Sydowia polyspora 526529 99 ITS FR822985Sydowia polyspora 526530 99 ITS FR717223

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 245

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

depth of the other two lakes (Ershovskoe Nizhnee andKislosladkoe) is less than 5 m and they evolve presum-ably in the same way The evolution of all the lakesexplored is followed by the uniform processes ofchange such as succession of plants change of organicsediments and physical-chemical properties of thelakes All these factors influence species compositionof fungi in the boggy lakes

Whereas the fungal communities from the peat-lands studied have similarities at higher taxonomiclevels the species composition at lower taxonomiclevels change depending on the distance of thelakes from the sea and differences in the age ofthe peatlands (TABLE I FIG 3) However despitethe mentioned similarities the fungal communities

of the studied peatlands are different (FIG 4) Con-sistently pairs Verkhnee-Krugloe and Krugloe-Ershovskoe have the highest similarity The estab-lished Ershovskoe Peatland and the newly formingKislosladkoe Peatland have the lowest similaritywhich can be attributed to the unique species com-position of the sediments of Lake ErshovskoeVerkhnee

Fungal communities from the Verkhnee Krugloeand Ershovskoe peatlands are similar in spite of the dif-ferences in the altitude and age This stability could beexplained primarily by the chemical constitution ofSphagnum moss because it consists of complex pheno-lic compounds that can be decomposed by a specificgroup of fungi Taxa such as Oidiodendron griseum O

TABLE II Continued

GenBank accession No

Species ITS LSU SSU BLAST

Talaromyces funiculosus JX507726 Penicillium funiculosum 516516 100 ITS JX045839Teberdinia hygrophilaa JQ780641 JQ780642 JQ780643 Teberdinia hygrophila 446447 99 ITS AY129291

Pseudoeurotium zonatum 13111319 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 733734 99 SSU AY129282

Teberdinia hygrophilaa JQ780645 JQ780646 JQ780647 Teberdinia hygrophila 447447 100 ITS AY129291Teberdinia hygrophila 10531055 99 SSU AY129282Pseudoeurotium zonatum 819822 99 LSU AF096198

Teberdinia hygrophilaa JQ780653 JQ780654 JQ780655 Teberdinia hygrophila 448449 99 ITS AY129291Pseudoeurotium zonatum 13071315 99 LSU DQ470988Pseudoeurotium sp 785791 99 LSU AB470594Teberdinia hygrophila 10451047 99 SSU AY129282

Tolypocladiumcylindrosporum JX535129 Tolypocladium cylindrosporum 497497 100 ITS FJ025179

Tolypocladiumcylindrosporum JX507699 Tolypocladium cylindrosporum 499499 100 ITS FJ025179

Tolypocladium geodesa JX507694 Tolypocladium geodes 467470 99 ITS FJ973059Tolypocladuim inflatuma JQ780640 Tolypocladuim inflatum 493494 99 ITS JX488470Tolypocladuim inflatuma JX507695 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507696 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507697 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JX507698 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780650 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780652 Tolypocladuim inflatum 494495 99 ITS JX488470Tolypocladuim inflatuma JQ780664 Tolypocladuim inflatum 494495 99 ITS JX488470Trichoderma polysporuma JQ780637 Hypocrea pachybasioides 555557 99 ITS FJ860796

Trichoderma polysporum 532537 99 ITS DQ093710Trichoderma polysporuma JQ780636 JQ768400 Hypocrea parapilulifera 539540 99 ITS FJ860799

Trichoderma sp 10181018 100 LSU AY283550Volutella sp JX507700 Volutella sp 517521 99 ITS FR822789

Volutella ciliata 517521 99 ITS GU479901

a Species names identified by morphology

246 MYCOLOGIA

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE III Isolated species with frequencies () of their occurrence and media of isolation

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Acremonium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Acremonium sp 2h mdash mdash mdash 188 mdash mdash mdash 34 mdash 4 AA

Acremonium sp 3h mdash mdash mdash mdash 36 mdash mdash mdash 63 2 SWA

Acrodontium crateriforme (JFH Beyma) de Hoog 36 mdash 34 mdash 71 mdash mdash mdash mdash 4 MA CA WA

Acrodontium simplex (F Mangenot) de Hoog mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Agaricomycetes sph mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Alternaria alternata (Fr) Keissl 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 SEA

Alternaria sph mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 MA CA

Amylostereum areolatum (Chaillet ex Fr) Boidinh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Antrodia xantha (Fr) Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodia sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Antrodia sp 2h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Antrodiella romellii (Donk) Niemelaumlh mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Ascomycota sp 1h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Ascomycota sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Ascomycota sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 AA

Ascomycota sp 4h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Ascomycota sp 5h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Ascomycota sp 6h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SWA

Aspergillus repens (Corda) Sacc mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Aspergillus tubingensis Mosseray mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Aspergillus ustus (Bainier) Thom et Church 36 mdash mdash mdash 36 mdash mdash mdash mdash 2 MA SEA

Aspergillus versicolor (Vuill) Tirab mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Aureobasidium pullulans (de Bary) G Arnaud mdash 74 103 mdash 36 mdash 69 69 mdash 10 MA WASEA SWA

Basidiomycota sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Basidiomycota sp 2h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Basidiomycota sp 3h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Basidiomycota sp 4h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Beauveria bassiana (Bals-Criv) Vuill 107 148 69 63 mdash mdash mdash mdash mdash 10 MA CA SEA

Beauveria brongniartii (Sacc) Petch mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Botryotinia sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Botrytis cinerea Pers 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 MA CA

Cadophora fastigiata Lagerb et Melinh mdash mdash mdash 63 mdash mdash mdash 34 mdash 2 CA SWA

Cadophora luteo-olivacea (JFH Beyma) TC Harret McNewh

mdash mdash mdash 125 mdash mdash mdash 69 63 5 MA CA WASEA SWA

Cadophora sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Cadophora sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Ceriporiopsis subvermispora (Pilaacutet) Gilb et Ryvardenh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Chrysosporium sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA

Cladophialophora humicola Crous et U Braun 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium antarcticum K Schub Crous et UBraun

mdash mdash mdash 188 mdash mdash mdash mdash mdash 3 AA

Cladosporium bruhnei Linder mdash 37 69 188 mdash 37 mdash mdash mdash 7 MA CA AAWA SWA

Cladosporium cladosporioides (Fresen) GA deVriesh

107 37 69 125 mdash mdash 34 mdash 125 11 MA CA WASEA SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 247

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Cladosporium herbarum (Pers) Linkh 36 74 34 188 mdash mdash mdash mdash mdash 7 MA WASEA SWA

Cladosporium langeronii (Fonseca Leatildeo etNogueira) Vuillh

71 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sphaerospermum Penz 321 111 mdash mdash 36 mdash mdash mdash mdash 13 MA CA WASEA SWA

Cladosporium sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Cladosporium sp 2h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Cladosporium sp 3h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Clavulinaceae sph mdash mdash mdash mdash mdash 37 mdash 34 mdash 2 MA

Coniochaeta sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Crocicreas sph mdash mdash 34 mdash mdash mdash mdash 34 mdash 2 CA SEA

Dothideales sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Dothideomycetes sp 1h mdash mdash mdash mdash mdash mdash mdash 34 63 1 MA SEA

Dothideomycetes sp 2h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Elaphocordyceps subsessilis (Petch) GH Sung JMSung et Spataforah

214 mdash 34 125 179 74 mdash mdash 63 17 All

Emericellopsis minima Stolk mdash mdash mdash mdash mdash mdash mdash 69 mdash 2 WA

Emericellopsis sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Engyodontium album (Limber) de Hoog mdash 37 mdash 63 mdash 37 mdash mdash mdash 3 MA CA SEA

Fungal sph mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Fusarium sp mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Geomyces pannorum (Link) Sigler et JW Carmichh 71 37 34 63 mdash mdash mdash 69 mdash 7 MA CAWA SEA

Geotrichum candidum Link 36 mdash mdash mdash 36 mdash mdash 69 mdash 4 MA CA SEA

Gibellulopsis nigrescens (Pethybr) Zare W Gams etSummerb

36 mdash mdash mdash mdash mdash mdash 34 mdash 2 MA SWA

Gloeophyllum sepiarium (Wulfen) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Gnomoniaceae sph mdash mdash mdash mdash 36 mdash mdash 34 mdash 2 MA SEA

Hansfordia sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Helotiales sp 1h mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Helotiales sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Helotiales sp 3h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Helotiales sp 4h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Helotiales sp 5h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 SEA

Helotiales sp 6h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Helotiales sp 7h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 CA

Helotiales sp 8h mdash mdash mdash mdash 71 37 mdash mdash mdash 3 MA CA SEA

Helotiales sp 9h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 WA

Helotiales sp 10h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 11h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 CA

Helotiales sp 12h mdash mdash mdash mdash 36 mdash mdash mdash mdash 2 MA

Helotiales sp 13h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Helotiales sp 14h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SWA

Helotiales sp 15h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Helotiales sp 16h mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Helotiales sp 17h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Helotiales sp 18h mdash mdash mdash mdash mdash mdash mdash 34 mdash 2 CA SWA

248 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Helotiales sp 19h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Humicola fuscoatra Traaen mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Humicola sp mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 SWA

Lecanicillium evansii Zare etW Gams mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Lecanicillium muscarium (Petch) Zare et W Gams mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 AA

Leotiomycetes sp 1h mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Leotiomycetes sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Leotiomycetes sp 3h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Leotiomycetes sp 4h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Leotiomycetes sp 5h mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Massarinaceae sph mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Mollisia sp 1h mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Mollisia sp 2h mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Mollisia sp 3h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Mortierella elongata Linnemh mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Mortierella lignicola (GW Martin) W Gams et RMoreau

mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 WA

Mortierella longicollis Dixon-Stew mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

Nectriaceae sph mdash mdash mdash 125 mdash mdash mdash mdash mdash 2 MA

Neolentinus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 CA

Neoscytalidium dimidiatum (Penz) Crous etSlippers

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Oidiodendron ambiguum Peyronel et Malan mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Oidiodendron echinulatum GL Barron mdash mdash mdash mdash mdash mdash 34 34 mdash 2 SWA

Oidiodendron griseum Robak 179 37 mdash 63 36 mdash mdash mdash mdash 8 MA CA WA

Oidiodendron maius var citrinum (Barron) Rice aCurrah

36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Oidiodendron periconioides Morrall mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 CA

Oidiodendron sp mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 SEA

Penicillium aculeatum Raper et Fennell mdash mdash mdash mdash mdash mdash mdash mdash 63 1 MA

Penicillium aurantiogriseum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 WA CA

Penicillium brevicompactum Dierckx 36 111 mdash mdash mdash mdash mdash mdash mdash 4 MAWA SEA

Penicillium chermesinum Biourge mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium citreonigrum Dierckx 36 37 34 mdash mdash mdash mdash mdash mdash 3 MA CA

Penicillium citrinum Thom mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 SEA

Penicillium corylophilum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium dierckxii Biourge mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Penicillium expansum Link 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium glabrum (Wehmer) Westling 36 185 mdash 63 mdash mdash mdash mdash mdash 7 MA CA WASEA SWA

Penicillium griseofulvum Dierckx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Penicillium implicatum Biourge mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium janczewskii KM Zalessky mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 CA

Penicillium multicolor Grig-Man et Porad mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Penicillium nalgiovense Laxa mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 WA

Penicillium purpurascens (Sopp) Biourge mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SWA

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 249

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Penicillium restrictum JC Gilman et EV Abbott 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Penicillium rolfsii Thom mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Penicillium roseopurpureum Dierckx 36 mdash mdash mdash 71 mdash mdash mdash 63 3 CA WA SEA

Penicillium sclerotiorum JFH Beyma mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Penicillium solitum var solitum Westling mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 SEA

Penicillium spinulosum Thomh 143 185 103 25 36 74 mdash 34 mdash 20 MA CA WASEA SWA

Penicillium thomii Maire 36 37 172 mdash mdash mdash mdash mdash 63 8 MA CA WA

Penicillium verrucosum Dierckx mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Penicillium vinaceum JC Gilman et EV Abbott 36 mdash 34 mdash mdash mdash mdash mdash mdash 2 SEA

Penicillium waksmanii KM Zalessky mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Peniophora piceae (Pers) J Erikssh mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Peniophora sp 1h mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 CA

Peniophora sp 2h mdash mdash mdash mdash mdash mdash mdash mdash 63 1 WA

Pezizomycotina sp 1h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Pezizomycotina sp 2h 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phaeosphaeria sp mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 WA

Phellinus sph 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 SEA

Phialophora europaea de Hoog Mayser et Haase 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Phialophora lagerbergii (Melin et Nannf) Conant mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Phialophora verrucosa Medlar mdash mdash 34 63 mdash mdash mdash mdash mdash 2 CA WA

Phlebiopsis gigantea (Fr) Juumllichh 36 mdash 69 mdash mdash mdash mdash 34 mdash 4 MA CA WA

Pholiota sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 MA

Phoma poolensis (Ellis et Kellerm) Aa et Boeremah mdash mdash 69 mdash mdash mdash mdash mdash mdash 2 MA CA

Piptoporus betulinus (Bull) P Karsth mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 MA

Pochonia bulbillosa (W Gams et Malla) Zare et WGamsh

36 mdash mdash 125 mdash mdash mdash mdash mdash 3 MA CA

Polyporus sph mdash mdash mdash mdash mdash 37 mdash mdash mdash 1 MA

Polyporales sph mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 CA

Polyscytalum fecundissimum Riess 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 WA

Resinicium bicolor (Alb et Schwein) Parmastoh mdash 37 34 mdash mdash mdash mdash mdash mdash 2 MA

Resinicium sph mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 SEA

Sclerotinia sp 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 MA

Scopulariopsis brumptii Salv-Duval mdash mdash mdash mdash mdash mdash 69 mdash mdash 2 SWA

Sistotrema brinkmannii (Bres) J Erikssh mdash mdash 34 mdash 71 mdash mdash 34 125 6 MA CA AAWA SWA

Sistotrema sph 36 37 mdash mdash 36 mdash mdash mdash 63 4 MA CASEA SWA

Stachybotrys chartarum (Ehrenb) S Hughes 36 mdash mdash mdash mdash mdash mdash mdash 1 SEA

Stachybotrys dichroa Grove mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SEA

Stephanosporium atrum Dal Vesco mdash mdash mdash mdash mdash mdash 34 mdash mdash 1 WA SEA

Stereum sph mdash mdash mdash mdash mdash mdash mdash mdash 63 1 AA SEA

Strobilurus tenacellus (Pers) Singerh mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

Sydowia polyspora (Bref et Tavel) E Muumlllh 36 mdash mdash 63 mdash mdash mdash mdash mdash 2 CA SEA

Talaromyces diversus (Raper et Fennell) SamsonYilmaz et Frisvad

mdash 37 mdash mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces duclauxii (Delacr) Samson YilmazFrisvad et Seifert

mdash mdash mdash mdash mdash mdash mdash 34 mdash 1 MA

250 MYCOLOGIA

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

TABLE III Continued

Species

Sampling site

Total FeNo of

isolates Medium

Peat Sediments

Aa Bb Cc Dd Aa BbC

(1)cC

(2)c Dd

Talaromyces funiculosus (Thom) Samson YilmazFrisvad et Seiferth

36 148 207 63 107 37 mdash 69 mdash 18 MA CA WASEA SWA

Talaromyces rugulosus (Thom) Samson YilmazFrisvad et Seifert

mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 MA

Talaromyces variabilis (Sopp) Samson YilmazFrisvad et Seifert

mdash 74 34 mdash mdash mdash mdash mdash 63 4 MA CA SEA

Talaromyces verruculosus (Peyronel) SamsonYilmaz Frisvad et Seifert

36 mdash mdash mdash mdash mdash mdash mdash 63 2 WA SEA

Teberdinia hygrophila Sogonov W GamsSummerb et Schroersh

mdash 74 34 mdash mdash mdash mdash mdash 3 WA

Tolypocladium cylindrosporum W Gamsh mdash mdash mdash 188 36 mdash mdash mdash 63 5 MAAA SWA

Tolypocladium geodes W Gamsh mdash 111 mdash mdash 36 mdash mdash 34 mdash 5 WA AA SEA

Tolypocladium nubicola Bissett mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 WA

Tolypocladium tundrense Bissett mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 AA

Trichoderma asperellum Samuels Lieckf etNirenberg

mdash mdash mdash mdash 36 mdash mdash mdash mdash 1 WA SEA

Trichoderma hamatum (Bonord) Bainier mdash mdash mdash mdash mdash 37 69 69 mdash 5 MA CA WASEA SWA

Trichoderma harzianum Rifai mdash 37 69 63 mdash mdash mdash 34 mdash 5 CA WASEA SWA

Trichoderma koningii Oudem mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Trichoderma piluliferum J Webster et Rifai mdash mdash 34 mdash mdash mdash mdash mdash mdash 1 WA

Trichoderma polysporum (Link) Rifaih 36 mdash 34 mdash mdash 74 69 34 mdash 7 MA CA WASEA SWA

Trichoderma viride Pers mdash 74 69 mdash 71 mdash 34 mdash mdash 7 WASEA SWA

Trichosporon lignicola (Diddens) Fell et Scorretti 36 mdash mdash mdash mdash mdash mdash mdash mdash 1 CA

Umbelopsis isabellina (Oudem) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis ramanniana (Moumlller) W Gams mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 MA

Umbelopsis vinacea (Dixon-Stew) Arx mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 CA

Umbelopsis sp mdash mdash mdash 63 mdash mdash mdash mdash mdash 1 SWA

Volutella sph mdash mdash mdash mdash mdash 74 mdash mdash mdash 2 AA

Zythiostroma pinastri (P Karst) Houmlhn 71 mdash mdash mdash mdash mdash mdash mdash mdash 2 MA CA

Cladosporium sppf (3 morphotypes) 36 mdash mdash 63 mdash mdash mdash 34 mdash 3 MAWA SEA

Lecanicillium sppf (4 morphotypes) mdash 37 mdash 125 36 mdash mdash mdash mdash 4 MA AASEA SWA

Penicillium sppf (6 morphotypes) mdash 37 mdash mdash 107 37 mdash 34 mdash 6 MACA SWA

Phaeoacremonium sppf (4 morphotypes) mdash mdash 34 63 mdash 37 mdash 69 mdash 5 MAWA SEA

Trichoderma sppf (3 morphotypes) mdash mdash mdash mdash mdash mdash 34 69 mdash 3 SEA SWA

Sterile isolatesg (60 morphotypes) 143 185 69 188 464 259 207 276 750 60 All

a Frequency was calculated as percentage of 28 samples collected from peatland Ab Frequency was calculated as percentage of 27 samples collected from peatland Bc Frequency was calculated as percentage of 29 samples collected from peatland Cd Frequency was calculated as percentage of 16 samples collected from peatland De Frequency was calculated as percentage of 100 samples collected during the overall investigationf Morphotypes were not determined to species

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 251

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

maius O periconioides Talaromyces funiculosus Penicil-lium spinulosum P thomii Pochonia bulbillosa werefound they are known as decomposers of Sphagnummosses (Thormann et al 2002 2003 Rice et al 2006Thormann 2006) The community of the KislosladkoePeatland appears to be fundamentally different fromthe others The Sphagnum peat of the KislosladkoePeatland contains a higher frequency and quantity ofspecies of genera Cadophora Lagerb amp Melin AlternariaNees TolypocladiumW Gams Cladosporium and Acremo-nium Link when compared to the peat of the otherpeatlands (TABLE II) Presumably it could be explainedby the sea proximity and the youth of the peat depositThese factors influence physical-chemical features andorganic composition

Sediments present a more dynamic system due tosome differences in organic input as well as physical-chemical and hydrological exposures In the upperlake of the Ershovskoe Peatland large numbers ofinvertebrate animals were found such as leeches andfreshwater shrimp Apart from that numerous plantsand plant roots were discovered These facts couldindicate the existence of a different fungal communityin this lake (TABLE II) The results of the diatomresearch confirm the difference between the Ersovs-koe Peatland and other peatlands of the Kindo Penin-sula (Shilova 2011) Taxa such as Emericellopsis minimaand Acremonium spp were found in the sedimentswhich are characteristic for marine habitats (Joneset al 2009 Pivkin 2010)

The abundance of sterile isolates is typical for peat(Golovchenko et al 2002 Thormann 2006a) Signifi-cant amounts of sterile mycelium were found both inthe peat and in the sediments of all the peatlandsThe identification of a part of the sterile isolates bymolecular approaches revealed the abundance ofAscomycota isolates belonging to the Helotiales weremost abundant especially in the sediments examined(TABLE II) The fungi of this group can fulfill differentfunctions members of the Helotiales have beendescribed as plant pathogens endophytes nema-tode-trapping fungi mycorrhiza-forming (includingectomycorrhizae and ericoid mycorrhizae) ectomy-corrhizal parasites fungal parasites terrestrial

saprobes aquatic saprobes root symbionts andwood-rot fungi (Wang et al 2006)

One of the important results of using molecularapproaches for the identification of sterile isolateswas the detection of species of the Basidiomycota Thor-mann (2006a) considers five groups of fungi whichdecompose different types of organic substance inpeat One of these includes species that are known asrecalcitrant polymer degraders This group mostly con-sists of the basidiomycetes species which are capableof utilizing complex polymers including lignin tan-nins and other polyphenolics typical for peat Due toslow growth and difficulties related with identificationof these fungi they are difficult to find and study Inour work a significant number of the basidiomycetesisolates was identified which can be used for futureresearch

Apart from that fungi that are known as psychroto-lerant species were isolated The examples of thesefungi are Pseudogymnoascus pannorum and Tolypocla-dium inflatum (Bisset 1982 Bubnova 2005 Kochkinaet al 2007) Both species were found in almost all stu-died samples moreover T inflatum was successfullygrown on all media (TABLE II) These facts indicatethe adaptation of the species to a wide spectrum ofenvironmental conditions In addition to T inflatumother anamorphs of the Cordycipitaceae and Ophiocordy-cipitaceae were isolated these include Tolypocladiumcylindrosporum T geodes T nubicola T tundrense Beau-veria bassiana B brongniartii and Engyodontium album

Also fungi that are known as typical soil saprobes fornorthern regions and species associated with insectssuch as Tolypocladium inflatum Tolypocladium cylindros-porum T geodes Engyodontium album were found athigh frequency (Lam et al 1988 Hodge et al 1996Bubnova 2005) The high incidence of entomopatho-genic species is remarkable The abundance of insectsand larvae in the peatlands may present a proteinsource in this N-limited environment and may reflectadaptations similar to that of some carnivorous plantsfound in the peatlands such as Drosera spp (TABLE I)(Limpens et al 2011)

Our investigations revealed high fungal biodiversityand density in all components of the studied peatlandson the Kindo Peninsula at Kandalaksha Bay of the

TABLE III Continued

g Sterile morphotypes were not determined to divisionh Species identified by morphological and molecular approach Species not found in sphagnum peat before this research in

boldfaceAbbreviations MA5malt-extract agar CA5 citric agar AA5 alkaline agar WA5 water agar SEA5 sphagnum-extract agar

SWA 5 seawater agarA5 Verchnee Peatland B5 Krugloe Peatland C5 Ershovskoe Peatland C(1)5 Ershovskoe Verchnee Lake C(2)5 Ershovs-

koe Nizhnee Lake D 5 Kislosladkoe Peatland

252 MYCOLOGIA

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

White Sea The isolated fungi predominantly belong tosaprobiotic ascomycetous species In addition to thedata available on the biological diversity of the fungifrom the peatland ecosystems of the northern regionwe present molecular data on a large group of fungiof undetermined taxonomy and sterile mycelia amongwhich are a significant percentage of basidiomycetesas well as newly revealed taxa of ascomycetes Theinvestigations carried out in this study suggest a speci-ficity of the fungal community in aqueous-peatlandsystem of the coastal area of Kandalaksha BayIt is related to the characteristic properties of thecomplex communities of the isolated fungi in eachof the reservoirs and in particular in a high percen‐tage of entomopathogenic species as well as in theoccurrence of psychrotolerant species Our researchrevealed that fungal communities in peat can becharacterized by higher stability than those insediments

ACKNOWLEDGMENTS

We thank Alexander Tzetlin (director of the WSBS) for theopportunity to do this research Elena Vortsepneva and Alex-ander Semenov for their help with sample collection BerthaKoopmanschap Marijke Slakhorst and Alex Grum-Grzhi-maylo for technical assistance and Denis Landin for imageprocessing The work was supported by Erasmus MundusIAMONET-RU and the Laboratory of Genetics at Wagenin-gen University the research grants from St Peterburg StateUniversity No 101342010 and RFBR grants No 15-29-02553 No15-04-02722 (the field investigation and identifica-tion of the fungi) RSCF grant No 14-50-00029 (the cultiva-tion and collection of the fungi Bilanenko Grum-Grzhimaylo)

LITERATURE CITED

Andersen R Grasset L Thormann MN Rochefort L FrancezA-J 2010 Changes in microbial community structureand function following Sphagnum peatland restorationSoil Biol Biochem 42291ndash301 doi101016jsoilbio200911006

Bisset J 1982 Notes on Tolypocladium and related generaCan J Bot 611311ndash1329 doi101139b83-139

Bubnova EN 2005 Izmenenia komplexov pochvoobitaushihgribov pri perehode ot zonalnih pochv k morskim ekoto-pam (na primere poberezhia Kandalakshskogo zalivaBelogo moray) [doctoral dissertation] Moscow StateUniversity 141 p [In Russian]

Czeczuga B 1993 Studies of aquatic fungi XXVIII The pre-sence of predatory fungi in the waters of northeasternPoland Acta Mycol 28211ndash217

Filippova NV Thormann MN 2014 Lager fungi of ombro-trophic bogs in west Siberia Mires Peat 141ndash22

Gilbert D Mitchell EAD 2006 Microbial diversity in Sphag-num peatlands In Martini IP Martinez Cortizas AChesworth W eds Peatlands evolution and records of

environmental and climate changes Developments inearth surface processes Elsevier Science

Golovchenko AV Semenova TA Polyakova AV Inisheva LI2002 The structure of the micromycete complexes ofoligotrophic peat deposits in the southern taiga subzoneof west Siberia Microbiology 71575ndash581 doi101023A1020514904709

Grum-Grzhimaylo OA Bilanenko EN 2009 Microfungalcommunities of bogs of the northwest and central Rus-sia extreme inhabitations Asian Mycological Congress2009 and 11th International Marine and FreshwaterMycology Symposium Taichung Taiwan 15ndash19 Nov2009 Taichung Taiwan p 146ndash147

Hodge KT Krasnoff SB Humber RA 1996 Tolypocladiuminflatum is the anamorph of Cordyceps subsessilis Mycolo-gia 88715ndash719

Jones EBG Sakayaroj J Suetrong S Somrithipol S Pang KL2009 Classification of marine Ascomycota anamorphictaxa and Basidiomycota Fungal Divers 187 p

Kachalkin AV Chernov IYu Semyonova TA GolovchenkoAV 2005 Characteristic of the taxonomy structurehyphomycetes and yeast communities in peat soils of dif-ferent genesis Mat IV nauch konf Bolota i BiospheraTomsk Russian p 208ndash216 [In Russian]

Karakousis A Tan L Ellis D Alexiou H Wormald PJ 2006An assessment of the efficiency of fungal DNA extrac-tion methods for maximizing the detection of medicallyimportant fungi using PCR J Microbiol Methods 6538ndash48 doi101016jmimet200506008

Keraumlnen S Kalpio S Aapa mires The world of plantshttpjulkaisutmetsafijulkaisutpdfluoaapa_mires_plantspdf

Kochkina GA Ivanushkina NE Akimov VN Gilichinskii DAOzerskaya SM 2007 Halo- and psychrotolerant Geomycesfungi from arctic cryopegs and marine deposits Micro-biology 7631ndash38 doi101134S0026261707010055

Laitinen J Rehell S Huttunen A 2005 Vegetation-relatedhydrotopographic and hydrologic classification foraapa mires (Hirvisio Finland) Ann Bot Fennici42107ndash121

mdashmdashmdash mdashmdashmdash mdashmdashmdash Tahvanainen T Heikkila R Lind-holm T 2007 Mire systems in Finlandmdashspecial view toaapa mires and their water-flow pattern Suoseura FinPeatland Soc Suo 581ndash26

Lam TNC Goettel MS Soares GG Jr 1988 Host records forthe entomopathogenic hyphomycete Tolypocladium cylin-drosporum Florida Entomol 7186ndash89 doi1023073494898

Limpens J Granath G Gunnarsson U Aerts R Bayley SBragazza L Bubier J Buttler A Berg LJL Francez A-JGerdol R Grosvernier P Heijmans MMPD HoosbeekMR Hotes S Ilomets M Leith I Mitchell EAD MooreT Nilsson MB Nordbakken J-F Rochefort L Rydin HSheppard LJ Thormann M Wiedermann MM WilliamsBL Xu B 2011 Climatic modifiers of the response tonitrogen deposition in peat-forming Sphagnum mossesa meta analysis New Phytol 191496ndash507 doi101111j1469-8137201103680x

McIlvaine TC 1921 A buffer solution for colorimetric com-parison J Biol Chem 49183ndash186

GRUM-GRZHIMAYLO ET AL DIVERSITY OF MICROFUNGI 253

Nilsson M Ruumllcker C 1992 Seasonal variation of activefungal mycelium in an oligotrophic Sphagnum mirenorthern Sweden Soil Biol Biochem 24795ndash804doi1010160038-0717(92)90255-V

Olunina ES 2008 Bolota poluostrova Kindo I ostrova Velikiy(Kandalakshskiy zaliv Belogo moray) frola sovremen-naya rastitelnost stroenie torfyanoy zalezhi I istoriaformirovaniya Mat XI nauch konf posvyashennoy70-letiu Belomorskoy biologicheskoy stancii imeni NAPertsova Moscow Grif i K p 207ndash212 [In Russian]

Pankratov TA Belova SE Dedysh SN 2005 Evaluationof the phylogenetic diversity of prokaryotic micro-organisms in Sphagnum peat bogs by means offluorescence in situ hybridization (FISH) Micro-biology 74722ndash728 doi1010160038-0717(92)90255-V

Pantiulin AN Krasnonva ED 2011 Otdelyaushiesya vodoemiBelogo moray noviy objekt dlya mezhdisciplinarnihissledovaniy Mat XIX Mezhdunarodnoy nauch konf(shkoli) po morskoy geologii Geologia morey I okeanovMoscow p 241ndash245 [In Russian]

Pivkin MV 2010 Vtorichnie morskie gribi YaponskogoI Okhotskogo morey [doctoral dissertation] MoscowState University 407 p [In Russian]

Rice AV Tsuneda A Currah RS 2006 In vitro decomposi-tion of Sphagnum by some microfungi resembles whiterot of wood FEMS Microbiol Ecol 56372ndash382doi101111j1574-6941200600071x

Romanenko FA 2012 Poslelednikovoe podnyatiye Karels-kogo berega Belogo moray po dannim radiouglerod-nogo i diatomovogo analisa ozerno-bolotnih otlozheniypoluostrova Kindo Russia Dokladi Academii Nauk442544ndash548 [In Russian]

Schulze ED Prokuschkin A Arneth A Knorre N VaganovEA 2002 Net ecosystem productivity and peat accumu-lation in a Siberian Aapa mire Tellus A 54531ndash536

Shaporenko SI Koreneva GA Pantyulin AN Pertsova NM2005 Characteristics of the ecosystems of water bodiesseparating from Kandalaksha Bay of the White Sea WaterResources 32469ndash483 doi101007s11268-005-0060-x

Shilova OS 2011 Golotsenovie diatomei bolot Karelskogopoluostrova i Severo-Vostochnoy Karelii MoscowMAKS Press 177 p [In Russian]

Thormann MN 2006a Diversity and function of fungi inpeatlands a carbon cycling perspective Can J Soil Sci86281ndash293 doi104141S05-082

mdashmdashmdash 2006b The role of fungi in boreal peatlands EcolStud 188101ndash123

mdashmdashmdash Bayley SE Currah RS 2001a The microbial wildcardin peatland carbon storage implications for globalwarming Inf Rep NOR-X 38325ndash28

mdashmdashmdash Currah RS Bayley SE 1999 The mycorrhizal statusof the dominant vegetation along a peatland gradientin southern boreal Alberta Canada Wetlands 19438ndash450 doi101007978-3-540-31913-9_6

mdashmdashmdash mdashmdashmdash mdashmdashmdash 2001b Microfungi isolated fromSphagnum fuscum from a southern boreal bog in AlbertaCanada Bryologist 104548ndash559 doi1016390007-2745(2001)104[0548MIFSFF]20CO2

mdashmdashmdash mdashmdashmdash mdashmdashmdash 2002 The relative ability of fungifrom Sphagnum fuscum to decompose selected carbonsubstrates Can J Microbiol 48204ndash211 doi101139w02-010

mdashmdashmdash mdashmdashmdash mdashmdashmdash 2003 Succession of microfungalassemblages in decomposing peatland plants PlantSoil 250323ndash333 doi101023A1022845604385

mdashmdashmdash Rice AV 2007 Fungi from peatlands Fungal Divers24241ndash299

mdashmdashmdash mdashmdashmdash Beilman DW 2007 Yeasts in peatlands areview of richness and roles in peat decomposition Wet-lands 27761ndash773 doi1016720277-5212(2007)27[761YIPARO]20CO2

Tsuneda A Thormann MN Currah RS 2001 Modes of cell-wall degradation of Sphagnum fuscum by Acremonium cfcurvulum and Oidiodendron maius Can J Bot 7993ndash100

Undient E Muumlller K 1985 Colonization of Sphagnum cells byLyophillum palustre Can J Bot 63757ndash761

Vilgalys R Gonzalez D 1990 Organization of ribosomal DNAin the basidiomycete Thanatephorus praticola Curr Genet18277ndash280 doi101007BF00318394

Wang Z Binder M Schoch CL Johnston PR Spatafora JWHibbett DS 2006 Evolution of helotialen fungi (Leotio-mycetes Pezizomycotina) a nuclear rDNA phylogeny MolPhylogenet Evol 41295ndash312 doi101016jympev200605031

White TJ Bruns T Lee S Taylor JW 1990 Amplificationand direct sequencing of fungal ribosomal RNA genesfor phylogenetics In Innis MA Gelfand DH SninskyJJ White TJ eds PCR protocols a guide to methodsand applications New York Academic Press p315ndash322

Yurkovskaya TK 2004 Raised bogs on the north east of Eur-ope Annali di Botanika nuova serie IV19ndash28

Zak JC Willig MR 2004 Fungal biodiversity patterns InMueller GM Bills GF Foster MS eds Biodiversity offungi inventory and monitoring methods BurlingtonMassachusetts Elsevier Academic Press p 59ndash75

254 MYCOLOGIA