microbial communities in the litter of middle taiga bilberry-spruce forests

ISSN 10642293, Eurasian Soil Science, 2010, Vol. 43, No. 10, pp. 11321139. Pleiades Publishing, Ltd., 2010.Original Russian Text T.A. Sizonenko, S.V. Zagirova, F.M. Khabibullina, 2010, published in Pochvovedenie, 2010, No. 10, pp. 12211228.

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INTRODUCTION

The environmental function of treesedificatorsmanifests itself in their effects on the abovegroundcomponents of forest ecosystems and in their role inthe development of forest soils [5, 24]. The influenceof phytogenic tree fields is seen in the formation of thelight and temperature regimes, the moisture regime,and in the transformation of the quality and quantityof the rainfall passing through the forest canopy [24].It is known that the species composition and population density of the soil microbiota are determined bythe plantsedificators composing the phytocenosis.The number, distribution, and composition of themicroorganisms within and beyond the tree parcels ofthe forest community differ. Some authors noted adecrease in the amount of microbial biomass in theorganic horizon of the spruce parcels in the northerntaiga in comparison with the intercrown space andexplained this by the inhibiting activity of the phenolsand tannins contained in the stem and canopy waterson the microorganisms [21[. The population densityof the microorganisms in the soils of the pine parcelsin the northern taiga increases in the fall, when freshlitter falls onto the soils surface, whereas the population density of the microorganisms within the intercrown space decreases [14].

Our work was aimed at determining the structure ofthe microbial communities in the litters under thespruce crowns and within the intercrown spaces in abilberryspruce middletaiga forest.

OBJECTS AND METHODS

The study was performed in 20052006 in an oldbilberryspruce forest formed on a typical podzolicsoil in the Lyalsk Forest Reserve within the middletaiga subzone (6217N, 5040E). The tree stand consisted of Picea obovata, Abies sibirica, Betula pubescens, and Pinus sylvestris. Its detailed characteristicswere presented earlier [8]. The litter horizon was differentiated into the upper part consisting of weaklydecomposed residues of mosses, needles, and leaves(05 cm, A'O) and the lower part consisting of highlydecomposed plant residues with a thickness of up to1 cm (the A''0 horizon). The A2 horizon of the typicalpodzolic soil represented a compact pale grayishloamy sand. The lower horizons (A2BB1A2B1B2CaCCa) had a loamy texture [8].

Litter samples from the A'0 horizon were taken inthe fall of 2005 at distances of 1, 2, 3, 4, 5, and 6 mfrom the trunk of a selected spruce tree. In 2006, littersamples within the boundary of the tree crown weretaken several times during the growing season. Theaverage radius of the spruce crown was about 2 m.

SOILBIOLOGY

Microbial Communities in the Litter of Middle Taiga BilberrySpruce Forests

T. A. Sizonenko, S. V. Zagirova, and F. M. KhabibullinaInstitute of Biology, Komi Science Center, Ural Division, Russian Academy of Sciences,

ul. Kommunisticheskaya 28, Syktyvkar, 167982 RussiaReceived October 19, 2009

AbstractThe structure of the microbial communities in the litters of middletaiga bilberryspruce forestswas studied. It was found that ammonifying and oligonitrophilic microorganisms predominate in these communities. Two maximums in the population density of the microorganisms were observed in June and August.The number of microorganisms increased in the direction from the spruce trunks to the periphery of thecrowns. The species composition of the micromycetes in the litters under the spruce crowns and within theintercrown spaces differed. The maximum population density of the fungi was found in the litter under theperiphery of the spruce crowns, whereas the maximum diversity of the micromycetes was observed within theintercrown spaces. The Trichoderma, Trichosporiella, Penicillium, Paecilomyces, and Chaetomium generawere most abundant in the litters of the bilberry spruce forests. The Penicillium genus had the maximum abundance during the entire growing period, and the amount of Mycelia sterilia increased in the fall. The maximum diversity of the fungi was observed in May and June.

DOI: 10.1134/S1064229310100066

EURASIAN SOIL SCIENCE Vol. 43 No. 10 2010

MICROBIAL COMMUNITIES IN THE LITTER OF MIDDLE TAIGA 1133

Mixed samples from three replicates were used for theanalysis. Routine microbiological methods of inoculation onto solid nutrient media were used to evaluatethe contents of the ecologicaltrophic groups ofmicroorganisms [4, 12]. Petri dishes were used for theinoculation in triplicate. The number of ammonifyingmicroorganisms was determined on meat infusionagar; the microorganisms assimilating the mineralforms of nitrogen were cultivated on starchandammonia agar; the oligonitrophilic microorganisms,on Ashbys medium; the cellulolytic microorganisms,on Hutchinsons medium; saccharolytic bacteria, onCzapeks medium; and oligocarbophilic bacteria, onWinogradskys medium. The micromycetes werecounted on all the media but mostly on Czapeksmedium. The bacterial growth on Czapeks mediumwas inhibited via adding a 5% solution of lactic acidonto the surface. The species composition of themicromycetes was studied after their isolation intopure cultures according to manuals [1, 6, 10, 16, 2528] with the use of an MBI6 microscope (Russia,LOMO) at magnifications of 12 40 and 12 90. Thestructure of the fungal complex was characterized withthe use of the occurrence frequency parameter,according to which the fungal species were classified

into the dominant species (with a high frequency ofoccurrence), the frequent species, and the rare species; the species with an occurrence frequency of lessthan 30% were qualified as accidental species [11].The species composition of the saprotrophic micromycetes was determined on the basis of the index ofthe relative abundance calculated as the ratio betweenthe content of a particular species and the total number of grown colonies [9]. The statistical treatment ofthe data was performed with the use of MicrosoftExcel 2003 software.

RESULTS AND DISCUSSION

The quantitative analysis of the distribution of thedifferent groups of microorganisms (bacteria, micromycetes, and actinomycetes) showed the predominance of bacteria and the minimum number of actinomycetes in the litters of the bilberry spruce forest.

Two maximums of the population densities of themicroorganisms were observed in June and in August,which could be due to the optimum combination ofthe litter temperature and moisture favoring the development of microorganisms in these periods (Fig. 1). Adecrease in the population density of all the groups of

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Fig. 1. Seasonal dynamics of the microorganisms in the litter at the boundary of the spruce crown (23 m from the trunk):(1) microorganisms assimilating mineral nitrogen, (2) saccharolytic microorganisms, (3) cellulolytic microorganisms,(4) ammonifiers, (5) oligonitrophilic microorganisms, and (6) oligocarbophilic microorganisms. Summarized data on the numbers of bacteria, micromycetes, and actinomycetes are presented.

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SIZONENKO et al.

microorganisms took place in June with a relativelylow moisture content in the litter. The low microbiological activity of the soils in May and the high microbiological activity of the soils in August were alsonoted by other researchers studying bilberrysphagnum spruce forests [19]. As shown in [17], the mostfavorable period for the development of microorganisms is during the active falloff in AugustSeptember.

The maximum population density of the microorganisms was observed within a radius of 13 m fromthe tree trunk under the spruce crown. The maximumcontent of ammonifying and oligonitrophilic microorganisms was found at distances of 12 m from thetrunk. The population densities of the other groups ofmicroorganisms increased at a distance of 3 m fromthe trunk, which could be due to the additional supplyof nutrients with the crown waters (Fig. 2). Accordingto Pristova [15], rainwater passing through sprucecrowns is saturated with various nutrients, including

HC K+, and N (NHN + N

The total number of microorganisms somewhatdecreased at the distance of 45 m from the trunk,though ammonifying, saccharolytic, and oligonitrophilic microorganisms remained the most abundant.A sharp rise in the portion of ammonifying microorganisms was observed at the distance of 6 m from thespruce trunk with the appearance of the leaves of birchin the litter.

In all the samples, the number of ammonifiersexceeded the number of microorganisms assimilatingmineral forms of nitrogen, and this fact points to the

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, H4+ O3

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weakness of the mineralization processes in the litterof the spruce phytocenosis. The coefficient of the littermineralization varied from 5 to 23%, which agreedwith the results obtained by us earlier [23].

The population density of the microorganisms utilizing the mineral forms of nitrogen was low because ofthe permanent excess of ammonia nitrogen in the litter. Oligonitrophilic bacteria fixing molecular nitrogenassimilate a significant amount of organic carbon [20].Thus, a decrease or an increase in the amount oforganic matter affects the activity of these microorganisms. This could be the reason for the maximumamounts of oligonitrophilic and oligocarbophilicmicroorganisms under the spruce crown. Their number decreased at the distance of 3 m, and the numberof bacteria assimilating the mineral forms of nitrogenincreased at the same point, which could be due to theabsence of competition. The number of saccharolyticmicroorganisms also increased within this radius. Thenumber of cellulolytic organisms was minimal at thedistance of 23 m, increased sharply at the distance of4 m, and decreased at greater distances from thespruce trunk because of the influence of other trees.These microorganisms require considerable amountsof mineral nitrogen for cellulose destruction [20],which they could probably obtain in the intercrownspace, because they do not withstand competitionwith other microorganisms assimilating mineral nitrogen under the crown. The amount of saccharolyticmicroorganisms also increased within the intercrown

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Distance from the spruce trunk, m

Fig. 2. Number of microorganisms of different physiological groups in the litter of the bilberry spruce middletaiga forest onOctober 26, 2005. Summarized data on the numbers of bacteria, micromycetes, and actinomycetes are presented. Here and inFig. 3: (1) cellulolytic microorganisms, (2, 3) saccharolytic microorganisms, (4) microorganisms assimilating mineral nitrogen,(5) ammonifiers, (6) oligonitrophilic microorganisms, and (7) oligocarbophilic microorganisms.



space because of the greater input of nutrients from thecrown surface and because of the more favorable conditions due to the lower inhibiting action of phenoliccompounds from the spruce.

The distribution of micromycetes in the litter of thebilberryspruce forest at different distances from thetrunks differs from the distribution of the entire microbial population. The population densities of all thegroups of micromycetes were minimal at the distanceof 1 m from the tree and increased at the boundary of

the spruce crown (Fig. 3). This result agrees with thedata of the other researchers, who noted the dominance of fungal mycelium under spruce parcels incomparison with the intercrown space [13]. Thedecrease in the number of micromycetes at a short distance from the spruce trunk was due to the inhibitingaction of phenolic compounds entering the soil withthe stem flows [21].

Overall, 45 species of micromycetes belonging tothree divisions (Zygomycota, Ascomycota, and

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Fig. 3. Number of micromycetes of different physiological groups at different distances from the spruce trunk.

Trichosporiella15

18

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Cladosporium

Mycelia sterilia

Mucor

Acremonium Cephalosporium

Paecilomyces Fusidium Other

Mortierella Chaetomium

Gliocladium

Penicillium

Trichoderma

Fig. 4. Distribution of micromycetes by genera and their abundances (%) in the litter of the bilberry spruce forest at distances from1 to 6 m from the spruce trunk in October. Averaged data are presented. The group of other micromycetes includes those generawhose abundance was less than 0.1% (Geomyces, Stachybotris, Hormiscium, Pentardum, and Acremoniella).

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SIZONENKO et al. Table 1. The species composition of the micromycetes in the litter of the bilberry spruce forest at different distances fromthe spruce trunks

SpeciesDistance, m

1 2 3 4 5 6

Division Ascomycota Chaetomium globosum Kunz. R R F F R

Division Zygomycota Mucor sp. R R R R

Family Mortierellaceae Mortierella humicola Oudem. R M. longicollis DixonStevart R M. minutissima Tiegh R R R R M. polycephala Coem. F M. verticillata Linnem R R F R Umbelopsis isabellina (Outem.) W. Gams. = M. isabellina Outem. R U. vinaceae (DixonStewart) Arx. = M. vinaceae DixonStewart R R F R

Division Anamorphic fungi Acremoniella sp. R Acremonium sp. R A. charticola (Lindau) Gams = Cephalosporium charticola Lindau R R R A. implicatum (Gilman & Abbott) Gams = Fusidium terricola Mill, Giddens & Foster R A. vitis Catt. R Aureobasidium pullulans (d. By) Arn. PCephalosporium coremioides Raillo R C. humicola Oudem. R Geomyces pannorum Huges R Gliocladium sp. R Paecilomyces farinosus (Holmsk.) Brown et G. Sm. = Penicillium alboaurantium Smith R Paecilomyces variotii Bainier R DPenicillium sp. R P. camemberti Thom R F DP. chrysogenum Thom R P. decumbens Thom F P. decumbens Thom = P. glaucolanosum Chalab. R P. glabrum (Wehmer) Westl. = P. frequtens Westl. R P. griseolum Smith R P. lividum Westl. R R R P. purpurogenum Stoll R P. restrictum Gelman & Abbott = P. kursanovii Chalab. R R F P. roseopurpureum Dierckx R R P. rugulosum Thom, Pitt = P. tardum Thom R F R R R P. Pentardum sp. R Stachybotris alternans Bonord. PTaeniolella stilbospora (Corda) Hughes = Hormiscium stilbosporum (Corda) Sacc. R Thysanophora taxi (Schneid) Stoll & Hennebert = P. taxi Schneid R Trichoderma koningii Oudem. R T. polysporum (Link) Rifai D F F F R Trichosporiella sp. R R

Family Dematiaceae Cladosporium cladosporioides (Fresen) de Vries R C. transchelii Pidopl. et Deniak R

Order Mycelia sterilia Mycelia sterilia (with clamps) R R R R R R Mycelia sterilia (Mucedin.) D F F R R Mycelia sterilia (Dematiac.) R R R R R R Total species 13 15 12 18 21 15 Note: Here and in Table 2, R is the rare species, F is frequent species, and D is the dominant species. Averaged data for the inoculation per

formed on October 26, 2005, on different nutrient media are presented in the table.



Table 2. Seasonal dynamics of the species of micromycetes in the litter at the boundary of the spruce crown

Species 26.10.05 10.05.06 06.06.06 06.07.06 08.08.06 21.09.06

Division Ascomycota

Chaetomium globosum Kunz. R

Division Zygomycota

Mucor sp. R F R

Muc. racemosus f. sphaerosporus (Hagem) Schipper = Muc. globosus Fischer

F R

Family Mortierellaceae

Mortierella humicola Oudem. R

M. turficola Ling. R

M. minutissima Tiegh R

M. verticillata Linnem R F R R

Umbelopsis isabellina (Outem.) W. Gams. = M. isabellina Outem. R R

U. ramanniana (Mller) Gams. = M. ramanniana (Mller) Linnem R F

U. vinaceae (DixonStewart) Arx. = M. vinaceae DixonStewart R R R

Division Anamorphic fungi

Acremonium charticola (Lindau) Gams = Cephalosporium charticola Lindau

R

A. vitis Catt. R

Cilindrocephallum sp. R

Geomyces pannorum Huges R

Gliocladium sp. R

Hypocrea citrina (Pers.) = Fr Trichoderma album Preuss R

Paecilomyces variotii Bainier R

Penicillium sp. 1 R

Penicillium sp. 2 R R

P. canescens Sopp F R

P. decumbens Thom F F R

P. decumbens Thom = P. glaucolanosum Chalab. R

P. implicatum Biourge R

P. jensenii Zalessky = P. godlewski Zalessky F

P. lineatum Raper & Fennell = P. striatum Raper & Fennell R F

P. lividum Westl. R

P. restrictum Gelman & Abbott = P. kursanovii Chalab. R

P. roqueforti Thom R

P. rugulosum Thom, Pitt = P. tardum Thom F

P. spinulosum Thom F R F

P. velutinum Beyma = P. fuscum (Sopp.) Raper, Thom R

Pentardum sp. R

Thysanophora taxi (Schneid) Stoll & Hennebert = P. taxi Schneid R

Trichoderma koningii Oudem. R

T. polysporum (Link) Rifai F

T. viride Pers. = T. lignorum (Tode) Harz R

Trichosporiella sp. R R

Order Mycelia sterilia

Mycelia sterilia (with clamps) R R R R R R

Mycelia sterilia (Mucedin.) F F R R R F

Mycelia sterilia (Dematiac.) R R R R R

Total species 22 14 10 11 10 6

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SIZONENKO et al.

Anamorphic) were isolated from the litter samplesunder the spruce canopy and within the intercrownspace (Table 1). Among them, Paecilomyces variotii,Penicillium camemberti, Trichoderma polysporum, andlightcolored forms of sterile mycelium of Myceliasterilia predominated. The domination of sterile formsof fungi in the northern soils is explained by the loss oftheir capacity to form organs of sexual and asexualreproduction under the influence of low temperatures[3, 7]. The Penicillium and Trichoderma genera aremost typical of northern soils [2, 18, 22]. The greatnumber of representatives of the Penicillium genus isexplained by the diversity of their physiological functions and by their capacity to produce acids and todecompose cellulose and hemicellulose [2].

The following genera had the maximum abundance in the litter of the bilberryspruce forest: Mycelia sterilia, Trichoderma, Trichosporiella, Penicillium,Paecilomyces, and Chaetomium (Fig. 4). The speciescomposition of the micromycetes in the intercrownand undercrown areas had the high similarity index(the SorensenChekanovskii index equaled 52%).The Chaetomium, Mortierella, Mucor, Penicillium, ndTrichoderma genera typical of northern soils werecommon in both areas. The Penicillium, Acremonium,Acremoniella, and Cephalosporium genera reachedtheir maximum diversity in the intercrown area; theabundance of the cellulolytic Chaetomium globosumalso increased in the intercrown area due to the lessercompetition with other microorganisms. The Trichoderma genus was the most abundant under the sprucecrown.

The Penicillium genus had the maximum abundanceduring the entire growing season, and the amount ofMycelia sterilia increased in the fall upon some worseningof the hydrothermic regime in the litter.

Forty species of micromycetes were identified inthe samples taken under the spruce crown (Table 2).The sterile mycelium of Mycelia sterilia predominatedamong them. The list of frequent species includedMucor globosus, Mucor sp., Mortierella verticillata,M. ramanniana, Penicillium canescens, P. decumbens,P. godlewski, P. spinulosum, P. striatum, P. tardum, andTrichoderma polysporum. The number of micromycetal species varied during the growing season with themaximum in May and June. In the fall, the number ofmicromycetes sharply decreased, which could be dueto the lowering of the temperature.

CONCLUSIONS

The uneven distribution of microorganisms in thelitter of the bilberryspruce middletaiga forest wasshown. The physiological groups of ammonifying andoligonitrophilic microorganisms had the maximumpopulation densities. Two maximums of the population densities of the microorganisms were observed inJune and in August, which could be due to the optimalcombination of the litter temperature and moisture forthe development of microorganisms in these periods.The number of microorganisms increased in the direction from the spruce trunk toward the outer boundaryof the spruce crown and decreased in the intercrownspace, which could be caused by the impact of thephytogenic field of the tree. The species compositionof the micromycetes in the litter also differed in theundercrown and intercrown areas.

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microbial communities in the litter of middle taiga bilberry-spruce forests

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