forest soil bacteria: diversity, involvement in ecosystem ...and boreal forests. although most...

Forest Soil Bacteria DiversityInvolvement in Ecosystem Processesand Response to Global Change

Salvador Lladoacute Rubeacuten Loacutepez-Mondeacutejar Petr BaldrianLaboratory of Environmental Microbiology Institute of Microbiology of the CAS Vestec Czech Republic

SUMMARY 1INTRODUCTION 2BACTERIAL COMMUNITIES IN FOREST ECOSYSTEMS 4

Bacterial Communities on Plant Litter and Deadwood 4Bacteria in Forest Soils 7Rhizosphere Bacterial Communities 8

BACTERIAL INVOLVEMENT IN ECOSYSTEM PROCESSES 9Role of Bacteria in the Carbon Cycle 9Role of Bacteria in Nitrogen and Phosphorus Cycles 12

EFFECTS OF GLOBAL CHANGE ON BACTERIAL COMMUNITIES IN FORESTECOSYSTEMS 13

Carbon Dioxide 14Global Warming 14Nitrogen Deposition 17

CONCLUSIONS 18ACKNOWLEDGMENTS 19REFERENCES 19AUTHOR BIOS 27

SUMMARY The ecology of forest soils is an important field of research due tothe role of forests as carbon sinks Consequently a significant amount of infor-mation has been accumulated concerning their ecology especially for temperateand boreal forests Although most studies have focused on fungi forest soil bac-teria also play important roles in this environment In forest soils bacteria in-habit multiple habitats with specific properties including bulk soil rhizospherelitter and deadwood habitats where their communities are shaped by nutrientavailability and biotic interactions Bacteria contribute to a range of essential soilprocesses involved in the cycling of carbon nitrogen and phosphorus They takepart in the decomposition of dead plant biomass and are highly important forthe decomposition of dead fungal mycelia In rhizospheres of forest trees bacte-ria interact with plant roots and mycorrhizal fungi as commensalists or mycor-rhiza helpers Bacteria also mediate multiple critical steps in the nitrogen cycleincluding N fixation Bacterial communities in forest soils respond to the effectsof global change such as climate warming increased levels of carbon dioxide oranthropogenic nitrogen deposition This response however often reflects thespecificities of each studied forest ecosystem and it is still impossible to fully in-corporate bacteria into predictive models The understanding of bacterial ecol-ogy in forest soils has advanced dramatically in recent years but it is still incom-plete The exact extent of the contribution of bacteria to forest ecosystemprocesses will be recognized only in the future when the activities of all soilcommunity members are studied simultaneously

KEYWORDS bacteria decomposition ecosystem processes forest ecology globalchange litter nutrient cycling soil

Published 12 April 2017

Citation Lladoacute S Loacutepez-Mondeacutejar R Baldrian P2017 Forest soil bacteria diversityinvolvement in ecosystem processes andresponse to global change Microbiol Mol BiolRev 81e00063-16 httpsdoiorg101128MMBR00063-16

Copyright copy 2017 American Society forMicrobiology All Rights Reserved

Address correspondence to Petr Baldrianbaldrianbiomedcascz

SL and RL-M contributed equally to thisarticle

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INTRODUCTION

Forests represent one of the largest and most important ecosystems on Earthcovering more than 40 million km2 and representing 30 of the total global land

area (1) Forest ecosystems are found in most of Earthrsquos biomes and harbor a largeproportion of the global diversity For example temperate and boreal forests occupymost of the land surface of the Northern Hemisphere and contain 46 of all trees onEarthmdash 066 and 074 trillion respectively (2) Due to their global extension theprocesses occurring in these two biomes are of global importance and an understand-ing of the composition and function of their microbiomes is thus essential (Fig 1)

Forests typically represent important carbon (C) sinks with large amounts of recal-citrant organic matter in their soils especially the temperate forest soils which receivetons of litter per hectare yearly (3) The presence of large trees distinguishes forestsfrom grasslands wetlands and agricultural areas in multiple ways (4) Trees representa multitude of habitats such as the phyllosphere or rhizosphere but they also sub-stantially affect the remaining parts of the ecosystem This is mainly because as thedominant primary producers they supply the bulk of the C that enters the ecosystemand while some of this C is in the form of simple organic molecules a significantfraction such as the complex biomass of wood litter or roots is composed ofrecalcitrant biopolymers (4) Trees also largely contribute to the spatial heterogeneity offorest ecosystems by multiple means including the penetration of soils by variousguilds of roots generation of patches of litter and ground vegetation and changes ofthe morphology of the terrain during uprooting or the production of deadwood (4 5)

Temperate forests extend approximately from latitudes 25degN to 50degN graduallychanging into boreal forests further north (6) The southern limit of boreal forests isunderstood as the latitude at which conifers are competitively excluded by temperatetree species with higher rates of photosynthesis There is however no distinct bound-ary between the two biomes but rather a broad transition zone that includes a mix ofconiferous and deciduous tree species (7) Temperate forests are characterized bytemperature ranges between 30 and 30degC with hot summers and cold winters andwith 750 to 1300 mm of precipitation per year Boreal forestsmdash or mountainous forestsin the temperate zonemdashface lower temperatures with cold winters lasting more than6 months and average summer temperatures of around 10degC Despite the lowerprecipitation levels (300 to 900 mm of rain per year) boreal forests are typically moistbecause of the reduced evaporation at low temperatures In addition other factorssuch as elevation substrate drainage physical soil properties and nutrient availabilityare also responsible for the distribution of forest types on landscape scales

Temperate forests are composed of a large variety of deciduous trees whileconiferous trees dominate temperate forests at higher altitudes but also occur fre-quently in plantation forests (8 9) Boreal forests exhibit a reduced tree diversity witha larger proportion of coniferous trees (10)

Although temperate and boreal forests fulfill several important ecosystem servicestheir role as large C sinks has gained specific interest in recent decades especially in thecontext of global change Recent approximations indicate that the current C stockstored in forests worldwide is approximately 861 Pg of which 44 is in soil 42 inabove- and belowground biomass 8 in deadwood and 5 in litter (11) Of the globalstock of C stored by forests boreal forests contain 32 and temperate forests another14 indicating that their importance for global C sequestration is equivalent to that oftropical forests (11) The large amount of stored C has the potential to influence thefeedback between the climate and the global C cycle (12) In this sense global changeincluding both climate change and other changes linked to human activities has beenrecognized as a major threat to forests (13) Over the millennia human overexploitationhas been the most important risk for forests and the C balance of forests is largelyaffected by human activities including deforestation the management of productionforest reforestation afforestation and others (11 14) Other disturbances that areassociated with climate change and atmospheric drivers are also affecting the C

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balance of forests In this sense the effects of increasing temperature persistence ofdroughts recurrence of fires or expansion of native and invasive forest pests togetherwith the increasing loads of nitrogen (N) and carbon dioxide affect forest nutrient cyclesto a level where forests may potentially become net sources rather than sinks of CO2

(12 13 15) Therefore a better understanding of the role of forests in C fluxes that arelargely dependent on the activity of bacteria and fungi has been highlighted as anessential prerequisite for projecting future predictions of the health of our planet (16)

While plants are the key drivers of C uptake from the atmosphere in forests forestmicroorganisms contribute greatly to the C balance in these ecosystems They play animportant role as decomposers symbionts or pathogens influencing the C turnoverand retention and the availability of other nutrients (17ndash19) Microbial communities arevital in mediating the biogeochemical cycles and an understanding of their role inecosystem processes is essential for the prediction of the forest response to futureenvironmental conditions (8 17 20)

Fungi are the most well-studied microbes in temperate and boreal forest soils thatharbor abundant and diverse communities of saprotrophic and mycorrhizal fungal taxa(12 21 22) Fungi are considered the main decomposers in forest soils because of theirability to produce a wide range of extracellular enzymes that allow them to efficientlydegrade the recalcitrant fraction of dead plant biomass (23ndash25) Moreover mycorrhizalfungi play a pivotal role in the mobilization and sequestration of N and P in the forestsoil and are also responsible for significant soil transport of C (26ndash29) It is not surprisingthat most of the research on forest soil ecology so far has focused on fungi (18 19) Thistraditional emphasis on fungi however is slowly shifting with an increasing appreci-ation of the role of bacteria as the other major component of forest ecosystems (19)

Bacteria represent another important though less explored integral part of themicrobial community in forest soils For example recent findings indicate that bacteriacommonly harbor genes encoding plant cell wall-degrading enzymes (30) and contrib-

FIG 1 Distribution of temperate and boreal forests in the Northern Hemisphere Natural areas of deciduous and mixed temperate forest (light green) andevergreen coniferous forest (dark green) are shown in green and natural areas occupied by boreal forests are shown in blue The regions in which microbialcommunities inhabiting soil have been studied are shown as dots The bottom images show forest ecosystems dominated by Quercus Pinus Fagus and Piceatrees

Forest Soil Bacteria Diversity and Function Microbiology and Molecular Biology Reviews



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ute significantly to the decomposition of organic matter (31ndash35) In addition bacteriaare the major natural agents responsible for N fixation in forest ecosystems (36) and forother ecosystem processes such as mineral weathering leading to the release ofinorganic nutrients (37) The roles of bacteria and fungi however should not be viewedas separate The high abundance of fungal biomass in forest soils has multiple conse-quences for bacteria including the creation of specific niches in the soil patchescolonized by mycorrhizal fungi (ie the mycorrhizosphere) and soil mycelial mats (3839) provision of nutrients via organic matter decomposition (40) and an increase in soilconnectivity by fungal mycelia that allow certain bacteria to move across the environ-ment (41) Conversely the functioning of mycorrhiza is modulated by mycorrhizahelper bacteria (MHB) (42)

It is only recently that advances in analytical methods have allowed us to assess therole of bacteria in the complex forest ecosystem and to address the important ques-tions that previously remained unanswered such as the following Which habitats dobacteria inhabit and what are the major drivers of their abundance and diversity Whatis their role in nutrient cycling and the C balance How do they interact with otherforest organisms How do they respond to climate change and how does this responseaffect ecosystem processes The aim of this review is to answer these questions fortemperate and boreal forests to summarize the present knowledge about the role ofbacteria in ecosystem processes and about their response to global change as well asto motivate further research in the bacterial ecology of forests

BACTERIAL COMMUNITIES IN FOREST ECOSYSTEMS

Forest ecosystems provide a broad range of habitats for bacteria including soil andplant tissues and surfaces streams and rocks among others but bacteria seem to beespecially abundant on the forest floor in soil and litter (4) Five phyla AcidobacteriaActinobacteria Proteobacteria Bacteroidetes and Firmicutes appear to be abundant inmost soils (43) In addition to pH which seems to be the most important driver of thebacterial community composition in soils organic matter content nutrient availabilityclimate conditions and biotic interactions (especially the effect of vegetation) affect thecomposition of bacterial communities (43ndash47) The spatial variation of these parametersis responsible for the presence of hot spots of microbial activity with increasedabundance and activity in the soil such as in and on plant debris including litter anddeadwood or on and around plant roots (48ndash50) Each of these niches has specificproperties and consequently a specific bacterial community (Fig 2)

Bacterial Communities on Plant Litter and Deadwood

Due to the activity of primary producers dead plant biomassmdashlitter and dead-woodmdashrepresents the most important C sources for forest soil microbes The estimated1011 tons of fallen leaf litter that accumulates yearly on the forest floor surface and itstransformation are of great importance for the cycling of C and other nutrients (51ndash53)The litter habitat is dominated by a diverse community of fungi that have traditionallybeen considered to be key players in litter decomposition In addition to fungi recentstudies have demonstrated an active role of bacteria in litter transformation In the litterof coniferous forests bacteria incorporated relatively more cellulose-derived C thanthat incorporated by fungi (31) Cellulose-C was accumulated mainly by Betaproteo-bacteria Bacteroidetes and Acidobacteria Similar results were found in different pineforest soils in North America where members of the Proteobacteria (BurkholderialesCaulobacteriales Rhizobiales and Xanthomonadales) Bacteroidetes (Sphingobacteriales)and subdivision 1 Acidobacteria accumulated the most cellulose-derived C (32) Re-cently studies of deciduous forests reported that at least 10 of litter bacteria are ableto decompose cellulose Many of these bacteria belong to the Proteobacteria Actino-bacteria Bacteroidetes and Acidobacteria but members of other phyla are also active(33 54) Considering the frequency of cellulolytic genes in bacterial genomes (30)bacterial involvement in decomposition seems to be a relatively common trait




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While the acidic soils of coniferous forests harbor mainly Proteobacteria Acidobac-teria and Actinobacteria (8 55) in temperate deciduous forests litter bacterial com-munities seem to be especially enriched with Proteobacteria and Bacteroidetes (45 5657) Indeed significant differences in the chemical structure of litter and root exudatesamong tree species influence soil bacterial communities through changes in substratechemistry (45 58 59) Litter quality which includes the quantity of nutrients tissuestructure and the CN ratio varies between tree species and results in varying litterdecomposability (60ndash62) Higher litter quality is typically associated with faster litterturnover and the liberation of exchangeable basic cations such as Ca2 and Mg2helping to maintain low levels of soil acidification (63ndash65) When trees typical oftemperate and boreal forests were ranked in order of increasing acidification ability oftheir litter conifers appeared to be the most acidifying followed by beech oak andbirch Maple hornbeam ash and lime comprised the group with the least acidifyingforest trees (59) These effects of litter quality on soil nutrient status and pH indirectlydrive the bacterial community composition of forest soils and its activity (66ndash68)

The production of litter is not constant throughout the year it is limited to a shortautumnal period in deciduous forests These and other aspects of seasonality in thetemperate and boreal zones have been identified as key factors affecting the C inputinto the soil environment and its decomposition by soil bacteria Cold and dark wintersand warm summers with longer photoperiods affect the development and production

FIG 2 Drivers of bacterial community composition in forest soils and features of bacterial ecology in the rhizospherelitterdeadwood and soil compartments of the forest floor




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of foliage and consequently microbial community structure and activity in the litterand soil as well as in the foliage (69) Temperature differences affect decompositionrates by accelerating or decelerating enzymatic processes (55 70) On a shorter timescale selected weather events such as precipitation or snowmelt contribute to themobilization of nutrients that are washed into the forest soil and they representperiods of high microbial activity especially of fast-growing r-strategists (50)

During decomposition the chemical composition of litter changes with the gradualremoval of cellulose hemicellulose and lignin (58 71) In contrast to fungi bacteriainhabiting the phyllosphere of living leaves do not seem to be largely involved in litterdecomposition and are quickly replaced by other taxa (72) Proteobacteria and Bacte-roidetes are considered to be copiotrophs that preferentially consume the labile pool oforganic C (73) and are thus typical for freshly fallen litter The fresh litter is alsocharacterized by the quantitative dominance of fungi The biomass of bacteria in-creases gradually during decomposition (58 74) as does their diversity (57 72) Duringdecomposition the abundance of mycophagous bacteria coincides with the peak offungal biomass in the fresh litter In this stage of decomposition potentially mycolyticbacteria in Quercus litter represent as much as 40 of the total community (72)highlighting the importance of the fungal biomass as a nutrient source Bacterial taxathat associate with decomposing fungal mycelia represent a distinct subset of thebacterial community including members of the genera Pedobacter and Chitinophaga(Bacteroidetes) and Pseudomonas Variovorax Ewingella and Stenotrophomonas (Proteo-bacteria) (75) With ongoing litter decomposition the share of cellulolytic bacteriagradually increases (72)

Importantly a large proportion of plant inputs into forest soils are derived from organsother than leaves including fine roots seeds and twigs (76) While it has been shown thatthis type of litter represents an important source of soil organic matter (SOM) C (52 77)bacterial communities associated with this substrate remain unexplored

In addition to litter coarse deadwood is also an important structural component offorest ecosystems especially in unmanaged forests Wood debris represents a rich yetrecalcitrant source of organic matter mainly due to its physical impermeability andhigh lignin content These characteristics benefit filamentous macroscopic fungi (78)which are consequently the dominant decomposers of deadwood However bacteriaare also important inhabitants of decaying wood especially during the initial phases ofdecay (79 80) The physicochemical properties of wood that are tree specific such asthe density pH and water and N content determine the composition of bacterialcommunities (80 81) Proteobacteria Acidobacteria Actinobacteria and Firmicutes be-long to the most abundant phyla (79 80 82) Because fungal decomposition changesthe properties of wood substantially via the removal of easily available C acidificationand the production of fungal mycelia bacteria that can thrive at an acidic pH and utilizeC from fungal mycelia are positively selected (80 83 84) As observed for litterdecomposition the bacterial community in deadwood shows successional develop-ment with wood decay The assembly of the bacterial community appears to be astochastic process during the initial stage of wood decay and the bacterial abundancein fresh wood is very low with 02 109 16S rRNA copies g1 During decompositionthe bacterial abundance increases reaching levels as high as 3 109 to 13 109 16SrRNA copies g1 in highly decayed Picea abies wood with a density of 015 g cm3 (80)While the involvement of wood-associated bacteria in wood biopolymer decomposi-tion versus the use of substrates liberated by fungal decay remains largely unexploredrecent studies support a role for bacteria in other important processes including thedegradation of toxic wood compounds and N fixation Genera such as BurkholderiaPhenylobacterium and Methylovirgula which are abundant in the middle and latestages of wood decomposition are known to degrade aromatic compounds and to usemethanol as a sole carbon source (79 82) Moreover the N-fixation ability of bacteriathat are abundant during the late stages of wood decomposition (such as the membersof the Rhizobiales which may account for 25 of all bacteria in this phase) offers thepossibility of mutualistic interactions with fungi that provide C via wood decomposition




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(82) Despite these initial studies little is still known about the community dynamics ofwood-inhabiting bacteria or their interactions with wood-decaying fungi (81) Consid-ering that multiple bacteria are able to utilize cellulose and other recalcitrant plantpolymers and that the fungal biomass is highly abundant in deadwood the involve-ment of bacteria in the decomposition of lignocellulose and fungal mycelia appears tobe highly probable

Bacteria in Forest Soils

Forest soils are among the most diverse microbial habitats on Earth in whichbacteria are the most abundant group of microorganisms (4 85) Forest soils arecharacterized by a sharp vertical stratification resulting from the decomposition oflitter-derived organic matter and the weathering of the mineral matrix The decreasingcontent and quality of organic matter with soil depth are accompanied by decreases inmicrobial biomass respiration and activity of extracellular enzymes For example in aQuercus petraea forest soil organic matter decreased 10-fold bacterial biomass 8-foldand enzyme activity 5-fold to 20-fold across the top 5 cm of the soil profile (86) Thetemperate forest soil profile typically comprises the organic horizon representing amixture of processed plant-derived organic matter and soil components and themineral soil horizon with a lower content of organic matter originating from both thedecomposition of organic matter and exudation from abundant tree roots The bacte-rial communities are horizon specific although they display a high level of taxonoverlap (56) For example the organic and mineral horizons in a temperate Quercusforest are dominated by Acidobacteria (accounting for 40 to 50 of all sequences)together with members of the Actinobacteria Proteobacteria and Bacteroidetes (56)Bacterial communities in coniferous forest soils also differ among horizons AlthoughAcidobacteria Proteobacteria and Actinobacteria are most abundant in organic as wellas mineral horizons the organic horizon is richer in Proteobacteria and Bacteroidetes (887) which have been proposed to preferentially utilize easily accessible carbon sub-strates (73 88) In contrast communities in the mineral soil harbor a larger proportionof Firmicutes and Chlorofexi organisms that are more adapted to the use of recalcitrantcarbon substrates and inorganic nutrients

The high abundance of Acidobacteria Actinobacteria and Proteobacteria acrossforest soils (87 89ndash92) appears to indicate their functional importance These threephyla also dominated the active fraction of a P abies soil comprising 80 to 90 ofrRNA molecules and were responsible for the bulk of bacterial transcription (8 55)

The soil bacterial community composition has been shown to display biogeograph-ical patterns on a continental scale that are predictable but differ from the well-studiedplant and animal community patterns (44) The first comprehensive study indicatedthat the soil pH is the most important driver of the bacterial community compositionand this observation was confirmed in multiple studies that focused specifically onforest soils (43 93ndash97) Whereas Acidobacteria and Alphaproteobacteria are abundant inacidic soils (8 96 98 99) the abundances of Bacteroidetes and Actinobacteria increasewith a rising pH (43 94 100)

The preference of bacterial taxa for niches with certain nutrient contents andorganic matter quality is indicative of their ecological strategy The abundance ofAcidobacteria was initially negatively correlated with the C availability in soils corrob-orating the idea that Acidobacteria are slow-growing oligotrophs that have adapted toresource limitations (73 101 102) However the present results show that members ofthe Acidobacteria inhabit soils across a wide range of C contents representing onaverage 20 of all bacteria their abundance may exceed 60 in acidic forest soilswhere both the content of organic matter and the allocation of C by tree roots are high(43 103) Acidobacteria show a high level of metabolic versatility that allows them todecompose complex C substrates derived from the recalcitrant SOM pool (69 101)Recently subdivision 1 Acidobacteria from acidic coniferous forest soil were demon-strated to utilize C from cellulose and to produce high titers of extracellular enzymes(31 104) indicating their involvement in decomposition in these soils Unfortunately




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due to their limited culturability little is known about the ecophysiology of othersubdivisions of Acidobacteria and the Planctomycetes except that they are common inforest soils (105 106) Verrucomicrobia which are also abundant in forest soils (56 107108) show an increased abundance with soil depth (109) but it is unclear whether thisis due to their preference for the oligotrophic environment or to the occupation ofspecific microniches Members of the phylum Bacteroidetes such as the genus Muci-laginibacter which are common in forest soils have been shown to be potent decom-posers of cellulose and other biopolymers (31 33 104)

Importantly some soil bacteria are involved in the weathering of minerals a processof great importance in nutrient-poor soils where minerals represent an important poolof inorganic nutrients (37 110) Members of the Betaproteobacteria such as the generaBurkholderia and Collimonas have been recognized as efficient mineral-weatheringbacteria These taxa are common in both deciduous and coniferous forest soils (31 56106 108 110ndash112)

For linking of the presence of bacteria or their activity to soil properties it isimportant that soil is a complex of microniches with heterogeneous physicochemicalproperties on various scales Because bacteria inhabit small niches the properties oftheir immediate environment rather than the mean soil properties affect the localbacterial community This spatial heterogeneity has been shown to result in theheterogeneity of bacterial communities on small scales of 1 cm (113) Furthermorelocal dispersal limitations can also remarkably influence the bacterial communitycomposition (93 114) Considering the high level of spatial variation of forest C stockson the same scale (115) the occurrence of individual taxa in forest soil may actually behighly variable on a small scale and may differ among activity hot spots such as therhizosphere and the bulk soil (49 50) The transient nature of some physicochemicalfactors such as soil moisture can strongly influence the physical connectivity of the soilmatrix affecting bacterial and nutrient dispersion and as a consequence rates of keysoil processes (116ndash118) Our ability to define and identify activity hot spots and toanalyze their properties as well as the abundance composition and function of theirbacterial inhabitants will be critical in future analyses to increase our mechanisticunderstanding of the roles of bacteria in biogeochemical processes

Rhizosphere Bacterial Communities

In temperate and boreal forests most C enters the soil food web via the roots in theform of labile C compounds such as sugars amino acids and organic acids (119 120)with approximately one-third of the plant net primary production (NPP) allocated toroots and soil (121) Indeed root exudation water and nutrient uptake by roots decayrespiration and physicochemical changes in soil are important factors influencing thecomposition and function of the microbial community in the rhizosphere with bio-geochemical consequences for the entire soils (46 122)

The roots and rhizospheres of trees as well as ground vegetation associate withfungi to form mycorrhiza While the ground vegetation mostly forms a symbioticrelationship with arbuscular mycorrhizal (AM) or ericoid mycorrhizal (ErM) fungi (29)more than 90 of forest trees in temperate and boreal zones participate in ectomy-corrhizal (ECM) symbiosis and only a minority of trees associate with AM (123) ThusECM is the quantitatively most prevalent and explored mycorrhizal type in forests (124)ECM fungi form mantels around tree root tips and their mycelia extend into surround-ing soils that are used to provide mineral nutrients to their hosts (62 124 125) Fungalassociations of AM with trees are much less common and are confined to a few treespecies (38) Due to the large absorptive area and exudation of labile compounds byECM hyphae the mycorrhizosphere and mycosphere represent important niches withfeatures that differ from the nonmycorrhizal rhizosphere and bulk soil hosting differentbacterial communities (62 126 127) The exudation of labile C by tree roots ormycorrhizal hyphae enhances the availability of C in the rhizosphere and consequentlythe microbial abundance and activity of extracellular enzymes in comparison to thosein the bulk soil (128ndash131) The input of labile C compounds into the rhizosphere selects




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for bacterial strains with rapid growth and low-affinity substrate enzymes (r-strategists)that are enriched in comparison to the bulk soil profile (73 132) The quantity andquality of exudates select for specific microbial communities and the expression ofspecific genes and may prime the decomposition of recalcitrant organic matter (133134) Considering the seasonal changes in NPP seasonality is a major driver of microbialcommunity composition and functioning in the rhizosphere (135)

Despite the importance of the associated ecological processes bacterial communi-ties inhabiting rhizospheres in forests have been explored much less than those fromgrasslands or agricultural systems Recent studies from nonforest environments such asgrasslands (136 137) croplands (138ndash140) and other ecosystems (134 141ndash143)concluded that the rhizosphere contains a certain subset of the bulk soil microbiomewhich is enriched in members of the Proteobacteria Actinobacteria and Bacteroidetes(136 140 142 143) The dominance of Alphaproteobacteria Betaproteobacteria Actino-bacteria and Bacteroidetes was also observed in the rhizospheres of beeches in amountainous forest (144) These observations suggest the enrichment of copiotrophicbacterial taxa (73 138 145)

The microbiomes surrounding the ECM roots and hyphae also differ from those in bulksoil (106 127 136) An enrichment of Proteobacteria (eg Burkholderia Rhizobium andPseudomonas) and Actinobacteria (such as Streptomyces) in the mycorrhizosphere wasreported based on culture-dependent studies (41 124 146ndash148) A recent molecular studyof Pinus sylvestris mycorrhizospheres indicated that the community composition is muchmore complex and includes both copiotrophic and oligotrophic bacteria (149)

Various roles ranging from mycorrhiza helpers to mycophages have been assignedto the ECM-associated bacteria (124) The mycorrhiza helper bacteria (MHB) isolatedfrom the mycorrhizospheres of different ECM symbionts either enhance the formationof mycorrhiza or support the previously established symbiosis (126 150 151) In themycorrhizosphere plants ECM fungi and bacteria form tripartite associations in whicheach player critically affects the metabolism of the others It has been proposed thatECM fungi select for bacterial communities through the exudation of low-molecular-weight compounds such as organic acids and amino acids (116 152) Different ECMfungi in a similar environment can host very similar bacterial communities that aresuited for this niche (146) MHB influence both ECM fungi and their plant host Forexample MHB from the genera Pseudomonas and Streptomyces promote mycorrhizaformation by modifying the gene expression of the ECM leading to acceleratedmycelial growth and stimulating the formation of new lateral roots (92 150 153)Rhizosphere bacteria also provide additional benefits to plants For example StreptomycesAcH 505 is an antagonist of plant pathogens and can induce defense mechanisms in Pabies and Quercus robur (125 154 155) Other very-well-known bacteria promoting plantvigor are endophytes such as the members of the genus Rhizobium which form noduleson the roots of Alnus plants fix gaseous N and provide it to their host

BACTERIAL INVOLVEMENT IN ECOSYSTEM PROCESSESRole of Bacteria in the Carbon Cycle

Forest soils store two-thirds of the terrestrial C (156) The flux of C is initiated by thefixation of atmospheric CO2 by photosynthesis and mediated by the allocation ofrecalcitrant and simple organic compounds into the soil (Fig 3) When plant debris andsimple organic compounds are decomposed and used by microorganisms to build theirbiomass some C is returned to the atmosphere via respiration Because root exudatescan readily be assimilated by soil microorganisms decomposition of the dead plantbiomass has been highlighted as the key process regulating C flow in soil systems thatinfluences the ratio between C mineralization and immobilization (156)

Recent studies indicated that bacteria play a more important role in the transfor-mation of the dead plant biomass than was previously assumed and significantlycontribute to decomposition processes in litter and soil (31ndash33) The plant biomass iscomposed largely of lignocellulose a highly organized and interlinked mix of differentpolymers that contains various amounts of cellulose hemicelluloses and lignin (157)




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Because of the presence of hemicelluloses in a recalcitrant complex with lignincellulose represents the most accessible biopolymer and its degradation is thus akey step in the C cycle The most important enzymes involved in this process areendocellulases exocellulases and -glucosidases Together with these enzymes adiverse set of hemicellulases such as endoxylanases xylosidases xyloglucanasesendomannanases mannosidases fucosidases arabinosidases pectinases and ligni-nolytic enzymes are necessary for the hydrolysis of other polymers that are present inthe plant biomass (158) The genes encoding cellulases are present in 24 of allsequenced bacterial genomes (159) and glycosyl hydrolases that degrade other plantstructural biopolymers are also common (30) Recently Loacutepez-Mondeacutejar et al (33)isolated cellulolytic bacteria belonging to a variety of phyla from a deciduous foresttopsoil and they demonstrated for the first time the presence of cellulolytic membersamong some abundant soil genera eg Mucilaginibacter Luteibacter and PedobacterOther studies highlight the important ecological role of strains of the phyla Acidobac-teria and Actinobacteria as degraders of plant biomass polysaccharides in the acidicsoils of temperate forests (31 104 160)

Genomes of several forest soil bacteria encode proteins involved in decompositionof dead plant biomass (33 161ndash163) In addition to promotion by hydrolytic enzymesefficient hydrolysis is often promoted by the presence of carbohydrate-binding mod-ules (CBM) that are part of either the enzymes or bacterial cell surfaces (157) Genescoding for proteins that are involved in signal transduction nutrient binding andtransport are often found in the same operons as hydrolase genes Some of theseproteins such as the TonB-dependent receptors have been established as plantcarbohydrate scavengers (164) Other auxiliary proteins such as the substrate-bindingproteins (SBPs) from ATP-binding cassette (ABC) transporters have been shown to becapable of binding a variety of plant cell wall soluble and insoluble saccharidesincluding microcrystalline or amorphous cellulose xyloglucan xylan and mannan(165) The rich suite of these auxiliary proteins expressed by a Paenibacillus sp strainfrom a temperate forest soil suggests their important involvement in polysaccharide

FIG 3 Schematic view of the coupled biogeochemical cycles of carbon nitrogen and phosphorus in forest ecosystemsColored arrows show the transfer of elements (C in orange N in green and P in blue) between ecosystem compartmentsEcological processes with the active involvement of bacteria are highlighted in bold




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decomposition (162) A suite of carbohydrate-binding proteins such as type IV pili andan atypical oxidative cellulase in a cellulolytic Luteibacter species from temperate forestsoil demonstrates the variability among the cellulolytic systems of bacteria whichremain far from being completely described (33 166 167) Since plant biomassrepresents a renewable and abundant resource for the production of environmentallyfriendly chemicals and biofuels (168) forest topsoils represent a rich potential source ofbacterial strains with biotechnological relevance (169 170)

Soil bacteria are also able to contribute to the breakdown of phenolic compoundsincluding lignin although their efficiency is typically much lower than that of fungi (34160) Ligninolytic bacteria can be found among the Proteobacteria (genera such asSphingomonas Burkholderia Enterobacter Ochrobacterium and Pseudomonas amongothers) Firmicutes (Bacillus and Paenibacillus) and Actinobacteria (Rhodococcus Myco-bacterium Microbacterium and Streptomyces) (35 171) and there is evidence thatpotentially ligninolytic taxa are common in soils For example abundant bacteriallaccase genes have been found in temperate hardwood forests (172) and bacterial taxapossessing laccases such as Burkholderia Bradyrhizobium and Azospirillum are highlyactive in forest soils (173) However even if the enzymology of bacterial lignin degra-dation is poorly understood compared to that for fungi bacteria may use ligninolyticperoxidases and laccases to reduce the toxicity of phenolic compounds rather than todegrade lignin

In addition to plant biomass fungal mycelia represent an important pool of organicmatter in forest litter and soil (174) Forest ecosystems are dominated by ectomycor-rhizal fungi (ECM) with a biomass of up to 600 kg ha1 (147 151) and the annualproduction of fungal mycelia in a spruce forest ranges from 100 to 300 kg ha1 (77)Fungal mycelia represent a large C and N pool that typically contains chitin and otherpolysaccharides such as glucans and glucomannans as well as phenolics such asmelanin (75 175) Fungal biomass represents a more readily decomposable substratethan lignocellulose and bacteria have been reported to be more important contribu-tors than fungi to its decomposition (75 176) The bacteria associated with fungalbiomass decomposition represent a specific subset of the litter and soil communitiesdominated by Pseudomonas Ewingella Pedobacter Variovorax Stenotrophomonas andChitinophaga genera that are known to produce chitinolytic enzymes (75) Chitinolyticenzymes which are represented by chitinases and N-acetylglucosaminidases appear tobe widespread in bacterial genomes especially Actinobacteria (30 177) The membersof this phylum often contain several chitinase genes as well as a diverse array ofcorresponding CBMs and they often also possess -13-glucanases thus encompassinga complex set of enzymes that potentially target fungal cell walls (178) Chitinaseproduction by soil bacteria is a complex adaptation that combines a nutritional strategywith potential involvement in the antagonistic interactions with fungi (178 179)Although the bacterial biomass in forest soils has a size similar to that of fungi (55) theprocess of bacterial cell wall polymer decomposition is far less understood Theinvolvement of Planctomycetes Verrucomicrobia Armatinomonadetes or candidate di-vision OD1 in the degradation of bacterial exopolysaccharides produced in soil wasrecently demonstrated (180)

Finally a large fraction of C in forest ecosystems is allocated belowground duringthe vegetation period via tree roots in the form of root exudates (181 182) Up to 40of newly photosynthesized C can be allocated to the soil via roots where it is rapidlyrespired or incorporated into the microbial biomass (183 184) The rhizosphereincluding the root-associated mycelia of mycorrhizal fungi is thus probably the mostimportant C allocation hot spot in forest soils and is strongly influenced by plant activity(185) Because ECM fungi cover most of the fine roots and root tips the largest fractionof this C is allocated to them (186) The fraction of assimilates that is exuded directlyfrom roots into the rhizosphere is estimated to range from 1 to 5 and is composedmainly of carbohydrates amino acids and organic acids (120 187) The rhizodepositionof C by plants exhibits severalfold seasonal differences that correspond to the intensityof photosynthesis throughout the year (182) While direct evidence of a net C flux from




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plants to rhizosphere microbiota has been shown for many crops little is known aboutthe structure and function of bacterial and fungal communities that are activelyinvolved in the assimilation of root exudates in forest ecosystems (188) Althoughdecomposer fungi can find suitable conditions in the nonmycorrhizal rhizospheres oftrees this niche has traditionally been considered bacterium dominated because theirrapid growth favors their utilization of root exudates (185) Recent studies indicatedthat soil bacteria indeed use root exudates in forest soils (189) and the seasonalproduction of root exudates leads to an increase in bacterial biomass as well as in theshare of the rhizosphere- and mycorrhizosphere-specific bacteria in mineral soil insummer (56 70) In the same way as that of tree roots hyphae of ectomycorrhizal fungiexude low-molecular-weight organic compounds that support diverse bacterial com-munities (78 190) The rhizosphere of roots colonized by mycorrhizal fungi is specificin that a portion of the plant-derived C is released into the soil through the ECMmycelium (155) As a consequence ECM fungi constitute a nutrient hot spot for othermicroorganisms because the fungal symbionts have a very large surface area andreceive a direct supply of photosynthetic C (149) Soil bacteria have been found to growabundantly and rapidly at the expense of the exudates from P sylvestris roots colonizedby Piloderma supporting a role for the bacteria in the metabolism of the organic acidsand other compounds produced by the fungus (152) The observation that thesebacteria are able to utilize fungal sugars more readily than plant sugars supports theexistence of a bacterial guild that is specialized for hyphal exudates (191)

Methane represents a gaseous form of organic C that can be oxidized by certainforest soil bacteria under aerobic conditions (192) These methanotrophic bacteria arethe main consumers of atmospheric methane as well as methane generated bymethanogenic archaea in waterlogged anaerobic horizons of certain soils (193ndash196)Due to the presence of methanotrophic bacteria forest soils (especially those of theboreal forests) may represent a sink of atmospheric methane Although methanotrophsare phylogenetically located in two bacterial phyla most of the characterized isolatesbelong to the Alphaproteobacteria and Gammaproteobacteria (197) The discovery ofnew acidophilic methanotrophs related to Verrucomicrobia recently revealed a higherlevel of diversity of methanotrophic bacteria in as yet unexplored acidic environments(198) In addition to using organic C sources certain soil bacteria are able to fix CO2These autotrophic taxa were described for the genus Bradyrhizobium (Betaproteobac-teria) whose members are abundant inhabitants of forest soils (199 200) and a recenttranscriptomic study confirmed the expression of the components of a photosyntheticapparatus in the Cyanobacteria and Proteobacteria The input of C into forest soilsthrough fixation is however apparently minimal (55)

Role of Bacteria in Nitrogen and Phosphorus Cycles

Nitrogen is the most common limiting nutrient in soils entering the ecosystemlargely through fixation (Fig 3) This process is dominated by bacteria that are esti-mated to be responsible for more than 95 of the N input in unmanaged environments(36 201) The presence of the nifH gene of the Alphaproteobacteria (BradyrhizobiumAzospirillum Hyphomicrobium and Gluconacetobacter) and Deltaproteobacteria (Geo-bacter spp) was observed in different temperate forest soils demonstrating the ubiq-uity of some N-fixing bacteria not only as symbiotic but also as free-living taxa (200)The observed diversity of N-fixing bacteria may rapidly change if there is an exogenousinput of N (36) Particularly in temperate forest soils that are strongly affected byanthropogenic N deposition N input is a good predictor of N fixation activity (202)

Nitrification and denitrification lead to the loss of N from soils through NO N2O andN2 gas emissions as well as through the leaching of NO3 if its concentration exceeds theecosystem retention capacity (203 204) Among these nitrous oxide is a particularlypowerful greenhouse gas with a potentially warming effect that is almost 300 timeslarger than that of CO2 (205) Nitrification is the biological oxidation of ammonia tonitrate via a multienzymatic process The amoA gene encoding ammonia oxidasewhich performs the first step of nitrification is present in ammonia-oxidizing bacteria




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(AOB) as well as ammonia-oxidizing archaea (AOA) but AOB rather than AOA seem todominate in soils (206 207) The reaction catalyzed by this enzyme is often limiting intemperate and boreal forest soils (208) All known AOB belong to the Betaproteobac-teria and Gammaproteobacteria and they are mostly represented by the genera Nitro-somonas Nitrosococcus and Nitrosospira Nitrosomonas and Nitrosospira are furthersubdivided into clusters with different responses to environmental drivers such asacidity pH and ammonia availability and due to that changes in soil N availability canresult in dramatic shifts in the composition of the AOB community (206 208 209)Nitrosospira seems to be the most abundant AOB in acidic forest soils with low NH4

contents (206 210 211) The amoA gene content however appears to vary acrossforest soils (212) Nitrification rates seem to be correlated with the AOB abundance insoil (209 213) AOB are also involved in N losses from soil by producing N2O duringdenitrification (214) Denitrification is essential for the global N cycle maintaining thereduction of nitrate or nitrite to gaseous nitrogen compounds such as N2 and nitrousoxide The denitrification pathway is known as dissimilatory nitrate reduction becausenitrate or nitrogen oxides are the final electron acceptors allowing bacteria to produceenergy at the expense of reduced electron donors in the absence of oxygen Denitri-fying bacteria are not always able to perform all the steps of the dissimilatory pathwayand incomplete denitrification is the major source of N2O emissions from soils (215)Denitrification can be addressed by studying marker genes involved in the individualenzymatic steps such as the reduction of nitrate (narG) nitrite (nirKnirS) nitric oxide(norB) and nitrous oxide (nosZ) (205) Denitrifying bacteria are abundant and wide-spread in forest soils and denitrification genes have been found in bacterial strainsbelonging to the Acidobacteria Proteobacteria and Firmicutes as well as in otherbacterial phyla (216ndash218) A significant correlation was described among gene abun-dances denitrification rates and NO and N2O fluxes confirming the importance of theircarriers for the environmental processes that occur in forest soils (69 203 219) Inaddition to mineral N forms bacteria may obtain N from a range of organic compoundspresent in forest soils namely the chitin present in the polysaccharides of fungalmycelia and the amino acids and proteins in dead organic matter The utilization ofthese compounds is expected to be subject to intensive competition among ectomy-corrhizal fungi saprotrophic fungi and bacteria (146)

While the potential source of Nmdashthe atmospheremdashis theoretically unlimited this isnot the case for phosphorus (P) which is supplied mostly by weathering of minerals Pthus represents the limiting nutrient in many soils (Fig 3) Bacteria are importantmediators of the P cycle because some are able to solubilize mineral P while others mayimmobilize it in their biomass Unfortunately the involvement of bacteria in the P cyclehas received far less attention than that in the N and C cycles The main mechanismresponsible for P uptake by bacteria is through the solubilization and uptake ofinorganic P its most abundant source The ability to solubilize inorganic P has beendescribed for different bacteria and ectomycorrhizal fungi present in the rhizosphereand soil This ability is related to the release of organic anions such as citrategluconate oxalate and succinate into the soil (220) Phosphatase enzymes releasephosphate from organic phosphate esters during organic matter decay (221) In arecent metagenomic analysis of temperate forest soils it was highlighted that membersof the Alphaproteobacteria Betaproteobacteria Actinobacteria and Acidobacteria dom-inated the processes related to P turnover (222 223) While genes related to Psolubilization are more abundant in P-rich soil those that play a role in P uptakesystems are more abundant in P-limited soil (222)

EFFECTS OF GLOBAL CHANGE ON BACTERIAL COMMUNITIES IN FORESTECOSYSTEMS

Bacteria strongly contribute to key ecological processes that are important forsociety in light of the ongoing global change (114) The determination of how rela-tionships between site factors and bacterial communities affect the equilibrium be-tween soil organic matter decomposition and C sequestration in forests is of para-




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mount importance for prediction of the responses of terrestrial ecosystems to climatechange (224) Future climatic conditions are predicted to produce tree species migra-tion (225 226) an increase in extreme events such as droughts and wildfires and anincrease in vegetation productivity due to longer growth seasons (13 227 228) Theseeffects in combination with other phenomena such as increased N deposition maycause dramatic shifts in global C fluxes in particular affecting the boreal and temperateforests of the northern continental regions (229ndash231) The high diversity of C com-pounds released into the soils and the complex structures of bacterial and fungalcommunities with their overlapping functions create a very complex system that isdifficult to incorporate into predictive models (16) The complex nonlinear interactionsbetween forest and atmosphere have the capacity to constrain or amplify climatechange-associated processes depending on the activity of soil bacteria and fungi(232ndash234) Recent studies investigating the effects of global change on ecosystemproperties offer the first clues to the prediction of future developments (Table 1)

Carbon Dioxide

Increasing CO2 concentrations are predicted to boost NPP in boreal and temperateforests (235) however their capacity to maintain such high levels of NPP will stronglydepend on their ability to overcome nutrient limitations (236) Unfortunately thedegree to which forests will persist as C sinks remains uncertain (237) in particular therhizosphere priming effect may be reduced and the increased NPP may increase soil Cstorage (238 239) It is clear that the degree to which rising CO2 levels will be offset byC sequestration in forest ecosystems will strongly depend on the adaptation of bothtrees and soil microorganisms to the altered environmental conditions

Thus how do CO2 levels affect bacterial populations in forest topsoils And is itpossible to generalize the observations obtained across ecosystems for different soilswith various vegetations The effects of elevated CO2 levels do not directly affect soilbacterial populations CO2 concentrations in soil pores are normally higher than thosein the atmosphere and the response of bacteria to small CO2 changes is thus negligible(240) As a result the observed effects are mostly indirectly driven by altered plantproduction and root exudation which are both tree species specific In additionchanges in organic acid exudation by mycorrhizal fungi as a result of the presence ofCO2 will affect the bacterial community composition (152) and this process alsodepends on the vegetation properties It is difficult to determine whether the functionalresponses of bacterial communities to CO2 will be similar across forests or will dependon soil and vegetation characteristics The expected increase in root exudation shouldgenerally favor the development of soil copiotrophic bacteria over specialized olig-otrophs A good example of this response is the decrease in abundance of oligotrophicAcidobacteria in various soils following an increase in CO2 (144 152 238 240) Such ageneral response is rather exceptional considering that different members of the samephylum often respond differently to the same disturbance (241) The increased abun-dance of certain bacterial taxa will have functional consequences only if their functionaltraits do not change in response to the treatment which may explain the sometimescontroversial results obtained for responses to CO2 in different forest soils despite thefairly consistent response of bacterial abundance after an increase in CO2 (238 240242) For example while some studies have indicated that an elevated CO2 level doesnot affect the AOB abundance or nitrifying activity (207) others have described anincrease in nitrification or nitrifying taxa (240 243) even in an unaltered bacterialcommunity Thus it is unclear whether the effects of increased CO2 levels on bacterialbiomass richness community composition and functionality will be consistent acrossdifferent forest ecosystems

Global Warming

The rise in temperature is intimately linked to the increased CO2 concentration inthe atmosphere because the latter largely causes the former Although both processesappear globally the extent of the rise in temperature is predicted to be pronounced in




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TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

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rial

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mun

ities

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bio

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hem

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fore

sts

inm

anip

ulat

ive

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erim

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a

Man

ipul

atio

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abit

atV

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atio

nEf

fect

son

bio

geo

chem

istr

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fect

son

bac

teri

alp

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atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

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aPo

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273

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274

275

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263

267

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tinue

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(exc

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site

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site

)

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2m

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lb

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spec

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nom

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its

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257

266

268

Tem

per

ate

and

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277

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ses

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the Northern Hemisphere where temperate and boreal forest ecosystems dominateThe long-term scenarios are however not clear because multiple long-term eventssuch as the depletion of labile C limiting bacterial growth thermal adaptation ofmicrobial processes and shifts in microbial communities or in the expression of theirmetabolic potential may attenuate positive feedbacks of warming (244) The C balanceafter warming will largely depend on the efficiency of soil microbes in accessing andusing C in response to the altered environmental conditions (12) A very recent workshowed that an increase in temperatures can increase tree exudation rates (229) As aconsequence warming can alter soil drivers through exudation which in turn mightproduce different responses of soil rhizosphere bacterial communities affecting SOMdecomposition differently in different environments depending on the tree-specificexudation (229)

After years of experimentally increased warming in boreal and temperate forestsoils bacterial biomass values are usually not significantly different from those ofnonwarmed controls suggesting an attenuation effect (234 245ndash248) However it hasbeen demonstrated that warming affects bacterial diversity and that these changesreflect the magnitude of the temperature change (249) These shifts in bacterialcommunities may affect the C cycling processes that involve bacteria Multiple studieshave shown that short- and long-term warming can affect the composition of the soilbacterial community toward populations that are more adapted to the use of complexsources of C (234 250) Members of the Alphaproteobacteria and Acidobacteria displayincreased abundances after simulated warming suggesting a change in soil bacteriallifestyle from copiotrophy to oligotrophy which coincides with the depletion of labileC while maintaining high levels of respiration (16 234) This finding is contradictory tothe aforementioned effect of increased atmospheric CO2 which should boost copi-otrophic bacterial populations highlighting the necessity of studies that combine themanipulation of both variables However other studies have documented no shifts inbacterial communities after years of warming (90 246)

Considering the warming effects on N cycle processes we may rely only upon a fewcontradictory works examining that topic An increase in temperature was observed toaccelerate nitrification and denitrification processes affecting the N cycle in soils (229251) The warming effect may be offset by other factors such as N deposition whichcan increase the temperature sensitivity of the enzymes involved in SOM decom-position or suppress the decomposition process counterbalancing the primingeffects (245 252)

Nitrogen Deposition

Global anthropogenic N inputs are estimated to be 30 to 50 higher than thosefrom natural sources They have increased 10-fold in the past 150 years and areprojected to double during the next century (253 254) In contrast to global warmingand increased levels of CO2 however their effects are largely local Since N is a limitingnutrient in most terrestrial ecosystems including boreal and temperate forests (255)anthropogenic N deposition may strongly influence NPP in these environments byreducing this limitation (256) N deposition also has a range of additional consequencesthat range from shifts in the soil CN ratio soil acidification and root exudation tochanges in the vegetation and microbiota (257) Bacterial soil communities are clearlysensitive to increased levels of N itself as well as to all the associated soil physicochem-ical changes (213 258 259)

There appears to be a general consensus that N deposition increases soil C seques-tration due to the decline in SOM decomposition via the reduction of biomass andactivity of soil microbial populations in many different soil environments includingtemperate and boreal forests (258 260ndash264) The most probable reason for C seques-tration is the observed reduction of tree root exudation (256) although direct effects ofa pH decrease induced by N deposition were proposed as an alternative explanation(265) Although the reduction of biomass following N input was mostly observed infungi (256 266) it was recently noted that the biomass of soil bacteria can be reduced




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as well by up to 50 (258 263 267) Reduction of the bacterial biomass howeverdepends on the level of N input At chronically low levels of N which are typical ofboreal and temperate forest soils the bacterial biomass may remain stable while thefungal biomass markedly drops This decrease in the fungalbacterial biomass ratio dueto N addition is consistently found across forest soils where it ranges from 25 to 70(256 257 263 266)

N deposition also changes the composition of bacterial communities in forest soilsThe abundances of Acidobacteria and Verrucomicrobia decrease while those of Actino-bacteria and Firmicutes increase following the addition of N to a variety of soils (264)In a report on a temperate forest the share of Acidobacteria did not respond to Naddition but some groups within the phylum were significantly affected suggestingthat the response of the bacterial community may be complex (268) Also in othercases the deposition of N significantly affected relative abundances of core bacterialphyla but it reduced bacterial diversity and altered the bacterial composition at lowertaxonomic levels (258 261)

A decrease in oligotrophic bacteria is often found concomitantly with a decrease inthe activity of enzymes related to cellulose breakdown again supporting the hypoth-esis that the addition of N negatively affects microbial SOM decomposition (262 264)When genes of the N cycle (fixation nitrification and denitrification) were assessed inN deposition experiments the metabolic potential of the bacterial community re-mained stable or even decreased in terms of gene abundance (213 267) However instudies assessing the effects of N addition on N cycle processes in forest soils it wasreported that after N saturation of the environment bacterial and archaeal nitrificationand denitrification gain importance initiating the cycle and result in the efflux of Ncompounds such as nitrate N2 or nitrous oxide gas from the soil ecosystem (150 269270) This phenomenon suggests that the abundances of particular genes in this caseare not correlated with the rates of ecological processes In this sense it was recentlyproposed that even in forest soil environments where the addition of N highly increasesnitrification it is possible that bacteria with more efficient nitrification pathways areselected and that this leads to higher rates of nitrification despite the reduced abun-dance of nitrifiers and genes related to N cycle processes (213) Clearly metatranscrip-tomic or metaproteomic studies are needed to gain insight into the regulation of theN cycle by N availability

CONCLUSIONS

Undoubtedly boreal and temperate forests will be important for the global Cbalance considering the global change The role of bacteria in these ecosystems hasbeen understudied and it will be important to clarify whether these biomes willcontinue to be a large C sink for anthropogenic emissions Here we show that despitethe important role of fungi in forest soils bacteria fulfill multiple important ecosystemroles in the forest environment including organic matter decomposition regulation ofmycorrhizal symbiosis and involvement in N cycle processes More complex andcomparable studies to assess the variables affected by global change in a wide rangeof ecosystems will be required to predict the future of these environments The effectsproduced by greenhouse gas emissions and anthropogenic deposition of chemicalcompounds may provide a counterbalancing effect in some ecosystems while thechanges may be dangerous in others due to positive feedback Although our knowl-edge is still very limited we stress that the scientific data collected over the past yearsand even decades is never contradictory with regard to the need for boreal andtemperate forest ecosystem protection by strict policies A greater decrease in globalforest area will be particularly detrimental because it will prevent other climate changemitigation efforts such as the reduction of greenhouse emissions

Considering the importance of the transfer of C from the roots of primary producersto soil the rhizosphere is likely the most important hot spot of bacterial activity in soilsThe available nutrients provided by plants and mycorrhizal fungi lead to the formationof an interactive network of different soil microbes (not only bacteria) that makes the




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rhizosphere a fascinating and very complex system in which conditions are far fromthose in individual pores of the bulk soil The number of drivers to consider includingthe specificities of compounds and microbial diversity depending on the type of treeor plant and a large influence of seasonal effects (among others) hampers the acces-sibility to microbial ecologists of the processes that occur in the rhizosphere Howeverthe function of this niche very likely offers the key to understanding the biogeochem-istry of forest soils Studies combining the assessment of metabolites present in therhizosphere at different times their turnovers and transformations and the effects andimplications of bacterial taxa in terms of fluxes are the next step toward elucidating theeffects of forest trees on the rhizospheres and how they relate to the cycling of C andother nutrients

The large number of studies examining the bacterial communities in forest ecosys-tems that were published in recent years are shedding light on the high diversity andcomplex structure of these communities However to provide insights into the eco-logical roles and contributions of individual bacterial taxa to biogeochemical processesit is necessary to link the community composition to specific functions AlthoughDNA-based analyses aid in unraveling community dynamics and changes in microbialactivity RNA-based studies offer important information about the active bacterialcommunity and the processes that occur in ecosystems RNA-based studies of forestsconfirm how thousands of microbial taxa are transcriptionally active in forest litter andsoil underscoring the involvement of many players in important processes that occurin soil and the importance of taxa with a low abundance of DNA

ACKNOWLEDGMENTSThis work was supported by the Czech Science Foundation (grant 14-09040P) the

Ministry of Education Youth and Sports of the Czech Republic (grant LD15086) and theInstitutional Research Concept of the Institute of Microbiology of the CAS (grantRVO61388971)

We declare that we have no conflicts of interest

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21 Voriacuteškovaacute J Brabcovaacute V Cajthaml T Baldrian P 2014 Seasonal dynam-ics of fungal communities in a temperate oak forest soil New Phytol201269 ndash278 httpsdoiorg101111nph12481

22 Sterkenburg E Bahr A Brandstrom Durling M Clemmensen KE LindahlBD 2015 Changes in fungal communities along a boreal forest soilfertility gradient New Phytol 2071145ndash1158 httpsdoiorg101111nph13426

23 Eichlerovaacute I Homolka L Žifcaacutekovaacute L Lisaacute L Dobiaacutešovaacute P Baldrian P2015 Enzymatic systems involved in decomposition reflects the ecol-ogy and taxonomy of saprotrophic fungi Fungal Ecol 1310 ndash22 httpsdoiorg101016jfuneco201408002

24 van den Brink J de Vries RP 2011 Fungal enzyme sets for plantpolysaccharide degradation Appl Microbiol Biotechnol 911477ndash1492httpsdoiorg101007s00253-011-3473-2

25 van der Wal A Geydan TD Kuyper TW de Boer W 2013 A threadyaffair linking fungal diversity and community dynamics to terrestrialdecomposition processes FEMS Microbiol Rev 37477ndash 494 httpsdoiorg1011111574-697612001

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27 Peršoh D 2015 Plant-associated fungal communities in the light ofmetarsquoomics Fungal Divers 751ndash25 httpsdoiorg101007s13225-015-0334-9

28 Averill C Turner BL Finzi AC 2014 Mycorrhiza-mediated competitionbetween plants and decomposers drives soil carbon storage Nature505543ndash545 httpsdoiorg101038nature12901

29 Clemmensen KE Finlay RD Dahlberg A Stenlid J Wardle DA LindahlBD 2015 Carbon sequestration is related to mycorrhizal fungal com-munity shifts during long-term succession in boreal forests New Phytol2051525ndash1536 httpsdoiorg101111nph13208

30 Berlemont R Martiny AC 2015 Genomic potential for polysaccharidesdeconstruction in bacteria Appl Environ Microbiol 811513ndash1519httpsdoiorg101128AEM03718-14

31 Štursovaacute M Žifcaacutekovaacute L Leigh MB Burgess R Baldrian P 2012 Cellu-lose utilization in forest litter and soil identification of bacterial andfungal decomposers FEMS Microbiol Ecol 80735ndash746 httpsdoiorg101111j1574-6941201201343x

32 Eichorst SA Kuske CR 2012 Identification of cellulose-responsive bac-terial and fungal communities in geographically and edaphically dif-ferent soils by using stable isotope probing Appl Environ Microbiol782316 ndash2327 httpsdoiorg101128AEM07313-11

33 Loacutepez-Mondeacutejar R Zuumlhlke D Becher D Riedel K Baldrian P 2016Cellulose and hemicellulose decomposition by forest soil bacteria pro-ceeds by the action of structurally variable enzymatic systems Sci Rep625279 httpsdoiorg101038srep25279

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35 Tian JH Pourcher AM Bouchez T Gelhaye E Peu P 2014 Occurrence

of lignin degradation genotypes and phenotypes among prokaryotesAppl Microbiol Biotechnol 989527ndash9544 httpsdoiorg101007s00253-014-6142-4

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39 Podila GK Sreedasyam A Muratet MA 2009 Populus rhizosphere andthe ectomycorrhizal interactome Crit Rev Plant Sci 28359 ndash367 httpsdoiorg10108007352680903241220

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41 Uroz S Calvaruso C Turpault MP Pierrat JC Mustin C Frey-Klett P2007 Effect of the mycorrhizosphere on the genotypic and metabolicdiversity of the bacterial communities involved in mineral weatheringin a forest soil Appl Environ Microbiol 733019 ndash3027 httpsdoiorg101128AEM00121-07

42 Izumi H Anderson IC Alexander IJ Killham K Moore ER 2006 Diversityand expression of nitrogenase genes (nifH) from ectomycorrhizas ofCorsican pine (Pinus nigra) Environ Microbiol 82224 ndash2230 httpsdoiorg101111j1462-2920200601104x

43 Lauber CL Hamady M Knight R Fierer N 2009 Pyrosequencing-basedassessment of soil pH as a predictor of soil bacterial communitystructure at the continental scale Appl Environ Microbiol 755111ndash5120 httpsdoiorg101128AEM00335-09

44 Fierer N Jackson RB 2006 The diversity and biogeography of soilbacterial communities Proc Natl Acad Sci U S A 103626 ndash 631 httpsdoiorg101073pnas0507535103

45 Urbanovaacute M Šnajdr J Baldrian P 2015 Composition of fungal andbacterial communities in forest litter and soil is largely determined bydominant trees Soil Biol Biochem 8453ndash 64 httpsdoiorg101016jsoilbio201502011

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47 Chemidlin Prevost-Boure N Maron P-A Ranjard L Nowak V Dufrene EDamesin C Soudani K Lata J-C 2011 Seasonal dynamics of the bac-terial community in forest soils under different quantities of leaf litterAppl Soil Ecol 4714 ndash23 httpsdoiorg101016japsoil201011006

48 Baldrian P Merhautovaacute V Cajthaml T Petraacutenkovaacute M Šnajdr J 2010Small-scale distribution of extracellular enzymes fungal and bacterialbiomass in Quercus petraea forest topsoil Biol Fertil Soils 46717ndash726httpsdoiorg101007s00374-010-0478-4

49 Baldrian P 2014 Distribution of extracellular enzymes in soils spatialheterogeneity and determining factors at various scales Soil Sci SocAm J 7811 httpsdoiorg102136sssaj2013040155dgs

50 Kuzyakov Y Blagodatskaya E 2015 Microbial hotspots and hot mo-ments in soil concept amp review Soil Biol Biochem 83184 ndash199 httpsdoiorg101016jsoilbio201501025

51 Austin AT Vivanco L Gonzalez-Arzac A Perez LI 2014 Therersquos no placelike home An exploration of the mechanisms behind plant litter-decomposer affinity in terrestrial ecosystems New Phytol 204307ndash314httpsdoiorg101111nph12959

52 Hatton PJ Castanha C Torn MS Bird JA 2015 Litter type control on soilC and N stabilization dynamics in a temperate forest Glob Chang Biol211358 ndash1367 httpsdoiorg101111gcb12786

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54 Kim M Kim WS Tripathi BM Adams J 2014 Distinct bacterial commu-nities dominate tropical and temperate zone leaf litter Microb Ecol67837ndash 848 httpsdoiorg101007s00248-014-0380-y




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55 Žifcaacutekovaacute L Vetrovskyacute T Howe A Baldrian P 2016 Microbial activity inforest soil reflects the changes in ecosystem properties between sum-mer and winter Environ Microbiol 18288 ndash301 httpsdoiorg1011111462-292013026

56 Loacutepez-Mondeacutejar R Voriacuteškovaacute J Vetrovskyacute T Baldrian P 2015 Thebacterial community inhabiting temperate deciduous forests is verti-cally stratified and undergoes seasonal dynamics Soil Biol Biochem8743ndash50 httpsdoiorg101016jsoilbio201504008

57 Purahong W Schloter M Pecyna MJ Kapturska D Daumlich V Mital SBuscot F Hofrichter M Gutknecht JL Kruger D 2014 Uncoupling ofmicrobial community structure and function in decomposing litteracross beech forest ecosystems in Central Europe Sci Rep 47014httpsdoiorg101038srep07014

58 Urbanovaacute M Šnajdr J Brabcovaacute V Merhautovaacute V Dobiaacutešovaacute P Ca-jthaml T Vanek D Frouz J Šantruckovaacute H Baldrian P 2014 Litterdecomposition along a primary post-mining chronosequence Biol Fer-til Soils 50827ndash 837 httpsdoiorg101007s00374-014-0905-z

59 Augusto L Ranger J Binkley D Rothe A 2002 Impact of severalcommon tree species of European temperate forests on soil fertilityAnn For Sci 59233ndash253 httpsdoiorg101051forest2002020

60 Gessner MO Swan CM Dang CK McKie BG Bardgett RD Wall DHHattenschwiler S 2010 Diversity meets decomposition Trends EcolEvol 25372ndash380 httpsdoiorg101016jtree201001010

61 Thoms C Gleixner G 2013 Seasonal differences in tree speciesrsquo influ-ence on soil microbial communities Soil Biol Biochem 66239 ndash248httpsdoiorg101016jsoilbio201305018

62 Brooks DD Chan R Starks ER Grayston SJ Jones MD 2011 Ectomy-corrhizal hyphae structure components of the soil bacterial communityfor decreased phosphatase production FEMS Microbiol Ecol 76245ndash255 httpsdoiorg101111j1574-6941201101060x

63 Nordeacuten U 1994 Influence of tree species on acidification and mineralpools on deciduous forest soils of south Sweden Water Air Soil Pollut76363ndash381 httpsdoiorg101007BF00482713

64 Langenbruch C Helfrich M Flessa H 2011 Effects of beech (Fagussylvatica) ash (Fraxinus excelsior) and lime (Tilia spec) on soil chemicalproperties in a mixed deciduous forest Plant Soil 352389 ndash 403 httpsdoiorg101007s11104-011-1004-7

65 Cesarz S Fender A-C Beyer F Valtanen K Pfeiffer B Gansert D HertelD Polle A Daniel R Leuschner C Scheu S 2013 Roots from beech(Fagus sylvatica L) and ash (Fraxinus excelsior L) differentially affect soilmicroorganisms and carbon dynamics Soil Biol Biochem 6123ndash32httpsdoiorg101016jsoilbio201302003

66 Landesman WJ Nelson DM Fitzpatrick MC 2014 Soil properties andtree species drive -diversity of soil bacterial communities Soil BiolBiochem 76201ndash209 httpsdoiorg101016jsoilbio201405025

67 Scheibe A Steffens C Seven J Jacob A Hertel D Leuschner C GleixnerG 2015 Effects of tree identity dominate over tree diversity on the soilmicrobial community structure Soil Biol Biochem 81219 ndash227 httpsdoiorg101016jsoilbio201411020

68 Thoms C Gattinger A Jacob M Thomas FM Gleixner G 2010 Directand indirect effects of tree diversity drive soil microbial diversity intemperate deciduous forest Soil Biol Biochem 421558 ndash1565 httpsdoiorg101016jsoilbio201005030

69 Rasche F Knapp D Kaiser C Koranda M Kitzler B Zechmeister-Boltenstern S Richter A Sessitsch A 2011 Seasonality and resourceavailability control bacterial and archaeal communities in soils of atemperate beech forest ISME J 5389 ndash 402 httpsdoiorg101038ismej2010138

70 Baldrian P Šnajdr J Merhautovaacute V Dobiaacutešovaacute P Cajthaml T ValaacuteškovaacuteV 2013 Responses of the extracellular enzyme activities in hardwoodforest to soil temperature and seasonality and the potential effects ofclimate change Soil Biol Biochem 5660 ndash 68 httpsdoiorg101016jsoilbio201201020

71 Šnajdr J Cajthaml T Valaskova V Merhautova V Petrankova M SpetzP Leppanen K Baldrian P 2011 Transformation of Quercus petraealitter successive changes in litter chemistry are reflected in differentialenzyme activity and changes in the microbial community compositionFEMS Microbiol Ecol 75291ndash303 httpsdoiorg101111j1574-6941201000999x

72 Tlaacuteskal V Voriacuteškovaacute J Baldrian P 2016 Bacterial succession on decom-posing leaf litter exhibits a specific occurrence pattern of cellulolytictaxa and potential decomposers of fungal mycelia FEMS Microbiol Ecol92fiw177 httpsdoiorg101093femsecfiw177

73 Fierer N Bradford MA Jackson R 2007 Toward an ecological classifi-

cation of soil bacteria Ecology 881354 ndash1364 httpsdoiorg10189005-1839

74 Voriacuteškovaacute J Baldrian P 2013 Fungal community on decomposing leaflitter undergoes rapid successional changes ISME J 7477ndash 486 httpsdoiorg101038ismej2012116

75 Brabcovaacute V Novaacutekovaacute M Davidovaacute A Baldrian P 2016 Dead fungalmycelium in forest soil represents a decomposition hotspot and ahabitat for a specific microbial community New Phytol 2101369 ndash1381httpsdoiorg101111nph13849

76 Freschet GT Cornwell WK Wardle DA Elumeeva TG Liu W Jackson BGOnipchenko VG Soudzilovskaia NA Tao J Cornelissen JHC Austin A2013 Linking litter decomposition of above- and below-ground organsto plant-soil feedbacks worldwide J Ecol 101943ndash952 httpsdoiorg1011111365-274512092

77 Ekblad A Wallander H Godbold DL Cruz C Johnson D Baldrian P BjoumlrkRG Epron D Kieliszewska-Rokicka B Kjoslashller R Kraigher H Matzner ENeumann J Plassard C 2013 The production and turnover of extra-matrical mycelium of ectomycorrhizal fungi in forest soils role incarbon cycling Plant Soil 3661ndash27 httpsdoiorg101007s11104-013-1630-3

78 de Boer W Folman LB Summerbell RC Boddy L 2005 Living in a fungalworld impact of fungi on soil bacterial niche development FEMSMicrobiol Rev 29795ndash 811 httpsdoiorg101016jfemsre200411005

79 Kielak AM Scheublin TR Mendes LW van Veen JA Kuramae EE 2016Bacterial community succession in pine-wood decomposition FrontMicrobiol 7231 httpsdoiorg103389fmicb201600231

80 Rinta-Kanto JM Sinkko H Rajala T Al-Soud WA Soslashrensen SJ TamminenMV Timonen S 2016 Natural decay process affects the abundance andcommunity structure of Bacteria and Archaea in Picea abies logs FEMSMicrobiol Ecol 92fiw087 httpsdoiorg101093femsecfiw087

81 Johnston SR Boddy L Weightman AJ 2016 Bacteria in decomposingwood and their interactions with wood-decay fungi FEMS MicrobiolEcol 92fiw179 httpsdoiorg101093femsecfiw179

82 Hoppe B Kruumlger K Kahl T Arnstadt T Buscot F Bauhus J Wubet T2015 A pyrosequencing insight into sprawling bacterial diversity andcommunity dynamics in decaying deadwood logs of Fagus sylvaticaand Picea abies Sci Rep 59456 httpsdoiorg101038srep09456

83 Folman LB Gunnewiek P Boddy L de Boer W 2008 Impact of white-rotfungi on numbers and community composition of bacteria colonizingbeech wood from forest soil FEMS Microbiol Ecol 63181ndash191 httpsdoiorg101111j1574-6941200700425x

84 Valaacuteškovaacute V de Boer W Gunnewiek PJ Pospiacutešek M Baldrian P 2009Phylogenetic composition and properties of bacteria coexisting withthe fungus Hypholoma fasciculare in decaying wood ISME J31218 ndash1221 httpsdoiorg101038ismej200964

85 Nacke H Engelhaupt M Brady S Fischer C Tautzt J Daniel R 2012Identification and characterization of novel cellulolytic and hemicellu-lolytic genes and enzymes derived from German grassland soil metag-enomes Biotechnol Lett 34663ndash 675 httpsdoiorg101007s10529-011-0830-2

86 Šnajdr J Valaacuteškovaacute V Merhautovaacute V Herinkovaacute J Cajthaml T BaldrianP 2008 Spatial variability of enzyme activities and microbial biomass inthe upper layers of Quercus petraea forest soil Soil Biol Biochem402068 ndash2075 httpsdoiorg101016jsoilbio200801015

87 Uroz S Ioannidis P Lengelle J Cebron A Morin E Bueacuteeacute M Martin F2013 Functional assays and metagenomic analyses reveals differencesbetween the microbial communities inhabiting the soil horizons of aNorway spruce plantation PLoS One 8e55929 httpsdoiorg101371journalpone0055929

88 Eilers KG Lauber CL Knight R Fierer N 2010 Shifts in bacterial com-munity structure associated with inputs of low molecular weight car-bon compounds to soil Soil Biol Biochem 42896 ndash903 httpsdoiorg101016jsoilbio201002003

89 Nacke H Thuumlrmer A Wollherr A Will C Hodac L Herold N Schoumlning ISchrumpf M Daniel R 2011 Pyrosequencing-based assessment ofbacterial community structure along different management types inGerman forest and grassland soils PLoS One 6e17000 httpsdoiorg101371journalpone0017000

90 Kuffner M Hai B Rattei T Melodelima C Schloter M Zechmeister-Boltenstern S Jandl R Schindlbacher A Sessitsch A 2012 Effects ofseason and experimental warming on the bacterial community in atemperate mountain forest soil assessed by 16S rRNA gene pyrose-




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Dow

nloaded from

quencing FEMS Microbiol Ecol 82551ndash562 httpsdoiorg101111j1574-6941201201420x

91 Lipson DA 2007 Relationships between temperature responses andbacterial community structure along seasonal and altitudinal gradientsFEMS Microbiol Ecol 59418 ndash 427 httpsdoiorg101111j1574-6941200600240x

92 Kurth F Zeitler K Feldhahn L Neu TR Weber T Krištufek V Wubet THerrmann S Buscot F Tarkka M 2013 Detection and quantification ofa mycorrhization helper bacterium and a mycorrhizal fungus in plant-soil microcosms at different levels of complexity BMC Microbiol 13205httpsdoiorg1011861471-2180-13-205

93 Ferrenberg S OrsquoNeill SP Knelman JE Todd B Duggan S Bradley DRobinson T Schmidt SK Townsend AR Williams MW Cleveland CCMelbourne BA Jiang L Nemergut DR 2013 Changes in assemblyprocesses in soil bacterial communities following a wildfire distur-bance ISME J 71102ndash1111 httpsdoiorg101038ismej201311

94 Jeanbille M Buee M Bach C Cebron A Frey-Klett P Turpault MP UrozS 2016 Soil parameters drive the structure diversity and metabolicpotentials of the bacterial communities across temperate beech forestsoil sequences Microb Ecol 71482ndash 493 httpsdoiorg101007s00248-015-0669-5

95 Houmlgberg MN Houmlgberg P Myrold DD 2007 Is microbial communitycomposition in boreal forest soils determined by pH C-to-N ratio thetrees or all three Oecologia 150590 ndash 601

96 Shen C Xiong J Zhang H Feng Y Lin X Li X Liang W Chu H 2013 SoilpH drives the spatial distribution of bacterial communities along ele-vation on Changbai Mountain Soil Biol Biochem 57204 ndash211 httpsdoiorg101016jsoilbio201207013

97 Norman JS Barrett JE 2016 Substrate availability drives spatial pat-terns in richness of ammonia-oxidizing bacteria and archaea in tem-perate forest soils Soil Biol Biochem 94169 ndash172 httpsdoiorg101016jsoilbio201511015

98 Bryant JA Lamanna C Morlon H Kerkhoff AJ Enquist BJ Green JL2008 Microbes on mountainsides contrasting elevational patterns ofbacterial and plant diversity Proc Natl Acad Sci U S A 105(Suppl1)S11505ndashS11511 httpsdoiorg101073pnas0801920105

99 Jones RT Robeson MS Lauber CL Hamady M Knight R Fierer N 2009A comprehensive survey of soil acidobacterial diversity using pyrose-quencing and clone library analyses ISME J 3442ndash 453 httpsdoiorg101038ismej2008127

100 Lauber CL Strickland MS Bradford MA Fierer N 2008 The influence ofsoil properties on the structure of bacterial and fungal communitiesacross land-use types Soil Biol Biochem 402407ndash2415 httpsdoiorg101016jsoilbio200805021

101 Naether A Foesel BU Naegele V Wust PK Weinert J Bonkowski M AltF Oelmann Y Polle A Lohaus G Gockel S Hemp A Kalko EK Linsen-mair KE Pfeiffer S Renner S Schoning I Weisser WW Wells K FischerM Overmann J Friedrich MW 2012 Environmental factors affect aci-dobacterial communities below the subgroup level in grassland andforest soils Appl Environ Microbiol 787398 ndash7406 httpsdoiorg101128AEM01325-12

102 Garcia-Fraile P Benada O Cajthaml T Baldrian P Lladoacute S 2015 Ter-racidiphilus gabretensis gen nov sp nov an abundant and activeforest soil acidobacterium important in organic matter transformationAppl Environ Microbiol 82560 ndash569 httpsdoiorg101128AEM03353-15

103 Vetrovskyacute T Baldrian P 2013 The variability of the 16S rRNA gene inbacterial genomes and its consequences for bacterial community anal-yses PLoS One 8e0057923 httpsdoiorg101371journalpone0057923

104 Lladoacute S Žifcaacutekovaacute L Vetrovskyacute T Eichlerovaacute I Baldrian P 2016 Func-tional screening of abundant bacteria from acidic forest soil indicatesthe metabolic potential of Acidobacteria subdivision 1 for polysaccha-ride decomposition Biol Fertil Soils 52251ndash260 httpsdoiorg101007s00374-015-1072-6

105 Kielak AM Barreto CC Kowalchuk GA van Veen JA Kuramae EE 2016The ecology of acidobacteria moving beyond genes and genomesFront Microbiol 7744 httpsdoiorg103389fmicb201600744

106 Uroz S Bueacuteeacute M Murat C Frey-Klett P Martin F 2010 Pyrosequencingreveals a contrasted bacterial diversity between oak rhizosphere andsurrounding soil Environ Microbiol Rep 2281ndash288 httpsdoiorg101111j1758-2229200900117x

107 Bergmann GT Bates ST Eilers KG Lauber CL Caporaso JG Walters WAKnight R Fierer N 2011 The under-recognized dominance of Verruco-

microbia in soil bacterial communities Soil Biol Biochem 431450 ndash1455 httpsdoiorg101016jsoilbio201103012

108 Sun H Terhonen E Koskinen K Paulin L Kasanen R Asiegbu FO 2014Bacterial diversity and community structure along different peat soils inboreal forest Appl Soil Ecol 7437ndash 45 httpsdoiorg101016japsoil201309010

109 Eilers KG Debenport S Anderson S Fierer N 2012 Digging deeper tofind unique microbial communities the strong effect of depth on thestructure of bacterial and archaeal communities in soil Soil BiolBiochem 5058 ndash 65 httpsdoiorg101016jsoilbio201203011

110 Collignon C Uroz S Turpault MP Frey-Klett P 2011 Seasons differentlyimpact the structure of mineral weathering bacterial communities inbeech and spruce stands Soil Biol Biochem 432012ndash2022 httpsdoiorg101016jsoilbio201105008

111 Leveau JH Uroz S de Boer W 2010 The bacterial genus Collimonasmycophagy weathering and other adaptive solutions to life in oligo-trophic soil environments Environ Microbiol 12281ndash292 httpsdoiorg101111j1462-2920200902010x

112 Uroz S Oger P Tisserand E Cebron A Turpault MP Buee M De Boer WLeveau JH Frey-Klett P 2016 Specific impacts of beech and Norwayspruce on the structure and diversity of the rhizosphere and soilmicrobial communities Sci Rep 627756 httpsdoiorg101038srep27756

113 OrsquoBrien SL Gibbons SM Owens SM Hampton-Marcell J Johnston ERJastrow JD Gilbert JA Meyer F Antonopoulos DA 2016 Spatial scaledrives patterns in soil bacterial diversity Environ Microbiol 182039 ndash2051 httpsdoiorg1011111462-292013231

114 Martiny JB Eisen JA Penn K Allison SD Horner-Devine MC 2011Drivers of b-diversity depend on spatial scale Proc Natl Acad Sci U S A1087850 ndash7854 httpsdoiorg101073pnas1016308108

115 Spielvogel S Prietzel J Koumlgel-Knabner I 2016 Stand scale variability oftopsoil organic matter composition in a high-elevation Norway spruceforest ecosystem Geoderma 267112ndash122 httpsdoiorg101016jgeoderma201512001

116 Izumi H Finlay RD 2011 Ectomycorrhizal roots select distinctive bac-terial and ascomycete communities in Swedish subarctic forests Envi-ron Microbiol 13819 ndash 830 httpsdoiorg101111j1462-2920201002393x

117 Brockett BFT Prescott CE Grayston SJ 2012 Soil moisture is the majorfactor influencing microbial community structure and enzyme activitiesacross seven biogeoclimatic zones in western Canada Soil BiolBiochem 449 ndash20 httpsdoiorg101016jsoilbio201109003

118 Lennon JT Aanderud ZT Lehmkuhl BK Schoolmaster DR 2012 Map-ping the niche space of soil microorganisms using taxonomy and traitsEcology 931867ndash1879 httpsdoiorg10189011-17451

119 Pollierer MM Langel R Korner C Maraun M Scheu S 2007 Theunderestimated importance of belowground carbon input for forestsoil animal food webs Ecol Lett 10729 ndash736 httpsdoiorg101111j1461-0248200701064x

120 Phillips RP Finzi AC Bernhardt ES 2011 Enhanced root exudationinduces microbial feedbacks to N cycling in a pine forest under long-term CO2 fumigation Ecol Lett 14187ndash194 httpsdoiorg101111j1461-0248201001570x

121 Beidler KV Taylor BN Strand AE Cooper ER Schonholz M Pritchard SG2015 Changes in root architecture under elevated concentrations ofCO2 and nitrogen reflect alternate soil exploration strategies NewPhytol 2051153ndash1163 httpsdoiorg101111nph13123

122 Fender A-C Leuschner C Schuumltzenmeister K Gansert D Jungkunst HF2013 Rhizosphere effects of tree speciesmdashlarge reduction of N2Oemission by saplings of ash but not of beech in temperate forest soilEur J Soil Biol 547ndash15 httpsdoiorg101016jejsobi201210010

123 Markkola AM 1996 Resource allocation in ectomycorrhizal symbiosis inScots pine affected by environmental changes University of OuluOulu Finland

124 Kluber LA Smith JE Myrold DD 2011 Distinctive fungal and bacterialcommunities are associated with mats formed by ectomycorrhizalfungi Soil Biol Biochem 431042ndash1050 httpsdoiorg101016jsoilbio201101022

125 Churchland C Grayston SJ 2014 Specificity of plant-microbe interac-tions in the tree mycorrhizosphere biome and consequences for soil Ccycling Front Microbiol 5261 httpsdoiorg103389fmicb201400261

126 Aspray TJ Eirian Jones E Whipps JM Bending GD 2006 Importance ofmycorrhization helper bacteria cell density and metabolite localization




httpmm

brasmorg

Dow

nloaded from

for the Pinus sylvestris-Lactarius rufus symbiosis FEMS Microbiol Ecol5625ndash33 httpsdoiorg101111j1574-6941200500051x

127 Vik U Logares R Blaalid R Halvorsen R Carlsen T Bakke I Kolsto ABOkstad OA Kauserud H 2013 Different bacterial communities in ecto-mycorrhizae and surrounding soil Sci Rep 33471 httpsdoiorg101038srep03471

128 Collignon C Calvaruso C Turpault M-P 2011 Temporal dynamics ofexchangeable K Ca and Mg in acidic bulk soil and rhizosphere underNorway spruce (Picea abies Karst) and beech (Fagus sylvatica L) standsPlant Soil 349355ndash366 httpsdoiorg101007s11104-011-0881-0

129 Drake JE Darby BA Giasson MA Kramer MA Phillips RP Finzi AC 2013Stoichiometry constrains microbial response to root exudationmdashinsights from a model and a field experiment in a temperate forestBiogeosciences 10821ndash 838 httpsdoiorg105194bg-10-821-2013

130 Finzi AC Abramoff RZ Spiller KS Brzostek ER Darby BA Kramer MAPhillips RP 2015 Rhizosphere processes are quantitatively importantcomponents of terrestrial carbon and nutrient cycles Glob Chang Biol212082ndash2094 httpsdoiorg101111gcb12816

131 Brzostek ER Greco A Drake JE Finzi AC 2012 Root carbon inputs tothe rhizosphere stimulate extracellular enzyme activity and increasenitrogen availability in temperate forest soils Biogeochemistry 11565ndash76 httpsdoiorg101007s10533-012-9818-9

132 Loeppmann S Blagodatskaya E Pausch J Kuzyakov Y 2016 Substratequality affects kinetics and catalytic efficiency of exo-enzymes in rhizo-sphere and detritusphere Soil Biol Biochem 92111ndash118 httpsdoiorg101016jsoilbio201509020

133 Tefs C Gleixner G 2012 Importance of root derived carbon for soilorganic matter storage in a temperate old-growth beech forestmdashevidence from C N and 14C content For Ecol Manage 263131ndash137httpsdoiorg101016jforeco201109010

134 Chaparro JM Badri DV Bakker MG Sugiyama A Manter DK Vivanco JM2013 Root exudation of phytochemicals in Arabidopsis follows specificpatterns that are developmentally programmed and correlate with soilmicrobial functions PLoS One 8e55731 httpsdoiorg101371journalpone0055731

135 Kaiser C Koranda M Kitzler B Fuchslueger L Schnecker J Schweiger PRasche F Zechmeister-Boltenstern S Sessitsch A Richter A 2010 Be-lowground carbon allocation by trees drives seasonal patterns of ex-tracellular enzyme activities by altering microbial community compo-sition in a beech forest soil New Phytol 187843ndash 858 httpsdoiorg101111j1469-8137201003321x

136 Shi S Nuccio E Herman DJ Rijkers R Estera K Li J da Rocha UN He ZPett-Ridge J Brodie EL Zhou J Firestone M 2015 Successional trajec-tories of rhizosphere bacterial communities over consecutive seasonsmBio 6e00746 httpsdoiorg101128mBio00746-15

137 Mao Y Li X Smyth EM Yannarell AC Mackie RI 2014 Enrichment ofspecific bacterial and eukaryotic microbes in the rhizosphere of switch-grass (Panicum virgatum L) through root exudates Environ MicrobiolRep 6293ndash306 httpsdoiorg1011111758-222912152

138 Peiffer JA Spor A Koren O Jin Z Tringe SG Dangl JL Buckler ES LeyRE 2013 Diversity and heritability of the maize rhizosphere micro-biome under field conditions Proc Natl Acad Sci U S A 1106548 ndash 6553httpsdoiorg101073pnas1302837110

139 Mendes LW Kuramae EE Navarrete AA van Veen JA Tsai SM 2014Taxonomical and functional microbial community selection in soybeanrhizosphere ISME J 81577ndash1587 httpsdoiorg101038ismej201417

140 Donn S Kirkegaard JA Perera G Richardson AE Watt M 2015 Evolu-tion of bacterial communities in the wheat crop rhizosphere EnvironMicrobiol 17610 ndash 621 httpsdoiorg1011111462-292012452

141 Bulgarelli D Rott M Schlaeppi K Ver Loren van Themaat E Ahmadine-jad N Assenza F Rauf P Huettel B Reinhardt R Schmelzer E Peplies JGloeckner FO Amann R Eickhorst T Schulze-Lefert P 2012 Revealingstructure and assembly cues for Arabidopsis root-inhabiting bacterialmicrobiota Nature 48891ndash95 httpsdoiorg101038nature11336

142 Lundberg DS Lebeis SL Paredes SH Yourstone S Gehring J Malfatti STremblay J Engelbrektson A Kunin V del Rio TG Edgar RC Eickhorst TLey RE Hugenholtz P Tringe SG Dangl JL 2012 Defining the coreArabidopsis thaliana root microbiome Nature 48886 ndash90 httpsdoiorg101038nature11237

143 Ai C Liang G Sun J Wang X He P Zhou W He X 2015 Reduceddependence of rhizosphere microbiome on plant-derived carbon in32-year long-term inorganic and organic fertilized soils Soil BiolBiochem 8070 ndash78 httpsdoiorg101016jsoilbio201409028

144 Gschwendtner S Engel M Lueders T Buegger F Schloter M 2016

Nitrogen fertilization affects bacteria utilizing plant-derived carbon inthe rhizosphere of beech seedlings Plant Soil 407203ndash215 httpsdoiorg101007s11104-016-2888-z

145 Lladoacute S Baldrian P 2017 Community-level physiological profiling anal-yses show potential to identify the copiotrophic bacteria present in soilenvironments PLoS One 12e0171638 httpsdoiorg101371journalpone0171638

146 Izumi H Cairney JW Killham K Moore E Alexander IJ Anderson IC2008 Bacteria associated with ectomycorrhizas of slash pine (Pinuselliottii) in south-eastern Queensland Australia FEMS Microbiol Lett282196 ndash204 httpsdoiorg101111j1574-6968200801122x

147 Tanaka M Nara K 2009 Phylogenetic diversity of non-nodulatingRhizobium associated with pine ectomycorrhizae FEMS Microbiol Ecol69329 ndash343 httpsdoiorg101111j1574-6941200900720x

148 Yu HX Wang CY Tang M 2013 Fungal and bacterial communities inthe rhizosphere of Pinus tabulaeformis related to the restoration ofplantations and natural secondary forests in the Loess Plateau north-west China Sci World J 2013606480 httpsdoiorg1011552013606480

149 Marupakula S Mahmood S Finlay RD 2016 Analysis of single root tipmicrobiomes suggests that distinctive bacterial communities are se-lected by Pinus sylvestris roots colonized by different ectomycorrhizalfungi Environ Microbiol 181470 ndash1483 httpsdoiorg1011111462-292013102

150 Labbe JL Weston DJ Dunkirk N Pelletier DA Tuskan GA 2014 Newlyidentified helper bacteria stimulate ectomycorrhizal formation in Popu-lus Front Plant Sci 5579 httpsdoiorg103389fpls201400579

151 Frey-Klett P Garbaye J Tarkka M 2007 The mycorrhiza helper bacteriarevisited New Phytol 17622ndash36 httpsdoiorg101111j1469-8137200702191x

152 Fransson P Andersson A Norstroumlm S Bylund D Bent E 2016 Ectomy-corrhizal exudates and pre-exposure to elevated CO2 affects soil bac-terial growth and community structure Fungal Ecol 20211ndash224httpsdoiorg101016jfuneco201601003

153 Aspray TJ Frey-Klett P Jones JE Whipps JM Garbaye J Bending GD2006 Mycorrhization helper bacteria a case of specificity for alteringectomycorrhiza architecture but not ectomycorrhiza formation Mycor-rhiza 16533ndash541 httpsdoiorg101007s00572-006-0068-3

154 Lang C Seven J Polle A 2011 Host preferences and differential con-tributions of deciduous tree species shape mycorrhizal species richnessin a mixed Central European forest Mycorrhiza 21297ndash308 httpsdoiorg101007s00572-010-0338-y

155 Korkama T Fritze H Pakkanen A Pennanen T 2007 Interactions be-tween extraradical ectomycorrhizal mycelia microbes associated withthe mycelia and growth rate of Norway spruce (Picea abies) clones NewPhytol 173798 ndash 807 httpsdoiorg101111j1469-8137200601957x

156 Xia M Talhelm AF Pregitzer KS 2015 Fine roots are the dominantsource of recalcitrant plant litter in sugar maple-dominated northernhardwood forests New Phytol 208715ndash726 httpsdoiorg101111nph13494

157 Van Dyk JS Pletschke BI 2012 A review of lignocellulose bioconversionusing enzymatic hydrolysis and synergistic cooperation between en-zymesmdashfactors affecting enzymes conversion and synergy BiotechnolAdv 301458 ndash1480 httpsdoiorg101016jbiotechadv201203002

158 Rytioja J Hildeacuten K Yuzon J Hatakka A de Vries RP Maumlkelauml MR 2014Plant-polysaccharide-degrading enzymes from Basidiomycetes Micro-biol Mol Biol Rev 78614 ndash 649 httpsdoiorg101128MMBR00035-14

159 Berlemont R Martiny AC 2013 Phylogenetic distribution of potentialcellulases in bacteria Appl Environ Microbiol 791545ndash1554 httpsdoiorg101128AEM03305-12

160 Vetrovskyacute T Steffen KT Baldrian P 2014 Potential of cometabolictransformation of polysaccharides and lignin in lignocellulose by soilActinobacteria PLoS One 9e89108 httpsdoiorg101371journalpone0089108

161 Brumm PJ 2013 Bacterial genomes what they teach us about cellulosedegradation Biofuels 4669 ndash 681 httpsdoiorg104155bfs1344

162 Lopez-Mondejar R Zuhlke D Vetrovsky T Becher D Riedel K BaldrianP 2016 Decoding the complete arsenal for cellulose and hemicellulosedeconstruction in the highly efficient cellulose decomposer Paeniba-cillus O199 Biotechnol Biofuels 9104 httpsdoiorg101186s13068-016-0518-x

163 Llado S Benada O Cajthaml T Baldrian P Garcia-Fraile P 2016 Sil-vibacterium bohemicum gen nov sp nov an acidobacterium isolated




httpmm

brasmorg

Dow

nloaded from

from coniferous soil in the Bohemian Forest National Park Syst ApplMicrobiol 3914 ndash19 httpsdoiorg101016jsyapm201512005

164 Blanvillain S Meyer D Boulanger A Lautier M Guynet C Denance NVasse J Lauber E Arlat M 2007 Plant carbohydrate scavengingthrough tonB-dependent receptors a feature shared by phytopatho-genic and aquatic bacteria PLoS One 2e224 httpsdoiorg101371journalpone0000224

165 Yokoyama H Yamashita T Morioka R Ohmori H 2014 Extracellularsecretion of noncatalytic plant cell wall-binding proteins by the cellu-lolytic thermophile Caldicellulosiruptor bescii J Bacteriol 1963784 ndash3792 httpsdoiorg101128JB01897-14

166 Vodovnik M Duncan SH Reid MD Cantlay L Turner K Parkhill J LamedR Yeoman CJ Miller ME White BA Bayer EA Marinsek-Logar R Flint HJ2013 Expression of cellulosome components and type IV pili within theextracellular proteome of Ruminococcus flavefaciens 007 PLoS One8e65333 httpsdoiorg101371journalpone0065333

167 Wegmann U Louis P Goesmann A Henrissat B Duncan SH Flint HJ2014 Complete genome of a new Firmicutes species belonging to thedominant human colonic microbiota (ldquoRuminococcus bicirculansrdquo) re-veals two chromosomes and a selective capacity to utilize plant glu-cans Environ Microbiol 162879 ndash2890 httpsdoiorg1011111462-292012217

168 Himmel ME Xu Q Luo Y Ding S Lamed R Bayer EA 2010 Microbialenzyme systems for biomass conversion emerging paradigms Biofuels1323ndash341 httpsdoiorg104155bfs0925

169 Sukharnikov LO Cantwell BJ Podar M Zhulin IB 2011 Cellulasesambiguous nonhomologous enzymes in a genomic perspectiveTrends Biotechnol 29473ndash 479 httpsdoiorg101016jtibtech201104008

170 Yang JK Zhang JJ Yu HY Cheng JW Miao LH 2014 Communitycomposition and cellulase activity of cellulolytic bacteria from forestsoils planted with broad-leaved deciduous and evergreen trees ApplMicrobiol Biotechnol 981449 ndash1458 httpsdoiorg101007s00253-013-5130-4

171 Bandounas L Wierckx NJ de Winde JH Ruijssenaars HJ 2011 Isolation andcharacterization of novel bacterial strains exhibiting ligninolytic potentialBMC Biotechnol 1194 httpsdoiorg1011861472-6750-11-94

172 Kellner H Luis P Zimdars B Kiesel B Buscot F 2008 Diversity ofbacterial laccase-like multicopper oxidase genes in forest and grasslandCambisol soil samples Soil Biol Biochem 40638 ndash 648 httpsdoiorg101016jsoilbio200709013

173 Nacke H Fischer C Thurmer A Meinicke P Daniel R 2014 Land usetype significantly affects microbial gene transcription in soil MicrobEcol 67919 ndash930 httpsdoiorg101007s00248-014-0377-6

174 Baldrian P Vetrovskyacute T Cajthaml T Dobiaacutešovaacute P Petraacutenkovaacute M ŠnajdrJ Eichlerovaacute I 2013 Estimation of fungal biomass in forest litter andsoil Fungal Ecol 61ndash11 httpsdoiorg101016jfuneco201210002

175 Fernandez CW Koide RT 2014 Initial melanin and nitrogen concen-trations control the decomposition of ectomycorrhizal fungal litter SoilBiol Biochem 77150 ndash157 httpsdoiorg101016jsoilbio201406026

176 Beier S Bertilsson S 2013 Bacterial chitin degradationmdashmechanismsand ecophysiological strategies Front Microbiol 4149 httpsdoiorg103389fmicb201300149

177 Talamantes D Biabini N Dang H Abdoun K Berlemont R 2016 Naturaldiversity of cellulases xylanases and chitinases in bacteria BiotechnolBiofuels 9133 httpsdoiorg101186s13068-016-0538-6

178 Bai Y Eijsink VG Kielak AM van Veen JA de Boer W 2016 Genomiccomparison of chitinolytic enzyme systems from terrestrial and aquaticbacteria Environ Microbiol 1838 ndash 49 httpsdoiorg1011111462-292012545

179 Tolonen AC Cerisy T El-Sayyed H Boutard M Salanoubat M ChurchGM 2015 Fungal lysis by a soil bacterium fermenting cellulose EnvironMicrobiol 172618 ndash2627 httpsdoiorg1011111462-292012495

180 Wang X Sharp CE Jones GM Grasby SE Brady AL Dunfield PF 2015Stable-isotope probing identifies uncultured Planctomycetes as pri-mary degraders of a complex heteropolysaccharide in soil Appl Envi-ron Microbiol 814607ndash 4615 httpsdoiorg101128AEM00055-15

181 Kaiser C Kilburn MR Clode PL Fuchslueger L Koranda M Cliff JBSolaiman ZM Murphy DV 2015 Exploring the transfer of recent plantphotosynthates to soil microbes mycorrhizal pathway vs direct rootexudation New Phytol 2051537ndash1551 httpsdoiorg101111nph13138

182 Houmlgberg MN Briones MJ Keel SG Metcalfe DB Campbell C MidwoodAJ Thornton B Hurry V Linder S Nasholm T Houmlgberg P 2010 Quan-

tification of effects of season and nitrogen supply on tree below-ground carbon transfer to ectomycorrhizal fungi and other soil organ-isms in a boreal pine forest New Phytol 187485ndash 493 httpsdoiorg101111j1469-8137201003274x

183 Kuzyakov Y Cheng W 2001 Photosynthesis controls of rhizosphererespiration and organic matter decomposition Soil Biol Biochem 331915ndash1925 httpsdoiorg101016S0038-0717(01)00117-1

184 Houmlgberg P Nordgren A Buchmann N Taylor AFS Ekblad A HoumlgbergMN Nyberg G Ottosson-Lofvenius M Read DJ 2001 Large-scale forestgirdling shows that current photosynthesis drives soil respiration Na-ture 411789 ndash792 httpsdoiorg10103835081058

185 Bueacutee M de Boer W Martin F van Overbeek L Jurkevitch E 2009 Therhizosphere zoo an overview of plant-associated communities of mi-croorganisms including phages bacteria archaea and fungi and ofsome of their structuring factors Plant Soil 321189 ndash212 httpsdoiorg101007s11104-009-9991-3

186 Clemmensen KE Bahr A Ovaskainen O Dahlberg A Ekblad A Wal-lander H Stenlid J Finlay RD Wardle DA Lindahl BD 2013 Roots andassociated fungi drive long-term carbon sequestration in boreal forestScience 3391615ndash1618 httpsdoiorg101126science1231923

187 Wang Y Li C Wang Q Wang H Duan B Zhang G 2016 Environmentalbehaviors of phenolic acids dominated their rhizodeposition in borealpoplar plantation forest soils J Soils Sediments 161858 ndash1870 httpsdoiorg101007s11368-016-1375-8

188 Haichar FE Heulin T Guyonnet JP Achouak W 2016 Stable isotopeprobing of carbon flow in the plant holobiont Curr Opin Biotechnol419 ndash13 httpsdoiorg101016jcopbio201602023

189 Churchland C Weatherall A Briones MJI Grayston SJ 2012 Stable-isotopelabeling and probing of recent photosynthates into respired CO2 soilmicrobes and soil mesofauna using a xylem and phloem stem-injectiontechnique on Sitka spruce (Picea sitchensis) Rapid Comm Mass Spectrom262493ndash2501 httpsdoiorg101002rcm6368

190 Uroz S Courty PE Pierrat JC Peter M Bueacuteeacute M Turpault MP Garbaye JFrey-Klett P 2013 Functional profiling and distribution of the forest soilbacterial communities along the soil mycorrhizosphere continuumMicrob Ecol 66404 ndash 415 httpsdoiorg101007s00248-013-0199-y

191 Izumi H Anderson IC Alexander IJ Killham K Moore ER 2006 Endo-bacteria in some ectomycorrhiza of Scots pine (Pinus sylvestris) FEMSMicrobiol Ecol 5634 ndash 43 httpsdoiorg101111j1574-6941200500048x

192 Lau E Nolan EJ IV Dillard ZW Dague RD Semple AL Wentzell WL2015 High throughput sequencing to detect differences in metha-notrophic Methylococcaceae and Methylocystaceae in surface peatforest soil and sphagnum moss in Cranesville Swamp Preserve WestVirginia USA Microorganisms 3113ndash136 httpsdoiorg103390microorganisms3020113

193 Savi F Di Bene C Canfora L Mondini C Fares S 2016 Environmentaland biological controls on CH4 exchange over an evergreen Mediter-ranean forest Agric For Meteorol 226 ndash22767ndash79

194 Covey KR Wood SA Warren RJ Lee X Bradford MA 2012 Elevatedmethane concentrations in trees of an upland forest Geophys Res Lett39L15705 httpsdoiorg1010292012GL052361

195 Serrano-Silva N Sarria-Guzmaacuten Y Dendooven L Luna-Guido M 2014Methanogenesis and methanotrophy in soil a review Pedosphere24291ndash307 httpsdoiorg101016S1002-0160(14)60016-3

196 Shoemaker JK Keenan TF Hollinger DY Richardson AD 2014 Forestecosystem changes from annual methane source to sink depending onlate summer water balance Geophys Res Lett 41673ndash 679 httpsdoiorg1010022013GL058691

197 Esson KC Lin X Kumaresan D Chanton JP Murrell JC Kostka JE 2016Alpha- and gammaproteobacterial methanotrophs codominate theactive methane-oxidizing communities in an acidic boreal peat bogAppl Environ Microbiol 822363ndash2371 httpsdoiorg101128AEM03640-15

198 Nazaries L Murrell JC Millard P Baggs L Singh BK 2013 Methanemicrobes and models fundamental understanding of the soil methanecycle for future predictions Environ Microbiol 152395ndash2417 httpsdoiorg1011111462-292012149

199 Okubo T Tsukui T Maita H Okamoto S Oshima K Fujisawa T Saito AFutamata H Hattori R Shimomura Y Haruta S Morimoto S Wang YSakai Y Hattori M Aizawa S-I Nagashima KVP Masuda S Hattori TYamashita A Bao Z Hayatsu M Kajiya-Kanegae H Yoshinaga I Saka-moto K Toyota K Nakao M Kohara M Anda M Niwa R Jung-Hwan PSameshima-Saito R Tokuda S-I Yamamoto S Yamamoto S Yokoyama




httpmm

brasmorg

Dow

nloaded from

T Akutsu T Nakamura Y Nakahira-Yanaka Y Takada Hoshino Y Hi-rakawa H Mitsui H Terasawa K Itakura M Sato S Ikeda-Ohtsubo WSakakura N Kaminuma E Minamisawa K 2012 Complete genomesequence of Bradyrhizobium sp S23321 insights into symbiosis evolu-tion in soil oligotrophs Microb Environ 27306 ndash315

200 VanInsberghe D Maas KR Cardenas E Strachan CR Hallam SJ MohnWW 2015 Non-symbiotic Bradyrhizobium ecotypes dominate NorthAmerican forest soils ISME J 92435ndash2441 httpsdoiorg101038ismej201554

201 Berthrong ST Yeager CM Gallegos-Graves LV Steven B Eichorst SAJackson RB Kuske CR 2014 Nitrogen fertilization has a stronger effecton soil nitrogen-fixing bacterial communities than elevated atmo-spheric CO2 Appl Environ Microbiol 803103ndash3112 httpsdoiorg101128AEM04034-13

202 Hsu SF Buckley DH 2009 Evidence for the functional significance ofdiazotroph community structure in soil ISME J 3124 ndash136 httpsdoiorg101038ismej200882

203 Levy-Booth DJ Prescott CE Grayston SJ 2014 Microbial functionalgenes involved in nitrogen fixation nitrification and denitrification inforest ecosystems Soil Biol Biochem 7511ndash25 httpsdoiorg101016jsoilbio201403021

204 Pajares S Bohannan BJM 2016 Ecology of nitrogen fixing nitrifyingand denitrifying microorganisms in tropical forest soils Front Microbiol71045 httpsdoiorg103389fmicb201601045

205 Jung J Yeom J Han J Kim J Park W 2012 Seasonal changes innitrogen-cycle gene abundances and in bacterial communities in acidicforest soils J Microbiol 50365ndash373 httpsdoiorg101007s12275-012-1465-2

206 Isobe K Koba K Otsuka S Senoo K 2011 Nitrification and nitrifyingmicrobial communities in forest soils J For Res 16351ndash362 httpsdoiorg101007s10310-011-0266-5

207 Long X Chen C Xu Z Oren R He J-Z 2012 Abundance and communitystructure of ammonia-oxidizing bacteria and archaea in a temperateforest ecosystem under ten-years elevated CO2 Soil Biol Biochem46163ndash171 httpsdoiorg101016jsoilbio201112013

208 Laverman AM Speksnijder AG Braster M Kowalchuk GA Verhoef HAVan Verseveld HW 2001 Spatiotemporal stability of an ammonia-oxidizing community in a nitrogen-saturated forest soil Microb Ecol4235ndash 45 httpsdoiorg101007s002480000038

209 Szukics U Hackl E Zechmeister-Boltenstern S Sessitsch A 2012 Rapidand dissimilar response of ammonia oxidizing archaea and bacteria tonitrogen and water amendment in two temperate forest soils Micro-biol Res 167103ndash109 httpsdoiorg101016jmicres201104002

210 Hynes HM Germida JJ 2012 Relationship between ammonia oxidizingbacteria and bioavailable nitrogen in harvested forest soils of centralAlberta Soil Biol Biochem 4618 ndash25 httpsdoiorg101016jsoilbio201110018

211 Malchair S Carnol M 2012 AOB community structure and richnessunder European beech sessile oak Norway spruce and Douglas fir atthree temperate forest sites Plant Soil 366521ndash535 httpsdoiorg101007s11104-012-1450-x

212 Cong J Yang Y Liu X Lu H Liu X Zhou J Li D Yin H Ding J Zhang Y2015 Analyses of soil microbial community compositions and func-tional genes reveal potential consequences of natural forest succes-sion Sci Rep 510007 httpsdoiorg101038srep10007

213 Freedman Z Eisenlord SD Zak DR Xue K He Z Zhou J 2013 Towardsa molecular understanding of N cycling in northern hardwood forestsunder future rates of N deposition Soil Biol Biochem 66130 ndash138httpsdoiorg101016jsoilbio201307010

214 Shaw LJ Nicol GW Smith Z Fear J Prosser JI Baggs EM 2006 Ni-trosospira spp can produce nitrous oxide via a nitrifier denitrificationpathway Environ Microbiol 8214 ndash222 httpsdoiorg101111j1462-2920200500882x

215 Orellana LH Rodriguez-R LM Higgins S Chee-Sanford JC Sanford RARitalahti KM Loumlffler FE Konstantinidis KT 2014 Detecting nitrous oxidereductase (NosZ) genes in soil metagenomes method developmentand implications for the nitrogen cycle mBio 5e01193-14 httpsdoiorg101128mBio01193-14

216 Priyanka J Mukherjee K 2015 Diversity study of nitrate reducingbacteria from soil samplesmdasha metagenomics approach J Comp SciSyst Biol 8191ndash198

217 Rosch C Mergel A Bothe H 2002 Biodiversity of denitrifying anddinitrogen-fixing bacteria in an acid forest soil Appl Environ Microbiol683818 ndash3829 httpsdoiorg101128AEM6883818-38292002

218 Nelson MB Martiny AC Martiny JBH 2016 Global biogeography ofmicrobial nitrogen-cycling traits in soil Proc Natl Acad Sci U S A1138033ndash 8040 httpsdoiorg101073pnas1601070113

219 Szukics U Hackl E Zechmeister-Boltenstern S Sessitsch A 2009 Con-trasting response of two forest soils to nitrogen input rapidly alteredNO and N2O emissions and nirK abundance Biol Fertil Soils 45855ndash 863 httpsdoiorg101007s00374-009-0396-5

220 Richardson AE Simpson RJ 2011 Soil microorganisms mediating phos-phorus availability update on microbial phosphorus Plant Physiol 156989 ndash996 httpsdoiorg101104pp111175448

221 Barton LL Northup DE 2011 Microbial ecology Wiley-Blackwell Hobo-ken NJ

222 Bergkemper F Scholer A Engel M Lang F Kruger J Schloter M SchulzS 2016 Phosphorus depletion in forest soils shapes bacterial commu-nities towards phosphorus recycling systems Environ Microbiol 181988 ndash2000 httpsdoiorg1011111462-292013188

223 Bergkemper F Kublik S Lang F Kruger J Vestergaard G Schloter MSchulz S 2016 Novel oligonucleotide primers reveal a high diversity ofmicrobes which drive phosphorous turnover in soil J Microbiol Meth-ods 12591ndash97 httpsdoiorg101016jmimet201604011

224 Singh BK Bardgett RD Smith P Reay DS 2010 Microorganisms andclimate change terrestrial feedbacks and mitigation options Nat RevMicrobiol 8779 ndash790 httpsdoiorg101038nrmicro2439

225 Mouri G Nakano K Tsuyama I Tanaka N 2016 The effects of futurenationwide forest transition to discharge in the 21st century withregard to general circulation model climate change scenarios EnvironRes 149288 ndash296 httpsdoiorg101016jenvres201601024

226 Ruosch M Spahni R Joos F Henne PD van der Knaap WO Tinner W2016 Past and future evolution of Abies alba forests in Europemdashcomparison of a dynamic vegetation model with palaeo data andobservations Glob Chang Biol 22727ndash740 httpsdoiorg101111gcb13075

227 Ma W Liang J Cumming JR Lee E Welsh AB Watson JV Zhou M 2016Fundamental shifts of central hardwood forests under climate changeEcol Model 33228 ndash 41 httpsdoiorg101016jecolmodel201603021

228 Crabbe RA Dash J Rodriguez-Galiano VF Janous D Pavelka M MarekMV 2016 Extreme warm temperatures alter forest phenology andproductivity in Europe Sci Total Environ 563ndash564486 ndash 495 httpsdoiorg101016jscitotenv201604124

229 Zhang Z Qiao M Li D Yin H Liu Q 2016 Do warming-induced changesin quantity and stoichiometry of root exudation promote soil N trans-formations via stimulation of soil nitrifiers denitrifiers and ammonifi-ers Eur J Soil Biol 7460 ndash 68 httpsdoiorg101016jejsobi201603007

230 Vanhala P Bergstroumlm I Haaspuro T Kortelainen P Holmberg M Forsius M2016 Boreal forests can have a remarkable role in reducing greenhousegas emissions locally land use-related and anthropogenic greenhouse gasemissions and sinks at the municipal level Sci Total Environ 557ndash55851ndash57 httpsdoiorg101016jscitotenv201603040

231 Vanhala P Karhu K Tuomi M Bjoumlrkloumlf K Fritze H Hyvaumlrinen H Liski J2011 Transplantation of organic surface horizons of boreal soils intowarmer regions alters microbiology but not the temperature sensitivityof decomposition Glob Chang Biol 17538 ndash550 httpsdoiorg101111j1365-2486200902154x

232 Bonan GB 2008 Forests and climate change forcings feedbacks andthe climate benefits of forests Science 3201444 ndash1449 httpsdoiorg101126science1155121

233 Dooley SR Treseder KK 2011 The effect of fire on microbial biomassa meta-analysis of field studies Biogeochemistry 10949 ndash 61 httpsdoiorg101007s10533-011-9633-8

234 Pold G Melillo JM DeAngelis KM 2015 Two decades of warmingincreases diversity of a potentially lignolytic bacterial community FrontMicrobiol 6480 httpsdoiorg103389fmicb201500480

235 Norby RJ Delucia EH Gielen B Calfapietra C Giardina CP King JSLedford J McCarthy HR Moore DJ Ceulemans R De Angelis P Finzi ACKarnosky DF Kubiske ME Lukac M Pregitzer KS Scarascia-MugnozzaGE Schlesinger WH Oren R 2005 Forest response to elevated CO2 isconserved across a broad range of productivity Proc Natl Acad SciU S A 10218052ndash18056 httpsdoiorg101073pnas0509478102

236 Luo Y Su B Currie WS Dukes JS Finzi A Hartwig U Hungate BAMcMurtrie RE Oren R Parton WJ Pataki DE Shaw MR Zak DR FieldCB 2004 Progressive N limitation of ecosystem responses to rising




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CO2 Bioscience 54731ndash739 httpsdoi org1016410006-3568(2004)054[0731PNLOER]20CO2

237 Meier IC Pritchard SG Brzostek ER McCormack ML Phillips RP 2015The rhizosphere and hyphosphere differ in their impacts on carbon andnitrogen cycling in forests exposed to elevated CO2 New Phytol 2051164 ndash1174 httpsdoiorg101111nph13122

238 Dunbar J Eichorst SA Gallegos-Graves LV Silva S Xie G HengartnerNW Evans RD Hungate BA Jackson RB Megonigal JP Schadt CWVilgalys R Zak DR Kuske CR 2012 Common bacterial responses in sixecosystems exposed to 10 years of elevated atmospheric carbon diox-ide Environ Microbiol 141145ndash1158 httpsdoiorg101111j1462-2920201102695x

239 Sulman BN Phillips RP Oishi AC Shevliakova E Pacala SW 2014Microbe-driven turnover offsets mineral-mediated storage of soil car-bon under elevated CO2 Nat Clim Chang 41099 ndash1102 httpsdoiorg101038nclimate2436

240 Dunbar J Gallegos-Graves LV Steven B Mueller R Hesse C Zak DRKuske CR 2014 Surface soil fungal and bacterial communities in aspenstands are resilient to eleven years of elevated CO2 and O3 Soil BiolBiochem 76227ndash234 httpsdoiorg101016jsoilbio201405027

241 Lesaulnier C Papamichail D McCorkle S Ollivier B Skiena S Taghavi SZak D van der Lelie D 2008 Elevated atmospheric CO2 affects soilmicrobial diversity associated with trembling aspen Environ Microbiol10926 ndash941 httpsdoiorg101111j1462-2920200701512x

242 Garcia-Palacios P Vandegehuchte ML Shaw EA Dam M Post KHRamirez KS Sylvain ZA de Tomasel CM Wall DH 2015 Are there linksbetween responses of soil microbes and ecosystem functioning toelevated CO2 N deposition and warming A global perspective GlobChang Biol 211590 ndash1600 httpsdoiorg101111gcb12788

243 Schleppi P Bucher-Wallin I Hagedorn F Koumlrner C 2012 Increasednitrate availability in the soil of a mixed mature temperate forestsubjected to elevated CO2 concentration (canopy FACE) Glob ChangBiol 18757ndash768 httpsdoiorg101111j1365-2486201102559x

244 Reich PB Sendall KM Stefanski A Wei X Rich RL Montgomery RA2016 Boreal and temperate trees show strong acclimation of res-piration to warming Nature 531633ndash 636 httpsdoiorg101038nature17142

245 Zhao C Zhu L Liang J Yin H Yin C Li D Zhang N Liu Q 2014 Effectsof experimental warming and nitrogen fertilization on soil microbialcommunities and processes of two subalpine coniferous species inEastern Tibetan Plateau China Plant Soil 382189 ndash201 httpsdoiorg101007s11104-014-2153-2

246 Schindlbacher A Rodler A Kuffner M Kitzler B Sessitsch AZechmeister-Boltenstern S 2011 Experimental warming effects on themicrobial community of a temperate mountain forest soil Soil BiolBiochem 431417ndash1425 httpsdoiorg101016jsoilbio201103005

247 Rousk K Rousk J Jones DL Zackrisson O DeLuca TH 2013 Feathermoss nitrogen acquisition across natural fertility gradients in borealforests Soil Biol Biochem 6186 ndash95 httpsdoiorg101016jsoilbio201302011

248 Peltoniemi K Laiho R Juottonen H Kiikkila O Makiranta P MinkkinenK Pennanen T Penttilauml T Sarjala T Tuittila ES Tuomivirta T Fritze H2015 Microbial ecology in a future climate effects of temperature andmoisture on microbial communities of two boreal fens FEMS MicrobiolEcol 91fiv062 httpsdoiorg101093femsecfiv062

249 Wu J Xiong J Hu C Shi Y Wang K Zhang D 2015 Temperaturesensitivity of soil bacterial community along contrasting warming gra-dient Appl Soil Ecol 9440 ndash 48 httpsdoiorg101016japsoil201504018

250 Xue K Xie J Zhou A Liu F Li D Wu L Deng Y He Z Van Nostrand JDLuo Y Zhou J 2016 Warming alters expressions of microbial functionalgenes important to ecosystem functioning Front Microbiol 7668httpsdoiorg103389fmicb201600668

251 Schuumltt M Borken W Spott O Stange CF Matzner E 2014 Temperaturesensitivity of C and N mineralization in temperate forest soils at lowtemperatures Soil Biol Biochem 69320 ndash327 httpsdoiorg101016jsoilbio201311014

252 Li J Ziegler SE Lane CS Billings SA 2013 Legacies of native climateregime govern responses of boreal soil microbes to litter stoichiometryand temperature Soil Biol Biochem 66204 ndash213 httpsdoiorg101016jsoilbio201307018

253 Galloway JN Dentener FJ Capone DG Boyer EW Howarth RW Seitz-inger SP Asner GP Cleveland CC Green PA Holland EA Karl DMMichaels AF Porter JH Townsend AR Vorosmarty CJ 2004 Nitrogen

cycles past present and future Biogeochemistry 70153ndash226 httpsdoiorg101007s10533-004-0370-0

254 Galloway JN Townsend AR Erisman JW Bekunda M Cai Z Freney JRMartinelli LA Seitzinger SP Sutton MA 2008 Transformation of thenitrogen cycle recent trends questions and potential solutions Sci-ence 320889 ndash 892 httpsdoiorg101126science1136674

255 Tamm CO 1991 Nitrogen in terrestrial ecosystems Springer BerlinGermany

256 Houmlgberg MN Blaško R Bach LH Hasselquist NJ Egnell G Naumlsholm THoumlgberg P 2014 The return of an experimentally N-saturated borealforest to an N-limited state observations on the soil microbial com-munity structure biotic N retention capacity and gross N mineralisa-tion Plant Soil 38145ndash 60 httpsdoiorg101007s11104-014-2091-z

257 Wallenstein MD McNulty S Fernandez IJ Boggs J Schlesinger WH2006 Nitrogen fertilization decreases forest soil fungal and bacterialbiomass in three long-term experiments For Ecol Manage 222459 ndash 468 httpsdoiorg101016jforeco200511002

258 Frey SD Ollinger S Nadelhoffer K Bowden R Brzostek E Burton ACaldwell BA Crow S Goodale CL Grandy AS Finzi A Kramer MG LajthaK LeMoine J Martin M McDowell WH Minocha R Sadowsky JJ Tem-pler PH Wickings K 2014 Chronic nitrogen additions suppress decom-position and sequester soil carbon in temperate forests Biogeochem-istry 121305ndash316 httpsdoiorg101007s10533-014-0004-0

259 Fierer N Lauber CL Ramirez KS Zaneveld J Bradford MA Knight R2012 Comparative metagenomic phylogenetic and physiological anal-yses of soil microbial communities across nitrogen gradients ISME J61007ndash1017 httpsdoiorg101038ismej2011159

260 Zak DR Holmes WE Burton AJ Pregitzer KS Talhelm AF 2008 Simu-lated atmospheric NO3 deposition increases soil organic matter byslowing decomposition Ecol Appl 182016 ndash2027 httpsdoiorg10189007-17431

261 Freedman ZB Zak DR 2015 Atmospheric N deposition alters connectancebut not functional potential among saprotrophic bacterial communitiesMol Ecol 243170ndash3180 httpsdoiorg101111mec13224

262 Freedman ZB Upchurch RA Zak DR Cline LC 2016 Anthropogenic Ndeposition slows decay by favoring bacterial metabolism insights frommetagenomic analyses Front Microbiol 7259 httpsdoiorg103389fmicb201600259

263 Maaroufi NI Nordin A Hasselquist NJ Bach LH Palmqvist K GundaleMJ 2015 Anthropogenic nitrogen deposition enhances carbon seques-tration in boreal soils Glob Chang Biol 213169 ndash3180 httpsdoiorg101111gcb12904

264 Ramirez KS Craine JM Fierer N 2012 Consistent effects of nitrogenamendments on soil microbial communities and processes acrossbiomes Glob Chang Biol 181918 ndash1927 httpsdoiorg101111j1365-2486201202639x

265 Kamble PN Rousk J Frey SD Baringaringth E 2013 Bacterial growth andgrowth-limiting nutrients following chronic nitrogen additions to ahardwood forest soil Soil Biol Biochem 5932ndash37 httpsdoiorg101016jsoilbio201212017

266 Frey SD Knorr M Parrent JL Simpson RT 2004 Chronic nitrogenenrichment affects the structure and function of the soil microbialcommunity in temperate hardwood and pine forests For Ecol Manage196159 ndash171 httpsdoiorg101016jforeco200403018

267 Long X Chen C Xu Z Linder S He J 2012 Abundance and communitystructure of ammonia oxidizing bacteria and archaea in a Sweden borealforest soil under 19-year fertilization and 12-year warming J Soils Sedi-ments 121124ndash1133 httpsdoiorg101007s11368-012-0532-y

268 Turlapati SA Minocha R Bhiravarasa PS Tisa LS Thomas WK MinochaSC 2013 Chronic N-amended soils exhibit an altered bacterial com-munity structure in Harvard Forest MA USA FEMS Microbiol Ecol83478 ndash 493 httpsdoiorg1011111574-694112009

269 Aber J McDowell WH Nadelhoffer K Magill A Berntson G Kamakea MMcNulty SG Currie WS Rustad L Fernandez IJ 1998 Nitrogen satura-tion in temperate forests Bioscience 48921ndash934 httpsdoiorg1023071313296

270 Zak DR Holmes WE Tomlinson MJ Pregitzer KS Burton AJ 2006Microbial cycling of C and N in northern hardwood forests receivingchronic atmospheric NO3 deposition Ecosystems 9242ndash253 httpsdoiorg101007s10021-005-0085-7

271 Zak DR Pregitzer KS Kubiske ME Burton AJ 2011 Forest productivityunder elevated CO2 and O3 positive feedbacks to soil N cycling sustaindecade-long net primary productivity enhancement by CO2 Ecol Lett141220 ndash1226 httpsdoiorg101111j1461-0248201101692x




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272 Li J Ziegler S Lane CS Billings SA 2012 Warming-enhanced preferen-tial microbial mineralization of humified boreal forest soil organicmatter interpretation of soil profiles along a climate transect usinglaboratory incubations J Geophys Res Biogeosci 117G2008

273 Luo X Fu X Yang Y Cai P Peng S Chen W Huang Q 2016 Microbialcommunities play important roles in modulating paddy soil fertility SciRep 620326 httpsdoiorg101038srep20326

274 Savage KE Parton WJ Davidson EA Trumbore SE Frey SD 2013Long-term changes in forest carbon under temperature and nitrogenamendments in a temperate northern hardwood forest Glob ChangBiol 192389 ndash2400 httpsdoiorg101111gcb12224

275 Stone MM Weiss MS Goodale CL Adams MB Fernandez IJ German DPAllison SD 2012 Temperature sensitivity of soil enzyme kinetics underN-fertilization in two temperate forests Glob Chang Biol 181173ndash1184httpsdoiorg101111j1365-2486201102545x

276 Schindlbacher A Schnecker J Takriti M Borken W Wanek W 2015Microbial physiology and soil CO2 efflux after 9 years of soil warming ina temperate forestmdashno indications for thermal adaptations GlobChang Biol 214265ndash 4277 httpsdoiorg101111gcb12996

277 Yue K Peng Y Peng C Yang W Peng X Wu F 2016 Stimulation ofterrestrial ecosystem carbon storage by nitrogen addition a meta-analysis Sci Rep 619895 httpsdoiorg101038srep19895

Salvador Lladoacute is a researcher whose maincareer focus is to relate bacterial identity tofunctionality related to the C cycle in tem-perate forest soils During his PhD researchin the Department of Microbiology of theUniversity of Barcelona he worked on char-acterizing bacterial populations involved inthe decomposition of hydrocarbon pollut-ants in contaminated soils After he obtainedhis PhD in December 2013 he moved tothe laboratory of Petr Baldrian in the Labo-ratory of Environmental Microbiology of the Czech Academy of Sci-ences where he is applying DNA and RNA high-throughput sequencingand metabolomics combined with classical microbiological methods ofisolation and physiological characterization to obtain a better under-standing of the roles of the most abundant bacteria in the C and Ncycles in forest soils His broader interest is to be able to relate bacterialcommunity structure and functionalities in soils with the changing Cfluxes due to climate change

Rubeacuten Loacutepez-Mondeacutejar studied biology atthe University of Murcia (Spain) and carriedout his research in the Department of Soiland Water Conservation at the CEBAS-CSIC(Spain) working on the application of mo-lecular methods to improve the use of ben-eficial microorganisms in agriculture and hereceived his PhD in applied biology fromthe University of Alicante (Spain) in 2011Afterwards he become a postdoctoral re-searcher in the Laboratory of EnvironmentalMicrobiology of the CAS (Czech Republic) and worked on the study ofthe composition and ecology of soil bacteria by using multiomicsmethods His current research is focused on exploring the bacterialsystems involved in polysaccharide degradation in forest soil and indiscovering new microorganisms and enzymes useful for biomass con-version and for the production of environmentally friendly chemicalsand biofuels His broader interest is to unveil the enormous potentialof microbial strains as natural resources for the different fields ofbiotechnology

Petr Baldrian received his PhD in microbi-ology at the Charles University in PragueCzech Republic based on work describingthe effects of metals on wood-rotting fungiHe later changed his topic to environmentalmicrobiology focusing on enzyme activitiesand the fungal contribution to decomposi-tion of litter and soil organic matter as wellas the characterization of enzymatic systemsof microorganisms and their biotechnologi-cal potential He is now Head of the Labora-tory of Environmental Microbiology of the Institute of Microbiology ofthe Czech Academy of Sciences in Prague Recently he contributed tothe identification of the active fraction of the soil microbiome and theanalysis of the relative contributions of bacteria and fungi to ecosystemprocesses His work is mostly focused on the functioning of forest soilsthe seasonality of microbial processes and the drivers of communityassembly of soil bacteria and fungi




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INTRODUCTION

Forests represent one of the largest and most important ecosystems on Earthcovering more than 40 million km2 and representing 30 of the total global land

area (1) Forest ecosystems are found in most of Earthrsquos biomes and harbor a largeproportion of the global diversity For example temperate and boreal forests occupymost of the land surface of the Northern Hemisphere and contain 46 of all trees onEarthmdash 066 and 074 trillion respectively (2) Due to their global extension theprocesses occurring in these two biomes are of global importance and an understand-ing of the composition and function of their microbiomes is thus essential (Fig 1)

Forests typically represent important carbon (C) sinks with large amounts of recal-citrant organic matter in their soils especially the temperate forest soils which receivetons of litter per hectare yearly (3) The presence of large trees distinguishes forestsfrom grasslands wetlands and agricultural areas in multiple ways (4) Trees representa multitude of habitats such as the phyllosphere or rhizosphere but they also sub-stantially affect the remaining parts of the ecosystem This is mainly because as thedominant primary producers they supply the bulk of the C that enters the ecosystemand while some of this C is in the form of simple organic molecules a significantfraction such as the complex biomass of wood litter or roots is composed ofrecalcitrant biopolymers (4) Trees also largely contribute to the spatial heterogeneity offorest ecosystems by multiple means including the penetration of soils by variousguilds of roots generation of patches of litter and ground vegetation and changes ofthe morphology of the terrain during uprooting or the production of deadwood (4 5)

Temperate forests extend approximately from latitudes 25degN to 50degN graduallychanging into boreal forests further north (6) The southern limit of boreal forests isunderstood as the latitude at which conifers are competitively excluded by temperatetree species with higher rates of photosynthesis There is however no distinct bound-ary between the two biomes but rather a broad transition zone that includes a mix ofconiferous and deciduous tree species (7) Temperate forests are characterized bytemperature ranges between 30 and 30degC with hot summers and cold winters andwith 750 to 1300 mm of precipitation per year Boreal forestsmdash or mountainous forestsin the temperate zonemdashface lower temperatures with cold winters lasting more than6 months and average summer temperatures of around 10degC Despite the lowerprecipitation levels (300 to 900 mm of rain per year) boreal forests are typically moistbecause of the reduced evaporation at low temperatures In addition other factorssuch as elevation substrate drainage physical soil properties and nutrient availabilityare also responsible for the distribution of forest types on landscape scales

Temperate forests are composed of a large variety of deciduous trees whileconiferous trees dominate temperate forests at higher altitudes but also occur fre-quently in plantation forests (8 9) Boreal forests exhibit a reduced tree diversity witha larger proportion of coniferous trees (10)

Although temperate and boreal forests fulfill several important ecosystem servicestheir role as large C sinks has gained specific interest in recent decades especially in thecontext of global change Recent approximations indicate that the current C stockstored in forests worldwide is approximately 861 Pg of which 44 is in soil 42 inabove- and belowground biomass 8 in deadwood and 5 in litter (11) Of the globalstock of C stored by forests boreal forests contain 32 and temperate forests another14 indicating that their importance for global C sequestration is equivalent to that oftropical forests (11) The large amount of stored C has the potential to influence thefeedback between the climate and the global C cycle (12) In this sense global changeincluding both climate change and other changes linked to human activities has beenrecognized as a major threat to forests (13) Over the millennia human overexploitationhas been the most important risk for forests and the C balance of forests is largelyaffected by human activities including deforestation the management of productionforest reforestation afforestation and others (11 14) Other disturbances that areassociated with climate change and atmospheric drivers are also affecting the C




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Carbon Dioxide



Global Warming





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onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from










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brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























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brasmorg

Dow

nloaded from












































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brasmorg

Dow

nloaded from









































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brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























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Dow

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httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from










httpmm

brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from











httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























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brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from







httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from








httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























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brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from









httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























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brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from


Carbon Dioxide



Global Warming





httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

lco

mm

unity

com

pos

ition

2G

ram

-neg

ativ

eb

acte

ria

1A

cido

bact

eria

1

Alp

hapr

oteo

bact

eria

162

462

76

Tem

per

ate

fore

stA

cer

rubr

umB

etul

apa

pyrif

era

Que

rcus

velu

tina

Ace

rpe

nsyl

vani

cum

1ox

idat

ive

activ

ity1

bac

teria

ldi

vers

ity1

Aci

doba

cter

ia1

Act

inob

acte

ria23

4

NBo

real

fore

stPi

cea

abie

s1

soil

C(h

igh

Nde

pos

ition

)2

soil

resp

iratio

n(h

igh

Nde

pos

ition

)

2b

acte

rial

bio

mas

s

amoA

gene

abun

danc

e

AO

Bco

mm

unity

com

pos

ition

263

267

Tem

per

ate

fore

stA

cer

sacc

haru

m2

SOM

deco

mp

ositi

on2

soil

resp

iratio

n

NPP

1O

Min

fore

stflo

or2

extr

acel

lula

ren

zym

eac

tivity

1N

inso

ilor

gani

cm

atte

r1

NO

3

leac

hing

2b

acte

rial

dive

rsity

(site

spec

ific)

1

carb

ohyd

rate

met

abol

ism

gene

s1

arom

atic

met

abol

ism

gene

s1

resp

iratio

nm

etab

olis

mge

nes

2ch

itin

deco

mp

ositi

onge

nes

(site

spec

ific)

2lig

noce

llulo

sede

com

pos

ition

gene

s(s

itesp

ecifi

c)

2N

cycl

ege

nes

(site

spec

ific)

2Ba

cter

oide

tes2

Gam

map

rote

obac

teria

1

Firm

icut

es1

Act

inob

acte

ria

2A

cido

bact

eria

2Ve

rruc

omic

robi

a

213

260ndash

262

264

Tem

per

ate

fore

stFa

gus

gran

difo

liaA

cer

sacc

haru

m

Ace

rru

brum

Pic

earu

bens

2so

ilre

spira

tion

(Pr

uben

ssi

te)

2m

icro

bia

lb

iom

ass

(Pr

uben

ssi

te)

257

(Con

tinue

don

follo

win

gp

age)




httpmm

brasmorg

Dow

nloaded from

TAB

LE1

(Con

tinue

d)

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

Tem

per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

extr

acel

lula

ren

zym

eac

tivity

1lig

nin

reca

lcitr

ant

C1

NO

3

1ni

trifi

catio

n

litte

rfa

ll(e

xcep

t1

atPi

nus

site

)

root

bio

mas

s(e

xcep

t2

atPi

nus

site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

bac

teria

lric

hnes

s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

Tem

per

ate

and

bor

eal

fore

sts

1ab

oveg

roun

dN

PP

1b

elow

grou

ndC

1tr

eegr

owth

1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

Csi

nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

sin

dica

tein

crea

ses

and

decr

ease

sof

the

liste

dp

aram

eter

s

no

sign

ifica

ntch

ange

inth

ep

aram

eter

s

igni

fican

tch

ange

inth

ep

aram

eter




httpmm

brasmorg

Dow

nloaded from




Nitrogen Deposition






httpmm

brasmorg

Dow

nloaded from




CONCLUSIONS






httpmm

brasmorg

Dow

nloaded from



























httpmm

brasmorg

Dow

nloaded from












































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from











































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from










































httpmm

brasmorg

Dow

nloaded from









































httpmm

brasmorg

Dow

nloaded from













httpmm

brasmorg

Dow

nloaded from

TAB

LE1

Effe

cts

ofca

rbon

diox

ide

tem

per

atur

ean

dni

trog

enin

crea

ses

onb

acte

rial

com

mun

ities

and

bio

geoc

hem

istr

yin

nort

hern

fore

sts

inm

anip

ulat

ive

exp

erim

ents

a

Man

ipul

atio

nH

abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

[CO

2]

Tem

per

ate

fore

stPi

nus

taed

aPo

pulu

str

emul

oide

sPo

pulu

sal

baP

inus

nigr

aA

cer

sacc

haru

mB

etul

apa

pyrif

era

1N

PP1

effic

ienc

yof

C-fi

xing

enzy

mes

1N

sequ

estr

atio

n

bac

teria

lb

iom

ass

A

OB

bio

mas

s1

bac

teria

ldi

vers

ity

Prot

eoba

cter

ia(2

Brad

yrhi

zobi

um

1Rh

odop

lane

s1

Pseu

dom

onas

1

Nitr

osos

pira

)1

Act

inob

acte

ria

1Ba

cter

oide

tes2

Aci

doba

cter

ia(e

xcep

tG

p4

and

Gp

6)

207

235

236

241

271

Tem

per

ate

fore

stPi

nus

taed

a1

dich

otom

ous

bra

nchi

ngin

dex

1ro

otso

ilex

plo

ratio

n1

exud

atio

n(g

row

ing

seas

on)

1N

AG

ase

activ

ity1

phe

nol

oxid

ase1

NH

4tu

rnov

er

1m

icro

bia

lb

iom

ass

(gro

win

gse

ason

)12

012

1

Tem

per

ate

fore

stPo

pulu

str

emul

oide

sBe

tula

papy

rifer

aA

cer

sacc

haru

m

Pinu

ssy

lves

tris

1SO

Mde

com

pos

ition

1

deco

mp

ositi

onof

low

-m

olec

ular

-wei

ght

orga

nic

acid

s

b

acte

rial

abun

danc

e1

bac

teria

ldi

vers

ity2

Aci

doba

cter

ia2

Bact

eroi

dete

s1

Burk

hold

eria

1N

itros

ospi

ra15

224

0

Tem

per

ate

fore

stFa

gus

sylv

atic

a

NPP

1SO

Mde

com

pos

ition

1

gene

sfo

rde

com

pos

ition

ofla

bile

C

NH

41

NO

3

dep

letio

n1

exud

atio

n

2b

acte

rial

dive

rsity

1Ps

eudo

mon

as1

Act

inob

acte

ria

1Pl

anct

omyc

etes

1Fi

rmic

utes

2

Aci

doba

cter

ia(e

xcep

tG

p5

Gp

6an

dG

p7)

144

Tem

per

ate

fore

stFa

gus

sylv

atic

aQ

uerc

usro

bur

Que

rcus

petr

aea

Carp

inus

betu

lus

N

PP

NH

41

NO

3

accu

mul

atio

n

CN

ratio

for

tree

s

243

Tem

pBo

real

fore

stA

bies

bals

anea

Pin

ussy

lves

tris

Pi

cea

abie

s1

soil

resp

iratio

n1

enzy

me

activ

ities

onla

bile

C

SOM

deco

mp

ositi

on

m

icro

bia

lb

iom

ass

m

icro

bia

lco

mm

unity

com

pos

ition

231

272

Tem

per

ate

fore

stPi

cea

aspe

rata

1ro

otex

udat

ion

rate

s1

CN

ratio

for

exud

ates

1SO

Mde

com

pos

ition

273

Tem

per

ate

fore

stPi

cea

rube

nsA

bies

bals

amea

Fa

gus

gran

difo

liaA

cer

sacc

haru

mA

cer

rubr

umB

etul

ale

nta

Prun

usse

rotin

eQ

uerc

usru

bra

1so

ilre

spira

tion1

SOM

deco

mp

ositi

on1

V ma

xof

enzy

mes

274

275

Tem

per

ate

fore

stBe

tula

papy

rifer

aBe

tula

lent

aA

cer

rubr

umQ

uerc

usve

lutin

aQ

uerc

usru

bra

Fagu

sgr

andi

folia

Pic

eaab

ies

Fagu

ssy

lvat

ica

Abi

esal

ba

1so

ilre

spira

tion1

extr

acel

lula

ren

zym

eac

tivity

C

N

b

acte

rial

bio

mas

s

bac

teria

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ition

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unity

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ition

263

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per

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ific)

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ssi

te)

257

(Con

tinue

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win

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age)




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TAB

LE1

(Con

tinue

d)

Man

ipul

atio

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abit

atV

eget

atio

nEf

fect

son

bio

geo

chem

istr

yEf

fect

son

bac

teri

alp

opul

atio

ns

Effe

cts

onb

acte

rial

taxa

Sele

cted

refe

ren

ce(s

)

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per

ate

fore

stPi

nus

resi

nosa

Que

rcus

velu

tina

Que

rcus

rubr

aBe

tula

lent

aA

cer

rubr

umF

agus

gran

difo

lia

2so

ilre

spira

tion2

SOM

deco

mp

ositi

on1

Cst

ocks

(exc

ept

atPi

nus

site

)1

tree

bio

mas

s2

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acel

lula

ren

zym

eac

tivity

1lig

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reca

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ant

C1

NO

3

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catio

n

litte

rfa

ll(e

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t1

atPi

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site

)

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mas

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atPi

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site

)

root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

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teria

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s1

spec

ific

oper

atio

nal

taxo

nom

icun

its

1Pr

oteo

bact

eria

A

cido

bact

eria

257

266

268

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per

ate

and

bor

eal

fore

sts

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oveg

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PP

1b

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ndC

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ter

fall

lit

ter

deco

mp

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on

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resp

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n1

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nk

2m

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bia

lb

iom

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277

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inth

ep

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CONCLUSIONS






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TAB

LE1

(Con

tinue

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Man

ipul

atio

nH

abit

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geo

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istr

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son

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teri

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ce(s

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Tem

per

ate

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rcus

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cer

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umF

agus

gran

difo

lia

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tion2

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mp

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on1

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ocks

(exc

ept

atPi

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site

)1

tree

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mas

s2

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zym

eac

tivity

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C1

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3

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n

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ll(e

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site

)

root

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mas

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site

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root

pro

duct

ivity

2m

icro

bia

lb

iom

ass1

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teria

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hnes

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spec

ific

oper

atio

nal

taxo

nom

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its

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eria

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cido

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eria

257

266

268

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per

ate

and

bor

eal

fore

sts

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roun

dN

PP

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elow

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ndC

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1lit

ter

fall

lit

ter

deco

mp

ositi

on

soil

resp

iratio

n1

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nk

2m

icro

bia

lb

iom

ass

277

aA

rrow

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ifica

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ep

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Nitrogen Deposition






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CONCLUSIONS






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CONCLUSIONS






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forest soil bacteria: diversity, involvement in ecosystem ...and boreal forests. although most...

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