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Ecology and Evoluon 2017; 7: 855–862
|
855
www.ecolevol.org
Received:20July2016
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Revised:30October2016
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Accepted:27November2016
DOI:10.1002/ece3.2700
ORIGINAL RESEARCH
Links between soil microbial communies and plant traits in a
species- rich grassland under long- term climate change
Emma J. Sayer1,2,3 | Anna E. Oliver4 | Jason D. Fridley5 | Andrew P. Askew5 |
Robert T. E. Mills1 | J. Philip Grime6
ThisisanopenaccessarcleunderthetermsoftheCreaveCommonsAribuonLicense,whichpermitsuse,distribuonandreproduconinanymedium,
providedtheoriginalworkisproperlycited.
©2017TheAuthors.Ecology and Evoluon publishedbyJohnWiley&SonsLtd.
1LancasterEnvironmentCentre,Lancaster
University,Lancaster,UK
2SmithsonianTropicalResearchInstute,
Panama,RepublicofPanama
3DepartmentofEnvironment,Earthand
Ecosystems,TheOpenUniversity,Milton
Keynes,UK
4CentreforEcologyandHydrology,
Wallingford,UK
5DepartmentofBiology,SyracuseUniversity,
Syracuse,NY,USA
6DepartmentofAnimalandPlant
Sciences,UniversityofSheeld,Sheeld,UK
Correspondence
EmmaJ.Sayer,LancasterEnvironmentCentre,
LancasterUniversity,Lancaster,UK.
Email:e.sayer@lancaster.ac.uk.
Funding informaon
USNaonalScienceFoundaon,Grant/Award
Number:DEB1242529;EcologicalConnuity
Trust
Abstract
Climatechangecaninuencesoilmicroorganismsdirectlybyalteringtheirgrowthand
acvitybutalsoindirectlyviaeectsonthevegetaon,whichmodiestheavailability
ofresources.Directimpactsofclimatechangeonsoilmicroorganismscanoccurrap-
idly,whereasindirecteectsmediatedbyshisinplantcommunitycomposionare
notimmediatelyapparentandlikelytoincreaseoverme.Weusedmolecularnger-
prinngofbacterialand fungal communies in the soil to invesgate the eects of
17years of temperature and rainfall manipulaons in a species-rich grassland near
Buxton,UK.Wecomparedshisinmicrobialcommunitystructuretochangesinplant
speciescomposionandkeyplanttraitsacross78micrositeswithinplotssubjectedto
winterheang, rainfall supplementaon, or summerdrought. We observed marked
shisinsoilfungalandbacterialcommunitystructureinresponsetochronicsummer
drought. Importantly, although dominant microbial taxa were largely unaected by
drought,thereweresubstanalchangesintheabundancesofsubordinatefungaland
bacterialtaxa.Incontrasttoshort-termstudiesthatreporthighresistanceofsoilfungi
todrought,weobservedsubstanallossesoffungaltaxainthesummerdroughttreat-
ments. There was moderate concordance between soil microbial communies and
plant species composion within microsites. Vector ng of community-weighted
meanplanttraitstoordinaonsofsoilbacterialandfungalcommuniesshowedthat
shisin soilmicrobialcommunitystructure wererelatedtoplant traitsrepresenng
thequalityofresourcesavailabletosoilmicroorganisms:theconstruconcostofleaf
material,foliarcarbon-to-nitrogenraos,andleafdrymaercontent.Thus,ourstudy
providesevidencethatclimate change could aect soil microbial communies indi-
rectlyvia changesinplant inputsandhighlights theimportanceofconsidering long-
termclimate change eects, especially innutrient-poor systems with slow-growing
vegetaon.
KEYWORDS
Buxton,drought,grassland,resilience,resistance,soilbacteria,soilfungi,subordinatetaxa
856
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SAYER Et Al.
1 | INTRODUCTION
Theextremelyhigh diversityofsoil microorganismsmakesitdicult
toestablishlinksbetweenindividualmicrobialtaxaandspecicfunc-
ons(Allison&Marny,2008).Shisincommunitystructurecangive
arstindicaonofwhenandhowmicrobialadaptaonwillinuence
the rate of ecosystem processes (McGuire & Treseder, 2010), and
hence,idenfyingthe responsesofmicrobialcommuniestochange
isanimportantrststeptodeterminingthefunconalconsequences
for ecosystems (Wallenstein & Hall, 2012; Zak, Pregitzer, Burton,
Edwards,&Kellner,2011).
Soil microbial communies carryout the bulk of decomposion
(Swi, Heal, & Anderson, 1979) and catalyse many important pro-
cessesthat drive terrestrialcarbon and nutrientcycling(Schlesinger,
1991). Changes in precipitaon and temperature can aect soil
microbial communies directlyby altering their growth and acvity
butalsoindirectlyviaeectsonthevegetaon(Bardge,Freeman,&
Ostle,2008).Plant-mediatedeectsincludechangesinplantgrowth,
biomassallocaon,photosynthecrate, lier quality, and wateruse
eciency, which are all likely to aect soil microbial communies
(Gutknecht,Field,&Balser,2012).Atthe sameme,plant growthis
alsostronglyinuencedbythesoilmicrobialcommunitybecauseplant
nutrientrequirementsarelargelymetbythebreakdownandmineral-
izaon of organicmaer, which requires the combined acvies of
many dierent microorganisms (Burns etal., 2013). This reciprocal
exchange ofresources between plants and soil microbial communi-
es underpins ecosystem funcon, succession, and recovery from
disturbance(Reynoldsetal.2003)and ishence centraltoecosystem
responsestoglobalchange.
Contrary to the widely held view that high funconal redun-
dancyof microorganisms confers resilienceandresistanceof com-
muniestoperturbaons,soil microbial communies are generally
sensiveto change and not immediatelyresilientaer disturbance
(Allison & Marny,2008). Shis in microbial community composi-
oninresponsetodisturbanceariseprimarilyasaresultofvariaon
inthegrowthratesandresource-useecienciesofthe constuent
organisms,aswellastheirinherentresistanceandacclimaoncapac-
ies(Schimel,Balser,&Wallenstein,2007).Ingeneral,soilfungihave
higherC:Nbiomassstoichiometry,slowergrowthandturnoverrates,
and higher potenal carbon use eciency compared to bacteria
(Waring,Averill,&Hawkes,2013). The lower nutrient requirement
of fungi and their ability to degrade recalcitrant plant lier gives
them an advantage when resource quality is low, whereas rapid
growth and turnover make bacteria beer competors for labile,
high-qualitysubstrates(Waringetal.,2013).Thesegeneralpaerns
ofresourceuseand turnoversupportthe widelyheldviewthatsoil
foodwebsdominatedbyfungiaremoreresistanttoclimatechanges,
whereas bacteria-dominated systems are more resilient (De Vries
etal.,2012a). Nonetheless,there arealso substanaldierencesin
thephysiologies,adapvecapacies,andresourceuseoforganisms
withinagiventaxonomicgroup, which will shape community-level
responsestoclimatechange.
Soilmicrobialcommuniesthatexperiencehighnaturalvariaonin
environmentalcondionsarelikelytobedominatedbygeneralisttaxa
with broad tolerances and resourceuse (Wallenstein & Hall, 2012).
Bycontrast, taxa with specialist funcons or high resourcespecic-
ityarelikelytobemoresensivetodisturbance(Schimel,1995).The
responsesofthesesubordinatetaxatoclimatechangesmaybeparc-
ularlyimportantforthefunconingofnutrient-poorsystemsbecause
species-richplantassemblages havehighchemical diversity(vander
Heijden,Bardge,&vanStraalen,2008),whichrequiresgreatermicro-
bial resourcespecicity and reduces funconal redundancy (Waring
etal.,2013).Assoilmicrobesfacilitatenutrient-drivennicheparon-
inginplants(Reynolds&Haubensak,2008),changesinmicrobialcom-
munitystructureoracvityasaresultofalteredresourceavailability
willfeedbacktoaectplantnutrientavailability.
Althoughtherearemulplelinesofevidencethatclimatechange
can rapidly aect soil microbial communies (Allison & Marny
2008),long-termexperimentsare requiredtoassessindirect eects
viachangesinplantspecies composion, especially in systemswith
stress-tolerant, slow-growing vegetaon.Importantly, dierences in
the resource use and adapve capacies of generalist and special-
ist soil microorganisms also make plant-mediated eectsof climate
changemuch hardertopredict thanthedirect eectsofchangesto
the abioc environment.As a result, community-level responses to
long-termchronicchangescoulddiersubstanallyfromtheimmedi-
ateresponsestoshort-termperturbaons(Schimeletal.,2007).
We invesgated long-term changes in soil bacterial and fungal
communiesattheBuxtonClimateChangeImpactsStudy(henceforth
“Buxton”), where temperature and rainfall have been manipulated
since 1993. Although the vegetaon in this nutrient-poor ancient
grasslandhas proven remarkablyresistant to changeatthecommu-
nitylevel (Grimeetal.,2008), there hasbeensubstanalsmall-scale
turnoverin plant speciescomposionwithin microsites (100cm2) in
responseto summerdrought andwinter heangtreatments(Fridley,
Grime,Askew,Moser,&Stevens,2011).Detailedexisngdataonplant
speciescomposionand plant traits in small-scale microsites within
thetreatmentplots(Fridley,Lynn,Grime,&Askew,2016;Fridleyetal.,
2011)makethisexperimentanidealplaormtoinvesgatepotenal
linksbetweenplantandmicrobialresponsestolong-termchange.We
hypothesized that long-term climate manipulaons would alter soil
microbialcommuniesandthat theshis insoilfungal andbacterial
community structure would be related to changes in plant species
composionviathequalityofplantinputstothesoil.
2 | METHODS
The Buxton study was established in 1993 on calcareous grassland
in Derbyshire, UK. Climate treatments are applied to 3-m×3-m
plotsinvefullyrandomizedblocks;afulldescriponofthesiteand
experimentaldesign is giveninGrime etal. (2000,2008).The treat-
ments sampled in the present study were: “heated” to 3°C above
ambient temperature from November to April; “drought” in which
rainfall is excluded during July and August; “watered” with water
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SAYER Et Al.
supplementaonof20% above the long-term averagefromJuneto
September;and nonmanipulated controls. Between2006and 2008,
eight 10-cm×10-cm microsites were established in each plot; the
microsites were characterized by detailed measurements of surface
soilpH(0–3cmdepth)andsoildepth(Fridleyetal.,2011),andallvas-
cularplantsinthemicrositesweresurveyedin2008and2012.
2.1 | Sampling
Soildepth variessubstanally acrossthestudy site,andas themost
pronounceddierences inplantspecies composion wereobserved
betweenthe shallowest anddeepestmicrosites within plots(Fridley
etal., 2011), we collected two soil samples from each of the two
shallowest(0–7cmsoil depth) and the two deepest (>20cm depth)
micrositesperplotinSeptember2011.Toexcludeimmediateabioc
eectsof the treatments, we sampled1monthaer the end of the
annual drought and rainfall treatments but before the start of the
winterwarmingtreatment.Weuseda1-cm-diameterpunchcorerto
minimizedisturbancetothevegetaon andthesamplingdepthin all
micrositeswas ≤10cm. Two oftheshallowestmicrosites were bare
bedrockandnosampleswerecollected;allothersampleswerecom-
positedtomakeonesampleper microsite,makingatotalof78sam-
ples.Allsamplesweretransportedtothelaboratoryoniceandfrozen
at−20°Conthesameday.
2.2 | Molecular analyses
To invesgate the eects of climate treatments on soil microbial
communies,weperformed communityngerprinngusingterminal
restriconfragmentlengthpolymorphism(TRFLP)analysisofsoilbac-
teriaand fungi. This low-cost high-throughputmethod can perform
as well as deep sequencing when invesgang ecological paerns
inmicrobial communies atlocalto regional scales(vanDorst etal.,
2014)andprovidesqualitavelysimilardataformodelingcommunity
dynamics(Powelletal.,2015).DNAwasextractedfrom0.25gofsoil
andresuspendedfollowing Griths,Whiteley,O’Donnell,andBailey
(2000) as described in Sayer etal. (2013). Briey, we targeted the
bacterial16SrRNA geneusingtheprimers63F and530R(Thomson,
Ostle,&McNamara,2010)andthefungalITSregionusingtheprimers
ITS1-FandITS4 (Klamer &Hedlund,2004;Klamer, Roberts, Levine,
Drake,&Garland,2002).Forwardprimerswerelabeledatthe5′end
with6FAMuorescentdye,andPCRwasconductedin50μlreacon
volumesusing50ngoftemplateDNA.Ampliconswerepuriedusing
PureLinkPCRpuricaon kits (Invitrogen, Paisley, UK)anddigested
using restricon endonuclease MspI for bacteria (Thomson etal.,
2010) and Taq1 for fungi (Jasalavich, Ostrofsky, & Jellison, 2000;
Singh, Dawson, Macdonald, & Buckland, 2009). Fragment analysis
wasperformedusinga3730DNA analyser(AppliedBiosystems,CA,
USA)andindividualterminalrestriconfragments(TRFs)werebinned
manuallyusingGenemarkersoware(SoGenecs,PA,USA).Priorto
stascalanalyses, theintensity ofeachTRFwasconverted torela-
veabundancebasedonthetotalintensityofalldetectedTRFs;for
plot-levelanalyses,we used themeanabundanceof each TRFfrom
the four microsites per plot. This approach provides a semiquan-
tave measure of abundance to assess dierences in soil microbial
communitystructureamongsitesbutprecludesmeasuresofdiversity
(Bent,Pierson,&Forney,2007)andexcludesrarespecies(Woodcock,
Curs,Head,Lunn,&Sloan,2006).
2.3 | Data analyses
All stascal analyses were carried out in R version 3.2.3 (R Core
Team2014), and allmulvariate analyses wereperformedusing the
vegan (Oksanen etal., 2011) package. As soil depth and pH within
microsites were inversely correlated, we used the rst axis scores
froma principal components analysis of mulple soil depth and pH
measurements to characterize each microsite (Fridley etal., 2011;
henceforth“micrositescores”).Foreach microsite, we also included
plantspeciesdatafromFridleyetal.(2011,2016)represenngeight
10-cm×10-cm quadrats within each 3×3-m plot and community-
weightedplant trait datafromFridley etal. (2016),represenngthe
quality and quanty of resources available to soil microorganisms:
specic leaf area (measured as fresh leaf area per gram dry mass);
maximumphotosynthec capacity(measured fromlightcurves); leaf
construconcost(ingramglucosepergramleaffollowingHeberling
&Fridley,2013);leafdrymaercontent(dry-to-freshmassrao);and
leafC:Nrao.Community-weighted trait values were calculated by
takingthe weightedaverageof trait valuesofthose speciespresent
inagivenmicrositefromtheirabundances,usingvisualcoverclasses
(0–4,5–24,25–49,50–74,75%+;Fridleyetal.,2016).
Theeectsofclimatetreatmentsonsoilfungalandbacterialcom-
munitycomposionattheplotlevelwereexaminedbypermutaonal
mulvariateanalysisofvariance(PerMANOVA;adonisfuncon)aer
tesngforhomogeneityofdispersionsamongtreatments(betadisper
funcon); modelswere tested with 9,999 permutaons constrained
within blocks of replicateplots (permutest funcon). We used non-
metricmuldimensionalscaling(NMDS)basedonBray–Cursdissim-
ilaries to represent shis in soil microbialcommunies (metaMDS
funcon);stablesoluonswithstressscores<0.2 andr2>.95were
usedforsubsequentanalyses,resulnginatwo-dimensionalsoluon
forbacteriaandathree-dimensionalsoluonforfungi.Wethenused
vectorngtotheNMDSordinaons(envtfuncon)todetermine
the eects of microsite, climate treatments, extracellular enzyme
acvies,andkeyplanttraits;signicancevaluesweregeneratedwith
9,999randompermutaonsstraedwithinexperimentalblocks.
Pairwise concordance between plant species composion and
soil fungal or bacterial communies in micrositeswithin each treat-
mentwasinvesgatedusingProcrustesrotaon(Procrustesfuncon)
basedonthemoststableNMDSsoluons forallthreecommunies;
theProcrustes stascwas testedwith 9,999 permutaons(protest
funcon).As no vegetaonsurveywas conducted in the soil micro-
bialsamplingyear (2011), werstcomparedplant species composi-
onfromthe 2008 and 2012 surveysand then performed separate
comparisons for each year. Plant species composion was highly
correlated between survey years (Procustes correlaon: m2=.58,
r2=.65, p<.001), and we found the same degree of concordance
858
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SAYER Et Al.
betweenplantspeciesandmicrobialcommunitycomposionregard-
lessofsurveyyear.Wethereforeusedthe2012vegetaondataforall
subsequentanalyses.
Todierenatetheresponsesof dominantandsubordinatefun-
galandbacterialtaxa,weperformedallordinaonswithandwithout
themostabundantTRFs.Weusedconservavecutopointsso that
<10%ofalltaxawereconsideredabundant.Consequently,dominant
taxaweredenedasthosewithtotalrelaveTRFabundance>0.75%
across all plots forfungi and >1% for bacteria; all other TRFswere
consideredassubordinatetaxa.
3 | RESULTS
Seventeenyearsofclimatetreatmentsresultedindivergentsoilfungaland
bacterialcommuniesatthewhole-plotlevel(PerMANOVAF3,19=1.00,
p=.028andF3,19=1.47,p=.01forfungiandbacteria,respecvely).We
idenedatotal of 230 fungal and 112bacterialtaxaacrossall micro-
sites;the dominant taxa (22fungaland19 bacterial taxa) werepresent
inalltreatmentsatsimilarrelaveabundances(Fig.S1),butweobserved
pronounceddierencesinsubordinate taxa(fungi:F3,19=1.20,p=.003;
bacteria:F3,19=1.53,p=.008;Figures1c,d,S2,andS3).
VectorngtoNMDSordinaonsofplot-leveldatarevealedthat
theheang andwateredtreatmentshadlileornoeect,butthere
weresubstanalchangesinsoilmicrobialcommuniesinthedrought
plots.Therewasonlyaminoreectofthesummerdroughttreatment
on the whole soil fungal community (r2=.12, p=.073; Figure1a)
but subordinate fungal taxa were signicantly aected by drought
(r2=.27, p=.044; Figure1c) and 66 of the 208 subordinate fun-
galtaxawere enrelyabsentfrom the drought treatments.Drought
alsoalteredbacterial communitystructure(r2=.2, p=.02;Figure1b)
but subordinate taxa werenot disproporonately aected (r2=.25,
p=.033;Figure1d)andonlysix ofthe 93subordinatebacterialtaxa
wereenrelyabsentfromthedroughtplots.
There was moderateconcordance between plant species and
soilmicrobialcommunitycomposioninmicrosites(Procrustescor-
relaon:m2=.81, r2=.44,p=.001for fungiandm2=.84, r2=.4,
p=.001 for bacteria; Figure2); the strength of the relaonships
decreased slightly when dominant taxawere excluded (m2=.88,
r2=.34andm2=.86,r2=.37forfungiandbacteria,respecvely).
Vector ng of microsite scoresand plant trait data to NMDS
ordinaons of soil microbial taxa revealed a signicant correlaon
between microsite characteriscs and soil fungal (r2=.16, p=.003)
andbacterial communitystructure(r2=.15,p=.003),but individual
planttraitsexplainedasimilaror greater amount ofvariaon in soil
microbialcommuniesamongmicrosites:Leafconstruconcostwas
the best predictor of shis in community structure for both fungi
(r2=.14, p=.004) and bacteria (r2=.20, p=.001). Soil fungal com-
munitystructurewasalsorelatedtoleafdrymaercontent(r2=.08,
p=.03;Figure3a),whereasbacterialcommunitystructurewasrelated
toplantC:Nraos(r2=.15,p=.009;Figure3b).Changesintherela-
ve abundances ofsubordinate microbial taxa were also associated
with the construcon cost of plant material (r2=.1, p=.025 and
r2=.09,p=.018 for fungiandbacteria,respecvely; Figure3c),and
shisinsubordinatebacterialtaxawerealsorelatedtotheC:Nrao
ofplantmaterial(r2=.13,p=.037;Figure3d).
FIGURE1 NMDSrepresentationof(a)
soilfungalcommunities,(b)soilbacterial
communities,(c)subordinatefungaltaxa,
and(d)subordinatebacterialtaxain
grasslandplotssubjectedtolong-term
climatetreatments;ordinationswere
basedonBray–Curtisdissimilaritiesand
hullsenvelopeallplotswithinatreatment,
where“C”iscontrol,“H”isheated,“D”is
drought,and“W”iswatered;significant
correlations(p<.05)betweenordination
axesandtreatmentsorcommunity-
weightedplanttraitsareshownasarrows,
where“Ccost”istheconstructioncostof
plantmaterial
–0.6 –0.20.2 0.40.6 0.8
–0.6
–0.4
–0.2
0.0
0.2
0.4
0.6
Ccost
C
D
H
W
NMDS Axis 2
–0.6 –0.4 –0.2 0.00.2 0.
40
.6
–0.4
–0.2
0.0
0.2
0.4
Drought
Ccost
C
DH
W
Control
Drought
Warming
Irrigated
–2.0 –1.5 –1.0 –0.50.0 0.51.0
–1.0
–0.5
0.0
0.5
1.0
1.5
Drought
Ccost
C
D
H
W
NMDS Axis 2
NMDS Axis 1
–0.5 0.00.5 1.0
–0.5
0.0
0.5
1.0
Drought
Ccost
C
D
H
W
(a) All fungi (b) All bacteria
(c) Subordinate fungi (d) Subordinate bacteria
NMDS Axis 1
|
859
SAYER Et Al.
4 | DISCUSSION
Long-term climate treatments at Buxton modied the communies
of bacteria and fungi in the soil. Whereas the relave abundances
of dominant microorganisms were similar among treatments, we
observedchangesinsubordinatefungalandbacterialtaxa.Wefound
evidence for potenal links between the observed changes in soil
microbial community structure and specic traits of the plant com-
munieswithinmicrosites.
4.1 | Climate treatment eects on soil microbial
community structure
In contrast to previous studies, we found a strong eect of drought
on soil fungal community structure in microsites within the climate
FIGURE2 ResidualsofProcrustes
rotations(unitless)showingthe
associationsbetweenNMDSsolutions
ofplantspeciescompositionand(a)soil
fungalcommunitiesor(b)soilbacterial
communitiesforeachmicrositewithinthe
Buxtonclimatetreatments,wherepale
shadedbarsdenoteshallowmicrositesand
solidbarsdenotedeepmicrosites;median
(dashedline)andupperandlowerquartiles
(dottedlines)areshown;largeresiduals
indicateindividualmicrositeswithaweak
concordancebetweenplantandmicrobial
communities
0.00
0.05
0.10
0.15
0.20
0.25
0.30
Procrustes residuals
(a)
0.00
0.05
0.10
0.15
0.20
0.25
0.30
Procrustes residuals
(b)
ControlDrought Heated Watered
FIGURE3 NMDSrepresentationof
(a)thesoilfungalcommunity,(b)thesoil
bacterialcommunity,(c)subordinatefungal
taxa,and(d)subordinatebacterialtaxa
inmicrositeswithintheBuxtonclimate
treatments;ordinationswerebasedon
Bray–Curtisdissimilaritiesandsignificant
correlationsofcommunity-weighted
plantfunctionaltraitsandenvironmental
variableswithordinationaxesareshownas
arrows,where“Msite”isamicrositescore
basedonmultiplemeasurementsofsoil
depthandpH,“Ccost”istheconstruction
costofplantmaterial,“C:N”isthecarbon-
to-nitrogenratioofplantmaterial,and
“LDMC”isleafdrymattercontent
–2 –1 012
–2
–1
0
1
2
Microsite
Drought
Ccost
LDMC
(a) All fungi
Control
Drought
Warming
Irrigated
NMDS Axis 2
–2 –1 012
–1.5
–1.0
–0.5
0.0
0.5
1.0
1.5
Microsite
Drought
C:N
Ccost
(b) All bacteria
–2 –1 012
–2
–1
0
1
2
Drought
Ccost
(c) Subordinate fungi
NMDS Axis 2
NMDS Axis 1
–2 –1 012
–1.5
–1.0
–0.5
0.0
0.5
1.0
1.5
Drought C:N
Ccost
(d) Subordinate bacteria
NMDS Axis 1
860
|
SAYER Et Al.
treatments,whichwaslargelyaresultofchangesinthe relaveabun-
dancesofsubordinatefungi (Figures1cand S2).This wasunexpected
becausefungi are widely regarded as drought-tolerant (Harris,1981;
Schimeletal.,2007)andpreviousstudieshavereportedhighresistance
ofsoilfungitodroughttreatments(DeVriesetal.,2012a;Fuchslueger,
Bahn,Fritz,Hasibeder,&Richter,2014;Yusteetal.,2011).Wepropose
twopossibleexplanaonsforthisapparentdiscrepancy:
1. Changes in the abundances of fungal taxa may be more im-
portant and more readily apparent in grasslands such as Buxton,
becausefungal decomposers are more importantinsystems with
low soil ferlity and slow-growing perennial plant species (De
Vries etal., 2012b). Conversely, many of the studies reporng
high resistance of soil fungi to drought were conducted in pro-
ducve grasslands with bacteria-dominated soil food webs (e.g.
De Vries etal., 2012a,b; Fuchslueger etal., 2014).
2. Toourknowledge,ourstudyisthersttodisnguishtheresponses
ofdominant and subordinate microbial taxa to long-term climate
treatments.Ontheonehand,thedominanttaxawerelargelyunaf-
fected by drought, which supports the hypothesis that they are
likelytobegeneralistswithabroadrangeoftolerances(Wallenstein
&Hall,2012).Ontheotherhand,32%ofallsubordinatefungaltaxa
wereenrelyabsentfromthedroughttreatments.Assubordinate
taxarepresentonlyasmallproporonof thetotal fungalcommu-
nity,thesechangeswouldgoundetectedinstudiesusingindiscrim-
inateorlow-resoluonmethodssuchasmicrobialbiomassorlipid
biomarkers,becausethosemeasurements would primarily reect
changesinmostabundanttaxa.
Weused generalfungal primers that donotspecically targetmy-
corrhizal fungi, and consequently, the observed shis in the drought
treatmentswillmainlyreectdierencesinthe abundancesofdecom-
poserandpathogenicfungi(Klamer&Hedlund,2004;Sayeretal.,2013).
Nonetheless,apreviousstudyatBuxtonshowedthatthedroughttreat-
mentsreducedthedensityofextraradicalmycorrhizalhyphaeinthesoil
(Staddonetal.,2003),whichcouldalsocontributetotheshisinfungal
communitystructureinourstudy.
Drought also alteredbacterial community structure in the soil but
subordinate taxa were not disproporonately aected (Figure1b,d)
and only six taxawere enrely absent from the droughtplots. As the
treatmentswereappliedduringtwosummermonthseachyear,thehigh
resilience of bacteria to short-term “pulse” disturbances (Shade etal.,
2012)couldallowmostsoilbacterialtaxatopersistinalltreatmentsand
microsites.Furthermore,dormant organisms,which areincluded inour
communityngerprints (Rastogi& Sani, 2011),canpersist under unfa-
vorablecondions,andrapidgrowthrateswouldallowdormantbacteria
torecoverrapidlyaertheendofatreatmentperiod(Shadeetal.,2012).
4.2 | Links between plant funconal traits and soil
microbial responses to change
Theorecally, the soil microbial communies at Buxton should be
adaptedtodroughtbecausetheynaturallyexperiencehigh variaon
in soil moisture (Schimel etal., 2007; Wallenstein & Hall, 2012).
Nonetheless,17yearsofchronicsummerdroughtalteredsoilmicro-
bialcommunies and the relaonships between soil microbial com-
munity structure, plant species composion, and plant traits within
themicrositesatBuxtonprovideevidencetosupportourhypothesis
for indirect eects of climate change on soil microbial community
structure via plant inputs. The climate treatments at Buxton have
resultedindisnctplantcommuniesinmicrositeswithinthedrought
andheatedplots (Fridleyetal.,2011).Arecentstudyof community-
weightedplanttraitsdemonstratedgreaterinvestmentinleafmaterial
by slow-growing, stress-tolerant plant species in the drought plots,
whereas the plant traits in the heated plots reect greater produc-
vityof more compevespecies (Fridley etal.,2016).We hypoth-
esizedthatshis inplanttraitsrepresenngthequalityandquanty
ofresourcesavailable to microorganisms could explain some of the
observedchangesinsoilmicrobialcommunies.
Changesin soil microbialcommuniesin the droughtplotswere
related to the high leaf construcon cost of slow-growing, stress-
tolerant vegetaon (Figures1 and 3; Fridley etal., 2011). Shis in
the relave abundances of microbial taxa could therefore reect
increased abundance oforganisms that are able to degrade recalci-
trantplantmaterial,withconcomitantdeclinesin taxadependent on
labile,nutrient-richplantmaterial.Shisinthesoilfungalcommunity
werealsorelatedtoleaf drymaercontent,whereaschangesinsoil
bacteria were related to dierences in plant C:N raos (Figure3).
These relaonships indicate that shis in the abundances of spe-
cictaxacouldbelinkedtodecomposionprocessesbecausefungal
decomposersarespecializedindegradingtough,nutrient-poorcarbon
sources,whereas many soil bacterial groups preferenally use more
labileplantmaterialandhavehighernutrientrequirements(DeBoer,
Folman,Summerbell,&Boddy,2005).
Changesin therelaveabundanceofsubordinate taxawerealso
relatedtofunconaltraitsassociatedwiththequalityof plantmate-
rial(Figure3b,d),butintriguingly,theconcordancebetweenplantand
microbialcommuniesdecreasedwhendominanttaxawereexcluded.
Thissuggests that the observedlinksbetweenmicrobial community
structureandvegetaon within microsites could be associated with
resource quality,rather than with parcular plant species. Species-
rich plant assemblages have high chemical diversity,which requires
greatermicrobial resource specicity and reduces funconal redun-
dancy(vanderHeijdenetal.,2008).Thesubstanallossesofsubordi-
natefungaltaxainthedroughtplotscouldthereforeindicategreater
sensivityofspecialists withhigh resourcespecicityorcompeve
exclusionbyorganismsthathavebeneedfromthechangesinplant
inputs. As the relave abundances of the dominant microbial taxa
remainedlargelyunchanged(Fig.S1),theshisinsoilmicrobialcom-
munitystructureamongclimatetreatmentswerelargelydrivenbythe
responsesofsubordinate taxaandweproposethatchangesin plant
inputswithinmicrositesrepresentaplausiblemechanismfortheshis
insubordinatesoilmicrobialtaxa.
As the aim of our study was to invesgate the possibility of
indirect, bioc eects of climate changes, we collected soil sam-
pleswhennotreatmentswereacvelybeingapplied;thisprecludes
|
861
SAYER Et Al.
analysisofseasonalchanges inmicrobialcommuniesbutensured
comparable soil temperature and soilwater content among treat-
ments (Fridleyetal., 2016). We found evidence of links between
plant traits and soil microbial communiesdespite the breadth of
microbialfunconalgroupsincludedinourcommunityngerprints;
theseeminglysmalleectsizesinourstudyareunsurprising,given
the high microbial diversityand the potenal inuence of numer-
oussoilphysical and chemical properes.SoilpHin parcular has
an overriding eect on soil bacteria (Fierer, Bradford, & Jackson,
2007;Griths etal., 2011), anditis conceivable thatsomeof the
observeddierencesinbacterialcommunitystructurearearesultof
lowersoilpHinthedroughtplotsanddeepmicrosites(Fridleyetal.,
2011) or a directeect of dierences in soil depth. Nevertheless,
plant C:N raos explained a greaterproporon of the variaonin
soil bacteria compared to micrositecharacteriscs (soil depth and
pH)andthecarbonconstruconcostsofplantmaterialexplained
anequivalentamountofvariaoninbothbacterialandfungalcom-
munity structures. Inaddion, the eect of microsite was weaker
or enrely absentwhen dominant microbial taxa were excluded,
whereastheeectofdroughtandtherelaonshipwithplantfunc-
onaltraitsremained(Figure3).Thissuggeststhatsubordinatetaxa
maybemoresensivetochangesinresourcequalitythansoildepth
orpH.Hence,wesuggestthattheconcordancebetweenplantspe-
cies composion and microbial community structure in our study
providesevidence forplant-mediated eects ofclimate change on
soilmicrobialcommuniesandthelinkstospecicplanttraitssug-
gest that decomposion processes mayplay an important role in
concertedabove-andbelowgroundresponsestolong-termclimate
change(McGuire&Treseder,2010).
5 | CONCLUSIONS
Our study highlights the importance of considering long-term and
indirect eects of climate changes on soil microbial communies,
especially in nutrient-poor systems with slow-growing vegetaon.
Whereasclimatechangescanrapidlymodifytheabiocenvironment,
comprehensive shis in community-level plant funconal traits are
likely to become more relevant and more apparent over me. The
unexpected drought response of soil fungi and the links between
microbialcommuniesandkeyplantfunconaltraitsinourstudysug-
gestthatmicrobial resistanceoracclimaontodirectclimatechange
eectscouldbesubsumedbyalteredplantspeciescomposioninthe
longrun,withasyetunknownconsequencesforecosystemfuncon.
ACKNOWLEDGMENTS
The Buxton Climate Change Impacts Laboratory is funded by the
USNaonalScienceFoundaon(DEB1242529)andtheEcological
Connuity Trust. The authors thank R.I. Griths for guidance on
analyses, M.S. Heard for help with eldwork, and L. Heernam for
technicalassistance.
CONFLICT OF INTEREST
Theauthorshavenoconictofinteresttodeclare.
DATA ACCESSIBILITY
AlloriginaldatausedinthispaperwillbearchivedinDryadandmade
publicly accessible upon publicaon; previously published data on
plant species composion and plant traits, which were used in the
analyses,arereferencedinthetext.
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inginformaontabforthisarcle.
How to cite this arcle:SayerEJ,OliverAE,FridleyJD,
AskewAP,MillsRTE,GrimeJP.Linksbetweensoilmicrobial
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long-termclimatechange.Ecol Evol. 2017;7:855–862.
doi:10.1002/ece3.2700.
