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ORIGINALARTICLEMicrobialregulationofthesoilcarboncycle:evidencefromgene–enzymerelationshipsPankajTrivedi1,ManuelDelgado-Baquerizo1,ChandaTrivedi1,HangweiHu2,IanCAnderson1,ThomasCJeffries1,JizhongZhou3,4,5andBrajeshKSingh1,61HawkesburyInstitutefortheEnvironment,WesternSydneyUniversity,PenrithSouth,NewSouthWales,Australia;2FacultyofVeterinaryandAgriculturalSciences,TheUniversityofMelbourne,Parkville,Victoria,Australia;3InstituteforEnvironmentalGenomicsandDepartmentofBotanyandMicrobiology,TheUniversityofOklahoma,Norman,OK,USA;4EarthSciencesDivision,LawrenceBerkeleyNationalLaboratory,Berkeley,CA,USA;5StateKeyJointLaboratoryofEnvironmentSimulationandPollutionControl,SchoolofEnvironment,TsinghuaUniversity,Beijing,Chinaand6GlobalCentreforLandBasedInnovation,WesternSydneyUniversity,PenrithSouth,NewSouthWales,AustraliaAlackofempiricalevidenceforthemicrobialregulationofecosystemprocesses,includingcarbon(C)degradation,hindersourabilitytodevelopaframeworktodirectlyincorporatethegeneticcompositionofmicrobialcommunitiesintheenzyme-drivenEarthsystemmodels.HereinweevaluatedthelinkagebetweenmicrobialfunctionalgenesandextracellularenzymeactivityinsoilsamplescollectedacrossthreegeographicalregionsofAustralia.Wefoundastrongrelationshipbetweendifferentfunctionalgenesandtheircorrespondingenzymeactivities.Thisrelationshipwasmaintainedafterconsideringmicrobialcommunitystructure,totalCandsoilpHusingstructuralequationmodelling.ResultsshowedthatthevariationsintheactivityofenzymesinvolvedinCdegradationwerepredictedbythefunctionalgeneabundanceofthesoilmicrobialcommunity(R240.90inallcases).OurfindingsprovideastrongframeworkforimprovedpredictionsonsoilCdynamicsthatcouldbeachievedbyadoptingagene-centricapproachincorporatingtheabundanceoffunctionalgenesintoprocessmodels.TheISMEJournaladvanceonlinepublication,10May2016;doi:10.1038/ismej.2016.65IntroductionSoilcarbon(C)hasavitalroleinregulatingclimate,nutrientcyclingandbiodiversityandthereforeinprovidingtheecosystemservicesthatareessentialtohumanwell-being(Schmidtetal.,2011;Victoriaetal.,2012).Managingsoilstoobtainmultipleeconomic,societalandenvironmentalbenefitsrequiresintegratedpoliciesandincentivesthatmaintainandenhancesoilC(Singhetal.,2010;Victoriaetal.,2012;Trivedietal.,2013).SoilmicroorganismscontributegreatlytoecosystemCbudgetsthroughtheirrolesasdecomposers,plantsymbiontsorpathogens,therebymodifyingnutrientavailabilityandinfluencingCturnoverandretentioninsoil(Bardgettetal.,2008;Singhetal.,2010;BardgettandvanderPutten,2014).Theincrediblenumbersandenormousdiversityofsoilmicrobescreateshugechallengetoestablishthelinksbetweendiversityandfunctionsrelatedtosoilorganicmatterdecompositionandstabilization(Hubbell,2005).Despitethevalidassumptionthatsoilmicrobesinfluencethewayinwhichecosystemsfunction,thereisaverylimitedevidenceonwhetherthereisadirectlinkbetweenmicrobialcommunitystructureandfunctionintheglobalbiogeochemicalcyclesofterrestrialecosystems(Roccaetal.,2014;Kubartováetal.,2015;vanderWaletal.,2015).Thesegapshavekeptsoilmicrobesoutsideoftheongoingdebatesaboutglobalbiodiversityloss,conservationandsustainablemanagementpolicies(BardgettandvanderPutten,2014)andhaveprecludedtheinclusionofmicrobialcommu-nitiesinglobalbiogeochemicalmodelssuchasEarthsystemmodels(ESMs)thatinformcitizensandpolicymakersofCdynamicsandexchangebetweenthebiosphereandtheatmosphere(Wiederetal.,2013,2015).UnderstandingtheextenttowhichsoilmicrobialcommunitiescontrolecosystemprocessesisthuscriticaltoestablisheffectivepoliciestopreservemicrobialdiversityhotspotsandthekeyecosystemfunctionsandservicesthatCorrespondence:PTrivediorBKSingh,HawkesburyInstitutefortheEnvironment,WesternSydneyUniversity,BuildingL9,LockedBag1797,HawkesburyCampus,PenrithSouth,NewSouthWales2751,Australia.E-mail:p.trivedi@westernsydney.edu.auorB.Singh@westernsydney.edu.auReceived27September2015;revised21March2016;accepted22March2016TheISMEJournal(2016),1–12©2016InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/16(Singhetal.,2010;BardgettandvanderPutten,2014).Extensivebodiesofworkhaveprovideddetailedinsightsintothemechanism(s)onthetransformationofsoilCpoolsbyextracellularenzymesexcretedintothesoilbymicrobes,thusallowingresearcherstodevelopenzyme-drivenESMsthatprovideabetterfittoobservations,especiallyinchangingenviron-ments(Allisonetal.,2010;Tresederetal.,2012;Wiederetal.,2013;Hararuketal.,2015).Process-levelanalysessuchasrespirationandenzymatictransformationofaddedsubstrateareusedasaproxyofmicrobialfunction,whichgivesvaluableinsightintooverallmicrobial-mediatedtransformationsinsoils.However,suchmeasurementsdonotprovideconcretelinksonmechanisms,microbialfunctionalcompositionanddiversitythatunderpinsprocess-leveldifferences(Reeveetal.,2010;Talbotetal.,2014;Youetal.,2014).Fewstudiesconductedatlocalscalehaveobservedrelationshipsbetweencommunitycompositionandbiochemicalfunctionofmicrobesinsoils(Fiereretal.,2012;Talbotetal.,2014;Suetal.,2015),suggestingthatthecomposi-tionofmicrobialcommunities,perse,maybe