58Decreasedplantproductivityresultingfrompla

AcceptedArticleThisarticlehasbeenacceptedforpublicationandundergonefullpeerreviewbuthasnotbeenthroughthecopyediting,typesetting,paginationandproofreadingprocess,whichmayleadtodifferencesbetweenthisversionandtheVersionofRecord.Pleasecitethisarticleasdoi:10.1111/gcb.13783Thisarticleisprotectedbycopyright.Allrightsreserved.DR.XIMEIZHANG(OrcidID:0000-0003-0314-9452)Articletype:PrimaryResearchArticlesTitle:DecreasedplantproductivityresultingfromplantgroupremovalexperimentconstrainssoilmicrobialfunctionaldiversityRunninghead:plant-microbefunctionalrelationshipAuthors:XimeiZhang1,2*,EricR.Johnston3,AlbertBarberán4,YiRen5,XiaotaoLü2,XingguoHan2,6*Affiliations:1KeyLaboratoryofDrylandAgriculture,MOA,InstituteofEnvironmentandSustainableDevelopmentinAgriculture,ChineseAcademyofAgriculturalSciences,Beijing100081,China.2InstituteofAppliedEcology,ChineseAcademyofSciences,Shenyang110016,China.3SchoolofCivilandEnvironmentalEngineering,GeorgiaInstituteofTechnology,Atlanta,GA30332,USA.4DepartmentofSoil,Water,andEnvironmentalScience,UniversityofArizona,Tucson,Arizona85721,USA.5ShanghaiMajorbioBio-pharmBiotechnologyCo.,Ltd,Shanghai201318,China.6StateKeyLaboratoryofVegetationandEnvironmentalChange,InstituteofBotany,ChineseAcademyofSciences,Beijing100093,China.AcceptedArticleThisarticleisprotectedbycopyright.Allrightsreserved.*Correspondingauthor:XimeiZhang(Tel:[phone];Email:[e-mail])orXingguoHan(Tel:[phone];Email:[e-mail]).Keywords:biodiversity;biodiversityloss;functionaldiversity;grassland;InnerMongolia;metagenome;microbialdiversityTypeofPaper:PrimaryResearchArticlesAbstractAnthropogenicenvironmentalchangesareacceleratingtherateofbiodiversitylossonEarth.Plantdiversitylossispredictedtoreducesoilmicrobialdiversityprimarilyduetothedecreasedvarietyofcarbon/energyresources.However,thisintuitivehypothesisissupportedbysparseempiricalevidence,andmostunderlyingmechanismsremainunderexploredorobscurealtogether.Weconstructedfourdiversitygradients(0-3)inafive-yearplantfunctionalgroupremovalexperimentinasteppeecosysteminInnerMongolia,China,andquantifiedmicrobialtaxonomicandfunctionaldiversitywithshotgunmetagenomesequencing.Thetreatmentshadlittleeffectonmicrobialtaxonomicdiversity,butwerefoundtodecreasefunctionalgenediversity.However,theobserveddecreaseinfunctionalgenediversitywasmoreattributabletoalossinplantproductivity,ratherthantothelossofanyindividualplantfunctionalgroupperse.Reducedproductivitylimitedfreshplantresourcessuppliedtomicroorganisms,andthus,intensifiedthepressureofecologicalfiltering,favoringgenesresponsibleforenergyproduction/conversion,materialtransport/metabolismandaminoacidrecycling,andaccordinglydisfavoredmanygeneswithotherfunctions.Furthermore,microbialrespirationwascorrelatedwiththevariationinfunctionalAcceptedArticleThisarticleisprotectedbycopyright.Allrightsreserved.compositionbutnottaxonomiccomposition.Overall,theamountofcarbon/energyresourcesdrivingmicrobialgenediversitywasidentifiedtobethecriticallinkagebetweenabove-andbelow-groundcommunities,contrarytothetraditionalframeworkoflinkingplantclade/taxonomicdiversitytomicrobialtaxonomicdiversity.IntroductionAnthropogenicenvironmentalchanges,suchasincreasedlandallocationforagriculturaluse,nitrogendeposition,andtherisingglobalmeantemperature,areacceleratingtherateofbiodiversitylossonEarth(Dirzo&Raven,2003;Bálintetal.,2011).Itisacentralgoalinecologyresearchtoinvestigatetheeffectofplantdiversitylossonsoilmicrobialcommunities,forsoilhabitatspossessthehighestbiodiversityonEarthandplaycriticalrolesindrivingmultipleecosystemfunctionssuchascarbonandnutrientcycling(Garbevaetal.,2004;Fierer&Jackson,2006;Fiereretal.,2012;Jingetal.,2015;Langeetal.,2015).However,therelationshipsbetweenplantandbelowgroundmicrobialcommunitiesremainelusive,owingtoahighdegreeofheterogeneityinsituandinresponsetoenvironmentalstimuli/change,makingconsistent,reproduciblepatternsdifficulttoascertain(Wardleetal.,1999;Stephanetal.,2000;Zaketal.,2003;Liuetal.,2007;Culmanetal.,2010;Eisenhaueretal.,2011;Milcuetal.,2013;Gobernaetal.,2015;Proberetal.,2015).Thus,predictinghowplantdiversitylosswillaffectsoilmicrobialdiversityremainschallenging,despitenumerousrecentinnovationsthathaveexpandedourcapacitytocharacterizecomplexmicrobialcommunities.Plantdiversitylossislikelytobothreduceplantproductivityandcommunitystructure(diversityandcomposition),andsoilmicrobialcommunitiesmayAcceptedArticleThisarticleisprotectedbycopyright.Allrightsreserved.respondatboththetaxonomicandfunctionallevels.Itisnotwellunderstoodwhichplantcommunityattributesmostcruciallyinfluencebelowgroundcommunities,norwhichmicrobialfeaturesaremostresponsivetoabovegroundalterations.Ontheonehand,plantproductivitydeterminestheamountofcarbon/energyresourcessuppliedtosoilmicrobialcommunities.Infact,netprimaryproductivityhasbeendemonstratedtoplayafundamentalroleindrivingbothplantandanimaldiversity(Hutchinson,1959;Rosenzweig,1995).Formicroorganismsinparticular,thedecreaseinproductivityreducestheamountofplant-derivedorganicmaterial