6Grazinginducedmicrobiomealterationsdrivesoi

RESEARCHOpenAccessGrazing-inducedmicrobiomealterationsdrivesoilorganiccarbonturnoverandproductivityinmeadowsteppeWeibingXun1,2,RuiruiYan3,YiRen1,DongyanJin3,WuXiong1,GuishanZhang2,ZhongliCui1,XiaopingXin3*†andRuifuZhang1,2*†AbstractBackground:Grazingisamajormodulatorofbiodiversityandproductivityingrasslands.However,ourunderstandingofgrazing-inducedchangesinbelow-groundcommunities,processes,andsoilproductivityislimited.Here,usingalong-termenclosedgrazingmeadowsteppe,weinvestigatedtheimpactsofgrazingonthesoilorganiccarbon(SOC)turnover,themicrobialcommunitycomposition,resistanceandactivityunderseasonalchanges,andthemicrobialcontributionstosoilproductivity.Results:Theresultsdemonstratedthatgrazinghadsignificantimpactsonsoilmicrobialcommunitiesandecosystemfunctionsinmeadowsteppe.Thehighestmicrobialα-diversitywasobservedunderlightgrazingintensity,whilethehighestβ-diversitywasobservedundermoderategrazingintensity.Grazingshiftedthemicrobialcompositionfromfungidominatedtobacteriadominatedandfromslowgrowingtofastgrowing,therebyresultinginashiftfromfungi-dominatedfoodwebsprimarilyutilizingrecalcitrantSOCtobacteria-dominatedfoodwebsmainlyutilizinglabileSOC.Moreover,thehigherfungalrecalcitrant-SOC-decomposingactivitiesandbacteriallabile-SOC-decomposingactivitieswereobservedinfungi-andbacteria-dominatedcommunities,respectively.Notably,therobustnessofbacterialcommunityandthestabilityofbacterialactivitywereassociatedwithα-diversity,whilethiswasnotthecasefortherobustnessoffungalcommunityanditsassociatedactivities.Finally,weobservedthatmicrobialα-diversityratherthanSOCturnoverratecanpredictsoilproductivity.Conclusions:Ourfindingsindicatethestronginfluenceofgrazingonsoilmicrobialcommunity,SOCturnover,andsoilproductivityandtheimportantpositiveroleofsoilmicrobialα-diversityinsteeringthefunctionsofmeadowsteppeecosystems.Keywords:Temperatemeadowsteppe,Cattlegrazing,Microbialcomposition,Soilincubation,SOC-decompositionenzymaticactivity,Soilproductivity*Correspondence:[e-mail];[e-mail]†XiaopingXinandRuifuZhangcontributedequallytothiswork.3NationalHulunberGrasslandEcosystemObservationandResearchStation,InstituteofAgriculturalResourcesandRegionalPlanning,ChineseAcademyofAgriculturalSciences,Beijing100081,China1JiangsuProvincialKeyLabforOrganicSolidWasteUtilization,NationalEngineeringResearchCenterforOrganic-basedFertilizers,JiangsuCollaborativeInnovationCenterforSolidOrganicWasteResourceUtilization,NanjingAgriculturalUniversity,Nanjing210095,ChinaFulllistofauthorinformationisavailableattheendofthearticle©TheAuthor(s).2018OpenAccessThisarticleisdistributedunderthetermsoftheCreativeCommonsAttribution4.0InternationalLicense(),whichpermitsunrestricteduse,distribution,andreproductioninanymedium,providedyougiveappropriatecredittotheoriginalauthor(s)andthesource,providealinktotheCreativeCommonslicense,andindicateifchangesweremade.TheCreativeCommonsPublicDomainDedicationwaiver()appliestothedatamadeavailableinthisarticle,unlessotherwisestated.Xunetal.Microbiome(2018)6:170[1].Overgrazinghasbeenreportedtoreducefloristicdiversityandbiomassandisprobablythemostpervasiveandsignificantprocessofdegradationingrasslands[2].Theimportanceoffloristicdiversityindrivingtheprod-uctivityandotherecosystemfunctionshasbeendemon-stratedbymanystudies[3,4].However,theimportanceoffloristicdiversityhasbeenquestionedrecently[5,6].Someofthesequeriessuggestthattheproductivityofmanyter-restrialecosystemsdependsontheavailabilityofresources[7–9].Inparticular,soilmicrobesareimportantcompo-nentsinmaintainingecosystemfunctionsandenhancesoilproductivityduetotheircriticalroles,includinglitterdecomposition,biogeochemicalnutrientcycling,soilag-glomeration,andfertilitypromotion[10–12].Therefore,itisimportanttopromotethetransitionfromabove-groundstudiestobelow-groundonestoincreaseourunder-standingofthesoilmicrobialbehaviors.Thesestudiesmayprovideecologistswithinsightsintotheseeminglydivergentresultsobservedabovetheground.Todate,althoughsomeinvestigationshavestudiedtop-downin-teractions[13–15],ourknowledgeofthemechanismsbywhichsoilmicrobialcommunitiesandecosystemsfunctiontomaintainsoilproductivityislimited,espe-ciallythegrazing-inducedchangesinbelow-groundcommunities[16].Ithasbeenwellestablishedthatboththecompositionandfunctionalcapabilitiesofsoilmicrobialcommunitycanbestronglyinfluencedbyenvironmentalvariablessuchasclimate[17],vegetation[18],andsoilconditions[19].Insteppeecosystems,grazingisakeyregulatorthatcandirectlyorindirectlyaffecttheabovementionedenvironmentalvariables[20,21]andthenaffectthediver-sityandcompositionofsoilmicrobialcommunity[22],resultinginthealterationofthefunctionalperformanceandnutrientprovisionpatternsinsoil[23].Indeed,somestudieshavedemonstratedthatgrazinghasasignificanteffectonsoilmicrobialcommunityan