3Alpinesoilcarbonisvulnerabletorapidmicrob

ORIGINALARTICLEAlpinesoilcarbonisvulnerabletorapidmicrobialdecompositionunderclimatecoolingLinweiWu1,2,11,YunfengYang1,11,ShipingWang3,4,HaoweiYue1,QiaoyanLin5,YigangHu5,6,ZhiliHe2,JoyDVanNostrand2,LaurenHale2,XiangzhenLi7,JackAGilbert8,9andJizhongZhou1,2,101StateKeyJointLaboratoryofEnvironmentSimulationandPollutionControl,SchoolofEnvironment,TsinghuaUniversity,Beijing,China;2InstituteforEnvironmentalGenomics,DepartmentofMicrobiologyandPlantBiology,andSchoolofCivilEngineeringandEnvironmentalSciences,UniversityofOklahoma,Norman,OK,USA;3KeyLaboratoryofAlpineEcologyandBiodiversity,InstituteofTibetanPlateauResearch,ChineseAcademyofSciences,Beijing,China;4CASCenterforExcellenceinTibetanPlateauEarthScience,Beijing,China;5KeyLaboratoryofAdaptionandEvolutionofPlateauBiota,NorthwestInstituteofPlateauBiology,ChineseAcademyofSciences,Xining,China;6ShapotouDesertExperimentandResearchStation,ColdandAridRegionsandEnvironmental&EngineeringResearchInstitute,ChineseAcademyofSciences,Lanzhou,China;7ChengduInstituteofBiology,ChineseAcademyofSciences,Chengdu,China;8TheMicrobiomeCenter,BioScienceDivision,ArgonneNationalLaboratory,Argonne,IL,USA;9DepartmentofSurgery,UniversityofChicago,Chicago,IL,USAand10EarthandEnvironmentalSciences,LawrenceBerkeleyNationalLaboratory,Berkeley,CA,USAAsclimatecoolingisincreasinglyregardedasimportantnaturalvariabilityoflong-termglobalwarmingtrends,thereisaresurginginterestinunderstandingitsimpactonbiodiversityandecosystemfunctioning.Here,wereportasoiltransplantexperimentfromlowertohigherelevationsinaTibetanalpinegrasslandtosimulatetheimpactofcoolingonecosystemcommunitystructureandfunction.Threeyearsofcoolingresultedinreducedplantproductivityandmicrobialfunctionalpotential(forexample,carbonrespirationandnutrientcycling).Microbialgeneticmarkersassociatedwithchemicallyrecalcitrantcarbondecompositionremainedunchangeddespiteadecreaseingenesassociatedwithchemicallylabilecarbondecomposition.Asaconsequence,cooling-associatedchangescorrelatedwithadecreaseinsoilorganiccarbon(SOC).Extrapolationoftheseresultssuggeststhatforevery1°Cdecreaseinannualaverageairtemperature,0.1Pg(0.3%)ofSOCwouldbelostfromtheTibetanplateau.Theseresultsdemonstratethatmicrobialfeedbackstocoolinghavethepotentialtodifferentiallyimpactchemicallylabileandrecalcitrantcarbonturnover,whichcouldleadtostrong,adverseconsequencesonsoilCstorage.Ourfindingsarealarming,consideringthefrequencyofshort-termcoolinganditsscaletodisruptecosystemsandbiogeochemicalcycling.TheISMEJournaladvanceonlinepublication,23May2017;doi:10.1038/ismej.2017.75IntroductionGlobalclimatechangesciencehaspredominantlytargetedclimatewarming(Luo,2007;Freyetal.,2013;Nieetal.,2013),butthisfocusischanging,asitisincreasinglyrecognizedthattemporary,localcoolingeventsarecommonamidstlong-termglobalwarmingtrends(Alleyetal.,2003;Jietal.,2014).TherehasbeensignificantcoolingintheAntarcticPeninsulaasthelate1990s,arisingfromnaturalvariabilityoftheregionalatmosphericcirculation(Turneretal.,2016).Ithasbeenprojectedthattheclimateinthe21stcenturyislikelytoproduceperiodsaslongasoneortwodecade(s)ofcooling(EasterlingandWehner,2009;LyubushinandKlyashtorin,2012),whichisalarmingbecausehistoricevidenceshowsthatcoolingmayperturbecosystemsandbiogeochemicalcyclingatascalecomparabletowhatisknownforwarming(McAnenaetal.,2013).Forinstance,coolingontheAntarcticcontinentbetween1966and2000ledtoarapiddecreaseintheprimaryproductivityoflakes(6–9%peryear)aswellasthenumberofsoilinvertebrates(morethan10%lossperyear)(Doranetal.,2002).Therefore,furtherunderstandingofthefullrangeofpossibleclimatechangescenariosandCorrespondence:YYang,StateKeyJointLaboratoryofEnviron-mentSimulationandPollutionControl,SchoolofEnvironment,TsinghuaUniversity,1TsinghuaGardenRoad,HaidianDistrict,Beijing100084,China.E-mail:[e-mail]27September2016;revised14March2017;accepted23March2017TheISMEJournal(2017),1–10©2017InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/17(CampbellandMcAndrews,1993;Doranetal.,2002)ormodelsimulation(Luchtetal.,2002),owingtothedifficultyofcarryingoutinsitustudies.Soiltransplantexperimentsprovideanopportunitytoquantifythedirectinfluenceofsubstantialclimatechangesontheplantandsoilmicrobialcommunitystructureandfunction(Breeuweretal.,2010;Vanhalaetal.,2011;Luanetal.,2014).Forexample,soiltransplantsintowarmerclimateshaveshowncomparableresultstolong-terminsituartificialwarming(Petcheyetal.,1999;Vanhalaetal.,2011;Zhouetal.,2012;Luanetal.,2014;Yueetal.,2015).Inthisstudy,weconductedasoiltransplantstudyinaTibetanalpinegrassland,whichisthelargestgrasslandontheEurasiancontinent(Yangetal.,2008).SoilsontheTibetanalpinestorealargeamountoforganicC(about10%oftheterrestrialCinChina)and