5Warmingenhancesoldorganiccarbondecompositio

OPENORIGINALARTICLEWarmingenhancesoldorganiccarbondecompositionthroughalteringfunctionalmicrobialcommunitiesLeiCheng1,2,3,NaifangZhang1,MengtingYuan2,3,JingXiao1,YujiaQin2,3,YeDeng2,3,QichaoTu2,3,KaiXue2,3,JoyDVanNostrand2,3,LiyouWu2,3,ZhiliHe2,3,XuhuiZhou4,MaryBethLeigh5,KonstantinosTKonstantinidis6,EdwardAGSchuur7,YiqiLuo2,JamesMTiedje8andJizhongZhou2,3,9,10,111KeyLaboratoryofConservationBiologyforEndangeredWildlifeoftheMinistryofEducation,CollegeofLifeSciences,ZhejiangUniversity,Hangzhou,China;2DepartmentofMicrobiologyandPlantBiology,UniversityofOklahoma,Norman,OK,USA;3InstituteforEnvironmentalGenomics,UniversityofOklahoma,Norman,OK,USA;4CenterforGlobalChangeandEcologicalForecasting,SchoolofEcologicalandEnvironmentalSciences,EastChinaNormalUniversity,Shanghai,China;5InstituteofArcticBiology,UniversityofAlaskaFairbanks,Fairbanks,AK,USA;6CenterforBioinformaticsandComputationalGenomics,SchoolofBiologyandSchoolofCivilandEnvironmentalEngineering,GeorgiaInstituteofTechnology,Atlanta,GA,USA;7CenterforEcosystemScienceandSociety,NorthernArizonaUniversity,Flagstaff,AZ,USA;8CenterforMicrobialEcology,MichiganStateUniversity,EastLansing,MI,USA;9SchoolofCivilEngineeringandEnvironmentalSciences,UniversityofOklahoma,Norman,OK,USA;10StateKeyJointLaboratoryofEnvironmentSimulationandPollutionControl,SchoolofEnvironment,TsinghuaUniversity,Beijing,Chinaand11EarthandEnvironmentalSciences,LawrenceBerkeleyNationalLaboratory,Berkeley,CA,USASoilorganicmatter(SOM)stockscontainnearlythreetimesasmuchcarbon(C)astheatmosphereandchangesinsoilCstocksmayhaveamajorimpactonfutureatmosphericcarbondioxideconcentrationsandclimate.Overthepasttwodecades,muchresearchhasbeendevotedtoexaminingtheinfluenceofwarmingonSOMdecompositionintopsoil.MostSOM,however,isoldandstoredinsubsoil.ThefateofsubsoilSOMunderfuturewarmingremainshighlyuncertain.Here,bycombiningalong-termfieldwarmingexperimentandameta-analysisstudy,weshowedthatwarmingsignificantlyincreasedSOMdecompositioninsubsoil.WealsoshowedthatadecadeofwarmingpromoteddecompositionofsubsoilSOMwithturnovertimesofdecadestomillenniainatallgrassprairieandthiseffectwaslargelyassociatedwithshiftsinthefunctionalgenestructureofmicrobialcommunities.Bycouplingstableisotopeprobingwithmetagenomics,wefoundthatmicrobialcommunitiesinwarmedsoilspossessedahigherrelativeabundanceofkeyfunctionalgenesinvolvedinthedegradationoforganicmaterialswithvaryingrecalcitrancethanthoseincontrolsoils.ThesefindingssuggestwarmingmayconsiderablyalterthestabilityofthevastpoolofoldSOMinsubsoil,contributingtothelong-termpositivefeedbackbetweentheCcycleandclimate.TheISMEJournaladvanceonlinepublication,21April2017;doi:10.1038/ismej.2017.48IntroductionAmajoruncertaintyinprojectingfutureatmosphericcarbondioxide(CO2)concentrationsandclimateishowwarminginfluencesdecompositionofSOM(DavidsonandJanssens,2006;Stockeretal.,2013).ConsiderableeffortshavebeenmadetoassesstheeffectsofwarmingonSOMdecompositioninthesurfacesoillayer(thatis,topsoil,0–20cmdeep)(DavidsonandJanssens,2006;vonLutzowandKogel-Knabner,2009;Conantetal.,2011;Crowtheretal.,2016).SoilorganicC(SOC)intopsoilaccountsforonequarteroftheglobalSOCpoolandisrelativelyyoung,withtypicalturnovertimesofdecadesorless(Hopkinsetal.,2012).TopsoilSOMhasbeendeemedtobevulnerabletomicrobialdecompositionunderwarming(Yergeauetal.,2012;Karhuetal.,2014;Crowtheretal.,2016),andhencemayhaveacriticalimpactonclimate(DavidsonandJanssens,2006;Conantetal.,2011;Hopkinsetal.,2012).MostSOCisstoredindeeperCorrespondence:LChengorJZhou,KeyLaboratoryofConserva-tionBiologyforEndangeredWildlifeoftheMinistryofEducation,CollegeofLifeSciences,ZhejiangUniversity,866YuhangtangRd,Hangzhou,Zhejiang310058,China.E-mail:[e-mail]@ou.eduReceived10September2016;revised14February2017;accepted28February2017TheISMEJournal(2017),1–11(0.2–3m)(JobbagyandJackson,2000),ofwhichthemajorityofCisconsiderablyolder,withturnovertimesofcenturiestomillennia(Trumboreetal.,1996;Rumpeletal.,2002;Fontaineetal.,2007).Asignificantandlong-termfeedbacktoclimatewouldalsooccurifongoingandprojectedwarmingcouldconsiderablyalterdecompositionofSOMinthesubsoillayers(thosebelowthesurfacesoil)ofglobalsoils.Yet,theinfluenceofwarmingonthestabilityofSOMinsubsoilhasrarelybeenexamineddirectly.IthasbeentraditionallythoughtthatthelongresidencetimeofSOMinsubsoilisduemainlytothechemicalrecalcitranceoforganiccompoundsthemselves(Rumpeletal.,2002;DavidsonandJanssens,2006;Fontaineetal.,2007;vonLutzowandKogel-Knabner,2009),althougharecentviewhasascribedittobioticandabioticprotection(Schmidtetal.,2011).KinetictheorypredictsthatoldSOM,ifmorechemicallyrecalcitrant,wouldhavehighersensitivitiestotemperaturechangesincomparisonwithyoungSOM(Knorretal.,2005;DavidsonandJanssens,2006).ButthetemperaturesensitivityofrecalcitrantSOMdecompositionhasbeendocumentedtobeeitherhigherthan(Knorretal.,2005;Hakkenbergetal.,2008;HartleyandIneson,2008;Craineetal.,2010;Hopkinsetal.,2012),similartoorlowerthanlabileSOM(Liskietal.,1999;GiardinaandRyan,2000;Melilloetal.,2002;Fan