17Identifyingthemicrobialtaxawhichconsistent

AcceptedArticleThisarticlehasbeenacceptedforpublicationandundergonefullpeerreviewbuthasnotbeenthroughthecopyediting,typesetting,paginationandproofreadingprocess,whichmayleadtodifferencesbetweenthisversionandtheVersionofRecord.Pleasecitethisarticleasdoi:10.1111/gcb.13557Thisarticleisprotectedbycopyright.Allrightsreserved.ReceivedDate:11-Jul-2016RevisedDate:17-Oct-2016AcceptedDate:19-Oct-2016Articletype:PrimaryResearchArticlesTitleIdentifyingthemicrobialtaxawhichconsistentlyrespondtosoilwarmingacrosstimeandspaceAuthorsAngelaM.Oliverio1,2,MarkA.Bradford3,NoahFierer1,2*1DepartmentofEcologyandEvolutionaryBiology,UniversityofColorado,Boulder,CO80309,UnitedStates2CooperativeInstituteforResearchinEnvironmentalSciences,UniversityofColorado,Boulder,CO80309,UnitedStates3SchoolofForestryandEnvironmentalStudies,YaleUniversity,NewHaven,CT06511,UnitedStates*CorrespondingauthorNoahFiererPhone:303-492-5615Email:[e-mail],temperature,warming,microbialbioindicators,bacteriaTypeofpaperPrimaryResearchArticleAbstractSoilmicrobialcommunitiesarethekeydriversofmanyterrestrialbiogeochemicalprocesses.However,wecurrentlylackageneralizableunderstandingofhowthesesoilcommunitieswillchangeinresponsetopredictedincreasesinglobaltemperaturesandwhichmicrobiallineageswillbemostimpacted.Here,usinghigh-throughputmarkergenesequencingofsoilscollectedfrom18sitesthroughoutNorthAmericaincludedina100-daylabincubationexperiment,weidentifiedacoregroupofabundantandnearlyubiquitoussoilmicrobesthatshiftinrelativeabundancewithelevatedsoiltemperatures.Wethenvalidatedandnarrowedourlistoftemperaturesensitivemicrobesbycomparingtheresultsfromthislaboratoryexperimentwithdatacompiledfrom210soilsrepresentingmultiple,independentglobalfieldstudiessampledacrossspatialgradientswithawiderangeinmeanannualtemperatures.Ourresultsrevealpredictableandconsistentresponsestotemperatureforacoregroupof189ubiquitoussoilbacterialandarchaealtaxa,withthesetaxaexhibitingsimilartemperatureresponsesacrossabroadrangeofsoiltypes.Thesemicrobial‘bioindicators’areusefulforunderstandinghowsoilmicrobialcommunitiesrespondtowarmingandtodiscriminatebetweenthedirectandindirecteffectsofsoilwarmingonmicrobialcommunities.Thosetaxathatwerefoundtobesensitivetotemperaturerepresentedawiderangeoflineagesandthedirectionofthetemperatureresponseswerenotpredictablefromphylogenyalone,indicatingthattemperatureresponsesaredifficulttopredictfromsimplydescribingsoilmicrobialcommunitiesatbroadtaxonomicorphylogeneticlevelsofresolution.TogethertheseresultslaythefoundationforamoreAcceptedArticleThisarticleisprotectedbycopyright.Allrightsreserved.predictiveunderstandingofhowsoilmicrobialcommunitiesrespondtosoilwarmingandhowwarmingmayultimatelyleadtochangesinsoilbiogeochemicalprocesses.IntroductionClimatechangeiswarmingsoilsinmanyregionsworldwide,likelyalteringbiogeochemicalprocessrates(Butleretal.,2012;Grimmetal.,2013).Soilmicrobialcommunitiesmediatemanyoftheseprocesses(Lietal.,2014;Tresederetal.,2012;Wiederetal.,2015),includingthosethatarecentraltocarbonandnitrogencyclingatlocaltoglobalscales.Yethowwarmingaffectsthestructureandfunctioningofsoilmicrobialcommunitiesisunclear.Thisknowledgegappersistsbecausetheenormousdiversityofsoilmicrobialcommunitieshindersourabilitytodiscerntheorganismalresponsesthatdeterminethecollectivephysiology,abundanceandfunctionaldiversityofthemicrobialbiomass,whichinturnshapebiogeochemicalcycling(Amendetal.,2016).Ataxon-specificfocusforplantsandanimalshascontributedtothedevelopmentoftrait-basedapproachesthathaveyieldeddetailedinsightsintohowandwhyplantandanimalcommunitiesmayshiftinresponsetowarming(CorlettandWestcott,2013;Garcia-Robledoetal.,2016).Similarinsightsintomicrobialcommunitiesrequirecomparableworkwithsoilmicrobialtaxa.Identifyingthosemicrobialtaxathatspecificallyrespondtotemperaturewillenabledeterminationoftemperature-responsetraitsfromamongthemultitudeofothertraitsthatdictatetheresponsesofhighly-diversesoilcommunitiestootherenvironmentalfactors.Thefirstchallenge,however,istoidentifythatsubsetofmicrobialtaxa,fromthehundredsorthousandsthatcanbefoundinanygivensoilsample,thatconsistentlychangeinabundanceinresponsetochangesinsoiltemperature.Thereareseveralreasonswhywestillhavealimitedunderstandingofhowsoilmicrobialcommunitieswillrespondtochangesintemperature.First,mostofthebacterialtaxafoundinsoilremainunderstudied(Ramirezetal.,2014),withtheirspecificresponsestotemperatureunknown.Althoughtherehasbeenextensiveresearchonthermophilicandpsychrophilicbacteria(e.g.AannizetAcceptedArticleThisarticleisprotectedbycopyright.Allrightsreserved.al.,2015;Bottosetal.,2008;Siddiquietal.,2013),thesetaxaarenotlikelytobeabundantinmostsoilsandthetemperatureoptimathatdefinethermophilesandpsychrophiles(40-70°Cand-20to10°C,respectively)areeitheroutsideoroverlapminimallywiththerangeoftemperaturesexperiencedbymanysoils.Thus,knowingwhattaxaarethermophilicorpsychrophilicisunlikelytobeusefulforpredictinghowmicrobialcommuni