9Microbialtemperaturesensitivityandbiomassch

LettersédeLausanne,Lausanne,Switzerland.3InstituteofAppliedSystemsAnalysis,Laxenburg,Austria.4DepartmentofMicrobiology&EcosystemScience,DivisionofMicrobialEcology,UniversityofVienna,Vienna,Austria.5DepartmentofBiology,UniversityofAntwerp,Antwerp,Belgium.6AgriculturalUniversityofIceland,Hvanneyri,Borgarnes,Iceland.*e-mail:[e-mail];[e-mail]rolcarbonlossesfromsoilstotheatmosphere1–3,yettheirresponsestoclimatewarmingareoftenshort-livedandunpredictable4–7.Twomechanisms,microbialacclimationandsubstratedepletion,havebeenproposedtoexplaintemporarywarmingeffectsonsoilmicro-bialactivity8–10.However,empiricalsupportforeithermecha-nismisunconvincing.Hereweusedgeothermaltemperaturegradients(50yearsoffieldwarming)11andashort-termexperimenttoshowthatmicrobialactivity(grossratesofgrowth,turnover,respirationandcarbonuptake)isintrinsi-callytemperaturesensitiveanddoesnotacclimatetowarm-ing(+6 °C)overweeksordecades.Permanentlyacceleratedmicrobialactivitycausedcarbonlossfromsoil.However,soilcarbonlosswastemporarybecausesubstratedepletionreducedmicrobialbiomassandconstrainedtheinfluenceofmicrobesovertheecosystem.Amicrobialbiogeochemicalmodel12–14showedthattheseobservationsarereproduciblethroughamodest,butpermanent,accelerationinmicrobialphysiology.Thesefindingsrevealamechanismbywhichintrinsicmicrobialtemperaturesensitivityandsubstratedepletiontogetherdictatewarmingeffectsonsoilcarbonlossviatheircontrolovermicrobialbiomass.Wethusprovideaframeworkforinterpretingthelinksbetweentemperature,microbialactivityandsoilcarbonlossontimescalesrelevanttoEarth’sclimatesystem.Soil-dwellingbacteriaandfungicontrolthebreakdownoforganicmatterinsoilanditsreleaseascarbondioxidetotheatmo-sphere1.Climatewarmingisexpectedtoacceleratetheactivityofsoilmicrobes,stimulatingfurtherCO2releaseandapositivefeed-backtoclimatechange2,3.Abetterunderstandingofmicrobialpro-cessesislikelytoimproveclimatechangepredictions15,16.Researchinrecentdecadeshasthussoughttoquantifytheconsequencesofwarmingforsoilmicrobesandthecarboncycleprocessestheygov-ern,andtodescribethisusingmetricssuchasmicrobialcarbonuseefficiency(CUE)17,18.However,therelationshipsbetweentempera-tureandsoilmicrobesremainapparentlyinconsistentinbothspaceandtime3–9,preventingconsensusontheseverityoffeedbacksfrommicrobialactivitytofutureclimatechange.Soilmicrobesdegradeorganicmatterinsoil,takeupthecar-bontherein,allocateaportiontogrowth,andreleasetheremain-derchieflyasCO2throughrespiration19.Theenzymaticreactionscontrollingtheseprocessesareintrinsicallytemperaturesensitive20.However,warmingeffectsonsoilCO2releaseareoftenshort-lived5,9.First,warmingbeginsaphaseofacceleratedrespirationthatcausesexcessCO2releasefromsoil.Then,withinyearsofinitiatingwarm-ing,thereisadecelerationofrespirationand,inmostcases(butseerefs4,7),areturntopre-warmedratesofsoilCO2release.Thetem-poraldynamicsofsoilCO2releasewilldictatethemagnitudeofsoilcarbonlostwithclimatewarming.Nevertheless,themechanismsbehinditarethesubjectofintensescientificdebate.Microbialcommunitiesmayacclimatetosustainedwarmingthroughphysi-ologicaladjustments(forexample,CUE)orshiftsincommunitycomposition9,21.Herewedefinemicrobialacclimationasareturnofmicrobialactivitytowardspre-warmedratesovertime.Atthesametime,acceleratedmicrobialactivitycancausesubstratedepletion,limitingresourceavailabilityandnegativelyimpactingmicrobialprocesses8,10.Microbialacclimationandsubstratedepletionarenotmutuallyexclusive,andbothmaycauseadecelerationofsoilcarbonlossundersustainedwarming.Despitethis,microbialactivitydoesnotalwaysattenuatetowarming4,8,andneithermechanismcanexplainthevariablepatternsofwarming-inducedsoilcarbonlossobservedatbiomeandglobalscales6,7.Indeed,whilelinksbetweenmicrobialactivityandthecarboncyclehavebeenrepeatedlydem-onstrated,researchershaveyettoquantifytheinterplaybetweentemperature,microbialphysiologyandsoilcarbonlossoverperiodsgreaterthanhourstomonths.Thisisespeciallytrueformicrobialgrowth,turnoverandCUE,whichuntilnowhavebeenestimatedindirectlyorusingcarbonsubstratesthatbiastheexperimentalsys-tem17,18,22.Amechanisticunderstandingisurgentlyneededtoiden-tifytheroleofmicroorganismsinwarming-inducedsoilcarbonlossanditsimportanceovertimescalesrelevanttotheclimatesystem.Weusedthelongestknowninsitunaturalwarmingstudy(atleast50years11)todeterminethemicrobialmechanismresponsi-bleforwarming-inducedsoilcarbonloss.Thestudyexploitsnatu-ralgeothermalactivityinasub-arcticgrasslandthathascreatedgradientsofwarmingfromambienttemperatureto+6°C(n=5).Itprovidesauniqueplatformforassessingthelong-termresponsesofmicrobestowarminginaregionthatholdslargecarbonstocksandisvulnerabletorapidtemperaturechange1.Weuseddirect,substrate-independentmetricsofmicrobialphysiology(grossratesofgrowth,respiration,turnover,organiccarbonuptakeandCUE23)tocha