7SoilexchangeratesofCOSandCO18Odifferwith

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TheISMEJournal●JérômeOgée3●KristinBoye4●EstherSinger5●LisaWingate3●ChristianvonSperber6,7●AditiSengupta8●MaryWhelan9●ErinPang1●MarcoKeiluweit10●NicolasBrüggemann11●JoeA.Berry9●PaulaV.Welander1Received:9January2018/Revised:30April2018/Accepted:4August2018©TheAuthor(s)2018.ThisarticleispublishedwithopenaccessAbstractDifferentiatingthecontributionsofphotosynthesisandrespirationtotheglobalcarboncycleiscriticalforimprovingpredictiveclimatemodels.Carbonicanhydrase(CA)activityinleavesisresponsibleforthelargestbiosphere-atmospheretracegasfluxesofcarbonylsulfide(COS)andtheoxygen-18isotopologueofcarbondioxide(CO18O)thatbothreflectgrossphotosyntheticrates.However,CAactivityalsooccursinsoilsandwillbeasourceofuncertaintyintheuseofCOSandCO18Oascarboncycletracersuntilprocess-basedconstraintsareimproved.Inthisstudy,wemeasuredCOSandCO18OexchangeratesandestimatedthecorrespondingCAactivityinsoilsfromarangeofbiomesandlandusetypes.SoilCAactivitywasnotuniformforCOSandCO2,andpatternsofdivergencewererelatedtomicrobialcommunitycompositionandCAgeneexpressionpatterns.Insomecases,thesamemicrobialtaxaandCAclassescatalyzedbothCOSandCO2reactionsinsoil,butinothercasesthespecificitytowardsthetwosubstratesdifferedmarkedly.CAactivityforCOSwasrelatedtofungaltaxaandβ-D-CAexpression,whereasCAactivityforCO2wasrelatedtoalgalandbacterialtaxaandα-CAexpression.Thisstudyintegratesgasexchangemeasurements,enzymeactivitymodels,andcharacterizationofsoiltaxonomicandgeneticdiversitytobuildconnectionsbetweenCAactivityandthesoilmicrobiome.Importantly,ourresultsidentifykineticparameterstorepresentsoilCAactivityduringapplicationofCOSandCO18Oascarboncycletracers.IntroductionCOSandCO18OareatmospherictracersforpartitioningthenetexchangeofCO2overlandintoitsrespiratoryandphotosyntheticcomponents,whichiscriticalforbench-markingpredictionsofclimate-carbonfeedbacksandtheirimpactsonlargeterrestrialcarbonstocks[1,2].Thebasisof*LauraK.Meredithlaurameredith@email.arizona.edu1DepartmentofEarthSystemScience,StanfordUniversity,Stanford,CA94305,USA2SchoolofNaturalResourcesandtheEnvironment,UniversityofArizona,Tucson,AZ85721,USA3INRA/BordeauxScienceAgro,UMR1391ISPA,BordeauxScienceAgro,Villenaved’Ornon,Bordeaux33140,France4SLACNationalLaboratory,StanfordSynchrotronRadiationLightsource,MenloPark,CA94025,USA5DepartmentofEnergyJointGenomeInstitute,WalnutCreek,CA94598,USA6InstituteforCropScienceandResourceConservation(INRES),SoilScienceandSoilEcology,UniversityofBonn,Bonn53115,Germany7DepartmentofGeography,McGillUniversity,805SherbrookeSt.W.,Montreal,QCH3A0B9,Canada8UniversityofArizona,Biosphere2,Tucson,AZ85721,USA9DepartmentofGlobalChangeEcology,CarnegieInstitutionforScience,Stanford,CA94305,USA10StockbridgeSchoolofAgriculture,UniversityofMassachusetts,Amherst,MA01003,USA11ForschungszentrumJülich,InstituteofBio-andGeosciences,Agrosphere(IBG-3),Wilhelm-Johnen-Strasse,Jülich52428,GermanyElectronicsupplementarymaterialTheonlineversionofthisarticle()containssupplementarymaterial,whichisavailabletoauthorizedusers.1234567890();,:1234567890();,:thesetracersistheirreactionwithcarbonicanhydraseenzymes(CAs)inleaves,whichfacilitatephotosyntheticcarbonfixationbycatalyzingthereversiblehydrationofcarbondioxide(CO2+H2O⇔HCO3−+H+).CAsarenotlimitedtoplants[3],andarepresentinsoil-dwellingmicroorganisms[4].Inleavesandsoils,CAsdriveCOSconsumptionandCO2–H2Oisotopicequilibration,andthisactivityinfluencespatternsinatmosphericcompositionthatcanbeusedtoconstrainterrestrialphotosynthesis.Specifi-cally,duringCO2hydration,oxygenisotopesareexchangedbetweenCO2andwatermoleculesinleavesandsoils(CO2+H218O⇔CO18O+H2O)[5–7],therebyinfluencingtheconcentrationofCO18Ointheatmosphere[8,9].Conse-quently,variationsofatmosphericCO18OreflecttheextentofCO2interactionwiththeleafandsoilwaterpools,andCO18Ocanbeusedtotracelandphotosynthesisandsoilrespirationatlargescales[10–13].CAsalsocatalyzetheirreversiblehydrolysisofCOSinleavesandsoils(COS+H2O→CO2+H2S).AsCOSuptakebytheterrestrialbio-sphereisdominatedbyphotosyntheticuptakeduringthegrowingseason[14],fluctuationsofatmosphericCOSconcentrationcanalsoserveasatraceroflandphoto-synthesis,independentlyofthosefromCO18O[14–22].SoilexchangeratesofCOSandCO18Oaresignificantandthedriversoftheirvariabilityarenotwellunderstood.BiologicalactivityinsoilshasbeenobservedtoaccelerateoxygenisotopeexchangebetweenatmosphericCO2andsoilwater10to1000timesaboveuncatalyzedCO2hydrationrates[13,23–26]andtodrivesignificantCOSuptakeinavarietyofecosystems[27–29].SoilexchangeofCOSandCO18O[9,13,23,24,28,30–34]andsoilCAactivity[13,35]arespatiallyandtemporallyvariable,whichintroducesuncertaintyduringtheinversionofatmosphericCO18OandCOStoestimateprimaryproductivity.Sys-tematicinvestigationsofsoilCAactivityforCOSandCO18Oareneededtodeterminehowecologicalandenvir-onmentaldriversimpactsoilexchangerates.Knowledgeofthekeymic

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