8Alteredcarbonturnoverprocessesandmicrobiome

Alteredcarbonturnoverprocessesandmicrobiomesinsoilsunderlong-termextremelyhighCO2exposureFelixBeulig1,TimUrich2,3,MartinNowak4,SusanE.Trumbore4,GerdGleixner4,GregorD.Gilfillan5,KristineE.Fjelland5andKirstenKüsel1,6*Thereisonlylimitedunderstandingoftheimpactofhighp(CO2)onsoilbiomes.Wehavestudiedafloodplainwetlandwherelong-termemanationsoftemperatevolcanicCO2(mofettes)areassociatedwithaccumulationofcarbonfromtheEarth’smantle.Withanintegratedapproachusingisotopegeochemistry,soilactivitymeasurementsandmulti-omicsanalyses,wedemonstratethathigh(nearlypure)CO2concentrationshavestronglyaffectedpathwaysofcarbonproductionanddecompositionandthereforecarbonturnover.Inparticular,apromotionofdarkCO2fixationsignificantlyincreasedtheinputofgeogeniccarboninthemofettewhencomparedtoareferencewetlandsoilexposedtonormallevelsofCO2.RadiocarbonanalysisrevealedthathighquantitiesofmofettesoilcarbonoriginatedfromtheassimilationofgeogenicCO2(upto67%)viaplantprimaryproductionandsubsurfaceCO2fixation.However,thepreservationandaccumulationofalmostundegradedorganicmaterialappearedtobefacilitatedbythepermanentexclusionofmeso-tomacroscopiceukaryotesandassociatedphysicaland/orecologicaltraitsratherthananimpairedbiochemicalpotentialforsoilorganicmatterdecomposition.OurstudyshowshowCO2-inducedchangesindiversityandfunctionsofthesoilcommunitycanfosteranunusualbiogeochemicalprofile.Mofettesarelow-temperature(100°C)fumarolesthatemanatealmostpurevolcanicCO2totheatmosphere.Theseterrestrialventingspotsmayrelease0.5tCO2d–1,leadingtoconsistentlyhighCO2soilgas-phaseconcentrations(90vol%)1,whichmightbesimilartotheEarth’satmosphereduringthetimewhenphotosynthesisevolved2–4.ThedirectandindirecteffectsofextremelyhighCO2levelsonsoilbiotaarepoorlystudied,butanimprovedunderstandingmightbeimportantforevaluatingtheenvironmentalconsequencesofCO2leakagesafterundergroundinjectionorcarboncaptureandstorage(CCS).Becauseoftheoftenstronglylocalizedventingincloseproximitytounaffectedreferencesites,studiesofmofettescanalsoexpandourknowledgeofmicrobialinteractionsinsoilfoodwebsdevelopedunderlong-termstablehypoxia,incontrasttothosesitesthatexperiencefluctuationsinredoxconditions.DependingonthetimeanddegreeofCO2exposure,mofettesshowdistinctgeochemicalcharacteristicswithfeaturesofreducto-morphicandacidicsoils5.Forexample,loweredpHandredoxcon-ditionssignificantlyimpactmetal(loid)dynamics,therebypotentiallyaffectingsoilnutrientavailability6.Ofparticularinterestistheturnoverandstorageofcarbon(C)inmofettes,asthesefactorsareoftenassociatedwiththeaccumulationofsoilorganicmatter(SOM),whichappearstoincreasewithdepthandp(CO2)(refs6,7).Itremainsunclearwhetherthisaccumulationistheresultofanoverallshifttowardsincreasedbelow-groundCinputand/ordecreasedCmineralization.Intriguingly,arecentstudyataflood-plainwetlandmofette8suggestedthatadditionalCinputsmightresultfrommicrobiallydrivensubsurfaceCO2assimilationcarriedoutbyanaerobicCO2-utilizingprokaryotes,forexample,acetogensandmethanogens.Theseprokaryotesarealsoknowntobeimpor-tantendmembersinthecomplexanaerobicbreakdownprocessforSOM,whichistransformedinacatabolicnetworkofconsecutivefermentative,syntrophic,acetogenicand/ormethanogenicsteps,incontrasttooxygen-dependentSOMturnover9.Thedirectorindirecteffectsoflong-termCO2emanationscouldalsoimpairoverallsoilactivityorspecificSOMdegradationpro-cesses,forexample,duetoanoxicconditions.SOMdegradationisgenerallydependentonthephysicalandbiochemicalcapabilitiesofthesoilbiota10,andismediatedbyamultitudeofligninandcarbohydratemetabolizingenzymesunderlyingbioticandabioticcontrols,whichweexpectedtobesignificantlyalteredbyCO2degassings11.AssessingthemetabolicpotentialandactivityofsoilcommunitiesasdriversforchangesinCcyclinghasbeenafocusofecologicalresearchfordecades,butlargelyremainsachallenge.Withtheapplicationof‘meta-omics’approachesinsoilecology12,itisnowpossibletoputpopulations,activitiesandmicrobialinter-actionsintocontextwithcurrentperceptionsofecosystemfunctionssuchasthebiogeochemicalcyclingofC.Todate,onlyafewsoilstudieshavemadeuseofthecomprehensiveenzymeactivityinfor-mationpotentialofmetatranscriptomics.Prominentexamplesareinvestigationsofhigh-Arcticpeat13,14,permafrostsoilandthermo-karstbog15.Thesestudiesdemonstratedthat‘omics’datacancorre-latewithactualratesofkeyprocessesandmaythushelptoelucidatechangesincomplexsoilbiochemicalnetworks.1AquaticGeomicrobiology,InstituteofEcology,FriedrichSchillerUniversityJena,DornburgerStr.159,D-07743Jena,Germany.2DivisionofArchaeaBiologyandEcogenomics,DepartmentofEcogenomicsandSystemsBiology,UniversityofVienna,Althanstraße14,1090Vienna,Austria.3BacterialPhysiology,InstituteforMicrobiology,ErnstMoritzArndtUniversityGreifswald,Friedrich-Ludwig-Jahnstr.15,17489Greifswald,Germany.4MaxPlanckInstituteforBiogeochemistry,POB10016410,07701Jena,Germany.5MedicalGenetics,OsloUniversityHospitalandUniversityofOslo,Kirkeveien166,0407Oslo,Norway.6GermanCentreforIntegrativeBiodiversityResearch(iDiv)Halle-Jena-Leipzig,DeutscherPlatz5e,D-04103Leipzig,Germany.*e-mail:kirsten.kuesel@uni-jena.d