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ORIGINALARTICLESoilmicrobialdiversitydrivestheprimingeffectalongclimategradients:acasestudyinMadagascarKantoRazanamalala1,TantelyRazafimbelo1,Pierre-AlainMaron2,LionelRanjard2,NicolasChemidlin2,MélanieLelièvre3,SamuelDequiedt3,VolaniainaHRamaroson1,ClaireMarsden4,ThierryBecquer5,JeanTrap5,6,EricBlanchart5,6andLaetitiaBernard5,61LaboratoiredesRadio-Isotopes,Antananarivo,Madagascar;2INRA,UMR1347Agroécologie,Dijon,France;3INRA,PlateformeGenoSol,UMR1347Agroécologie,Dijon,France;4Supagro,UMR210Eco&Sols,MontpellierCedex1,France;5IRD,UMR210Eco&Sols,MontpellierCedex1,Franceand6IRD,UMR210Eco&Sols,LaboratoiredesRadio-Isotopes,Antananarivo,MadagascarTheprimingeffectinsoilisproposedtobegeneratedbytwodistinctmechanisms:‘stoichiometricdecomposition’and/or‘nutrientmining’theories.Eachmechanismhasitsowndynamics,involvesitsownmicrobialactors,andtargetsdifferentsoilorganicmatter(SOM)pools.Thepresentstudyaimstoevaluatehowclimaticparametersdrivetheintensityofeachprimingeffectgenerationmechanismviathemodificationofsoilmicrobialandphysicochemicalproperties.SoilsweresampledinthecenterofMadagascar,alongclimaticgradientsdesignedtodistinguishtemperaturefromrainfalleffects.Abioticandbioticsoildescriptorswerecharacterizedincludingbacterialandfungalphylogeneticcomposition.PotentialorganicmattermineralizationandPEwereassessed7and42daysafterthebeginningofincubationwith13C-enrichedwheatstraw.Bothprimingmechanismsweremainlydrivenbythemeanannualtemperaturebutinoppositedirections.Theprimingeffectgeneratedbystoichiometricdecompositionwasfosteredundercolderclimates,becauseofsoilenrichmentinlessdevelopedorganicmatter,aswellasinfast-growingpopulations.Conversely,theprimingeffectgeneratedbynutrientminingwasenhancedunderwarmerclimates,probablybecauseofthelackofcompetitionbetweenslow-growingpopulationsminingSOMandfast-growingpopulationsfortheenergy-richresidueenteringthesoil.OurstudyleadstohypothesesabouttheconsequencesofclimatechangeonbothPEgenerationmechanismsandassociatedconsequencesonsoilcarbonsequestration.TheISMEJournaladvanceonlinepublication,17October2017;doi:10.1038/ismej.2017.178IntroductionPrimingeffectisanincreaseinsoilorganicmattermineralizationbymicroorganismsfollowingfreshorganicmatter(FOM)input(Bingemanetal.,1953;Kuzyakovetal.,2000).Aftermorethantwodecadesofincreasingresearcheffort,PE-generatingmechanisms,determinantsandactorsstillneedtobeelucidated(Fontaineetal.,2003;Bernardetal.,2007,2009,2012;Pascaultetal.,2013;Chenetal.,2014).Basedonaliteraturereview,Fontaineetal.(2003)proposedthatPEcanbegeneratedbytwodifferentmechanisms:(1)indirectlyviacollateraldamageexertedonsoilorganicmatter(SOM)byextracellularenzymesreleasedbyFOMfeeders,and(2)directlyviatheco-metabolismofenergy-richFOMcatabolitesbySOMfeederswhomineSOMfornutrients.RecentlyChenetal.(2014),usedthedenominationof‘stoichiometricdecompositiontheory’and‘nutrientminingtheory’foreachmechanismrespectively.Theseauthorsshowedthatthefirstprocessisfavoredbyhighnitrogenconcentrationwhilethesecondtakesplaceincaseofnitrogendepletion.Therefore,whenfreshcarboninputsarenotaccompaniedbynutrientinputs,PEshouldfirstbegeneratedbystoichiometricdecom-position,followedbynutrientminingafterexhaustionofavailablenutrientsinthesoilsolution.OtherauthorshaveshownthatduringPEgeneration,earlyPEcorrespondedtothemineralizationofyoung,labileSOMbyfast-growingmicrobeswhereaslatePEtargetedoldSOMandinvolvedslow-growingpopula-tions(Blagodatskayaetal.,2014;Derrienetal.,2014).Asaconsequence,PEgeneratedbystoichiometricdecompositionshouldresultfromtheactivityoffaster-growingmicrobesthanPEgeneratedbynutrientmining(Fontaineetal.,2003;Chenetal.,2014).Usingthecouplingofisotopicandmolecularapproaches,asmallnumberofstudieshaveidentifiedphylogeneticgroupsinvolvedinthemineralizationofwheatresiduesandpotentiallyinvolvedinthedifferentPEprocessesatdifferentdecompositionstages(BernardCorrespondence:LBernard,UMR210Eco&Sols,2placeVialaBt12,MontpellierCedex1,F-34060,France.E-mail:laetitia.bernard@ird.frReceived10May2017;revised7September2017;accepted14September2017TheISMEJournal(2017),1–12©2017InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/17).However,exceptforthesoilnitrogenstatus,sofarnootherdeterminantofPE-generatingprocessesisknown.ThePEhasbeensuspectedtoincreaseSOMmineralizationinthecontextofglobalwarmingviathepotentialincreaseinlabilecarbon(C)inputsbyplantstothesoilinresponsetoCO2elevation(HeimannandReichstein,2008).However,itisnotknownwhethertemperatureelevation(orrainfallvariation)willbeabletodrivePEthroughtheselectionofdifferentmicrobialguildsand/orthemodificationofthemetabolismofthepopulations.Thisquestioniscrucialforsoilcarbonsequestration,becauseifPEgeneratedbynutrientminingleadstostableSOMdepletion,PEgeneratedbystoichio-metricdecompositioncanbeconsideredasastimulationofthedecompositionofyoungSOMandthereforeastimulationofthehumificationroute.Theobjectiveofthisstudywastodeterminehowclimaticparametersdrivethecapacityofmicrobialcommunitiestomineralizeorganicma