28Differentialsensitivityoftotalandactiveso

PRIMARYRESEARCHARTICLEDifferentialsensitivityoftotalandactivesoilmicrobialcommunitiestodroughtandforestmanagementFelipeBastida1|IreneF.Torres1|ManuelaAndr
es-Abell
an2|PetrBaldrian3|Rub
enL
opez-Mond
ejar3|Tom
asVetrovsk
y3|HansH.Richnow4|RobertStarke5|SaraOndo~no1|CarlosGarc
ıa1|FranciscoR.L
opez-Serrano2|NicoJehmlich51DepartmentofSoilandWaterConservation,CEBAS-CSIC,Murcia,Spain2DepartmentofScienceandAgroforestryTechnologyandGenetics,HigherTechnicalSchoolofAgriculturalandForestryEngineering,UniversityofCastilla-LaMancha,Albacete,Spain3LaboratoryofEnvironmentalMicrobiology,InstituteofMicrobiologyoftheCAS,Praha4,CzechRepublic4DepartmentofIsotopeBiogeochemistry,Helmholtz-CentreforEnvironmentalResearch-UFZ,Leipzig,Germany5DepartmentofMolecularSystemsBiology,Helmholtz-CentreforEnvironmentalResearch-UFZ,Leipzig,GermanyCorrespondenceFelipeBastida,CEBAS-CSIC.DepartmentofSoilandWaterConservation.CampusUniversitariodeEspinardo,Murcia,Spain.Email:[e-mail]CO,Grant/AwardNumber:AGL2014-54636-R;Ram
onyCajalMINECOandFEDERfunds,Grant/AwardNumber:RYC-2012-10666;MINECO,Grant/AwardNumber:AGL2014-55658-R;Fundaci
onS
eneca,Grant/AwardNumber:19896/GERM/15;InstituteofMicrobiologyoftheCAS,Grant/AwardNumber:RVO61388971AbstractClimatechangewillaffectsemiaridecosystemsthroughseveredroughtsthatincreasethecompetitionforresourcesinplantandmicrobialcommunities.Inthesehabitats,adaptationstoclimatechangemayconsistofthinning—thatreducescom-petitionforresourcesthroughadecreaseintreedensityandthepromotionofplantsurvival.Wedecipheredthefunctionalandphylogeneticresponsesofthemicrobialcommunityto60yearsofdroughtinducedbyrainfallexclusionandhowforestmanagementaffectsitsresistancetodrought,inasemiaridforestecosystemdomi-natedbyPinushalepensisMill.AmultiOMICapproachwasappliedtorevealnovel,community-basedstrategiesinthefaceofclimatechange.Thediversityandthecompositionofthetotalandactivesoilmicrobiomewereevaluatedby16SrRNAgene(bacteria)andITS(fungal)sequencing,andbymetaproteomics.Themicrobialbiomasswasanalyzedbyphospholipidfattyacids(PLFAs),andthemicrobiallymedi-atedecosystemmultifunctionalitywasstudiedbytheintegrationofsoilenzymeactivitiesrelatedtothecyclesofC,N,andP.Themicrobialbiomassandecosystemmultifunctionalitydecreasedindrought-plots,asaconsequenceofthelowersoilmoistureandpoorerplantdevelopment,butthisdecreasewasmorenotableinunthinnedplots.Thestructureanddiversityofthetotalbacterialcommunitywasunaffectedbydroughtatphylumandorderlevel,butdidsoatgenuslevel,andwasinfluencedbyseasonality.However,thetotalfungalcommunityandtheactivemicrobialcommunityweremoresensitivetodroughtandwererelatedtoecosystemmultifunctionality.Thinninginplotswithoutdroughtincreasedtheactivediversitywhilethetotaldiversitywasnotaffected.Thinningpromotedtheresistanceofecosystemmultifunctionalitytodroughtthroughchangesintheactivemicrobialcommunity.Theintegrationoftotalandactivemicrobiomeanalysesavoidsmisinter-pretationsofthelinksbetweenthesoilmicrobialcommunityandclimatechange.KEYWORDSclimatechange,drought,forestmanagement,genomics,metaproteomics,microbialbiomass,microbialcommunity,semiaridReceived:13December2016|Accepted:30May2017DOI:10.1111/gcb.13790GlobChangeBiol.2017;23:4185–4203.wileyonlinelibrary.com/journal/gcb©2017JohnWiley&SonsLtd|41851|INTRODUCTIONClimatechangeisanunavoidablephenomenonthatwillaffectter-restrialecosystemsworldwide.InSouthernEurope,areductioninprecipitationisexpectedtoaffectplantdevelopmentandsoilfertility(IPCC,2013).However,droughtmayhaveadditionaladverseeffectsonecosystems.Theadventofreducedrainfallandhightempera-tures,aswellaspernicioushumanactions,isexpectedtoincreasethefrequencyoffiresinforestareasoftheIberianpeninsula(Lindneretal.,2010;HedoSantiado,Lucas-Borja,Wic-Baena,Andr
es-Abell
an,&lasHeras,2015).Aftersuchfires,plantdevelop-mentproceedsslowly,particularlyinsemiaridareaswithlimitedwateravailability.Hence,itisexpectedthatplantgrowthafterafirewillbeevenmoreconstrainedasaconsequenceofthedroughtintheseareas.Thisisthereasonwhyparticularsilviculturaltreatments,suchasthinning,arerequiredtofosterplantsurvivalintheseecosystems.Usually,thinningreducestreedensitiesand,tradition-ally,ithasbeencarriedouttomanageforeststandssothatcompeti-tionforresources(i.e.,waterandnutrients)betweenneighboringtreesisavoided,asawaytoimprovetreegrowthandsurvivalandecosystemproductivity(Gonz
alez-Ochoa,L
opez-Serrano,&lasHeras,2004;L
opez-Serrano,lasHeras,Gonz
alez-Ochoa,&Garc
ıa-Morote,2005).Moreover,ithasbeenobservedthatthinningaffectsthestructureofthesoilmicrobialcommunitythroughchangesinsoiltemperatureandtheabundanceoffungi-feedingnematodesinpineplantationineasternTibetanPlateau(Yang,Pang,Hu,Bao,&Tian,2017).Furthermore,RietlandJackson(2012)concludedthatthin-ningreducestheamountoflitterinamesicforestinnorthernMis-sissippiandpromotedtheefficiencyofsoilenzymesinvolvedinlitterdegradation.Moreover,ithasbeenhighlightedthatmanyoftheimpactsofclimatechangeonthesoilmicrobialcommunitymayoccurviadirectorindirecteffectsonplantcommunities(Bardgett