4Globalnegativeeffectsofnitrogendepositiono

TheISMEJournal’anZhang1●HanY.H.Chen2●HonghuaRuan1Received:24October2017/Revised:13February2018/Accepted:20February2018©InternationalSocietyforMicrobialEcology2018AbstractSoilmicrobescomprisealargeportionofthegeneticdiversityonEarthandinfluencealargenumberofimportantecosystemprocesses.Increasingatmosphericnitrogen(N)depositionrepresentsamajorglobalchangedriver;however,itisstilldebatedwhethertheimpactsofNdepositiononsoilmicrobialbiomassandrespirationareecosystem-typedependent.Moreover,theextentofNdepositionimpactsonmicrobialcompositionremainsunclear.Hereweconductaglobalmeta-analysisusing1408pairedobservationsfrom151studiestoevaluatetheresponsesofsoilmicrobialbiomass,composition,andfunctiontoNaddition.Weshowthatnitrogenadditionreducedtotalmicrobialbiomass,bacterialbiomass,fungalbiomass,biomasscarbon,andmicrobialrespiration.Importantly,thesenegativeeffectsincreasedwithNapplicationrateandexperimentalduration.Nitrogenadditionreducedthefungitobacteriaratioandtherelativeabundancesofarbuscularmycorrhizalfungiandgram-negativebacteriaandincreasedgram-positivebacteria.OurstructuralequationmodelingshowedthatthenegativeeffectsofNapplicationonsoilmicrobialabundanceandcompositionledtoreducedmicrobialrespiration.TheeffectsofNadditionwereconsistentacrossglobalterrestrialecosystems.OurresultssuggestthatatmosphericNdepositionnegativelyaffectssoilmicrobialgrowth,composition,andfunctionacrossallterrestrialecosystems,withmorepronouncedeffectswithincreasingNdepositionrateandduration.IntroductionSoilmicrobescomprisealargeportionofthegeneticdiversityonEarthandarecriticaltothemaintenanceofplantdiversityandalargenumberofessentialecosystemprocesses[1–6].Atmosphericnitrogen(N)depositionhasclimbedbythree-to-five-foldoverthecourseofthe20thcentury[7].Acrosstheglobe,theincreaseofNdepositionisstronglyassociatedwithregionalhumanpopulationdensity[8]withitsimpactsreachingfarbeyond[9].AlthoughatmosphericNdeposition,simulatedbyNferti-lizationexperiments,mayincreaseplantabovegroundandbelowgroundgrowth[10,11],itreducesterrestrialplantdiversity[12]andaltersplantbiomasscarbon(C),N,andphosphoruscycles[13].Althoughsoilmicrobesarecriticaldriversforplantdiversityandproductivityinterrestrialecosystems[3,5,14–16],ourunderstandingofatmosphericNdepositiononmicrobialgrowth,function,andcommunitycompositionremainselusive.AbetterunderstandingofsoilmicrobialresponsestoNadditioniscriticaltopre-dictingtheconsequencesofincreasinganthropogenicallyderivedNadditiononterrestrialecosystems.ExcessiveNinputscanhavemultipleeffectsonsoilmicrobialgrowth,composition,andfunction.First,weexpectedthatincreasedNwouldreducetotalmicrobialbiomassduetodirectinhibitionandreducedinvestmentinmicrobes[17–19].IncreasedNreducesfungalbiomassviachangesinplant-specificexudatesandalterationsinnutrientcompetitionbetweenplantsandrhizospheremicrobes[20]ordirectlybyinhibitingthegrowthofwhiterotfungi[21].Nitrogenadditioncanalsoreducethemetaboliccapabilitiesofsoilbacterialcommunities[22].UnderNfertilization,fungitobacteriaratio(F:B)isexpectedtodecreasesincefungihavelowerNdemandsthanbacteria[23].MicrobialbiomassCdecreasesfollowingNfertilizationdue*[e-mail]*[e-mail]1Co-InnovationCenterforSustainableForestryinSouthernChina,CollegeofBiologyandtheEnvironment,NanjingForestryUniversity,Nanjing210037,China2FacultyofNaturalResourcesManagement,LakeheadUniversity,955OliverRoad,ThunderBay,ONP7B5E1,CanadaElectronicsupplementarymaterialTheonlineversionofthisarticle()containssupplementarymaterial,whichisavailabletoauthorizedusers.1234567890();,:todecreasedsoilpHresultingingreaterosmoticpotentialandincreasedsolubilityofaluminumthatistoxictosoilmicrobes[24].MicrobialbiomassNcouldeitherincreasebecauseoffertilization-inducedNavailability[25]ordecreaseassoilmicrobesimmobilizeahighproportionofmineralizedNinfertilizedplots[26].MicrobialC:NcoulddecreaseconcomitantlywiththereductionofF:BasfungiexhibithigherC:Nthanbacteria[27].Second,weexpectedthatNadditionwouldalterrelativeabundancesofmicrobialgroups.ExcessiveNinducesashiftinthepredominantmicrobialstrategies,favoringamoreactive,copiotrophicmicrobialcommunity[28].UnderchronicNaddition,therelativeabundanceofectomycor-rhizalfungideclinesandoffsetbyanincreaseintherelativeabundanceofsaprotrophs[29].AlowerplantdemandforNfollowingNenrichmentcouldinducereductionsinrelativeabundanceofarbuscularmycorrhizalfungi[30].Further-more,reductionsinCallocationtotreerootscouldinduceadecreaseingram-negative(G−)abundanceandanincreaseingram-positive(G+)abundance[31]asG+bacteriacanusemorerecalcitrantCfractionswhileG−bacteriarelyonreadilydegradableplantCsources[32].Third,althoughtheincreasesinplantgrowthwithNaddition[10,11]couldleadtohigherautotrophicrespiration,weexpectedthatsoilacidificationfromexcessiveNwouldinhibitenzymaticactivities,decreasesoilorganicmatterdecomposition,andthusreducemicrobialrespiration[18,33