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OPENORIGINALARTICLENematodegrazingpromotesbacterialcommunitydynamicsinsoilattheaggregatelevelYujiJiang1,ManqiangLiu2,JiabaoZhang1,YanChen1,XiaoyunChen2,LijunChen1,HuixinLi2,Xue-XianZhang3andBoSun11StateKeyLaboratoryofSoilandSustainableAgriculture,InstituteofSoilScience,ChineseAcademyofSciences,Nanjing,China;2CollegeofResourcesandEnvironmentalSciences,NanjingAgriculturalUniversity,Nanjing,Chinaand3InstituteofNaturalandMathematicalSciences,MasseyUniversityatAlbany,Auckland,NewZealandNematodepredationhasimportantrolesindeterminingbacterialcommunitycompositionanddynamics,buttheextentoftheeffectsremainslargelyrudimentary,particularlyinnaturalenvironmentsettings.Here,weinvestigatedthecomplexmicrobial–microfaunalinteractionsintherhizosphereofmaizegrowninredsoils,whichwerederivedfromfourlong-termfertilizationregimes.Root-freerhizospheresoilsampleswereseparatedintothreeaggregatefractionswherebytheabundanceandcommunitycompositionwereexaminedfornematodeandtotalbacterialcommu-nities.Afunctionalgroupofalkalinephosphomonoesterase(ALP)producingbacteriawasincludedtotestthehypothesisthatnematodegrazingmaysignificantlyaffectspecificbacteria-mediatedecologicalfunctions,thatis,organicphosphatecyclinginsoil.Resultsofcorrelationanalysis,structuralequationmodelingandinteractionnetworkscombinedwithlaboratorymicrocosmexperimentsconsistentlyindicatedthatbacterivorousnematodesenhancedbacterialdiversity,andtheabundanceofbacterivoreswaspositivelycorrelatedwithbacterialbiomass,includingALP-producingbacterialabundance.Significantly,sucheffectsweremorepronouncedinlargemacroaggregatesthaninmicroaggregates.TherewasapositivecorrelationbetweenthemostdominantbacterivoresProtorhabditisandtheALP-producingkeystone'species'Mesorhizobium.Takentogether,thesefindingsimplicateimportantrolesofnematodesinstimulatingbacterialdynamicsinaspatiallydependentmanner.TheISMEJournaladvanceonlinepublication,25July2017;doi:10.1038/ismej.2017.120IntroductionResourcecompetitionandpredationarethetwomajordrivingforcesunderlyingthedynamicchangesofspeciescompositioninthebiologicalcommunity(ChessonandKuang,2008).Formicro-organismsinhabitingsoil,theimportanceofresourcecompetitionhasbeenwelldocumented,particularlywiththeimprovedaccessibilityofnext-generationsequencingandstableisotopetechniques(Bulgarellietal.,2013).Althoughtheimportanceofpredationbymicrofaunahaslongbeenrecognized,thepoten-tialeffectsofpredationremainpoorlydefined.Fewstudieshaveaddressedthecomplexmicrobial–microfaunalinteractionsinopen-fieldenvironments(Neher,2010).Forexample,nematodescanstimu-latemicrobialactivity,resultingineitheranincreaseoradecreaseofmicrobialbiomassinmicrocosmexperiments(Trapetal.,2016).Thegrazing-inducedinfluencesonmicrobialabundancevaryaccordingtoporestructureanddistributionoftheaccessibleresourcessuchassoilorganicmatterandplantroots(Rønnetal.,2012).Soilshaveacomplexhierarchicalstructureincludingporedistributionandaggregates.Soilaggregatesprovidespatiallyheterogeneoushabitatsformicroorganisms,whichvaryinnutrientavail-ability,waterpotentialandoxygenconcentrationaswellaspredationpressure(Ranjard,Richaume,2001;Jiangetal.,2013).Aggregatefractionsareassembledbyorganicmatterandmineralparticles(TisdallandOades,1982).Macroaggregatesnormallycontainmorelabilesubstratespredominantlyderivedfromplantresidues(BronickandLal,2005),andharborhigheramountsoffungalbiomassthanmicroaggregates(MAs,RilligandMummey,2006).Incontrast,MAsarecharacterizedbythehighestconcentrationofstableorganiccarbon,andmoreimportantly,theyprovideaprotectivemicro-environmentformicrobialgrowth(Sixetal.,2000).TherelativesmallporesizesmakeMAsinaccessibleCorrespondence:X-XZhangorBSun,StateKeyLaboratoryofSoilandSustainableAgriculture,InstituteofSoilScience,ChineseAcademyofSciences,No.71EastBeijingRoad,Nanjing210008China.E-mail:x.x.zhang1@massey.ac.nzorbsun@issas.ac.cnReceived26February2017;revised21May2017;accepted8June2017TheISMEJournal(2017),1–13(typically30–90μmindiameter;QuénéhervéandChotte,1996).Thus,itiscrucialtounderstandthepre-dator–preyinteractionsattheaggregatelevel(EttemaandWardle,2002).Ofparticularsignificanceistherhizospheresoilasitfunctionsasthecriticalinterfaceforresourceexchangebetweenplantsandsoil.Comparedwithbulksoil,therhizospherecontainsalargeamountofsmallorganiccompoundsexcretedfromtherootsoflivingplants,supportinghighlevelsofmicrobialactivity.Microorganismsareintegraltothecyclingofnutritionalelementssuchasnitrogenandphos-phorus(vanderHeijdenetal.,2008),andbacterial-feedingnematodespredationreleasesnutrientssequesteredinbacterialbiomassintherhizosphereniche(Bonkowskietal.,2009).However,nematodesnormallyhavespecialfoodpreferences,andbacteriawerenotequallysusceptibletopredationbynema-todes.Selectivegrazingbynematodescanalterthebacterialcommunitycomposition(Djigaletal.,2004).Thisleadstoanimportantbutunexploredhypothesisthatnematodegrazingaffectstotalbac-terialcommunityandspecificfunctionalgroupssuchasphosphorus(P)cyclingindifferentmanners.Microbial–microfaun
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