11Soilmicrobialcommunitiesandelkforagingint

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LETTERSoilmicrobialcommunitiesandelkforagingintensity:implicationsforsoilbiogeochemicalcyclinginthesagebrushsteppeLaurenC.Cline,1*DonaldR.Zak,2,3RimaA.Upchurch,2ZacharyB.Freedman4andAnnaR.Peschel5AbstractForagingintensityoflargeherbivoresmayexertanindirecttop-downecologicalforceonsoilmicrobialcommunitiesviachangesinplantlitterinputs.Weinvestigatedtheresponsesofthesoilmicrobialcommunitytoelk(Cervuselaphus)winterrangeoccupancyacrossalong-termforagingexclusionexperimentinthesagebrushsteppeoftheNorthAmericanRockyMountains,combin-ingphylogeneticanalysisoffungiandbacteriawithshotgunmetagenomicsandextracellularenzymeassays.Winterforagingintensitywasassociatedwithreducedbacterialrichnessandincreasinglydistinctbacterialcommunities.Althoughfungalcommunitiesdidnotrespondlinearlytoforagingintensity,agreaterb-diversityresponsetowinterforagingexclusionwasobserved.Furthermore,winterforagingexclusionincreasedsoilcellulolyticandhemicellulolyticenzymepotentialandhigherforagingintensityreducedchitinolyticgeneabundance.Thus,futurechangesinwinterrangeoccupancymayshapebiogeochemicalprocessesviashiftsinmicrobialcommuni-tiesandsubsequentchangestotheirphysiologicalcapacitiestocyclesoilCandN.KeywordsBacteria,communityassembly,decomposition,extracellularenzyme,foraging,functionalgene,fungi,herbivore,metagenome.EcologyLetters(2017)20:202–211INTRODUCTIONLargeherbivoresfunctionas‘engineers’inawidevarietyofecosystems(Frank&Groffman1998;Tanentzap&Coomes2012)throughtheremovalofplantbiomass,whichaltersplantphysiologyandlitterbiochemistry(Bardgettetal.1998;Olofssonetal.2004).Saprotrophicmicroorganismsarelim-itedbytheenergytheyenzymaticallyharvestfromplantdetri-tus;therefore,theproductionofplantdetritusanditsbiochemicalcompositionfunctionasselectiveforcesthatshapethecompositionofmicrobialcommunitiesinsoil(e.g.Cline&Zak2015).Itstandstoreasonthatforagingintensityoflargeherbivoresmaystructurethecompositionandfunc-tionofmicrobialcommunitiesinsoilviachangesintheabun-danceandbiochemistryofplantlittersubstrates.Understandingthispotentialisofecosystem-levelsignificance,becausesoilmicroorganismsregulatekeyecosystemfunctions,includingsoilCstorageandplantnutrientavailability(vanderHeijdenetal.2008;Clemmensenetal.2013).Althoughevidenceindicatesthatlargeherbivorescanmod-ifysoilCandNcycling(e.g.Olofssonetal.2004),under-standingthemechanismbywhichmigratoryungulatesstructurethecompositionandfunctionofthesoilmicrobialcommunityremainslargelyunknown.Selectiveforagingbylargemammalianherbivorescanreducesoilmicrobialbio-massandsignificantlymodifymicrobialcommunitycomposi-tion(Pastoretal.1993;Pescheletal.2015).Changesinthesizeandmembershipofthesoilcommunitycan,inturn,feed-backtoaltermicrobialmetabolicpotentialforbiogeochemicalcycling(Yangetal.2013),whichhasdirectimplicationsforthecyclingandstorageofsoilCandN.Forexample,ungu-lateforagingonwinterrangedecreasedtheabundanceofmicrobialfunctionalgenesencodingenzymesinvolvedinlig-nocellulosemetabolism,aswellassoilrespirationandnetNmineralisation(Pescheletal.2015).Incontrast,herbivorefor-agingcanalsoincreasetheabundanceoffunctionalgenesencodingenzymesmediatingthedecayofplantdetritus(Yangetal.2013).Thesemixedresponsesbysoilmicrobialcommu-nitiestoungulateforagingmaybetheresultofdifferencesinforagingintensitiesacrossregions(McSherry&Ritchie2013),althoughthishypothesisremainstobetested.NorthAmericanelk(Cervuselaphus)aredominantungulateherbivoresinthesagebrushsteppeandpresentauniqueopportunitytoinvestigatethemicrobialmechanismbywhichmigratoryungulatesinducebelowgroundresponses(Middle-tonetal.2013;Jonesetal.2014;Coleetal.2015).Inhabitingmountainousregions,NorthAmericanelkmigratefromhigh-elevationsummerrangeandcongregateinvalleybottoms1DepartmentofPlantandMicrobialBiology,UniversityofMinnesota,St.Paul,MN,USA2SchoolofNaturalResources&Environment,UniversityofMichigan,AnnArbor,MI,USA3DepartmentofEcology&Evolution,UniversityofMichigan,AnnArbor,MI,USA4DivisionofPlantandSoilSciences,WestVirginiaUniversity,Morgantown,WV,USA5DepartmentofConservationBiology,UniversityofMinnesota,St.Paul,MN,USA*Correspondence:E-mail:clinela@umn.edu©2017JohnWiley&SonsLtd/CNRSEcologyLetters,(2017)20:202–211doi:10.1111/ele.12722duringwinter,avoidingdeepsnowandaccessingforage(Boyce1991).Inspring,theselargeungulatesfollowthesnowmelttohighelevationsinwhichyoungplantsemergewithprotein-richfoliage(Sawyer&Kauffman2011).Becausewinterrangeoccupancybyelkandotherungulateherbivorescanalterthemembershipofsoilmicrobialcommunities(Pescheletal.2015),winterrangeoccupancymayhaveconse-quencesforratesofbiogeochemicalcycling.Specifically,netNmineralisationwassignificantlygreaterintheabsenceofelkwinterforagingacrossthesagebrushsteppe,suggestingthatsoilNcyclingratesmaybereducedbytheremovalofplantinputsandsubsequentchangestothesoilmicrobialcommunity(Pescheletal.2015).ToelucidatethemicrobialmechanismbywhichforagingintensityinwinterrangemayreduceratesofsoilCandNcycling,wecombinedphylogeneticanalysesofmicrobialcom-munitieswithshotgunmetagenomicsandextracellularenzymeassays.Weusedtheseappr

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