46Landscapetopographystructuresthesoilmicrob

ARTICLELandscapetopographystructuresthesoilmicrobiomeinarcticpolygonaltundraNeslihanTaş1,EmmanuelPrestat1,2,ShiWang1,YuxinWu1,CraigUlrich1,TimothyKneafsey1,SusannahG.Tringe3,MargaretS.Torn1,4,SusanS.Hubbard1&JanetK.Jansson5IntheArctic,environmentalfactorsgoverningmicrobialdegradationofsoilcarbon(C)inactivelayerandpermafrostarepoorlyunderstood.HerewedeterminedthefunctionalpotentialofsoilmicrobiomeshorizontallyandverticallyacrossacryoperturbedpolygonallandscapeinAlaska.Withcomparativemetagenomics,genomebinningofnovelmicrobes,andgasfluxmeasurementsweshowthatmicrobialgreenhousegas(GHG)productionisstronglycorrelatedtolandscapetopography.Activelayerandpermafrostharborcontrastingmicrobiomes,withincreasingamountsofActinobacteriacorrelatingwithdecreasingsoilCinpermafrost.Whilemicrobialfunctionssuchasfermentationandmethanogenesisweredominantinwetterpolygons,indrierpolygonsgenesforCmineralizationandCH4oxidationwereabundant.TheactivelayermicrobiomewaspoisedtoassimilateNandnottoreleaseN2O,reflectinglowN2Ofluxmeasurements.TheseresultsprovidemechanisticlinksofmicrobialmetabolismtoGHGfluxesthatareneededfortherefinementofmodelpredictions.DOI:10.1038/s41467-018-03089-zOPEN1EarthandEnvironmentalSciencesAreaLawrenceBerkeleyNationalLaboratory,OneCyclotronRoad,MSB74,Berkeley,CA94720,USA.2HalioDx,LuminyBiotechEntreprises,163AvenuedeLuminy,13288MarseilleCedex9,France.3DOEJointGenomeInstitute(DOE-JGI),2800MitchellDr,WalnutCreek,CA94598,USA.4EnergyandResourcesGroup,UniversityofCalifornia,Berkeley,California94720,USA.5BiologicalSciencesDivisionPacificNorthwestNationalLaboratory,902BattelleBoulevard,Richland,WA99352,USA.CorrespondenceandrequestsformaterialsshouldbeaddressedtoN.T.(email:[e-mail])ortoJ.K.J.(email:[e-mail])NATURECOMMUNICATIONS|(2018)9:777|DOI:10.1038/s41467-018-03089-z|():,;Icewedgepolygonsareimportanttopographicalandhydro-logicalfeaturesinotherwiselowreliefcoastalarctictundra1.Icewedgedevelopmentbeginsatthegroundsurfaceasfrostcracksandformsapolygonalpatterninthetopsoilasicewedgesenlargeovertime2.Approximately20%oftheArcticCoastalPlainofnorthernAlaskacontainspolygonalgroundsandthawlakesthatdevelopinice-richpermafrost3.Dependingontheirgrowthordegradationstate,icewedgescancreatevarioussizes(~5–20m)andtypesofpolygons.Developmentofthismicro-topographyregulateswaterdistributionoverlargeareasandeffectssoilpropertiesthatareimportantforCcycling,suchassoilmoisture,otherbiogeochemicalcycles,andfreeze-thawdynam-ics2.Withapredictedincreaseinsurfaceairtemperatureof5–6°Cbytheendofthiscentury4anacceleratedsoilwarming5inthepolygonaltundrawillleadtoadeepeningoftheseasonally-thawedactivelayer,enlargepermafrostthawareaandchangesinthedistributionofwateracrossthislandscape.Therefore,theestimated1035PgC6storedinarcticecosystemscouldundergorapidmicrobialdecomposition,resultinginasignificantpositivefeedbackontheclimateintheformofgreenhousegas(GHG)emissions7.AmajorchallengeinlinkingmicrobialfunctionstoGHGemissionsinarcticsoilsistheidentificationofenvironmentalfactorsthatgovernthedistributionofmicrobialfunctionsandCflux7.Besidesthecomplexityintroducedbythehighmicrobialdiversityinthesesoils7,ourunderstandingofenvironmentalcontrolsandspatialvariationonmicrobialCmetabolism,withrespecttohydrologicalpatterns8,islimited.ToresolvethemicrobialmetabolismleadingtoGHGemissionsacrossthepolygonaltundraintheArctic,weusedmultipleDNAsequen-cingapproachestodeterminethesoilmicrobialcommunitycompositionandmetabolicpotential.WefocusedourstudiesintheBarrowEnvironmentalObservatory(BEO)locatedinBarrow,Alaska.Polygonalgroundsconstitute65%ofthesurfaceintheBarrowPeninsula3.ThelandscapeoftheBEOincludesamosaicofdrainedthawlakesandinterstitialpolygonswheredifferentpolygontypes—high-centered(HC),flat-centered(FC)andlow-centered(LC)—representdifferentstatesofpermafrostdegra-dationandmoisturedistribution1(Fig.1).Varianceinlandscapefeatures(e.g.,rim,center,andtrough)havebeenhypothesizedtoresultindistinctmicrobialhabitatsthatmightresponddifferentlytowarming2.Wecollected29activelayersoilcoresalonga500mtransectthatextendedlaterallyacrossHC,FC,andLCpolygonsintheBEOinSeptember2011.Thetop0–50cm,includingsurfaceorganic(0–10cm)anddeepermineral(20–50cm)layersoftheactivelayer,wascollectedfromcenters,rims,andtroughsofthepolygonsalongthetransect1(Fig.1).Additionally,twodeepcores,1and2.65mindepth,weretakenfromaFCpolygonwithinthetransectinApril2012toaccesstheverticaldistributionofthemicrobialcommunitiesinthepermafrost.Thesoilmicrobiomecompositionsinthesamplesweredeterminedbysequencingof16SrRNAgenes(16S)andthefunctionalpotentialwasinferredbysequencingoftotalmetagenomicDNA.ThesequencedatawerecorrelatedtoinsituGHGfluxmeasurementsandgeophysicalandgeochemicalsoilcharacteristics1.Hereweshowthatsoilmicrobiomesandtheirfunctionalpotentialsinarcticpolygonalgroundsaregovernedbythelandscapemicrotopography.ResultsMicrobialcommunitycompositionislinkedtopolygontypes.Wefoundashiftinmicrobialcommunitycompositionalongthepolygontransect,withdifferentpolygonty