13Dynamicsofmicrobialcommunitycompositionand

ORIGINALARTICLEDynamicsofmicrobialcommunitycompositionandsoilorganiccarbonmineralizationinsoilfollowingadditionofpyrogenicandfreshorganicmatterTheaWhitman1,2,CharlesPepe-Ranney1,AkioEnders1,ChantalKoechli1,AshleyCampbell1,DanielHBuckley1andJohannesLehmann1,31SchoolofIntegrativePlantScience,CornellUniversity,Ithaca,NY,USA;2DepartmentofSoilScience,UniversityofWisconsin—Madison,Madison,WI,USAand3AtkinsonCenterforaSustainableFuture,CornellUniversity,Ithaca,NY,USAPyrogenicorganicmatter(PyOM)additionstosoilscanhavelargeimpactsonsoilorganiccarbon(SOC)cycling.AsthesoilmicrobialcommunitydrivesSOCfluxes,understandinghowPyOMadditionsaffectsoilmicrobesisessentialtounderstandinghowPyOMaffectsSOC.WestudiedSOCdynamicsandsurveyedsoilbacterialcommunitiesafterOMadditionsinafieldexperiment.Weproducedandmixedineither350°CcornstoverPyOMoranequivalentinitialamountofdriedcornstovertoaTypicFragiudeptsoil.StoverincreasedSOC-derivedandtotalCO2fluxes(upto6x),andcausedrapidandpersistentchangesinbacterialcommunitycompositionover82days.Incontrast,PyOMonlytemporarilyincreasedtotalsoilCO2fluxes(upto2x)andcausedfewerchangesinbacterialcommunitycomposition.Oftheoperationaltaxonomicunits(OTUs)thatincreasedinresponsetoPyOMadditions,70%alsorespondedtostoveradditions.TheseOTUslikelythriveoneasilymineralizablecarbon(C)thatisfoundbothinstoverand,toalesserextent,inPyOM.Incontrast,wealsoidentifieduniquePyOMresponders,whichmayrespondtosubstratessuchaspolyaromaticC.Inparticular,membersofGemmatimonadetestendedtoincreaseinrelativeabundanceinresponsetoPyOMbutnottofreshorganicmatter.WeidentifytaxatotargetforfutureinvestigationsofthemechanisticunderpinningsofecologicalphenomenaassociatedwithPyOMadditionstosoil.TheISMEJournaladvanceonlinepublication,29April2016;doi:10.1038/ismej.2016.68IntroductionLargeinputsofpyrogenicorganicmatter(PyOM)infire-affectedecosystemscanconstituteupto80%oftotalsoilorganiccarbon(SOC)(Lehmannetal.,2008).WhetherPyOMisproducednaturallyinfires(CzimczikandMasiello,2007),intentionallyforcarbon(C)managementand/orasanagriculturalamendment(Lehmann,2007;Laird,2008),itisimportanttounderstandhowitaffectstheCcycle(Whitmanetal.,2010).PyOMadditionstosoilcansignificantlyaffectplantgrowthandcropyields(Jefferyetal.,2011)andSOCdynamics(Maestrinietal.,2014;Watzingeretal.,2014;Whitmanetal.,2015).Forexample,amongothereffects,PyOMcanchangesoilpH(Guletal.,2015),addnutrientstosoils(Endersetal.,2012)andaltersoilwater-holdingcapacity(Abeletal.,2013).AlthoughPyOMadditionstosoilscanalterinorganicCdynamicsthroughchangestosoilpH,akeymechanismforchangesinSOCmineralizationisalteredmicrobialmineralizationofSOCinresponsetoPyOM(Maestrinietal.,2014;Whitmanetal.,2015).Hence,anunderstandingoftheeffectsofPyOMonthesoilmicrobialcommunitycompositionandfunctionisrequiredtounderstandtheeffectsofPyOMonSOCstocks.TherearemanywaysPyOMcouldaffectsoilmicroorganisms(KuzyakovandBol,2004;Lehmannetal.,2011;Amelootetal.,2013),including,butnotlimitedto,microbialuseofPyOMasasourceofenergyornutrients,changesinsoilphysicalorchemicalcharacteristics,impactsonplantgrowthandinterferencewithmicrobialsignaling(Masielloetal.,2013).RecentresearchhasonlybeguntoidentifyPyOMeffectsonsoilmicrobialcommunities,anditisclearthatPyOMadditionstosoilcaninducechangesinsoilmicrobialcommunitycomposition.Mostcurrentevidencehasbeengatheredusingfingerprintingapproaches,suchasterminalrestrictionfragmentlengthpolymorphism(Bingemanetal.,1953;Correspondence:TWhitman,DepartmentofSoilScience,UniversityofWisconsin—Madison,263SoilsBuilding,1525ObservatoryDrive,Madison,WI53706,USA.E-mail:[e-mail]6December2015;revised12February2016;accepted22March2016TheISMEJournal(2016),1–13©2016InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/16)ordenaturinggradientgelelectrophoresis(Koltonetal.,2011;Chenetal.,2013),orbysurveyingphospholipidfattyacidstoassessmicrobialdiversityatlowphylogeneticresolution(Dunavin,1969;Jindoetal.,2012;Gomezetal.,2014;Watzingeretal.,2014;Mitchelletal.,2015).Inaddition,clonelibrariestargetingfunctionalgenes(Songetal.,2014)andsomehigh-throughputDNAsequencingapproacheshavebeenappliedtosurveymicroorganismsinPyOMsystems.Forexample,significantdifferenceswerefoundbetweensoilbacterialcommunitiesinAmazonianDarkEarthsoils(amendedwithPyOMthousandsofyearsago),PyOMisolatedfromtheAmazonianDarkEarthsoilsandadjacentunamendedAcrisols,bysurveyingsmallsubunitribosomalRNA(SSUrRNA)genes(Taketanietal.,2013).Ahandfulofotherstudieshaveusedhigh-throughputsequencingapproachestocharacterizePyOMeffectsonsoilbacterialcommunitycomposition(forexample,Nielsenetal.,2014;Xuetal.,2014).However,owingtothelownumberofstudiesandthewidediversityofPyOMmaterials,additionrates,soilsandenvironmentalconditions,itisdifficulttodrawgeneralizableconclusionsabouttheeffectsofPyOMonsoilmicrobialcommunitycomposition,particularlyatthelevelofindividualtaxa.Inthisstudy,weinvestigatedtheeffectsofPyOMadditionsonSOCmineralizationandsoilbacterialcommunitycompositioninafieldsettingover12wee