29Modelingofsoilnitrificationresponsestotem

ORIGINALARTICLEModelingofsoilnitrificationresponsestotemperaturerevealsthermodynamicdifferencesbetweenammonia-oxidizingactivityofarchaeaandbacteriaAnneETaylor1,AndrewTGiguere1,ConorMZoebelein2,DavidDMyrold1andPeterJBottomley1,31DepartmentofCropandSoilScience,OregonStateUniversity,Corvallis,OR,USA;2DepartmentofEnvironmentalEngineering,OregonStateUniversity,Corvallis,OR,USAand3DepartmentofMicrobiology,OregonStateUniversity,Corvallis,OR,USASoilnitrificationpotential(NP)activitiesofammonia-oxidizingarchaeaandbacteria(AOAandAOB,respectively)wereevaluatedacrossatemperaturegradient(4–42°C)imposeduponeightsoilsfromfourdifferentsitesinOregonandmodeledwithboththemacromolecularratetheoryandthesquarerootgrowthmodelstoquantifythethermodynamicresponses.ThereweresignificantdifferencesinresponsebythedominantAOAandAOBcontributingtotheNPs.Theoptimaltemperatures(Topt)forAOA-andAOB-supportedNPsweresignificantlydifferent(Po0.001),withAOAhavingTopt412°CgreaterthanAOB.Thechangeinheatcapacityassociatedwiththetemperaturedependenceofnitrification(DCzP)wascorrelatedwithToptacrosstheeightsoils,andtheDCzPofAOBactivitywassignificantlymorenegativethanthatofAOAactivity(Po0.01).Modelresultspredicted,andconfirmatoryexperimentsshowed,asignificantlylowerminimumtemperature(Tmin)anddifferent,albeitverysimilar,maximumtemperature(Tmax)valuesforAOBthanforAOAactivity.TheresultsalsosuggestedthattheremaybedifferentformsofAOAAMOthatareactiveoverdifferenttemperaturerangeswithdifferentTmin,butnoevidenceofmultipleTminvalueswithintheAOB.Fundamentaldifferencesintemperature-influencedpropertiesofnitrificationdrivenbyAOAandAOBprovidessupportfortheideathatthebiochemicalprocessesassociatedwithNH3oxidationinAOAandAOBdifferthermodynamicallyfromeachother,andthatalsomightaccountforthedifficultiesencounteredinattemptingtomodeltheresponseofnitrificationtotemperaturechangeinsoilenvironments.TheISMEJournaladvanceonlinepublication,20December2016;doi:10.1038/ismej.2016.179IntroductionBothammonia-oxidizingarchaea(AOA)andbacteria(AOB)co-habitdiversesoils.Insomesituations,AOAoutnumberAOBbytwotothreeordersofmagnitude,andinothercases,theirabundancesaremoresimilar(Leiningeretal.,2006,AdairandSchwartz,2008,Schaussetal.,2009,Tayloretal.,2012).ConsiderabledebatehasoccurredabouttherelativecontributionsofAOAandAOBtosoilnitrification,andthefactorsthatmayinfluencethosecontributions(Schleper,2010,Hatzenpichler,2012,ProsserandNicol,2012).ThereisdirectandindirectevidencethatfactorssuchasincreasedCO2,Nconcentrationandform,pH,andtemperaturediffer-entiallyinfluenceAOAandAOBcontributionstonitrification(Huetal.,2015,Liuetal.,2015,Sunetal.,2015).Forexample,growthofpureculturesofAOBisolatesisusuallyoptimal⩽30°C(JiangandBakken,1999),andoneAOB,Nitrosomonascryoto-lerans,cangrowat4–5°C(Jonesetal.,1988).Theseobservationscorroborateseveralstudiesthatshowedthetemperatureoptimumofsoilnitrificationisoften⩽30°C(MalhiandMcGill,1982;Daliasetal.,2002;Avrahamietal.,2003;Fiereretal.,2003),andsoilnitrificationhasbeenmeasuredattemperaturesaslowas2°C(Cooksonetal.,2002).However,afewreportshavedescribednitrifica-tioninsoilsfromwesternUnitedStatesandAustraliawithtemperatureoptimaof35–40°C(Myers,1975;StarkandFirestone,1996).TheisolationoftheAOANitrososphaeragargensisandNitrosocaldusyellowstoniifromgeothermalsourceswithtemperatureoptimaof46and65–72°C,respectively(delaTorreetal.,2008;Hatzenpichleretal.,2008),andthediscoveryofAOAsoilisolates,NitrosotaleadevanaterraNd1,‘CandidatusNitroso-cosmicusfranklandus’andNitrososphaeraviennen-sis,growingoptimallyat35–40°C(Tournaetal.,Correspondence:AETaylor,DepartmentsofCropandSoilScience,OregonStateUniversity,3017AgLifeScienceBuilding,Corvallis,OR97331,USA.E-mail:[e-mail]11April2016;revised25October2016;accepted4November2016TheISMEJournal(2016),1–13©2016InternationalSocietyforMicrobialEcologyAllrightsreserved1751-7362/16),ledustospeculatethatAOAmightbeprimarilyresponsibleforsoilnitrification⩾30°C.Inafieldstudy,wepreviouslyobservedincreasesofAOAnumbers,andevidenceoftheiractivity,incroppedsoilsunderlatesummer/earlyfallconditionswhensoiltemperaturesreached30–35°C(Tayloretal.,2012),andstudiesfromaUKagriculturalsoilincubatedattemperaturesbetween10and30°Cshowedthatthethaumarch-aealcomposition(determinedbyanalysisoftherelativeabundanceof16SribosomalRNA)shiftedduringincubationat25and30°C,whereastherewasnochangeintheAOBcommunitycomposition(Tournaetal.,2008;Offreetal.,2009).Incontrast,AOAwereenrichedfromArcticsoilsincubatedat20°C,andratesofnitrificationweremeasuredinthreeArcticsoilsincubatedat15°C,whereAOBamoAnumberswerebelowdetection(Alvesetal.,2013).Inpreviousstudies,weshowedthattherelativecontributionsofAOBandAOAtonitrifyingactivityvariedamongfourpairsofnoncroppedandcroppedsoilssampledthroughoutthestateofOregon(Tayloretal.,2013,2015;Giguereetal.,2015).Inthisstudy,theAOAandAOBcontributionstothenitrificationpotential(NP)oftheabove-mentionedsoilswereevaluatedoveratemperaturerangetha