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LowtemperatureMBBRnitrification:MicrobiomeanalysisBradleyYounga,RobertDelatollaa,*,KevinKennedya,EdithLaflammeb,AlainStintzicaDepartmentofCivilEngineering,FacultyofEngineering,UniversityofOttawa,Ottawa,CanadabVeoliaWaterTechnologies,Montreal,Quebec,CanadacOttawaInstituteofSystemsBiology,DepartmentofBiochemistry,MicrobiologyandImmunology,FacultyofMedicine,UniversityofOttawa,Ottawa,CanadaarticleinfoArticlehistory:Received19July2016Receivedinrevisedform27December2016Accepted29December2016Availableonline5January2017Keywords:NitrificationBiofilmMBBRMicrobiomeanalysisNextgenerationsequencingLowtemperatureabstractThisstudyaimstoinvestigatepostcarbonremovalmovingbedbiofilmreactor(MBBR)nitrificationthroughthetransitionfrom20Cto1Candduringthroughlongtermoperationat1C.FourpilotnitrifyingMBBRreactorswereoperatedatvariousammonialoadingratestoelucidatethetemperatureeffectsonammoniaremovalrates,cellviabilityandbacterialcommunities.Thetransitionfrom20Cto1Candduringlongtermoperationat1CweremodeledusingArrheniustemperaturecorrectioncoefficients.Specifically,thesteadystateremovalratesat1Conaveragewere22.8%ofthemaximumammoniaremovalrateat20C,whichcorrespondstoanArrheniustemperaturecorrectionof1.086duringsteadyoperationat1C.ThemicrobialcommunitiesofthenitrifyingMBBRbiofilmwereshowntobesignificantlymorediverseat20Cascomparedto1Coperation.Althoughlessdiverseat1C,2000speciesofbacteriawereidentifiedinthenitrifyingbiofilmduringoperationatthislowtemper-ature.Nitrosomonadswereshowntobethedominantammoniaoxidizingbacteria(AOB)andNitrospirawasshowntobethedominantnitriteoxidizingbacteria(NOB)inallthepilotMBBRreactorsatalltemperatures.TheperformanceofthepostcarbonremovalnitrifyingMBBRsystemswereshowntobeenhancedat1Cbyanincreaseintheviableembeddedbiomassaswellasthickerbiofilm.Thiseffec-tivelyincreasesthenumberofviablecellpresentduringlowtemperatureoperation,whichpartiallycompensatesforthesignificantdecreaseinrateofammoniaremovalpernitrifyingcell.Operationatthehighestloadingconditionstestedinthisstudyat1Cwereshowntoreducetheammoniaremovalratecomparedtolowerloadingconditionsat1C.Thelowerperformanceathigherloadingconditionsat1Cdemonstratedanenrichmentinthestressresponsemetagenomicspathwaysofthesystem.©2017ElsevierLtd.Allrightsreserved.1.IntroductionTheregulatoryframeworkthroughouttheworldisbecomingmorestringentwithrespecttoeffluentammoniadischargefrommunicipalwastewatertreatmentplants.Theseregulationsarechallenginginnorthernclimateregionsduetosignificanttem-peratureeffectsinconventionalbiologicaltreatmentsystems(EEC,1991;CanadaGazette,2012;USEPA,2014).Thistemperatureeffectisexacerbatedinnorthernpassivebiologicalsystemswherethetemperatureofthefinaleffluentofdecreasesto1Candlowerforextendedoperation.Nitrification(biologicaloxidationofammoniatonitratethroughnitrite)isaneconomicalandsustainablemeansoffammoniaremovalasiteliminatestheneedforchemicaladdition.Thisbio-logicalprocess,however,isconventionallysensitivetolowtem-peratureswithnitrificationceasingbelow8C(HurseandConnor,1999;RandallandButh,1984;Shammas,1986).Inanefforttonitrifybelow8Ctherehasbeenanincreasedinterestinbiofilmtechnologiesasadd-onunitsformunicipalwastewatertreatmentplants.Oneofthepremierbiofilmtechnologiesisthemovingbedbiofilmreactor(MBBR),whichwasspecificallydesignedtoenhancethenitrificationprocess(Rustenetal.,1994;Ødegaard,2006).TheMBBRtechnologypromotesbiofilmattachmentandgrowthonengineeredcarriersthataremaintainedinconstantsuspension.TheattachedbiofilmsaremaintainedandprotectedfromabrasionwithothercarriersintheinteriorspacesoftheMBBRcarriers.Toachievenitrificationbelow8C,theMBBRtechnologyhasbeenimplementedatvariouslocationsinpassivetreatmentsys-tems.ImplementingtheMBBRtechnologyafterthefirstlagoonin*Correspondingauthor.DepartmentofCivilEngineering,UniversityofOttawa,Ottawa,ON,161LouisPasteur,K1N6N5,Canada.E-mailaddress:robert.delatolla@uottawa.ca(R.Delatolla).ContentslistsavailableatScienceDirectWaterResearchjournalhomepage:://dx.doi.org/10.1016/j.watres.2016.12.0500043-1354/©2017ElsevierLtd.Allrightsreserved.WaterResearch111(2017)224e233multi-lagoonsystemshasdemonstratedthepotentialforlongtermoperationoflowtemperatureMBBRnitrificationat4C.However,itshouldbenotedthatimplementationofanitrifyingMBBRunitafterthefirstlagoonalsodemonstratedthatnitrificationratesweresignificantlyimpededbyheterotrophicovergrowth(Houwelingetal.,2007;Delatollaetal.,2010).Morerecently,labandfieldscalenitrifyingMBBRsystemshavebeenstudiedafterthelastlagoonofmulti-lagoonsystems.Installationafterthelastlagoon,withoperationatconservativehydraulicandsubstrateloadingrates,hasshownthatnitrifyingMBBRunitsareabletoachievesignificantnitrificationkineticsat1C(Almomanietal.,2014;Hoangetal.,2014).However,recentpilotworkhasindicatedthatlongtermoperationathighammonialoadingratesandelevatedbulkphasetotalammoniaconcentrationscanreducethekineticperformanceoflowtemperaturenitrification(Youngetal.,2016b).Therelationshipbetweennitrifyingkineticsandtemperaturehasbeenadequatelymodeledinpreviousstudiesbetween