<%BANNER%>

UFIR



Drivers of archaeal ammonia-oxidizing communities in soil
CITATION PDF VIEWER
Full Citation
STANDARD VIEW MARC VIEW
Permanent Link: http://ufdc.ufl.edu/IR00001302/00001
 Material Information
Title: Drivers of archaeal ammonia-oxidizing communities in soil
Physical Description: Journal Article
Creator: Zhalnina, Kateryna
Dörr de Quadros, Patrícia
Triplett, Eric W.
Camargo, Flavio A. O.
Publisher: Frontiers (Switzerland)
Place of Publication: Switzerland
Publication Date: June 15, 2012
 Subjects
Subjects / Keywords: ammonia-oxidizing archaea
ammonia monooxygenase
soil
Genre:
Spatial Coverage:
 Notes
Abstract: Soil ammonia-oxidizing archaea (AOA) are highly abundant and play an important role in the nitrogen cycle. In addition, AOA have a significant impact on soil quality. Nitrite pro- duced by AOA and further oxidized to nitrate can cause nitrogen loss from soils, surface and groundwater contamination, and water eutrophication. The AOA discovered to date are classified in the phylum Thaumarchaeota. Only a few archaeal genomes are available in databases. As a result, AOA genes are not well annotated, and it is difficult to mine and identify archaeal genes within metagenomic libraries. Nevertheless, 16S rRNA and comparative analysis of ammonia monooxygenase sequences show that soils can vary greatly in the relative abundance of AOA. In some soils, AOA can comprise more than 10% of the total prokaryotic community. In other soils, AOA comprise less than 0.5% of the community. Many approaches have been used to measure the abundance and diversity of this group including DGGE, T-RFLP, q-PCR, and DNA sequencing. AOA have been studied across different soil types and various ecosystems from the Antarctic dry valleys to the tropical forests of South America to the soils near Mount Everest. Different studies have identified multiple soil factors that trigger the abundance of AOA. These factors include pH, concentration of available ammonia, organic matter content, moisture content, nitrogen content, clay content, as well as other triggers. Land use management appears to have a major effect on the abundance of AOA in soil, which may be the result of nitrogen fertilizer used in agricultural soils. This review summarizes the published results on this topic and suggests future work that will increase our understanding of how soil management and edaphoclimatic factors influence AOA.
Acquisition: Collected for University of Florida's Institutional Repository by the UFIR Self-Submittal tool. Submitted by Kateryna Zhalnina.
Publication Status: Published
Funding: Publication of this article was funded in part by the University of Florida Open-Access Publishing Fund.
 Record Information
Source Institution: University of Florida Institutional Repository
Holding Location: University of Florida
Rights Management: Applicable rights reserved.
System ID: IR00001302:00001

Downloads

This item is only available as the following downloads:

Zhalnina_Frontiers_fmicb-03-00210 ( PDF )


Full Text

PAGE 1

"fmicb-03-00210"2012/6/1321:04pag e1#1 REVIEWARTICLE published:15June2012 doi:10.3389/fmicb.2012.00210 Driversofarchaealammonia-oxidizingcommunitiesinsoil KaterynaZhalnina 1 ,Patr’ciaDšrrdeQuadros 2 ,FlavioA.O.Camargo 2 andEricW.Triplett 1 1 MicrobiologyandCellScienceDepartment,InstituteofFoodandAgriculturalSciences,UniversityofFlorida,Gainesville,FL,USA 2 SoilScienceDepartment,FederalUniversityofRioGrandedoSul,PortoAlegre,Brazil Editedby: RichBoden,UniversityofPlymouth, USA Reviewedby: JenniferF.Biddle,Universityof Delaware,USA J.MichaelBeman,Universityof California,Merced,USA NathanBasiliko,UniversityofToronto, Canada *Correspondence: EricW.Triplett,Departmentof MicrobiologyandCellScience, InstituteofFoodandAgricultural Sciences,UniversityofFlorida, 1052MuseumRoad,Gainesville, FL32611-0700,USA. e-mail:ewt@u.edu Soilammonia-oxidizingarchaea(AOA)arehighlyabundantandplayanimportantrolein thenitrogencycle.Inaddition,AOAhaveasignicantimpactonsoilquality.NitriteproducedbyAOAandfurtheroxidizedtonitratecancausenitrogenlossfromsoils,surface andgroundwatercontamination,andwatereutrophication.TheAOAdiscoveredtodate areclassiedinthephylumThaumarchaeota.Onlyafewarchaealgenomesareavailable indatabases.Asaresult,AOAgenesarenotwellannotated,anditisdifculttomine andidentifyarchaealgeneswithinmetagenomiclibraries.Nevertheless,16SrRNAand comparativeanalysisofammoniamonooxygenasesequencesshowthatsoilscanvary greatlyintherelativeabundanceofAOA.Insomesoils,AOAcancomprisemorethan10% ofthetotalprokaryoticcommunity.Inothersoils,AOAcompriselessthan0.5%ofthe community.Manyapproacheshavebeenusedtomeasuretheabundanceanddiversityof thisgroupincludingDGGE,T-RFLP,q-PCR,andDNAsequencing.AOAhavebeenstudied acrossdifferentsoiltypesandvariousecosystemsfromtheAntarcticdryvalleystothe tropicalforestsofSouthAmericatothesoilsnearMountEverest.Differentstudieshave identiedmultiplesoilfactorsthattriggertheabundanceofAOA.ThesefactorsincludepH, concentrationofavailableammonia,organicmattercontent,moisturecontent,nitrogen content,claycontent,aswellasothertriggers.Landusemanagementappearstohavea majoreffectontheabundanceofAOAinsoil,whichmaybetheresultofnitrogenfertilizer usedinagriculturalsoils.Thisreviewsummarizesthepublishedresultsonthistopicand suggestsfutureworkthatwillincreaseourunderstandingofhowsoilmanagementand edaphoclimaticfactorsinuenceAOA. Keywords:ammonia-oxidizingarchaea,ammoniamonooxygenase,soil DISCOVERYOFTHEAMMONIA-OXIDIZINGARCHAEA,THEIR TAXONOMY,PHYSIOLOGY,ANDMETABOLISM FIRSTDISCOVERIESOFNOVELGROUP Chemolithotrophicnitricationisatwo-stepprocess.Firststep includesoxidationofammoniatonitriteconductedbyammoniaoxidizingbacteria(AOB)andsecondstepisconversionofnitrite tonitratebynitrite-oxidizingbacteria(NOB; Hastingsetal.,2000 ; HermanssonandLindgren,2001 ; KowalchukandStephen,2001 ). Beforethediscoveryoflargenumbersofammonia-oxidizing archaea(AOA)intheenvironment,aerobicammonia-oxidizers werethoughttoberestrictedtoAOBfrom -and -subclasses oftheProteobacteria.Therstpublishedevidencethatarchaea mightbeinvolvedinammoniaoxidationcamefromthediscovery ofarchaealhomologstobacterialammoniamonooxygenasegene ( amoA )inarchaea-associatedscaffoldsfromthewholegenome shotgunsequencingprojectoftheSargassoSea( Venteretal., 2004 ).An insilico comparisontoenvironmentalsequencesfrom publicdatabasesrevealedthatthearchaeal amoA and amoB genes fromthelarge-insertenvironmentalfosmidlibraryofacalcareousgrasslandwerehighlysimilartoarchaea-associatedscaffolds fromtheSargassoSea( Treuschetal.,2005 ).Thisinsertalsocontaineda16SrRNAgenethatprovedthattheorganismfrom whichthis amoA homologoriginatedwasamesophilicCrenarchaeota.Atthesametime, Kšnnekeetal.(2005) isolatedamarine crenarchaeote(SCM1)thatgrowschemolithoautotrophicallyby aerobicallyoxidizingammoniatonitrite. Wuchteretal.(2006) enrichedacrenarchaeotefromNorthSeawaterandshowedthatits abundance,butnottheabundanceofAOB,correlateswithammoniumoxidationtonitrite.Thesamestudyalsofoundthatarchaeal amoA copynumberswerehigherthanbacterial amoA .Sincethe earlyworkonCrenarchaeota,multiplestudieshaveobserveda predominanceofAOAoverAOBinmultipleenvironments,particularlyinsoil( Leiningeretal.,2006 ; Nicoletal.,2008 ; Schauss etal.,2009 ; Zhangetal.,2010 ). CLASSIFICATION:THAUMARCHAEOTAORCRENARCHAEOTA? Initially,AOAwereclassiedasmesophilicCrenarchaeota ( Treuschetal.,2005 ). Brochier-Armanetetal.(2008) proposed thatthearchaealammoniaoxidizersweresufcientlydistinctto beseparatedfromtheCrenarchaeotaintoanewphylum,Thaumarchaeota.Thisdistinctionwasbasedonphylogeneticanalysis ofribosomalproteinencodinggenesandsomeprotein-coding genes.ComparativephylogeneticanalysisofmarineandsoilAOA revealedsixconservedsignatureindelsandmorethan250proteinsuniqueonlytotheThaumarchaeota( Spangetal.,2010 ). Also, Pelveetal.(2011) foundthattheCdvsystem,relatedto theeukaryoticESCRT-IIImachinery,istheprimarycelldivision systeminthethaumarchaeon Nitrosopumilusmaritimus andthat theFtsZproteinperformsafunctioninarchaeaotherthancell division. www.frontiersin.org June2012 | Volume3 | Article210 | 1

PAGE 2

"fmicb-03-00210"2012/6/1321:04pag e2#2 Zhalninaetal. DriversofAOAinsoils ECOPHYSIOLOGY Ammonia-oxidizingarchaeaandAOBoxidizeammoniabyusing ammoniamonooxygenase(AMO)enzyme.Althoughnitriteis thenalproductforbotharchaealandbacterialammoniaoxidation,bigdifferencesexistbetweentheAOAandAOBammonia oxidationprocesses.First,theintermediateproductofbacterial ammoniaoxidationtonitriteishydroxylamine( Kowalchukand Stephen,2001 ).Theintermediateproductofarchaealammoniaoxidationisnotasclear,butnitroxylhasbeenproposedas theintermediate( Walkeretal.,2010 ).Second,thestructureof AMOdiffersbetweenbacteriaandarchaea( Kšnnekeetal.,2005 ; Walkeretal.,2010 ).Third,archaealAMOhasahigherafnityforsubstratethandoesbacterialAMO( Martens-Habbena etal.,2009 ; Martens-HabbenaandStahl,2011 ).Fourth,while AOBareobligateautotrophs,AOAcanalsouseorganiccarbon ( Hallametal.,2006 ; Walkeretal.,2010 ; Blaineyetal.,2011 ; Tourna etal.,2011 ).DifferenceslistedabovebetweenAOAandAOB ledtotheideaofexistenceofdifferentphysiologicalapproaches inutilizingofavailablenutrientresourcesbetweenthesetwo groups. DIFFICULTIESINSTUDYINGAOA:CULTIVATION,LACKOF REFERENCEGENOMES Todate,onlyeightAOAspecieshavebeendescribedfrommarine, soil,sediment,andhotspringenvironments( Table1 ).Two ofthemwereisolatedinpurecultures,andvespeciescan growinenrichedculturesbutwerenotisolatedinpurecultures.OnlysixwholegenomesofAOAareavailableinthe databases.AstheAOAhavebeenfoundunderawidevarietyof conditionsincludingvariedtemperature,pH,ammoniaconcentrations,andoxygensupply,designingmediafortheircultivation hasbeendifcult.ThelackofavarietyofculturedAOAand AOAgenomeshaslimitedthestudyoftheirphysiologyand metabolism. ECOLOGICALROLEOFAOAANDWHYSTUDYTHEM? First,AOAarelikelyinvolvedinnitrateleachingfromsoils,which causessurfaceandgroundwatercontamination.Nitrogenlosscan occuratmanypointsduringthenitricationprocess( Kowalchuk andStephen,2001 ).Thenitrateproducedduringnitrication canleadtotheeliminationofxednitrogenfromanenvironmentalsystem.Nitrateleachingfromsoilisanotherimportant routeofnitrogenlossfromecosystems.Cationicammonium (NH 4 + )moleculesaremorestableinsoilthroughbindingto anionicsoilparticles,butnitrate(NO 3 )hasmoremobilityinsoil andcaneasilyleachfromthesoilsurfacetogroundwatercausing contamination( KowalchukandStephen,2001 ). Second,AOAactivitymaybeasignicantsourceofgreenhousegasemissionsfromthesoil.Recently,itwasfoundthat nitrousoxide(N 2 O)isthedominantozone-depletingsubstance emittedinthe21stcentury( Ravishankaraetal.,2011 ).Nitrous oxideistransportedtothestratospherewhereitdestroysozone throughanitrogenoxide-catalyzedprocess.Nitrousoxidehas 298timeshigherglobalwarmingpotentialthancarbondioxide (CO 2 ; vanGroenigenetal.,2011 ).Autotrophicnitricationisa mainpathwayofnitrousoxideproductioninsoilenvironments ( ColliverandStephenson,2000 ; KowalchukandStephen,2001 ; Shawetal.,2006 ). Santoroetal.(2011) suggestedthatAOAmay belargelyresponsibleforthenitrousoxideproductioninmarine environments.AsAOAoutnumberAOBinsoil,itispossiblethat archaeamaybethemajorsourceofsoilnitrousoxideemission. Jungetal.(2011) observedthatproductionofnitrousoxidebythe Table1 | Ammonia-oxidizingarchaeaisolatedfromdifferentenvironments. # AOAEnvironmentSourceofisolationClassi-CultureGenomeReferenceCountry cationsequence 1 Nitrosopumilus MarineGravelfromamarine1.1aPure + Kšnnekeetal.(2005) ,USA maritimus tropicalshtank Walkeretal.(2010) 2 Cenarchaeum MarinesymbiontMarinesponge1.1a + Prestonetal.(1996) ,USA symbiosumAxinellamexicana Hallametal.(2006) 3 Ca.Nitrososphaera Soil,hotspringsEnrichmentculturesfrom1.1bEnriched + Hatzenpichleretal.(2008) Austria gargensis microbialmatsofthe SiberianGargahotspring 4 Nitrososphaera SoilGardensoilinVienna,Austria1.1bPure + Tournaetal.(2011) Austria viennensis 5 Ca.Nitrosoarchaeum RhizosphereSoilsamplefromtherhizosphere1.1aEnriched + Kimetal.(2011) ,Republic koreensis of Caraganasinica Jungetal.(2011) ofKorea 6 Ca.Nitrosoarchaeum SedimentsSedimentsinthelow-salinity1.1aEnriched + Blaineyetal.(2011) USA limina regionofSanFranciscoBay 7 Ca.Nitrosocaldus HotspringsYellowstoneNationalPark,ThAOAEnriched delaTorreetal.(2008) USA yellowstonii hotsprings 8 Ca.Nitrosotalea SoilAcidicagriculturalsoil1.1a-Enriched Lehtovirta-Morleyetal. UK devanaterra associated( 2011 ) FrontiersinMicrobiology | TerrestrialMicrobiology June2012 | Volume3 | Article210 | 2

PAGE 3

"fmicb-03-00210"2012/6/1321:04pag e3#3 Zhalninaetal. DriversofAOAinsoils soilarchaeon Ca.Nitrosoarchaeumkoreensis andratesofnitrous oxideproductionaredependentonsoilammoniaanddissolved oxygen(DO)concentration.Todate,themechanismofnitrous oxideproductionbyarchaeaisunclear. Possibleconsequencesofautotrophicnitricationarecontaminationofsurfaceandgroundwater,lossofsoilfertility,emissionof greenhousegases,andchemicaldegradationofagriculturallands ( Oldemanetal.,1991 ; KowalchukandStephen,2001 ; Ghoshand Dhyani,2005 ; Santoroetal.,2011 ).AOAarefrequentlydominant ammoniaoxidizersinsoils( Leiningeretal.,2006 ),and,therefore,theiractivitycouldleadtotheseconsequences.Studying theabundanceandcompositionofarchaealammoniaoxidizersandunderstandinghowsoilpropertiesinuencethisgroup haslong-lastingimplicationsforsustainableagricultureandit attractstheattentionofmanyresearchgroupsfromaround theworld. EDAPHOCLIMATICFACTORSTHATMAYINFLUENCEAOA ABUNDANCEANDDIVERSITY Mainenvironmentalfactorsthatshapetheecologicalnichesof AOAfromtheocean,hotsprings,soils,andsedimentswere discussedinthereviewpaperby Erguderetal.(2009) .Recent advancesinecology,genetics,physiology,andculturinghappenedintheeldofAOA,suchassequencingofrstgenome ofnon-symbioticmarineAOA( Walkeretal.,2010 ),obtaining purecultures,andhighenrichmentsof Nitrososphaeraviennensis ( Tournaetal.,2011 ), Ca.Nitrosoarchaeumkoreensis Ca.Nitrosoarchaeumlimina Ca.Nitrosotaleadevanaterra andsequencingof theirgenome;discoveryofAOAecotypesinsoilsbasedondifferentpHlevels( Gubry-Ranginetal.,2011 )andanotherevidences oforganiccarbonutilizationprovidedmoreinformationabout physiologyandmetabolismofthisgroup. AMMONIAORAMMONIUMASSUBSTRATEFORAMMONIA MONOOXYGENASE Isammonia(NH 3 )orthecationammonium(NH 4 + )thesubstrateforthearchaealAMOenzyme?Ammoniaisknowntobe thesubstrateofthisinitialstepinbacterialammoniaoxidation ( Suzukietal.,1974 ; Arpetal.,2002 ).However,despiteseveral studiesdedicatedtostudyingthebiochemistryofAMOinbacteria, itstillremainsunknownwhetherammoniaorammoniumisthe substrateforarchaealAMO( Martens-HabbenaandStahl,2011 ). Bacterialoxidationofammoniatonitrite(NO 2 )isatwo-step process.AMOoxidizesammoniatohydroxylamine(NH 2 OH), andhydroxylamineoxidoreductase(HAO)catalyzesoxidationof hydroxylaminetonitrite( Arpetal.,2002 ).Structuraldifferences inthearchaealAMOandbacterialAMOandtheabsenceof genesencodingHAOandcytochrome c proteinsforrecyclingelectronssuggestimportantdifferencesbetweenbacterialandarchaeal ammoniaoxidation.Forexample,nitroxyl(HNO)ratherthan hydroxylaminemaybetheintermediateintheAMOenzymatic reaction,oradifferentcytochromesystemmayberesponsiblefor electronchannelinginAOA( Walkeretal.,2010 ). ThemajorityofAOAdiscoveredtodatewerefoundinoligotrophicconditions( Hatzenpichleretal.,2008 ; Walkeretal., 2010 ).Theafnityofmarinearchaeon Nitrosopumilusmaritimus forammonium/ammoniawas200-foldhigherthansubstrate afnityofAOB( Martens-Habbenaetal.,2009 ; Martens-Habbena andStahl,2011 ).Thesemicroorganismscanobtainenergyeven underverylowconcentrationsofsubstrate.Ithasbeensuggested thatthedifferencesinsubstrateafnitiesallowAOAandAOB toinhabitdistinctnichesseparatedbysubstrateconcentration andtherebyreducecompetition( Martens-Habbenaetal.,2009 ; Schleper,2010 ; Martens-HabbenaandStahl,2011 ; Verhamme etal.,2011 ).Therearestudiesthatsuggestsubstrateinhibition ofarchaealnitricationifhighconcentrationsofammoniaare present( Dietal.,2010 ; Tournaetal.,2010 ). BecauseAMOinAOAhasamuchhigherafnityforsubstratethantheanalogousprocessinAOB,ithasbeensuggested thatAOAdominateoverAOBwhereammoniaconcentrationsare particularlylow.Thisseemstobethecaseinoligotrophicenvironmentssuchasseawaterorhotsprings( Hatzenpichleretal., 2008 ; Walkeretal.,2010 ).Forexample, Ca.Nitrososphaeragargensis ,whichwasrstfoundinhotsprings,xesbicarbonateat lowerlevelswhentheammoniaconcentrationwashigherthan 3.1mM.Theoptimalammoniaconcentrationforbicarbonate xationwasmuchlower,between0.14and0.8mM( Hatzenpichleretal.,2008 ).Somestudiessuggestthatsubstrateconcentration doesnotinuencethaumarchaealammoniaoxidation( Stopnisek etal.,2010 ; Verhammeetal.,2011 ).Theseauthorsshowedthat AOAgrewsimilarlyatlow,medium,andhighammoniaconcentrations,whereasAOBgrewbestonlywithhighammonia concentrations.Otherfactorsweresuggestedtobeimportantin thegrowthofAOA. Dietal.(2009) observedinnitrogen-rich grasslandsoilsneitherAOAabundancenortheiractivityincreased withtheapplicationofalargedoseofammoniasubstrate.Inthis study,AOAabundancewasnotquantitativelyrelatedtonitricationrates.Similarly, KeandLu(2012) didnotseeanychanges inAOAinpaddyeldsoilsafterureawasappliedasnitrogen fertilizer. Insomestudies,highammoniaappearstopromoteAOA growthandactivity. Treuschetal.(2005) foundconsiderably higheramountsofarchaeal amoA transcriptsinthosesamples thathadbeenamendedwithadditionalammonia(10mM). Itwasdemonstratedthatthesoilarchaea Nitrososphaeraviennensis strainEN76growswellinmediacontainingammonium concentrationsashighas15mM,butitsgrowthisinhibited at20mM( Tournaetal.,2011 ).Thisisconsiderablyhigher thantheinhibitoryconcentrationof23mMreportedforthe aquaticAOA Nitrosopumilusmaritimus ( Walkeretal.,2010 )and Ca.Nitrososphaeragargensis ( Hatzenpichleretal.,2008 ).Toleranceforammoniatoxicityof Ca.Nitrosoarchaeumkoreensis strain MY1,isolatedfromanacidicagriculturalsoil,wasslightlylower, 5mM,thanthatof Nitrososphaeraviennensis ( Jungetal.,2011 ). Parketal.(2006) foundarchaeal amoA inwastewaterwith2mM ammonia. Thesourceofsubstrateanditslocationcaninuenceammonia concentrationinsoil( Offreetal.,2009 ; Stopniseketal.,2010 ; Verhammeetal.,2011 ).Ammoniumproductionviamineralization, additionsofammonicalfertilizers,animalwastes,andtheatmosphericdepositionofammoniumincreasessubstratesupply,while competingconsumptiveprocessesincludemicrobialassimilation (immobilization),plantassimilation,andammoniavolatilizationreduceammoniaconcentration( NortonandStark,2011 ). www.frontiersin.org June2012 | Volume3 | Article210 | 3

PAGE 4

"fmicb-03-00210"2012/6/1321:04pag e4#4 Zhalninaetal. DriversofAOAinsoils Inaddition,AOAdonotrespondtotheadditionofmineral nitrogentosoil( Dietal.,2009 ; JiaandConrad,2009 ; Stopnisek etal.,2010 ; Verhammeetal.,2011 ; KeandLu,2012 ).Incontrast, AOBincreaseinabundanceafteradditionofammoniumsulfate orurine( Dietal.,2009 2010 ; JiaandConrad,2009 ; Hofferle etal.,2010 ).Archaeal amoA genecopiesandnitrateconcentrationincreasedduringincubationsoilfor30days( Offreetal., 2009 ).Allammoniainthissoilwasgeneratedbynitrogenmineralizationsincenoammoniawasadded.Also,itwasshown inuplandeldsoilsarchaeal16SrRNAgenewassignicantly affectedbytheclassoffertilizer(chemicalororganicfertilizer).In fourdifferentsoiltypes16SrRNAabundanceofAOAwasabout 0.10.9 10 8 genecopynumberhigherintheplotswhereorganic fertilizerswereaddedthanintheplotswithchemicalfertilizer addition. Nitrateconcentrationslikelydiffergreatlybothspatiallyand temporallyunderthesetwoscenarios( Stopniseketal.,2010 ). Whileammoniafromorganicmattermineralizationisslowlyand constantlyliberatedresultinginlow,butsteady,levelsofammonia,anapplicationofmineralnitrogenfertilizerpromotesaburst ofammonia.Archaealammoniaoxidizersshouldbeexpectedto beinahigherabundanceinthesoilswithhighorganicmatter, whichwouldprovideaconstantsourceofsubstrate( Stopnisek etal.,2010 ). Adaptationtodifferentconcentrationsofammoniaandthe abilitytosurviveevenatextremelylowconcentrationsofammonia,togetherwithotherecologicalfactors,contributetothe ecologicaltnessandnicheadaptationofAOAandAOB.The presenceofdifferentecophysiologicaladaptationssuchasdifferent concentrationsofsubstratesuggeststhatawiderangeofecotypes canbeexpectedtooccuramongsoilAOA. DIFFERENTLINEAGESOFAOARESIDEATDIFFERENTpHLEVELS Ammonia(NH 3 ),notammonium(NH 4 + ),isthelikelysubstrate fortheAMOthatcatalyzestheinitialstepoftheoxidationof ammonia( Arpetal.,2002 ).TheammoniaformispHdependent (pKa = 9.25,25 # C)andconversionsbetweenionicandcationic formsmayoccurclosetooratthecellmembrane( Nortonand Stark,2011 ). Ammonia-oxidizingarchaeaaremoretoleranttolowpHthan AOB,andAOAaremainlyresponsiblefornitricationinacidic soils( Leiningeretal.,2006 ; Gubry-Ranginetal.,2010 ; Yaoetal., 2011 ; Zhangetal.,2011 ; Isobeetal.,2012 ).Archaeal amoA was foundinconditionsaslowaspH2.5interrestrialhotsprings ( Reigstadetal.,2008 ),ashighaspH8.2inNorthSeawater andsediments( Wuchteretal.,2006 ; Blaineyetal.,2011 ),and atpH9atEaglevillespringinCalifornia( Zhangetal.,2008 ), wheretheyweretheonlyrepresentativesofammoniaoxidizers. ThelowestpHlevelsofsoilinwhichAOAhavebeenfoundare 3.64.0( Heetal.,2007 ; Yaoetal.,2011 ). Nicoletal.(2008) reportedthatarchaeal amoA geneandtranscriptabundance decreasedwithhigherpHduringasoilmicrocosmexperiment. Furtherstudyrevealedanincreaseinarchaeal amoA geneandtranscriptabundanceduringnitricationandinhibitionofarchaeal amoA ,butnotbacterial amoA ,byacetyleneadditionintwoagriculturalacidicsoils( Gubry-Ranginetal.,2010 ).Quantication of1.1ccrenarchaeal16SrRNAgeneabundancethroughapH gradientfrom4.5to7.5showedagreaterproportionofthis groupinthemostacidicsoils( Lehtovirtaetal.,2009 ). Yaoetal. (2011) studiednitricationinteaorchardsoilswithlowpH(3.6 6.3)andfoundthatthehighlevelofnitricationwasdrivenby AOAbutnotAOB.Inaddition,AOAphylotypesfoundinhighly acidicsoils(pH < 4)werenegativelycorrelatedwithpH,and AOAfromsoilswithahigherpH( > 4)showedapositivecorrelationwithpH( Yaoetal.,2011 ). Zhangetal.(2011) found archaeainvestronglyacidicsoils(betweenpH4.2and4.47) wherearchaeal amoA geneabundancewasstronglycorrelated withnitrateconcentration.Recently Ca.Nitrosotaleadevanaterra therstobligateacidophilicammoniaoxidizer,wasdiscovered andculturedfromanagriculturalacidicsoil(pH4.5; LehtovirtaMorleyetal.,2011 ).Thisarchaeonisabletogrowatextremely lowconcentrationsofammonia(0.18nM)suggestingthatthis organismhasevolvedtotoleratetheacidicconditionsthatmake ammoniaconcentrationsverylow.AsAOBhavealowerafnity forammonia,thelowavailabilityofammoniaunderacidicconditionsisbelievedtobethemainreasonfordecreasingofammonia oxidationbyAOBinacidicsoils( deBoerandKowalchuk,2001 ). Incontrast,thehighafnityforammoniaallowscertainecotypesofAOAtogrowunderlowconcentrationsofammonia ( Nicoletal.,2008 ; Martens-Habbenaetal.,2009 ; Gubry-Rangin etal.,2010 ). Ammonia-oxidizingarchaeaalsoappeardominantunderalkalineconditionsaswellasacidicconditionsandareoftenmore abundantthanAOBathigherpH( Shenetal.,2008 ; Zhangetal., 2010 ; Batesetal.,2011 ). Shenetal.(2008) didnotobserveasignicantcorrelationbetweenAOAandpHinthealkalinesoils (pH8.38.7),butthenumberofarchaeal amoA genesdidnot declinewithincreasingpH.InCambisolsoils(pH66.5),AOA werepositivelycorrelatedwithpH( WessŽnetal.,2010 ). Nitricationinalkalinesoils(pH7.5)byAOAwasdemonstratedby Zhangetal.(2010) .Afterincubationofsoilwithcarbon dioxide,archaealbutnotbacterialDNAwasdetected,andthe numberofarchaeal amoA outnumberedbacterial amoA Bates etal.(2011) studiedchangesinbacterialandarchaealcommunitiesin146soilsacrosstheglobeandfoundapositivecorrelation betweenAOAwithsoilpH,especiallyinforestsandshrublands. Bruetal.(2011) investigatedthedistributionofAOAcommunitiesover107sitesinBurgundy,France,withpHrangingfrom 4.2to8.3andfoundthatinacidicsoilsAOAwerebelowthe detectionlevelandAOAabundancepositivelycorrelatedwith soilpH. DifferentAOAecotypeshaveevolvedtogrowthatdifferent pHlevels.Theexistenceofdifferentenvironmentallineageswas suggestedby Nicoletal.(2008) andsupportedby Gubry-Rangin etal.(2011) Gubry-Ranginetal.(2011) clusteredarchaeal amoA sequencesfromgloballydistributedsoilsthatvariedwidelyin pH.Theyfoundthatallstudiedphylogeneticlineageswereclassiedasacidophilic(lineag eCincludingGroup1.1a-associated), acido-neutrophilic(linageAincludingGroup1.1a),andalkalinophilic(linageBincludingGroup1.1b).Theselineagesvary intheirresponsetopHbutoverall,archaeal amoA abundance increasedwithincreasingpH.pHappearstobeastrongfactorinmanystudies,butAOAaresuccessfulacrossarangeof pHvalues. FrontiersinMicrobiology | TerrestrialMicrobiology June2012 | Volume3 | Article210 | 4

PAGE 5

"fmicb-03-00210"2012/6/1321:04pag e5#5 Zhalninaetal. DriversofAOAinsoils CARBON AreAOAautotrophic,heterotrophic,ormixotrophicwith regardtocarbonutilization?Componentsofthemodied 3-hydroxypropionate/4-hydroxybutyratecycleofautotrophiccarbonassimilationwereidentiedingenomesof Cenarchaeumsymbiosum ( Hallametal.,2006 ), Nitrosopumilusmaritimus ( Walker etal.,2010 ), Ca.Nitrosotaleadevanaterra ( Lehtovirta-Morley etal.,2011 ),and Ca.Nitrosoarchaeumlimnia ( Blaineyetal., 2011 ). Ca.Nitrososphaeragargensis ( Hatzenpichleretal.,2008 ) and Nitrososphaeraviennensis canusecarbondioxideassolecarbonsource( Tournaetal.,2011 ). Zhangetal.(2010) provided directevidencesforautotrophicactivityandautotrophicgrowth ofThaumarchaeotainsoil.Nitricationratesinthisstudycorrelatedwithincreasedarchaeal,butnotbacterial, amoA and hcd (keygenein3-hydroxypropionate/4-hydroxybutyratecycle)genes' abundances.Also,stableisotopeprobingshowedincorporation of 13 C-labeledcarbondioxideintoarchaeal amoA duringnitricationbutnotintobacterial amoA .Inaddition,mRNA-SIP supportedautotrophiccarbondioxidexationbyAOAusingthe 3-hydroxypropionate/4-hydroxybutyratecycleinanagricultural soil( Pratscheretal.,2011 ). LaterevidencebuildsthecasethatsomeAOAtakeuporganic carboncompounds,butothersmaybeinhibitedbyorganics.The rstndingoftheuptakeofaminoacidsbyplanktonicarchaea wasshownby OuverneyandFuhrman(2000) Herndletal.(2005) and Teiraetal.(2004) indicatedtheuptakeofaminoacidsby isotopicstudiesofmicrobialcommunitiesintheAtlanticOcean andspeculatedthatthiscouldbeanindicationoftheutilization ofthedissolvedorganicmatterasanenergysource. RecentsequencingofAOAgenomesandtheculturingofAOA havesupportedmixotrophybytheseorganisms.Oxidativeand reductivetricarboxylicacidcycle(TCA)geneswerefoundin thegenome Cenarchaeumsymbiosum ( Hallametal.,2006 ).In additiontothegenesthatcodeforthe3-hydroxypropionate/ 4-hydroxybutyratepathway,the Nitrosopumilusmaritimus genomecontainsgenesencodingforthecompleteoxidativeTCA cycle( Walkeretal.,2010 )aswellastransportersforamino acids,dipeptides/oligopeptides,sulfonates/taurine,andglycerol. Putativeorganiccarbonconsumptionwassuggestedbasedon genomesequenceof Ca.Nitrosoarchaeumlimnia ( Blaineyetal., 2011 ).Increasedgrowthof Nitrososphaeraviennensis culturesby smalladditionsofpyruvate( Tournaetal.,2011 )alsosupports mixotrophicgrowthbyAOA. Chenetal.(2008) reportedahigherabundanceofAOAinthe paddyrhizospherecomparedtonon-rhizospheresoil,presumably duetoorganiccarbonofrootexudates.Increasedabundanceof 1.1bAOAcladeoccurredupontheadditionofrootextractas anorganicamendmenttotheAOAenrichmentculture( Xuetal., 2012 ).Nevertheless,organicsubstrateshavebeenshowntoinhibit AOAorbenegativelycorrelatedwithAOAabundance( Kšnneke etal.,2005 ; WessŽnetal.,2010 ; Batesetal.,2011 ). Pesteretal. (2012) alsorevealednegativecorrelationofAOAspeciesrichnesstotheorganiccarboncontentinfourgeographicallyand chemicallydistinctsoils.Although,ge neticcapacitytopotentially useorganiccarbonandsomecasesofsmallorganicmolecules uptakebyAOAwerefoundbyrecentstudies,thereisstilllackof understandinghowexactlyAOAuseorganiccarbon. TEMPERATURE Temperatureisoneofthemostsignicantfactorsthataffectsoil organicmatterdecomposition,nitrication,andgreenhousegas productioninterrestrialenvironments( Kirschbaum,1995 ; Stark andFirestone,1996 ).Althoughoptimaltemperaturesforpotential nitricationareusuallybetween20and37 # C,theAOAproduce nitriteattemperaturesthatvaryfrom 1 # CinArcticcoastalwaters to97 # CinhotspringsofIceland( Reigstadetal.,2008 ; Kalanetra etal.,2009 ). Archaeal amoA wasdetectedinnear-freezingArcticandAntarcticwaterswith4.92 10 6 and0.18 10 6 copies,respectively ( Kalanetraetal.,2009 ). Christmanetal.(2011) analyzeddistributionofAOAduringsummer(T = 5.1 # C)andwinter(T = 1.7 # C) intheCoastalArcticOceanandfoundthatAOA amoA levelsand nitricationrateswerehigherinwinter. ThemajorityofAOAidentiedinsoilandmarineenvironmentsarenon-thermophilicandaretypicallyfoundattemperaturesfrom22to37 # C( Kšnnekeetal.,2005 ; Hallametal., 2006 ; Mulleretal.,2010 ; Blaineyetal.,2011 ; Jungetal.,2011 ; Kimetal.,2011 ; Lehtovirta-Morleyetal.,2011 ; Tournaetal., 2011 ).ThethermophilicAOAdetectedindeep-seahydrothermalventsandhotspringsperformnitricationattemperatures of4597 # C( delaTorreetal.,2008 ; Hatzenpichleretal.,2008 ; Reigstadetal.,2008 ; Wangetal.,2009 ; Zhangetal.,2011 ). Amoderatelythermophilic(46 # C)archaeon, Ca.Nitrososphaera gargensis ,discoveredinmicrobialmatsoftheSiberianGargahot springwasthedominantammoniaoxidizerinterrestrialnonthermophilicenvironments.Archaealadaptationstofunction underelevatedtemperatureswasdemonstratedwhendifferent temperaturesforfermentingcattlemanurecompostrevealed growthofAOBat37 # C,whereasAOAcontinuetogrowupto60 # C ( Oishietal.,2011 ). TheimpactofdifferenttemperaturesonAOApopulations wasexaminedineldandmicrocosmexperiments. Tournaetal. (2008) studiedtheresponsesofAOAandAOBduringincubationofsoilmicrocosmsattemperaturesintherange1030 # C. Theydeterminedthatthemostprofoundchangesinpatternsof archaeal amoA genetranscriptabundanceoccurredat30 # C. Stres etal.(2008) foundthatsoilarchaeal,butnotbacterial,communitystructurechangedduringincubationathighertemperatures. Aglobalsurveyofdifferentsoilsshowedapositivecorrelation betweenrelativearchaealabundanceandannualtemperatures, andtemperaturebecameevenmoresignicantfactorforthe relativeabundanceofarchaeafromforestsandshrublands( Bates etal.,2011 ). MOISTURE Soilmoistureandtemperatureimpactsonmainprocessesofnitrogencycle,suchasorganicmattermineralization,nitricandnitrous oxideproduction,nitrogenxing,andparticularly,nitrication ( Kirschbaum,1995 ; Zhengetal.,2000 ; Belnap,2001 ; Nortonand Stark,2011 ).Soilmoisturepromotedchangesinthearchaealcommunityingrasslandsoilmicrocosm( Stresetal.,2008 ). Batesetal. (2011) observedanegativecorrelationofsoilmoistureintallgrass prairieswithAOAabundance.Diversityofsoilmicrobialcommunitiesalongasteepprecipitationgradientrangingfromanarid areawithlessthan100mmannualraintoameso-Mediterranean www.frontiersin.org June2012 | Volume3 | Article210 | 5

PAGE 6

"fmicb-03-00210"2012/6/1321:04pag e6#6 Zhalninaetal. DriversofAOAinsoils forestreceivingover900mmprecipitationwasstudied.Ofmeasuredphysicochemicalfactors,watercontentwasfoundtohavethe strongestcorrelationwiththebacterialandarchaealcommunity structuresinstudiedsoils( Angeletal.,2010 ). Studyofnitrogenandwateramendmentintwotemperate forestsoilsrevealedthattheAOAcommunitycompositionwas sensitivetomoisturecontentinoneofthesoilsandarchaeal amoA genesweremoreabundantat40%than70%water-lled porespacesuggestingreducedoxygenlevelsloweredAOAgrowth ( Szukicsetal.,2012 ). OXYGENANDOTHERFACTORS Oxygenplaysanimportantroleinnitricationasasubstratefor theAMOenzymeandasterminalelectronacceptor( Arpetal., 2002 ).Insoil,oxygenlevelsarebalancedbyoxygenconsumption anddiffusionfromthesurfacethroughtheair-lledpores( Sexstoneetal.,1985 ).Nitricationusuallydeclinesinsoilifwater levelshaveexceededeldcapacityforseveraldays( Schjonning etal.,2003 )therebydecreasingoxygencontent.Tolerancetolow concentrationsofDOwasdemonstratedinactivatedsludgebioreactorswithlowDO( < 6.3 M; Parketal.,2006 ).Insubterranean estuariesatlow-oxygenfreshandbrackishstations,AOAwere 10timesmoreabundantthanAOB( Santoroetal.,2011 ). Bouskill etal.(2012) examinedthedistributionAOAacrosslarge-scalegradientsinDOasoneoftheimportantfactorsofAOAdistribution inmarineenvironments.ThehighestabundanceoftheAOA amoA genewasrecordedintheoxygenminimumzones(OMZs)ofthe EasternTropicalSouthPacic(ETSP)andtheArabianSea(AS). AOAintheASexhibitedaverynarrowrangeofpreferredoxygenconditions(52.5 M; Pitcheretal.,2011 ).Stoichiometry andkineticofammoniumoxidationby Nitrosopumilusmaritimus showedtheendogenousoxygenuptakeofthecellswasconsistentlybelow0.5 Mperhour,butafteradditionofammonium tothecells,oxygenuptakeincreasedwithinafewminutesupto 30 Mh 1 andremainedhighuntiltheammoniumleveldeclined below1 M( Martens-HabbenaandStahl,2011 ).AOAandAOB areadaptedtolifeinlow-oxygenorperiodicallyanoxichabitatsin paddysoils.Althoughoodingpaddysoilispredominantlyanaerobic,largenumbersofAOAweredetected(8.31 10 7 2.12 10 8 copiespergramdrysoil).Moreover,AOAreactedfastertothe presenceofoxygeninuctuatingoxicandanoxicrhizosphere ofriceplantscomparedtoAOB( Chenetal.,2008 ).Enrichment cultureof Ca.Nitrososphaeragargensis wasgrownaerobicallyat DOconcentrations0.151.18mM.Kineticrespirometryassays showedthat Ca.Nitrosoarchaeumkoreensis strainMY1'safnitiesforoxygen(1.08 M)weremuchhigherthanthoseofAOB ( Jungetal.,2011 ). Amongthefactorslistedabovetherearemanyotherfactors thatwereshowntohavesomeimpactonAOAcommunity.These includealtitude( Zhangetal.,2009 ),soiltypes( Hoshinoetal., 2011 ; Morimotoetal.,2011 ),sulde( Caffreyetal.,2007 ; Coolen etal.,2007 ),phosphate( Herfortetal.,2007 ),andsalinity( Bernhardetal.,2010 ).However,thesefactorseitherdonothavea signicantimpactonarchaealammoniaoxidationorhavenot beenfoundtoinuencesoilAOA. CONCLUDINGREMARKS TheAOAareaversatile,ubiquitous,andabundantgroupof microorganismsthathaveadaptedtosurviveinawidevariety ofharshenvironments.Moreover,theirimportantfunctionin thenitrogencycle,andtheirrolesinnitrateleaching,greenhousegasproduction,andsoilsubsidencemaketheAOAa groupthatdeservesfurtherstudies.Knowingthemaindrivers ofAOAabundanceanddistributioninsoilisofgrowinginterestaroundtheworld.Therearemanystudiesthatassessmarine environmentalAOAcommunities,butmuchlessisknownabout soilAOA.Soilfeaturesthathavemajorinuenceonshaping AOAcommunitiesincludeammoniaconcentration,pH,organic matter,moisture,temperature,andoxygen.AOApossesshigh afnitiesforammoniaandoxygenandcantolerateextremes oftemperatureandpH.ThesefeaturesexplainwhytheAOA greatlyoutnumbertheAOBinmanysoilsandotherenvironments,astheycaninhabitpotentialnichesthatarenotavailableto theAOB. ACKNOWLEDGMENT PublicationofthisarticlewasfundedinpartbytheUniversityof FloridaOpen-AccessPublishingFund. REFERENCES Angel,R.,Soares,M.I.,Ungar,E.D., andGillor,O.(2010).Biogeography ofsoilarchaeaandbacteriaalonga steepprecipitationgradient. ISMEJ 4,553563. Arp,D.J.,Sayavedra-Soto,L.A.,and Hommes,N.G.(2002).Molecularbiologyandbiochemistryof ammoniaoxidationby Nitrosomonas europaea.Arch.Microbiol. 178, 250255. Bates,S.T.,Berg-Lyons,D.,Caporaso,J.G.,Walters,W.A.,Knight, R.,andFierer,N.(2011).Examining theglobaldistributionofdominant archaealpopulationsinsoil. ISMEJ. 5,908917. Belnap,J.(2001)."Factorsinuencing nitrogenxationandnitrogenrelease inbiologicalsoilcrusts,"in BiologicalSoilCrusts:Structure,Function, andManagement EcologicalStudies Vol.150,edsJ.BelnapandO. L.Lange(SpringerVerlag:Berlin), 241261. Bernhard,A.E.,Landry,Z.C.,Blevins, A.,delaTorre,J.R.,Giblin,A. E.,andStahl,D.A.(2010).Abundanceofammonia-oxidizingarchaea andbacteriaalonganestuarinesalinitygradientinrelationtopotentialnitricationrates. Appl.Environ. Microbiol. 76,12851289. Blainey,P.C.,Mosier,A.C.,Potanina,A.,Francis,C.A.,andQuake,S. R.(2011).Genomeofalow-salinity ammonia-oxidizingarchaeondeterminedbysingle-cellandmetagenomicanalysis. PLoSONE 6, 112.doi:10.1371/journal.pone. 0016626 Bouskill,N.J.,Eveillard,D.,Chien, D.,Jayakumar,A.,andWard, B.B.(2012).Environmentalfactorsdeterminingammonia-oxidizing organismdistributionanddiversity inmarineenvironments. Environ. Microbiol. 14,714729. Brochier-Armanet,C.,Boussau,B., Gribaldo,S.,andForterre,P.(2008). Mesophiliccrenarchaeota:proposal forathirdarchaealphylum,the Thaumarchaeota. Nat.Rev.Microbiol. 6,245252. Bru,D.,Ramette,A.,Saby,N.P. A.,Dequiedt,S.,Ranjard,L,Jolivet, C.,ArrouaysD.,andPhilippot,L. (2011).Determinantsofthedistributionofnitrogen-cyclingmicrobial communitiesatthelandscapescale. ISMEJ. 5,532542. Caffrey,J.M.,Bano,N.,Kalanetra,K.,andHollibaugh,J. T.(2007).Ammoniaoxidation andammonia-oxidizingbacteriaand archaeafromestuarieswithdifferinghistoriesofhypoxia. ISMEJ. 1, 660662. Chen,X.,Zhu,Y.,Xia,Y.,Shen,J.,and He,J.(2008).Ammonia-oxidizing archaea:importantplayersinpaddy rhizospheresoil? Environ.Microbiol. 10,19781987. Christman,G.D.,Cottrell,M.T., Popp,B.N.,Gier,E.,andKirchman,D.L.(2011).Abundance, diversity,andactivityofammoniaoxidizingprokaryotesinthecoastal arcticoceaninsummerandwinter. FrontiersinMicrobiology | TerrestrialMicrobiology June2012 | Volume3 | Article210 | 6

PAGE 7

"fmicb-03-00210"2012/6/1321:04pag e7#7 Zhalninaetal. DriversofAOAinsoils Appl.Environ.Microbiol. 77,2026 2034. Colliver,B.B.,andStephenson,T. (2000).Productionofnitrogenoxide anddinitrogenoxidebyautotrophic nitriers. Biotechnol.Adv. 18, 219232. Coolen,M.J.L.,Abbas,B.,vanBleijswijk,J.,Hopmans,E.C.,Kuypers, M.M.M.,Wakeham,S.G.,andSinningheDamste,J.S.(2007).Putative ammonia-oxidizingcrenarchaeotain suboxicwatersoftheBlackSea:a basin-wideecologicalstudyusing16S ribosomalandfunctionalgenesand membranelipids. Environ.Microbiol. 9,10011016. deBoer,W.,andKowalchuk,G.A. (2001).Nitricationinacidsoils: microorganismsandmechanisms. SoilBiol.Biochem. 33,853866. delaTorre,J.R.,Walker,C.B.,Ingalls, A.E.,Kšnneke,M.,andStahl,D.A. (2008).Cultivationofathermophilic ammoniaoxidizingarchaeonsynthesizingcrenarchaeol. Environ.Microbiol. 10,810818. Di,H.J.,Cameron,K.C.,Shen,J. P.,Wineeld,C.S.,O'Callaghan, M.,Bowatte,S.,andHe,J.Z. (2009).Nitricationdrivenbybacteriaandnotarchaeainnitrogenrichgrasslandsoils. Nat.Geosci. 2, 621624. Di,H.J.,Cameron,K.C.,Shen,J. P.,Wineeld,C.S.,O'Callaghan, M.,Bowatte,S.,andHe,J.Z. (2010).Ammonia-oxidizingbacteria andarchaeagrowundercontrastingsoilnitrogenconditions. FEMS Microbiol.Ecol. 72,386394. Erguder,T.H.,Boon,N.,Wittebolle, L.,Marzorati,M.,andVerstraete, W.(2009).Environmentalfactors shapingtheecologicalnichesof ammonia-oxidizingarchaea. FEMS Microbiol.Ecol.Rev. 33,855869. Ghosh,P.,andDhyani,P.P.(2005). Nitrogenmineralization,nitricationandnitrierpopulationin aprotectedgrasslandandrainfed agriculturalsoil. Trop.Ecol. 46, 173181. Gubry-Rangin,C.,Hai,B.,Quince,C., Engel,M.,Thomson,B.C.,James, P.,Schloter,M.,Grifths,R.I., Prosser,J.I.,andNicol,G.W.(2011). Nichespecializationofterrestrial archaealammoniaoxidizers. Proc. Natl.Acad.Sci.U.S.A. 108,21206 21211. Gubry-Rangin,C.,Nicol,G.W.,and Prosser,J.I.(2010).Archaearather thanbacteriacontrolnitricationin twoagriculturalacidicsoils. FEMS Microbiol.Ecol. 74,566574. Hallam,S.J.,Mincer,T.J.,Schleper, C.,Preston,C.M.,Roberts,K., Richardson,P.M.,andDeLong, E.F.(2006).Pathwaysofcarbonassimilationandammoniaoxidationsuggestedbyenvironmental genomicanalysesofmarineCrenarchaeota. PLoSBiol. 4,05200536.doi: 10.1371/journal.pbio.0040095 Hastings,R.S.,Butler,C.,Singleton, I.,Saunders,J.R.,andMcCarthy, A.J.(2000).Analysisofammoniaoxidizingbacteriapopulationsinacid forestsoilduringconditionsofmoisturelimitation. Lett.Appl.Microbiol. 30,1418. Hatzenpichler,R.,Lebedeva,E.V., Spieck,E.,Stoecker,K.,Richter,A., Daims,H.,andWagner,M.(2008).A moderatelythermophilicammoniaoxidizingcrenarchaeotefromahot spring. Proc.Natl.Acad.Sci.U.S.A. 6,21342139. He,J.,Shen,J.,Zhang,L.,Zhu,Y., Zheng,Y.,Xu,M.,andDi,H. (2007).Quantitativeanalysesof theabundanceandcomposition ofammonia-oxidizingbacteriaand ammonia-oxidizingarchaeaofaChineseuplandredsoilunderlongtermfertilizationpractices. Environ. Microbiol. 9,23642374. Herfort,L.,Schouten,S.,andAbbas,B. (2007).VariationsinspatialandtemporaldistributionofArchaeainthe NorthSeainrelationtoenvironmentalvariables. FEMSMicrobiol.Ecol. 62,242257. Hermansson,A.,andLindgren,P.E. (2001).Quanticationofammoniaoxidizingbacteriainarablesoilby real-timePCR. Appl.Environ.Microbiol. 67,972976. Herndl,G.J.,Reinthaler,T.,Teira,E., Aken,H.,Veth,C.,Pernthaler,A., andPernthaler,J.(2005).Contributionof Archaea tototalprokaryoticproductioninthedeepAtlantic ocean. Appl.Environ.Microbiol. 71, 23032309. Hofferle,S.,Nicol,G.W.,Pal,L., Hacin,J.,Prosser,J.I.,andMandicMulec,I.(2010).Ammoniumsupply rateinuencesarchaealandbacterial ammoniaoxidizersinawetlandsoil verticalprole. FEMSMicrobiol.Ecol. 74,302315. Hoshino,Y.T.,Morimoto,S.,Hayatsu, M.,Nagaoka,K.,Suzuki,C.,Karasawa,T.,Takenaka,M.,andAkiyama, H.(2011).Effectofsoiltypeandfertilizermanagementonarchaealcommunityinuplandeldsoils. Microbes Environ. 26,307316. Isobe,K.,Koba,K.,Suwa,Y.,Ikutani, J.,Fang,Y.,Yoh,M.,Mo,J.,Otsuka, S.,andSenoo,K.(2012).Highabundanceofammonia-oxidizingarchaea inacidiedsubtropicalforestsoils insouthernChinaafterlong-termN deposition. FEMSMicrobiol.Ecol. 80, 193203. Jia,Z.J.,andConrad,R.(2009).BacteriaratherthanArchaeadominate microbialammoniaoxidationinan agriculturalsoil. Environ.Microbiol. 11,16581671. Jung,M.Y.,Park,S.J.,Min,D.,Kim,J. S.,Rijpstra,W.I.,DamstŽ,J.S.,Kim, G.J.,Madsen,E.L.,andRhee,S.K. (2011).Enrichmentandcharacterizationofanautotrophicammoniaoxidizingarchaeonofmesophilic crenarchaealGroupI.1afromanagriculturalsoil. Appl.Environ.Microbiol. 77,86358647. Kalanetra,K.M.,Bano,N.,andHollibaugh,J.T.(2009).AmmoniaoxidizingArchaeaintheArcticOcean andAntarcticcoastalwaters. Environ. Microbiol. 11,24342445. Ke,X.,andLu,Y.(2012).Adaptationofammonia-oxidizingmicrobes toenvironmentshiftofpaddyeld soil. FEMSMicrobiol.Ecol. 80, 8797. Kim,B.K.,Jung,M.Y.,Yu,D.S., Park,S.J.,Oh,T.K.,Rhee,S. K.,andKim,J.F.(2011).Genome sequenceofanammonia-oxidizing soilarchaeon," CandidatusNitrosoarchaeumkoreensis "MY1. J.Bacteriol. 193,55395540. Kirschbaum,M.U.(1995).Thetemperaturedependenceofsoilorganic matterdecomposition,andtheeffect ofglobalwarmingonsoilorganic Cstorage. SoilBiol.Biochem. 27, 753760. Kšnneke,M.,Bernhard,A.E.,dela Torre,J.R.,Walker,C.B.,Waterbury, J.B.,andStahl,D.A.(2005).Isolationofanautotrophicammoniaoxidizingmarinearchaeon. Nature 437,543546. Kowalchuk,G.A.,andStephen,J.A. (2001).Ammonia-oxidizingbacteria:amodelformolecularmicrobial ecology. Annu.Rev.Microbiol. 55, 485529. Lehtovirta,L.E.,Prosser,J.E.,and Nicol,G.W.(2009).SoilpHregulates theabundanceanddiversityofGroup 1.1cCrenarchaeota. FEMSMicrobiol. Ecol. 70,367376. Lehtovirta-Morley,L.E.,Stoecker,K., Vilcinskas,A.,Prosser,J.I.,andNicol, G.W.(2011).Cultivationofanobligateacidophilicammoniaoxidizer fromanitrifyingacidsoil. Proc.Natl. Acad.Sci.U.S.A. 108,1589215897. Leininger,S.,Urich,T.,Schloter, M.,Schwark,L.,Qi,J.,Nicol,G. W.,Prosser,J.I.,Schuster,S.C.,and Schleper,C.(2006).Archaeapredominateamongammonia-oxidizing prokaryotesinsoils. Nature 442, 806809. Martens-Habbena,W.,Berube,P. M,Urakawa,H.,delaTorre, J.R,andStahl,D.A.(2009). Ammoniaoxidationkineticsdeterminesnicheseparationofnitrifying ArchaeaandBacteria. Nature 461, 976979. Martens-Habbena,W.,andStahl,D. A.(2011).Nitrogenmetabolism andkineticsofammonia-oxidizing archaea. MethodsEnzymol. 496, 465487. Morimoto,S.,Hayatsu,M.,Hoshino, Y.T.,Nagaoka,K.,Yamazaki,M., Karasawa,T.,Takenaka,M.,and Akiyama,H.(2011).Quantitative analysesofammonia-oxidizingarchaea(AOA)andammonia-oxidizing bacteria(AOB)ineldswithdifferentsoiltypes. MicrobesEnviron. 26, 248253. Muller,F.,Brissac,T.,LeBris,N.,FelbeckH.,andGros,O.(2010).First descriptionofgiantArchaea(Thaumarchaeota)associatedwithputative bacterialectosymbiontsinasuldic marinehabitat. Environ.Microbiol. 12,23712383. Nicol,G.W.,Leininger,S.,Schleper, C.,andProsser,J.I.(2008).The inuenceofsoilpHonthediversity, abundanceandtranscriptionalactivityofammoniaoxidizingarchaea andbacteria. Environ.Microbiol. 10, 29662978. Norton,J.M.,andStark,J.M. (2011).Regulationandmeasurementofnitricationinterrestrial systems. MethodsEnzymol. 486, 343368. Offre,P.,Prosser,J.I.,andNicol, G.W.(2009).Growthofammoniaoxidizingarchaeainsoilmicrocosms isinhibitedbyacetylene. FEMS Microbiol.Ecol. 70,99108. Oishi,R.,Tada,C.,Asano,R.,Yamamoto,N.,Suyama,Y.,andNakai, Y.(2011).Growthofammoniaoxidizingarchaeaandbacteriaincattlemanurecompostundervarious temperaturesandammoniaconcentrations. MicrobesEcol. doi:10.1007/ s00248-011-9971-z[Epubaheadof print]. Oldeman,L.R.,Hakkeling,R.T.A.,and Sombroek,W.G.(1991). WorldMap oftheStatusofHuman-inducedSoil Degradation(GLASOD):AnExplanatoryNote .Wageningen:InternationalSoilReferenceandInformation Centre. Ouverney,C.C.,andFuhrman,J.A. (2000).Marineplanktonicarchaea takeupaminoacids. Appl.Environ. Microbiol. 66,48294833. Park,H.,Wells,G.F.,Bae,H.,Criddle,C. S.,andFrancis,C.A.(2006).Occurrenceofammonia-oxidizingarchaea www.frontiersin.org June2012 | Volume3 | Article210 | 7

PAGE 8

"fmicb-03-00210"2012/6/1321:04pag e8#8 Zhalninaetal. DriversofAOAinsoils inwastewatertreatmentplantbioreactors. Appl.Environ.Microbiol. 72, 56435647. Pelve,E.,LindŒs,A.C.,MartensHabbena,W.,delaTorre,J.R.,Stahl, D.A.,andBernander,R.(2011). Cdv-basedcelldivisionandcell cycleorganizationinthethaumarchaeon Nitrosopumilusmaritimus Mol.Microbiol. 82,555566. Pester,M.,Rattei,T.,Flench,S., Gršngršft,A.,Richter,A.,Overmann,J.,Reinhold-Hurek,B., Loy,A.,andWagner,M.(2012). amoA -basedconsensusphylogeny ofammonia-oxidizingarchaeaand deepsequencingofamoAgenesfrom soilsoffourdifferentgeographic regions. Environ.Microbiol. 14, 525539. Pitcher,A.,Villanueva,L.,Hopmans,E. C.,Schouten,S.,Reichart,G.,and SinningheDamste,J.S.(2011).Niche segregationofammonia-oxidizing archaeaandanammoxbacteriainthe ArabianSeaoxygenminimumzone. ISMEJ. 5,18961904. Pratscher,J.,Dumont,M.J.,andConrad,R.(2011).Ammoniaoxidation coupledtoCO 2 xationbyarchaea andbacteriainanagriculturalsoil. Proc.Natl.Acad.Sci.U.S.A. 108, 41704175. Preston,C.M.,Wu,K.M.,Molinski,T.F.,andDelong,E.F.(1996). Apsychrophiliccrenarchaeoninhabitsamarinesponge: Cenarchaeum symbiosum gen.nov.,sp.nov. Proc.Natl.Acad.Sci.U.S.A. 93, 62416246. Ravishankara,A.R.,Daniel,J. S.,andPortmann,R.W.(2011). Nitrousoxide(N 2 O):thedominant ozone-depletingsubstanceemitted inthe21stcentury. Science 326, 123125. Reigstad,L.J.,Richter,A.,Daims,H., Urich,T.,Schwark,L.,andSchleper, C.(2008).Nitricationinterrestrial hotspringsofIcelandandKamchatka. FEMSMicrobiol.Ecol. 64, 167174. Santoro,A.E.,Buchwald,C.,McIlvin, M.R.,andCasciotti,K.L.(2011).IsotopicsignatureofN 2 Oproducedby marineammonia-oxidizingarchaea. Science 333,12821285. Schauss,K.,Focks,A.,Leininger,S., Kotzerke,A.,Heuer,H.,ThieleBruhn,S.,Sharma,S.,Wilke, B.M.,Matthies,M.,Smalla,K., Munch,J.C.,Amelung,W.,Kaupenjohann,M.,Schloter,M.,and Schleper,C.(2009).Dynamicsand functionalrelevanceofammoniaoxidizingArchaeaintwoagriculturalsoils. Environ.Microbiol. 11, 446456. Schjonning,P.,Thomsen,I.K.,Moldrup,P.,andChristensen,B.T. (2003).Linkingsoilmicrobialactivitytowater-andair-phasecontents anddiffusivities. SoilSci.Soc.Am.J. 67,156165. Schleper,C.(2010).Ammoniaoxidation:differentnichesforbacteriaand archaea? ISMEJ. 4,10921094. Sexstone,A.J.,Revsbech,N.P.,Parkin, T.B.,andTiedje,J.M.(1985). Directmeasurementofoxygenprolesanddenitricationratesinsoil aggregates. SoilSci.Soc.Am.J. 49, 645651. Shaw,L.J.,Nicol,G.W.,Smith,Z., Fear,J.,Prosser,J.I.,andBaggs,E.M. (2006). Nitrosospira spp.canproduce nitrousoxideviaanitrierdenitricationpathway. Environ.Microbiol. 8, 214222. Shen,J.,Zhang,L.,Zhu,Y.,Zhang,J., andHe,J.(2008).Abundanceand compositionofammonia-oxidizing bacteriaandammonia-oxidizing archaeacommunitiesofanalkaline sandyloam. Environ.Microbiol. 10, 16011611. Spang,A.,Hatzenpichler,R.,BrochierArmanet,C.,Rattei,T.,Tischler, P.,Spieck,E.,Streit,W.,Stahl,D. A.,Wagner,M.,andSchleper,C. (2010).Distinctgenesetintwodifferentlineagesofammonia-oxidizing archaeasupportsthephylumThaumarchaeota. TrendsMicrobiol. 18, 331340. Stark,J.M.,andFirestone,M. K.(1996).Kineticcharacteristics ofammonium-oxidizercommunities inCaliforniaoakwoodland-annual grassland. SoilBiol.Biochem. 28, 13071317. Stopnisek,N.,Gubry-Rangin,C.,Hšfferle,S.,Nicol,G.W.,MandicMulec,I.,andProsser,J.I.(2010). Thaumarchaealammoniaoxidation inanacidicforestpeatsoilisnot inuencedbyammoniumamendment. Appl.Environ.Microbiol. 76, 76267634. Stres,B.,Danevcic,T.,Pal,L.,Fuka, M.M.,Resman,L.,Leskovec,S., Hacin,J.,Stopar,D.,Mahne,I., andMandic-Mulec,I.(2008).Inuenceoftemperatureandsoilwater contentonbacterial,archaealand denitrifyingmicrobialcommunities indrainedfengrasslandsoilmicrocosms. FEMSMicrobiol.Ecol. 66, 110122. Suzuki,I.,Dular,U.,andKwok,S.C. (1974).Ammoniaorammoniumion assubstrateforoxidationby Nitrosomonaseuropaea cellsandextracts. J.Bacteriol. 120,11811191. Szukics,U.,Hackla,E.,ZechmeisterBoltenstern,S.,andSessitsch, A.(2012).Rapidanddissimilarresponseofammoniaoxidizing archaeaandbacteriatonitrogenand wateramendmentintwotemperateforestsoils. Microbiol.Res. 67, 103109. Teira,E.,Reinthaler,T.,Pernthaler, A.,Pernthaler,J.,andHerndl, G.J.(2004).Combiningcatalyzed reporterdeposition-uorescence in situ hybridizationandmicroautoradiographytodetectsubstrateutilizationbybacteriaandarchaeainthe deepocean. Appl.Environ.Microbiol. 70,44114414. Tourna,M.,Freitag,T.E.,Nicol,G. W.,andProsser,J.I.(2008).Growth, activityandtemperatureresponses ofammonia-oxidizingarchaeaand bacteriainsoilmicrocosms. Environ. Microbiol. 10,13571364. Tourna,M.,Freitag,T.E.,andProsser,J. I.(2010).Stableisotopeprobinganalysisofinteractionsbetweenammonia oxidizers. Appl.Environ.Microbiol. 76,24682477. Tourna,M.,Stieglmeier,M.,Spang, A.,Kšnneke,M.,Schintlmeister,A., Urich,T.,Engel,M.,Schloter,M., Wagner,M.,Richter,A.,andSchleper, C.(2011). Nitrososphaeraviennensis anammoniaoxidizingarchaeonfrom soil. Proc.Natl.Acad.Sci.U.S.A. 20, 84208425. Treusch,A.H.,Leininger,S.,Kletzin, A.,Schuster,S.C.,Klenk,H.P., andSchleper,C.(2005).Novelgenes fornitritereductaseandAmo-related proteinsindicatearoleofuncultivatedmesophiliccrenarchaeotain nitrogencycling. Environ.Microbiol. 7,19851995. vanGroenigen,K.J.,Osenberg,C. W.,andHungate,B.A.(2011). Increasedsoilemissionsofpotent greenhousegasesunderincreased atmosphericCO 2 Nature 475, 214216. Verhamme,D.T.,Prosser,J.I.,and Nicol,G.W.(2011).Ammonia concentrationdeterminesdifferentialgrowthofammonia-oxidizing archaeaandbacteriainsoilmicrocosms. ISMEJ. 5,10671071. Venter,C.J.,Remington,K.,Heidelberg,K.J.,Halpern,A.L.,Rusch, D.,Eisen,J.A.,Wu,D.,Paulsen,I., Nelson,K.E.,Nelson,W.,Fouts,D. E.,Levy,S.,Knap,A.H.,Lomas,M. W.,Nealson,K.,White,O.,Peterson, J.,Hoffman,J.,Parsons,R.,BadenTillson,H.,Pfannkoch,C.,Rogers, Y.H.,andSmith,H.O.(2004).EnvironmentalgenomeshotgunsequencingoftheSargassoSea. Science 304, 6674. Walker,C.B.,delaTorre,J.R., Klotz,M.G.,Urakawa,H.,Pinela, N.,Arp,D.J.,Brochier-Armanet, C.,Chain,P.S.,Chan,P.P.,Gollabgir,A.,Hemp,J.,HŸgler,M., Karr,E.A.,Kšnneke,M.,Shin,M., Lawton,T.J.,Lowe,T.,MartensHabbena,W.,Sayavedra-Soto,L.A., Lang,D.,Sievert,S.M.,Rosenzweig, A.C.,Manning,G.,andStahl,D. A.(2010). Nitrosopumilusmaritimus genomerevealsuniquemechanisms fornitricationandautotrophyin globallydistributedmarinecrenarchaea. Proc.Natl.Acad.Sci.U.S.A. 107,88188823. Wang,S.,Xiao,X.,Jiang,L.,Peng, X.,Zhou,H.,Meng,J.,andWang, F.(2009).Diversityandabundance ofammonia-oxidizingarchaeain hydrothermalventchimneysofthe JuandeFucaRidge. Appl.Environ. Microbiol. 75,42164220. WessŽn,E.,Nyberg,K.,Jansson,J. K.,andHallin,S.(2010).Responses ofbacterialandarchaealammonia oxidizerstosoilorganicandfertilizeramendmentsunderlong-term management. Appl.SoilEcol. 45, 193200. Wuchter,C.,Abbas,B.,Coolen,M., Herfort,L.,Bleijswijk,J.,Timmers, P.,Strous,M.,Teira,E.,Herndl,G. J.,Middelburg,J.J.,Schouten,S., andSinningheDamstŽ,J.S.(2006). Archaealnitricationintheocean. Proc.Natl.Acad.Sci.U.S.A. 103, 1231712322. Yao,H.,Gao,Y.,Nicol,G.W.,Campbell,C.D.,Prosser,J.I.,Zhang,L., Han,W.,andSingh,B.K.(2011). Linksbetweenammoniaoxidizer communitystructure,abundance, andnitricationpotentialinacidic soils. Appl.Environ.Microbiol. 77, 46184625. Xu,M.,Schnorr,J.,BrandonKeibler, B.,andSimon,H.M.(2012). Comparativeanalysisof16SrRNA andamoAgenesfromarchaea selectedwithorganicandinorganicamendmentsinenrichment culture. Appl.Environ.Microbiol. 78, 21372146. Zhang,C.L.,Ye,Q.,Huang,Z.,Li,W., Chen,J.,Song,Z.,Zhao,W.,Bagwell, C.,Inskeep,W.P.,Ross,C.,Gao,L., Wiegel,J.,Romanek,C.S.,Shock,E. L.,andHedlund,B.P.(2008).Global occurrenceofarchaeal amoA genesin terrestrialhotsprings. Appl.Environ. Microbiol. 74,64176426. Zhang,L.,Hu,H.,Shen,J.,and He,J.(2011).Ammonia-oxidizing archaeahavemoreimportantrole thanammonia-oxidizingbacteriain ammoniaoxidationofstronglyacidic soils. ISMEJ .6,10321045. Zhang,L.,Offre,P.R.,He,J.Z.,Verhamme,D.T.,Nicol,G.W.,and FrontiersinMicrobiology | TerrestrialMicrobiology June2012 | Volume3 | Article210 | 8

PAGE 9

"fmicb-03-00210"2012/6/1321:04pag e9#9 Zhalninaetal. DriversofAOAinsoils Prosser,J.I.(2010).Autotrophic ammoniaoxidationbysoilthaumarchaea. Proc.Natl.Acad.Sci.U.S.A. 107,1724017245. Zhang,L.M.,Wang,M.,Prosser,J.I., Zheng,Y.M.,andHe,J.Z.(2009). Altitudeammonia-oxidizingbacteriaandarchaeainsoilsofMount Everest. FEMSMicrobiol.Ecol. 70, 208217. Zheng,X.,Wang,M.,Wang,Y.,Shen, R.,JiGou,J.,Li,J.,Jin,J.,andLi, L.(2000).Impactsofsoilmoisture onnitrousoxideemissionfromcroplands:acasestudyontherice-based agro-ecosysteminSoutheastChina. ChemosphereGlobalChangeSci. 2, 207224. ConflictofInterestStatement: The authorsdeclarethattheresearchwas conductedintheabsenceofanycommercialornancialrelationshipsthat couldbeconstruedasapotentialconictofinterest. Received:15March2012;paperpendingpublished:05May2012;accepted: 22May2012;publishedonline:15June 2012. Citation:ZhalninaK,DšrrdeQuadros P,CamargoFAOandTriplettEW(2012) Driversofarchaealammonia-oxidizing communitiesinsoil.Front.Microbio. 3 :210.doi:10.3389/fmicb.2012.00210 ThisarticlewassubmittedtoFrontiers inTerrestrialMicrobiology,aspecialtyof FrontiersinMicrobiology. Copyright2012Zhalnina,Dšrrde Quadros,CamargoandTriplett.Thisis anopen-accessarticledistributedunder thetermsoftheCreativeCommons AttributionNonCommercialLicense, whichpermitsnon-commercialuse,distribution,andreproductioninother forums,providedtheoriginalauthorsand sourcearecredited. www.frontiersin.org June2012 | Volume3 | Article210 | 9