Archaea in Biogeochemical Cycles - The Department of Ecology

24 Pages·2014·0.49 MB·English

MI67CH21-Schleper ARI 6August2013 11:13
Archaea in Biogeochemical
Cycles
Pierre Offre, Anja Spang, and Christa Schleper
g
or DepartmentofGeneticsinEcology,UniversityofVienna,A-1090Wien,Austria;
ws. email:[email protected],[email protected],[email protected]
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obiol. 2013.67:43sity of Arizona - AFJTuinhrnnseetuA2p.6nuR,nbe2ulvi0as.lh1MR3edeicvorieonwbliinoofel.Ma2si0ca1roR3b.eio6vl7ioeg:4wy3ii7sn–o5An7dlivnaenacteon KaArbcehsyatweraao,crbtdiosgeochemicalcycles,metabolism,carbon,nitrogen,sulfur
Micrniver micro.annualreviews.org ArchaeaconstituteaconsiderablefractionofthemicrobialbiomassonEarth.
ev. y U Thisarticle’sdoi: LikeBacteriatheyhaveevolvedavarietyofenergymetabolismsusingor-
Rb 10.1146/annurev-micro-092412-155614
u. ganicand/orinorganicelectrondonorsandacceptors,andmanyofthemare
nn Copyright(cid:2)c 2013byAnnualReviews. abletofixcarbonfrominorganicsources.Archaeathusplaycrucialrolesin
A
Allrightsreserved
the Earth’s global geochemical cycles and influence greenhouse gas emis-
sions.Methanogenesisandanaerobicmethaneoxidationareimportantsteps
in the carbon cycle; both are performed exclusively by anaerobic archaea.
OxidationofammoniatonitriteisperformedbyThaumarchaeota.Theyrep-
resenttheonlyarchaealgroupthatresidesinlargenumbersintheglobal
aerobic terrestrial and marine environments on Earth. Sulfur-dependent
archaeaareconfinedmostlytohotenvironments,butmetalleachingbyaci-
dophiles and reduction of sulfate by anaerobic, nonthermophilic methane
oxidizershaveapotentialimpactontheenvironment.Themetabolismsof
a large number of archaea, in particular those dominating the subsurface,
remaintobeexplored.
437
MI67CH21-Schleper ARI 6August2013 11:13
Contents
INTRODUCTION............................................................... 438
THEDOMAINARCHAEA....................................................... 438
ARCHAEALMETABOLISMSANDBIOGEOCHEMICALCYCLES............. 440
CarbonCycle.................................................................. 440
NitrogenCycle................................................................. 445
SulfurCycle.................................................................... 447
CONCLUSIONSANDPERSPECTIVES......................................... 450
INTRODUCTION
g
or Allcurrentlyknownlifeformsgainthefreeenergyrequiredtomeettheenergeticcostofmain-
s.
w tenance,growth,andreproductionthroughenzymaticallycatalyzedredoxreactions.Lifeexploits
evienly. manypairsofelectrondonorsandacceptors(redoxpairs)forthegenerationofbiochemicalenergy
nualruse o andtheassimilationofnutrients,butsinglespeciesuseonlyaspecificsubsetofthoseredoxpairs.
ww.ansonal Ttiohnessoufrevlievcatlroofnadllonliovirnsganodrgaacnceispmtosrtsh,wushdicehpaernedpsroensetnhteincolinmstitaendtasmupopulnytosfindtifhfeerbeinotspchoemrebiannad-
wer
om or p thereforeneedtobeconstantlyrecycled.Thecyclingofthesechemicalsubstancesemergesfrom
d fr4. F geophysicalprocessesandthecombinedmetabolismsofalllifeforms(96).Theseself-organized
e1 nutrient cycles, which are increasingly influenced by human activities, can be represented as
nload1/20/ networks of processes, connecting different reservoirs of substances and defining biogeochem-
own 0 ical cycles for various chemical elements and molecules. Owing to their versatile metabolisms,
Do
457. brary mbuiiclrdoinogrgbanloiscmkssodfrilvifee,mhoysdtroogfetnh,ecbairobloong,icnailtrflougxeens,osfutlfhuer,eolexmygeennts,—anpdarptihcouslparhloyrtuhse—saixndmtahjours
7-Li
013.67:43Arizona - s1h9a2Fp6eo,rtohmneloybriBeoagtchetaoencrhihaeamalnfidsatrcEyeunoktfauorryuya,rspwinleacrneeeVtco(l3an2ds)ii.mdeirreVdetronacdosnktyribcouitneesdigtnhiefictearnmtlybitooggeloocbhaelmniusttrriyenint
obiol. 2sity of c5y0clyeesa.rTshlaeteArr(c1h3a7e)a.,Uconntsiltittuhteinegartlhye1t9h9ir0ds,futhnedyamweernetapledrocmeivaeindomfaliifnel,ywaesreangorotudpesocrfimbeidcruonotri-l
Micrniver ganismsthrivinginextremehabitatsthathave,exceptforthemethanogens(130),littleinfluence
ev. y U onglobalnutrientcycling.However,thisviewbegantochangewhenmolecularbiologicaltech-
Rb niqueswereintroducedintomicrobialecology.Thediscoverythatarchaeaarefoundinoceanic
u.
n plankton(23,35)hastriggeredahugenumberoffollow-upstudiesshowingthatarchaearepre-
n
A
sent an abundant and diverse group of microorganisms in the whole biosphere and suggesting
that they have a significant impact on nutrient cycling. In addition to cultivation of novel ar-
chaeal strains, culture-independent techniques, in particular molecular biological, biochemical,
andisotope-basedmethods,havesinceremainedinstrumentalforrecognizingandcharacterizing
novelarchaealmetabolismsandforestimatingtheirenvironmentalimpact.Throughthesestudies
ithasbecomeincreasinglyevidentthatarchaeaareimportantplayersinbothcarbonandnitrogen
cycling.Inthisreview,thedistributionoftheArchaeainthebiosphereandtheirroleinextant
biogeochemicalcyclesarediscussedinlightofrecentdiscoveries.
THEDOMAINARCHAEA
Woese&Fox(137)andWoeseetal.(138)providedthefirstevidencethatArchaeaconstitutea
thirddomainalongsideBacteriaandEukaryawithinthephylogenetictreeoflife.Thisfindingwas
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438 Offre Spang Schleper
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Crenarchaeota
Thermoproteales/Sulfolobales/Desulfurococcales/Acidilobales/Fervidicoccales
Geoarchaeota
Geoarchaeota
Thaumarchaeota
Hot Water Crenarchaeotic Group III
ALOHA group/Group 1.1c/psL12 group/Marine Benthic Group A
Group 1.1a (and group 1.1a associated)/Group 1.1b
Aigarchaeota (Hot Water Crenarchaeotic Group I) Aigarchaeota and
candidate lineages
Miscellaneous Crenarchaeotal Groups
Deep Sea Archaeal Group/Marine Benthic Group B
Ancient Archaeal Group/Marine Hydrothermal Vent Group 2
Korarchaeota Korarchaeota
g
or Euryarchaeota
ws. Methanosarcinales/Methanocellales/Methanomicrobiales/ANME lineages 1–3/
evienly. Halobacteriales/Marine Group 4
nualruse o AThrcehrmaeoopgllaosbmaaletsales/Aciduliprofundum sp./Methanoplasmatales/Marine Group 2, 3, 5
w.anonal Marine Benthic Group E/South African Goldmine Group/Miscellaneous + Deep Sea Euryarchaeota Group
ws
ed from w14. For per NMMaeentthhoaasannlooinbcoaacrcucteamrlei assple.s
nload1/20/ Methanopyrales
w0
on Thermococcales
Do
457. brary Micrarchaeum sp.
7-Li Parvarcheum sp./Deep Sea Hydrothermal Vent Group 6
013.67:43Arizona - Nanoarchaeota
obiol. 2sity of FScighuemreat1icrepresentationofthephylogeneticdiversityofarchaeawiththemajorlineagesasreferredtointhetext.Themultifurcations
ev. Micry Univer itnodriecaadteertshwathtohearpelancoetmfaemntiloiafrmwoisthtlainrcehagaeeas.vParhiyelsaiinndgirffaeyretynptepfhacyelohgaevneetnioctabneaelynsevsa.liTdahteedtr.eeisintendedtogiveageneralorientation
Rb
u.
n
n overwhelmingly corroborated by genomic and biochemical data showing that all archaea share
A
uniquemembranesandhavecellwallsthatdifferfromthoseofbacteria(36).Furthermore,theyuse
distinctiveinformationalprocessingmachineries(e.g.,replicationandtranscription)consideredto
bederivedfromacommonancestorwithEukarya(36).Sincetheirdiscoveryasaseparatedomain,
thenumberofknowntaxawithintheArchaeahasbeenexpandedcontinuously.AsofNovember
2,2012,therewere116archaealgenerarepresenting450cultivatedandvalidlydescribedspecies
(http://www.bacterio.cict.fr).However,mostofthearchaealdiversity,currentlyreferencedin
publicdatabases,remainsuncultivated(117)andisknownonlyfrom16SrRNAgenesequences
obtainedfrommolecularsurveys(24).Manyoftheseuncultivatedarchaeaareonlydistantlyrelated
to their closest cultivated relatives and specify numerous lineages representing a wide range of
taxonomicranks,uptothephylumlevel.Cultivatedanduncultivatedarchaeallineageshavebeen
classifiedinafewhigh-ranktaxa(Figure1),andashortoverviewofcurrentlyproposedarchaeal
phylaisprovidedbelow.
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MI67CH21-Schleper ARI 6August2013 11:13
Most cultivated archaea are assigned to two major archaeal phyla, Euryarchaeota and
Crenarchaeota, that were originally defined by Woese et al. (138). Euryarchaeota include eight
taxonomicclasses(i.e.,Methanopyri,Methanococci,Methanobacteria,Methanomicrobia,Archaeoglobi,
MCG: Miscellaneous
Halobacteria,Thermococci,andThermoplasmata)thatincludemethanogens,methane-oxidizingar-
CrenarchaeotalGroup
chaea,denitrifiers,sulfatereducers,ironoxidizers,andorganotrophs(61).Membersofthisphylum
DSAG: DeepSea
aregloballydistributed,andsomelineages,oftenuncultivatedones,areabundantinmarinewaters,
ArchaealGroup
soils,andsediments(117,128),whereasmanyofthelong-knowneuryarchaeotesinhabitextreme
environmentsandarethereforerestrictedtospecificgeographicareas.Thehyperthermophilic,
parasitic Nanoarchaeum equitans, initially suggested to represent a new candidate phylum (49),
likelyconstitutesanadditionalfast-evolvinglineageoftheEuryarchaeota(14).
Crenarchaeotacontainonlyonetaxonomicclass(i.e.,Thermoprotei)andfivetaxonomicorders
(i.e., Acidilobales, Desulfurococcales, Fervidicoccales, Sulfolobales, and Thermoproteales), two of which
(AcidilobalesandFervidicoccales)werediscoveredonlyrecently(100,106).Allcrenarchaeoteshave
org beenfoundinhotenvironmentssuchasacidicterrestrialhotspringsandsubmarinehydrothermal
ws. vents,aswellassmolderingrefusepiles(61).
evienly. FeworganismsoftherecentlydefinedphylumThaumarchaeotahavebeencultivated(124),all
w.annualronal use o oaalnfsdowahoricecchuforguiannindexeintnrehermiggyehebnnyuvmairmboemnrmsoneinniatmsoaixnriidcnlauetdiaoinnndg.Ofhroergtshasnwpirasitmnegrsse.onfvtihriosnpmheynlutsm,saoriels,galonbdaslleydidmisetrnitbsuatnedd
ws
wer Onthebasisofgenomicdata,additionalarchaealphylahaverecentlybeenproposed.They
om or p includeKorarchaeota(5,29),Aigarchaeota(94),andGeoarchaeota(67).Theaffiliationofseveral
d fr4. F deep-branching lineages such as the Miscellaneous Crenarchaeotal Group (MCG), Deep Sea
e1
oad20/ ArchaealGroup(DSAG),andAncientArchaealGroup(AAG)isstillunclear(43).Membersof
wnl01/ thesenewphylahavebeenfoundintheterrestrialandmarinesubsurface(128)butalsoinhot
on
Do springsanddeep-seahydrothermalsystems,andnorepresentativehasyetbeenobtainedinpure
457. brary culture.
7-Li
013.67:43Arizona - ARCHAEALMETABOLISMSANDBIOGEOCHEMICALCYCLES
Microbiol. 2niversity of Aimacnraodclrhiepmaretophabalacanmtb2eolyt0fa%rtbheopeolrifAsemasrelcslnhsptauretsoahtk.aeaOinrdynotohmttheeiensparbinnoadtsoiugsccreotoaifuoncpnewloolafftcetomhruseinc(art5rso6coa)hnr,agdaeabomnomiuosamtles1ssc–uai5nnla%drmdsiatenurtidenuripeempss,ieunarberssctouhhiralefealbaaciyeaoecgsrceesodo(ui6cmnh,tee9nfm5ot)-rs,
ev. y U (76)andinmostgeothermalhabitats.Theirinvolvementinmajorgeochemicalcyclesisdiscussed
Rb
u. below.
n
n
A
CarbonCycle
Archaeadominatethebiogenicproductionofmethane(CH )butarealsokeytotheoxidationof
4
thisimportanthydrocarbon.Archaealorganismsalsoplaysignificantrolesintheproductionand
mineralizationoforganicmatter.
Carbonassimilation. ManycultivatedrepresentativesoftheCrenarchaeota,Thaumarchaeota,and
Supplemental Material Euryarchaeotaarecapableofautotrophicgrowth(SupplementalTable1;followtheSupplemen-
tal Material linkfromtheAnnualReviewshomepageathttp://www.annualreviews.org),as
theyassimilatecarbonfromoxidizedinorganiccompounds,i.e.,carbondioxide(CO )orbicar-
2
bonate (HCO −), reducing those substrates to form simple organic molecules (9) (Figure 2a).
3
Investigationofthegenomesequenceof“CandidatusCaldiarchaeumsubterraneum”(94)indicates
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440 Offre Spang Schleper
MI67CH21-Schleper ARI 6August2013 11:13
a Carbon cycle b Nitrogen cycle
M eth2anoMgeentehs1iasno- CH4 Moxeidthaatinoen xationN2 N2Nitrifier dNe2nOitrificationNO
genesis N fi Mineralization 3
Small 4
organics Acetogenesis CO2 OrgNanic NH3 Aoxmidmaotinoina NO2– Nitrite oxidation NO3– Oxic
a n a e Freorbmice rnetsaptiiorant,ion Fixation Areesrpoibraiction ation Annamox nitrification Anoxic
x e
org OrgCanic N fi D
ws. N N O NO NO –
evienly. Anoxic Oxic 2 2 2
w.annualronal use o c Sulfur cycle
ws
om wor per Metal sulfide Abiotic H2S
ownloaded frn 01/20/14. F OxidaOtioxnidation oxidSautlifounr Sreudlfuucrtion Sulfite reduction
Microbiol. 2013.67:437-457. Dniversity of Arizona - Library o S2O532–ThiroseSudlufulacofttiaexotined aretidounction/ SSulfur oxidationOS42– DismSutualtfioantSe urlefdatucet iroend HuctSi2o–n SO32–
ev. y U
Rb
u. Figure2
n
n Schematicrepresentationoftheinvolvementofarchaeain(a)carbon,(b)nitrogen,and(c)sulfurcycles.Redarrowsindicatemetabolic
A
stepsfoundinarchaeaandbacteria;orangearrowsindicatemetabolicpathwayspresentexclusivelyinarchaea;andgrayarrowsindicate
metabolismsknownonlyfrombacteria.Circlednumberscanbedefinedasfollows:1,hydrogenotrophicmethanogenesisisalithotrophic
processresultingfromthereductionofCO2withH2aselectrondonor;2,formatotrophic,acetotrophic,andmethylotrophic
methanogenesisareorganotrophicprocessessupportedbythedegradationofformate,acetate,andmethylatedcompounds,
respectively;3,nitrifierdenitrificationisthoughttooccurunderlowoxygenconditions;4,N2Omightbeadirectsideproduct
oftheammonia-oxidizingpathway;5,S2O32−isproducedinseveraldifferentwaysincludingabioticprocessesnotpresentedhere.
thatmembersoftheAigarchaeotamightalsobeabletoassimilateinorganiccarbon.Threedif-
ferentmetabolicpathwaysforautotrophiccarbonfixationhavebeencharacterizedincultivated
archaealautotrophs,andthesewerereviewedrecently(9).
ManyautotrophicmembersoftheArchaeagrowmixotrophically;i.e.,theycoassimilatesmall
organic compounds under suitable conditions or switch between an autotrophic and a het-
erotrophic lifestyle (61). Whereas Thaumarchaeota as described thus far depend on inorganic
www.annualreviews.org • ArchaeainBiogeochemicalCycles 441
MI67CH21-Schleper ARI 6August2013 11:13
carbonforassimilation,somelineagesofEuryarchaeotaandCrenarchaeotaincludeseveralfacul-
tative autotrophic organisms but also obligate heterotrophs, such as the representatives of the
HalobacterialesandThermococcales(61).
Stableisotope
Thedeterminationofthegrowthmodeofmostarchaeaisbasedoninvitroexperiments,which
probing(SIP):
asubstratehighly mightnotreflectthelifestyleoftheseorganismsintheirnaturalhabitatsandlimitsthecurrent
enrichedinastable knowledge of those organisms that have been successfully cultivated. However, some environ-
isotope(e.g.,13C)is mentalstudiesusingnaturalradiocarboncontent,stableisotopeprobing(SIP)techniques,ormi-
giventoan
croautoradiographycombinedwithcatalyzedreporterdeposition–fluorescenceinsituhybridiza-
environmentalsample
tion(MICRO-CARD-FISH)havebeenperformedtorevealthelifestyleofparticulararchaeain
todetectmetabolically
activeorganismsinside natural populations and microcosms.For example, the natural radiocarbon content of archaeal
acomplexmicrobial lipidsindicatesthatThaumarchaeotainoceanwaterspredominatelygrowautotrophically(50,99,
consortium 140).Modeledestimatesofarchaealbiomassproductionindeepwatersrangefrom0.7to0.8Gt
ANME: anaerobic C/year,suggestingthatThaumarchaeotamightcontribute∼1%oftheannualprimaryproduction
org methanotroph intheocean(47,50)andcouldprovide,atleastinsomeinstances,mostofthereducedcarbonfor
ws. Chemoorganotroph: heterotrophicmicroorganismsinoxygenminimumzones(45).Similarly,evidenceforautotrophic
w.annualrevieonal use only. ooeelnrreggecaartgnnroyiiscnmscodoutomhrncapoetosrususnaendsdsas gSoinrfIoPaowrc(cte1hha0an5oe,fam1aitna4rl4teg)hai.nesItnossecocdemoaimnnetesprunahsbtytss,luo(r1rtefy1pap)cr.eeesDsseoeunfdatTilamthSiaevIunPemst,soai(.rfe1c.1th,h,aae6eo8qMt,ua1aCh2naG8tsi)t,baawetniedevnreDepssrtShoaAbovGliwednelidistnooietnogagsprooeeiswl,pmrhdooeicbtmreionrinocgotaransopmtppgshrruoiocsaauicnlphlgys,
ws
wer suggestedthateuryarchaealanaerobicmethanotroph(ANME)lineagesarealsoautotrophs(59).
om or p
d fr4. F Organic carbon mineralization. The catabolic degradation of organic substrates by
e1
oad20/ chemoorganotrophsusuallyresultsintheproductionofCO2asthemainendproduct(Figure2a).
wnl01/ However,theabsenceofexternalelectronacceptors(fermentativeconditions)oralimitationin
on
Do respiratorycapacityisassociatedwiththeexcretionofpartiallyoxidizedcompounds,e.g.,organic
457. brary acidsoralcohols,inadditiontoCO2.Numerousarchaealorganisms,includingaerobesandanaer-
7-Li obes,cangroworganotrophically(seebelowforadiscussionoforganotrophicmethanogensand
013.67:43Arizona - mwheitchhanbee-looxnigditzointhgearEcuhrayeaar)c.hTaehootaseaonrdgaCnriesnmarscthhaaetohtaav(SeubpeepnlecmuletinvtaatledTtahbulsefa1r).aAreceoxmtrepmreohpehnislievse,
Microbiol. 2niversity of dcayaraecnrshccbhraeieapaeft,oaiolurencnpldaorsefisnstNehRneaetnafvoetahirvreaienlosocuaoesrfc6oht1rah.geeaOa,nKnaoonttrrhdoaeArpcbhRhaiMsaciesmoAotNefat,tahlGbienoeegloiaesagnmreocsshmmsaueeipogsepthaqot,uraAtelinsniogcgaegrcorcuohflwatuienvooacrttugael,adtintvhaoarettcrehpodarpoeehxavitlicrsaoeilormlnygoaa(nlp4ih,esu2iml9ric-s,
ev. y U 37,67,93,94).Recentmetagenomicstudiessuggestthateuryarchaealphototrophicorganotrophs
Rb
u. (MarinegroupII)couldbeubiquitousintheglobalocean(34,51),butcurrentlythereisnoproof
n
An thatarchaealorganismspresentinmoderateenvironmentsplayamajorroleinorganiccarbon
mineralization.
Methanogenesis. Methane, a major greenhouse gas but also an important source of energy
for humans, is the predominant hydrocarbon in Earth’s atmosphere. Methanogenic archaea
are strict anaerobes that produce methane (CH ) as the major product of their energy-
4
conservingmetabolism(Figure2a).Allmethanogenicarchaeacharacterizedsofarbelongtothe
Euryarchaeota (Supplemental Table 1) and are distributed among five taxonomic classes, i.e.,
Methanopyri,Methanococci,Methanobacteria,Methanomicrobia,andThermoplasmata(26,79,98).
Severalmethanogenicpathwaysthatrelyonvarioussubstrateshavebeendescribed(Figure2a
andSupplementalTable1):CO reductionwithhydrogen(hydrogenotrophicmethanogens)or
2
formate(formatotrophicmethanogens)aselectrondonors;methanolreductionwithhydrogen;
fermentationofacetate(acetotrophicmethanogens);anddismutationofmethylatedcompounds
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442 Offre Spang Schleper
MI67CH21-Schleper ARI 6August2013 11:13
(methylotrophic methanogens) such as methanol, methylamines, dimethylsulfide (DMS), or
methanethiol(33,79).WhereasmostcultivatedmethanogensreduceCO withhydrogen,only
2
members of Methanosarcinales have the ability to produce methane from the fermentation of
Syntrophic
acetate and the dismutation of methylated compounds. The recently discovered methanogenic
partnerships:
Thermoplasmata reduce methanol with hydrogen (26, 98) and might also use methylamines as electrontransfers
methanogenic substrate (104). Currently, none of these methanogenic metabolisms have been betweentwo
found in bacteria or eukaryotes. Although acetate fermentation is performed by only a few organismsenabling
growthonotherwise
cultivatedmethanogens,thisprocesscouldaccountforuptotwo-thirdsofthemethanereleased
thermodynamically
totheatmospherebyarchaealmethanogenesis;thereductionofCO accountsfortherestofthe
2 unfavorablereactions
archaealcontributiontoatmosphericmethane,withminoramountsofmethaneproducedbythe
dismutationofmethylcompounds(33).
Methanogens have been isolated from various anoxic environments (20, 79) (e.g., rice pad-
dies and peat bogs; freshwater, marine, and hypersaline sediments; hydrothermal vents; deep-
org subsurfacehabitats;thegastrointestinaltractofvariousanimals)andareusuallyabundantwhere
ws. electron acceptors such as NO3−, Fe3+, and SO42− are in short supply. Hydrogenotrophic
evienly. methanogensandacetogenicbacteriahavesimilarrequirements,includinganoxicconditions,a
w.annualronal use o psgoeeunrfreocsreimsoofecHdcau2trashseipglrehecftteerromennpdteioraanlltoyurra,etasnl(od2w,a6sHo5u,2r1cc3oe0no)c.feICnnOttera2rteaissoteninlsegcaltynr,domnaeattcahcaepnpHotoglreo(nwFiceigraurtrchehaan2eaa7);.hBiatuvcetamanlesatolhsbaoenebone-
ws
wer foundinoxicenvironments,i.e.,variousaeratedsoils(3,102)andtheoxygenatedwatercolumnof
om or p anoligotrophiclake(40).Themethanogensinaeratedsoilsbecameactiveunderwetanoxiccon-
d fr4. F ditions(3),andthoseinoxygenatedlakewaterswereattachedtophotoautotrophs,whichmight
e1
oad20/ enable anaerobic growth and supply of methanogenic substrates (40). Several other processes,
wnl01/ such as the microbial decomposition of methylphosphonate (55, 88), could be responsible for
on
Do methaneproductioninoxygenatedwaters(60),andfungi(74)andplants(15)arepossiblesources
457. brary of methane in aerated soils. The global significance of these alternative aerobic methanogenic
7-Li pathwaysremainstobeassessed.
013.67:43Arizona - forAarscihganeiafilcmanetthfraancotigoenneosfisthperondeutcaensnaubaoluetm1iGsstioonfsmoefthmaentehaenveertyoytehaer(a1tm11o,s1p3h0e)rean,dwiatchcosoumntes
Microbiol. 2niversity of eiMbnsetecuitmanhudaastneeereosgfrpaocrsuloihndmidugachtrteeiaoswsenar7vrb4moy%iirnmsg(be7tay9hn)tad.ankMioisngetgehtnhupiascanraoatmgricneahnjtaoihcereaafobriscciohusdasueesoagpfreacacludtseraordteipontrnotoadorruifcsccteeircucmordeneessteohiadiarlencr(he5ab2(tl)8hy2aa)nti.ndstacaroycsatlilco(1cs2ko6eil)ds.
ev. y U
Rb
u.
n
An Methanogenic syntrophies. Methanogenicarchaeaengageinvarioussyntrophicpartnerships
(121)thatinvolvethetransferofelectronsfromafermentativeorganismtothemethanogenvia
acarriermolecule,suchasH oracetate.Themethanogensusethecarriermoleculeaselectron
2
donorforenergyconservation,andthefermentativeorganismgainsenergyfromtheredoxre-
actionthatproducestheelectroncarrieronlyifthemethanogens oxidizethecarriermolecule,
keeping the carrier at a low concentration. Methanogens might also receive electrons directly
(121)viaconductivepiliornanowires(112)oracrossconductiveiron-oxideminerals(58).Syn-
trophicinteractionsenablemethanogenesiswhenmethanogenicsubstratesarelimiting,andtheir
establishmentcanalsoleadtoincreasedmethaneproductionrates(58,120).Theglobalbiogeo-
chemicalimpactofsyntrophicinteractionsinvolvingmethanogenicEuryarchaeotaisconsiderable
as they enable the complete degradation of complex organic molecules to carbon dioxide and
methaneinmethanogenichabitats(121).Acetotrophicmethanogenscanalsoproducehydrogen
andsupportthehydrogen-dependentdechlorinationofxenobioticcompoundsbydehalorespiring
www.annualreviews.org • ArchaeainBiogeochemicalCycles 443
MI67CH21-Schleper ARI 6August2013 11:13
microorganisms(46),furtherbroadeningthebiogeochemicalsignificanceofinteractionsinvolving
methanogenicarchaea.
AOM: anaerobic
Methaneoxidation. MethanogenicarchaeaareamajorsourceofCH emissions,butsomeof
oxidationofmethane 4
theirclosestrelativesinturnplayacriticalroleincontrollingtheseemissionsbyoxidizingCH
4
back to CO (Figure 2a). Methane-oxidizing archaea, also called methanotrophic archaea, are
2
strictanaerobesthatgainenergybycouplingtheoxidationofmethanetothereductionofsulfate
(SO 2−) (129, 131). These organisms belong to the Euryarchaeota and all are representatives of
4
a single taxonomic class, the Methanomicrobia, along with various methanogenic archaea. The
16S rRNA gene sequences of the euryarchaeal ANMEs determine three sequence clusters,
Supplemental Material namelyANME-1,ANME-2,andANME-3(SupplementalTable1),whicharedistantlyrelated
to each other (16S sequence similarity of 75–92%) and do not form a monophyletic lineage
(63).RepresentativesoftheANMElineageshavenotbeenobtainedinpureculture;therefore,
org their taxonomy has not been formally established. These archaea often, but not always, form
ws. microbial consortia with sulfate-reducing Deltaproteobacteria (reviewed in 63), which led to the
evienly. suggestion that the sulfate-dependent anaerobic oxidation of methane (AOM) is a syntrophic
w.annualronal use o pvthiraaobtcielAistNsy.MTofhEteh-2veesoeryrpgluaontwaitsiemvnesesrayglnoyntyreoieppldheiroefsofrt(mh12is9Am,O1e3Mta1b),cooaliunsmpdle,adhroetwcoeendvtiesrsb,irmleeaidlkatrtheorsroeyaursgcuhhlfesarttsuedtroyeqd(8uu9ec)stitsoihononw(tsheedee
ws
wer Sulfidogenesis,below).Nootherorganism,bacterialoreukaryotic,isknowntoperformasimilar
om or p process.
d fr4. F TheenvironmentaldistributionofANMEorganismshasbeenreviewedextensivelybyKnittel
e1
oad20/ & Boetius (63), and a short account of their report is presented here. Methanotrophic archaea
wnl01/ thriveinanoxicenvironmentswherebothmethaneandsulfatearepresent,whichoftenoccurs
on
Do in marine benthic systems. Accordingly, ANME organisms are widely distributed in methane
457. brary seep ecosystems as well as in marine sediments, where their habitat is restricted to the sulfate-
7-Li methanetransitionzone.Theabundanceofmethanotrophicarchaeaoftenmirrorstheratesof
Microbiol. 2013.67:43niversity of Arizona - afa(agr<rrnreccea1shhaeh0taarw6eeeoraaacbltteihhecmlalrasmvenhecteh1amatb0ahl−ins1at0o3oan)cttbesreoe,olcoeltpcsxnhuhicedrdsmaepait−ntrhie3eoymc)npstaieahrcmdreyoiesncifinaoheosuelausonmnergdedoiidcixcamaiatcillnmelwsynetetadhttstthio,eivnasrweengrchesshoeesalor.uebefTemiwtpphansrhet,ossi,hh;cchehoai.ysbtessddi.pt,irrafooadftetttereshrnasoenwsrfaegmirAdepeOaseollloopyMvfw,uetl,fnehauarttern.sito,AdMhnsNesosemritMl(hsiuan,alpEldan-pqitec1oou-a,opitdfAixueenNirlndgassit,MziitaotihinnEneadg-sst
ev. y U 2,andANME-3lineagesarenotidentical.ANME-1andANME-2aregloballydistributedand
Rb
u. present in similar environments, but one of these two groups usually dominates at a specific
n
An geographic location. ANME-3 organisms are essentially present at submarine mud volcanoes
sites.Thephysiologicalandmetabolicbasesofthesedifferences,ifany,arenotclear.
Iron(asferrihydrite)andmanganese(asbirnessite)arealternativeelectronacceptorssuitable
forAOM,andthereisevidencethattheseprocessesmayoccurinmarinesedimentswhereSO 2−-
4
dependentAOMmayalsotakeplace(7).ThepotentialrateofSO 2−-drivenAOMwasreported
4
tobe 4and10 times as fastas birnessite-and ferrihydrite-dependentAOMinEel River Basin
sediments,respectively,buttheglobalco-occurrenceoftheseprocesses,theirrelativecontribu-
tion to in situ rates of AOM, and the identity of the microorganisms responsible for the iron-
and manganese-dependent processes remain to be determined. AOM can also be coupled in a
fundamentallydifferentbiochemicalpathwaytothedenitrificationfromnitrite(NO −),aprocess
2
occurringinfreshwaterhabitats(31,145)andperformedbyrecentlydiscoveredbacteriabelong-
ingtotheNC10candidatedivision(30),butthereisnoindicationthatNO −-andSO 2−-driven
2 4
AOMcanoccurinthesameenvironment(see,e.g.,25).
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444 Offre Spang Schleper
MI67CH21-Schleper ARI 6August2013 11:13
AOMexertsastrongcontroloveroceanCH emissions,whichaccountforonly2%ofthe
4
CH releasedtotheatmosphere.GlobalestimatesoftherateofAOMinoceanicenvironments
4
suggestthatalargefraction(>50%)ofthegrossannualproductionofCH inmarinesystemsis
4
consumedbyanaerobicmethanotrophsbeforeCH isevenreleasedtooceanwaters(111).The
4
AOMinmarinesedimentshasbeenattributedtotheCH -oxidizingactivityofANMEarchaea,
4
butothermicroorganismsmaybeinvolved(7)andtheiridentityandcontributiontotheglobal
CH budget need to be determined. There are, however, some uncertainties about the ability
4
ofANMEarchaeatorespondtoapotentialincreaseinoceanmethaneproduction,whichcould
result from an accelerated melting of the massive reservoir of methane hydrates present in the
seabed(13).
Carbonateprecipitation. Anaerobicmethanotrophicarchaeapromotetheprecipitationofcar-
bonates from the inorganic carbon dissolved in the sediment pore water by locally increasing
org thealkalinityandinorganiccarbonconcentrationofthewater(16,134).Becausecarbonatesare
ws. relativelystableinsediments,theirformationresultsinthelong-termstorageofcarboninthe
evienly. lithosphere.Thecarbonofcarbonaterocksisre-emittedtotheatmosphereonlyslowlyoverge-
ww.annualrsonal use o otimhloepglaioccntaglo-tfitmemremasrcicnaaleerbsCotHhnr4copyucrglohed(vu1oc0ltc)io.aAnninnsmaoetraoosbnsoilcycimbatyeetodhxwaidnitiezh-iontxegicdCtiozHnini4cgtpoalraCctheOase2uabbbduuutfcaftelisroonthbs,eywgtrhlaoincbhsafleiscrlrpiimanrgatttoiocf
wer thelithospheresomeofthecarboncycledonashorttimescalebylivingorganisms.
om or p
d fr4. F
oade20/1 NitrogenCycle
ownln 01/ Archaeaarecentraltotheoxidationofammonia(NH3)tonitrite(NO2−)butarealsoinvolved
Do inthefixationofdinitrogen(N )gasanddenitrificationprocess.Themineralizationoforganic
457. brary nitrogencompoundsbyarchaea2lorganotrophsisnotdiscussed.
7-Li
013.67:43Arizona - Neitihtreorgferonmfixiantoiorgna.nMiconsittroorggeannissmousr,ciensc,lusudcinhgatsheNgHre3atamndajnoritirtyatoef(aNrcOha3−ea),,aosrsifmroilmatennitirtoroggeenn-
Microbiol. 2niversity of capthorreeonctianaetimsnssheionossgrpththoaseurtrgcpeaop.nnTlyitchiwnecuiotaohmtuminsplooytshuppnehrdobesdrioiu(cs1cpne7hi)st.eurroiTetga,hebaenlnseedenntoithtreregorsamgntehainciencaftooenmnodadpniocncuhoenaroidgnfsanmefrsiocosemsnntittltiihrafeeollglyfaoervnrgimaessaoreuibssrieodcregevspeo,oeirhnchoodfewemNnetvi2ceoiarnnl,
Rev. by U processcallednitrogenfixation,whichconsistsofthereductionofN2toNH3(Figure2b).This
u. process is performed naturally by a number of bacterial and archaeal microorganisms, but the
n
An industrialfixationofnitrogenthroughtheHaber-Boschprocessproducessimilarlylargequantities
ofammoniausedasfertilizersinagriculture,whichiscurrentlystronglydisturbingthenitrogen
cycle(19,41).
The ability to fix N gas, or diazotrophy, is a widespread feature of methanogenic archaea
2
and is also present in anaerobic methane-oxidizing euryarchaea (Supplemental Table 1), but
isexpressedonlyintheabsenceofothernitrogensourcesasforbacterialnitrogenfixers(17,22,
72). Diazotrophic methanogens belong to three major taxonomic classes, i.e., Methanobacteria,
Methanococci,andMethanomicrobia(SupplementalTable1),andhavebeenisolatedfromvarious
environments (17, 72, 87), suggesting a widespread occurrence in anoxic habitats (Figure 2b).
DiazotrophicmethanotrophsbelongtotheANME-2lineage(22,101)andareknownonlyfrom
methaneseepsediments.Cultivationexperimentshaveshownthatmethanotrophicdiazotrophs
notonlyfixbutalsosharenitrogenwithbacterialpartnersinAOMconsortia(22).Theprevalence
of in situ diazotrophic growth by methanogenic and methanotrophic archaea, however, is
www.annualreviews.org • ArchaeainBiogeochemicalCycles 445
MI67CH21-Schleper ARI 6August2013 11:13
uncertain, and the importance of archaeal nitrogen fixation in providing reduced nitrogen for
anaerobicmicrobialcommunitiesremainstobeassessed.
Lithoautotrophic:
Nitrification. Notonlyisammoniatakenupbymostorganismsandimmobilizedintheirbiomass,
describesanorganism
thatusesinorganic itisalsooxidizedtoNO3− inoxicenvironmentsviathenitrificationprocess(Figure2b),which
compoundsasenergy consists of two steps, i.e., the oxidation of NH to NO − and its further conversion to NO −.
3 2 3
sourcesandfixes Each step is catalyzed by different guilds of microorganisms, namely the ammonia and nitrite
carbonfrominorganic
oxidizers,respectively.Untilrecently,itwasassumedthatonlylithotrophicbacteria(66)and,to
compounds
alimitedextent,heterotrophicmicroorganisms(125)areinvolvedinnitrification.Thediscovery
AOA:
thatlithoautotrophicarchaeathrivinginoxicandmoderatehabitatshavethecapacitytooxidize
ammonia-oxidizing
NH toNO −(64,133)wasunexpected,andtheirhighnumbersinmarineandfreshwaters,soils
archaea 3 2
and surface sediments, and thermally heated environments suggest a prominent role in global
nitrogencycling(73,118,139).
org Ahandfulofammonia-oxidizingarchaea(AOA),allbelongingtoThaumarchaeota(Supplemen-
ws. talTable1),havebeenobtainedinpurecultureorenrichments.Theystemfrommarineandconti-
evienly. nentalhabitatsandareassignedtofourdifferentthaumarchaeallineages:group1.1a,group1.1aas-
ww.annualrsonal use o shvoiaecvnieantreeendcs,eigns”rtol(y1us3ph21o).wi1sbna,btahlneadttotThgherAoawmOmoAn/oHunrWiea-aCoaxsGiadnIizIaiInl(tgfeorsrnoaailtritevhceaesunomturarecrvceiheoawfeN,osnHee“3C1(2aSn4ud)p.idpPalhetuymssiNeonliottgraoilcsTaolasspbthuleade1ier)as,
wer andthereisevidencesuggestingthatureaisanimportantsubstrateforarchaealammoniaoxidation
om or p inpolarwaters(1).Furthermore,analysisofthe“CandidatusNitrososphaeragargensis”genome
d fr4. F indicatedthatcyanate(OCN−)mightbeusedassubstrateforarchaealammoniaoxidation(123)
e1
oad20/ (SupplementalTable1).However,thaumarchaealrelativesofcultivatedAOAmightnotalways
ownln 01/ growbyoxidizingNH3(91)ortheymightusedifferentelectronacceptors(54,128).
Do TherelativecontributionofarchaealandbacterialammoniaoxidizerstotheNH oxidation
457. brary processisuncertain,andtheirrespectiveecologicalnicheshavebeendiscussed(107).3Cultivated
Microbiol. 2013.67:437-niversity of Arizona - Li mlAifsboneiasOwwohc”nitAbess(i1utuiratui3bmourd2sermit)yuer,caspchi(,tstoAaeaAnrsOkcaOiceomcBeAnttni)ehcl,traaeariirlannz.setettoi.Arodo,ahOn2tbtaih1yoBrve.ene4a(psl8loo,mlo5osrww,uwMtee1cesd0hrttNo7fsailo)uneHs.rbrhtTa4ashin+tbnoorcigastAfeeetooeOttrrihonytAethhhocr,roecieitg.enhseJhahce.Ln,eosN2e2nlwd10tHdraaaamst3ttnetariMrcdoasosin,uhnnNwgacr(lhgeeH1fnpee-2s4srot7a+trerta)ttu.A(thepirHdOoaaHtntoAfiAsoow7,rmOn.ea5avniA)cgnedofhroona,ttursmhabtt“eccaemCconhroaomteir.gns(dpNKhpiiaeeonm-.tsngeo)vtsxifAgiteoibodnOrrloinezvBaweiefmnnotrahgy--rt
ev. y U mostoftheammoniaoxidation(85).MicrocosmexperimentsindicatethatAOAcanalsoplaya
Rb
nu. majorroleinsoilNH3 oxidation(42,97),eveninfertilizedsoils(116,135),whichcouldbeex-
An plainedbyanunevendistributionoffertilizerinthesoilporespace,definingamosaicofhigh-and
low-ammonianiches.Otherstudieshavealsoindicatedthatarchaealammoniaoxidationinsoils
mightbefueledbythemineralizationoforganicnitrogencompounds(75),suggestinginteractions
withammonifyingmicroorganisms.Furthermore,AOAseemtoberesponsibleformostofthe
ammoniaoxidationinsomeacidicsoils(42,81,143),andthefirstacidophilicammoniaoxidizer,
thethaumarchaeon“CandidatusNitrosotaleadevanaterra,”wascultivatedonlyrecently(71).
Ammoniaoxidationistherate-limitingstepofthenitrificationprocessandsupportstheox-
idation of NO − to NO − (Figure 2b) by nitrite-oxidizing bacteria (NOB), but the nature of
2 3
theinteractionsbetweenAOAandNOBisstillunclear.Inthemarineenvironment,especiallyin
oxygenminimumzones,AOAmightalsosupporttheanaerobicoxidationofNH + withNO −
4 2
(anammox)(Figure2b)bysupplyingnitriteandconsumingoxygen(69,141).
Nitrificationhasaglobalimpactontheformofinorganicnitrogen(NH orNO −)available
3 3
inecosystems.TheassimilationofNO − hasahigherenergeticcostthanthatofNH because
3 3
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446 Offre Spang Schleper