The growing tree of Archaea

19 Pages·2017·2.62 MB·English

by  Panagiotis S Adam

TheISMEJournal(2017)11,2407–2425
©2017InternationalSocietyforMicrobialEcology Allrightsreserved 1751-7362/17
www.nature.com/ismej
MINI REVIEW
The growing tree of Archaea: new perspectives on
their diversity, evolution and ecology
Panagiotis S Adam1,2, Guillaume Borrel1, Céline Brochier-Armanet3
and Simonetta Gribaldo1
1Unité de Biologie Moléculaire du Gène chez les Extrêmophiles, Département de Microbiologie, Institut
Pasteur, Paris, France; 2Université Paris Diderot, Sorbonne Paris Cité, Paris, France and 3Univ Lyon,
Université Lyon 1, CNRS, UMR5558, Laboratoire de Biométrie et Biologie Évolutive, 43 bd du 11 novembre
1918, F-69622, Villeurbanne, France
TheArchaeaoccupyakeypositionintheTreeofLife,andareamajorfractionofmicrobialdiversity.
Abundant in soils, ocean sediments and the water column, they have crucial roles in processes
mediatingglobalcarbonandnutrientfluxes.Moreover,theyrepresentanimportantcomponentofthe
humanmicrobiome,wheretheirroleinhealthanddiseaseisstillunclear.Thedevelopmentofculture-
independent sequencing techniques has provided unprecedented access to genomic data from a
largenumberofsofarinaccessiblearchaeallineages.Thisisrevolutionizingourviewofthediversity
and metabolic potential of the Archaea in awide varietyof environments, an important step toward
understanding their ecological role. The archaeal tree is being rapidly filled up with new branches
constituting phyla, classes and orders, generating novel challenges for high-rank systematics, and
providing key information fordissecting the origin of this domain, the evolutionary trajectories that
haveshapeditscurrentdiversity,anditsrelationshipswithBacteriaandEukarya.Thepresentpicture
isthat ofahuge diversityofthe Archaea, which we areonlystartingto explore.
TheISME Journal (2017) 11,2407–2425; doi:10.1038/ismej.2017.122; published online4August2017
Following the first report of the wide distribution of comparison, the number of isolates and newly
archaeal lineages in the marine environment described species has remained stationary (Figure 1),
(DeLong, 1992), a commentary by Gary Olsen stated and mainly concerns members of well-characterized
enthusiastically: ‘…overlooking the Archaea has lineages, stressing the need for a stronger isolation
been equivalent to surveying one square kilometre effort.Tothatend,metabolicpredictionsderivedfrom
of the African savanna and missing over 300 genomicdataofunculturedarchaeallineagescanalso
elephants’ (Olsen, 1994). Today, this analogy has provide unprecedented information to guide culture
been largely verified, and the initial expectations strategies.
have even been exceeded. A burst in the availability The analysis of the first genomic data from these
of the first genomic data from a large number of newly sequenced lineages has had a strong impact
uncultured archaeal lineages has been witnessed in on archaeal systematics, leading to the proposal of a
the past few years. According to the NCBI genome multitude of new clades at various taxonomic levels
database, 1062 archaeal genomes have been made (orders, classes, phyla, superclasses, superphyla),
available as of December 2016 (Figure 1), of which
with a wealth of new assigned names that have
186 are from metagenomes and 111 are single cell
replaced the original acronyms from environmental
genomes. Twice as many are sequenced but not yet
16S rRNA studies (Table 1). It is important to
releasedaccordingtotheGOLDdatabase.Giventhat
remember here that there is no established criterion
the symbolic number of 100 complete genomes was
to propose a new taxonomic status above the Class
reached only six years ago (Brochier-Armanet et al.,
level, an important priority to address in modern
2011), this provides a measure of how rapidly the
field of archaeal genomics is moving. As a microbial systematics (Gribaldo and Brochier-
Armanet, 2012). Moreover, the phylogenetic coher-
ence of already established high-rank systematics in
Correspondence: C Brochier-Armanet or S Gribaldo, Unité de both Bacteria and Archaea based on 16S rDNA
BiologieMoléculaireduGenechezlesExtrêmophiles,Department
divergence is far from uniform (Yarza et al., 2014).
ofMicrobiology,InstitutPasteur,28rueduDrRoux,75015Paris,
France. Thecurrentandfuturedelugeofgenomicsequences
E-mail:[email protected] from an ever-larger fraction of uncultured microbial
[email protected]
diversity prompts for the urgent establishment of
Received2December2016;revised7April2017;accepted7June
2017;publishedonline4August2017 commoncriteriabasedongenomicdata,particularly
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1200
Cumulative number of genomes Cumulative number of species
1062
Number of genomes Number of species
1000
s
e
ci
e
p 800
s
&
s 682
e
m
o 600
n
e
of g 481430 470 480
ber 400 354 367 410390
um 284 299 310 330
N 200 148 160 176 192 209 216 227 243 259 158 210
130
100
2 2 3 4 11 15 17 20 24 33 50 58 75
0
Years
Figure 1 Number of archaeal genome sequences and validly described archaeal species over the last 20 years. The orange line and
histogram indicate respectively the annual and cumulative number of novel archaeal genome sequences (that is, complete genomes,
chromosome, contigs and scaffolds) released in public databases (NCBI, latest update December 2016). The blue line and histogram
indicaterespectivelytheannualandcumulativenumberofvalidlydescribedarchaealspecies(Source:ListofProkaryoticNameswith
StandinginNomenclaturewithnamespublisheduntilJuly2016—http://www.bacterio.net/).
in the frame of nomenclature and classification constituting the proposed DPANN superphylum
consistency of major reference databases. (Rinke et al., 2013) have been treated separately,
Under such a deluge of genomic data, the estab- because their monophyly and phylogenetic place-
lishment of a robust phylogenetic frame for the ment are unclear, and will be discussed in a
Archaea, and, in particular, the placement of all the dedicated section.
new uncultured lineages, becomes of paramount
importance.Thisisessentialtoinferthenatureofthe
last ancestor of Archaea and the very origin of this The expanding TACK superphylum
domain of life, as well as its relationship with
eukaryotes. Also, it allows understanding the evolu- TheTACKsuperphylumwasproposedin2011based
tionary processes that led to present-day archaeal onphylogeneticproximityandsignaturessharedwith
diversity and drove the emergence of specific eukaryotes (Guy and Ettema, 2011). At that time, it
metabolic capacities and adaptations to different included the Thaumarchaeota, the Aigarchaeota, the
environments, well beyond extreme niches. CrenarchaeotaandtheKorarchaeota(GuyandEttema,
The majority of the new genomes originate from 2011; Table 1). An additional TACK phylum named
uncultured lineages representing a sizeable propor- Geoarchaeotawassuggested(Table1;Kozubaletal.,
tion of microbial life in sediments and water 2013),butwassubsequentlyindicated torepresenta
columns, and may significantly increase the already deep-branching lineage of the Crenarchaeota (Guy
well-recognized importance of Archaea as major et al., 2014; Table 1), consistently with our analysis
players in global biogeochemical cycles (Offre (Figure 2). Based on a large-scale phylogenomic
et al., 2013). Thus, access to genomic data and the analysisithasbeenrecentlyproposedthattheTACK
associated metabolic potential of the first represen- represents a kingdom-levelcladenamedProteoarch-
tatives of these lineages is an important step toward aeota (Petitjean et al., 2014). In recent years, the
understanding their role in the environment, and genomic coverage for members of the TACK has
providesanewoutlookonthemetabolicdiversityof substantially increased, providing a better view on
the Archaea (Table 2). its diversity and evolution.
Hereafter, we will present an overview of some of
the most significant recent findings, which are
discussed based on an updated robust phylogeny of Thaumarchaeota and the origin of archaeal
the Archaea obtained from a large taxonomic nitrification
sampling including all the new uncultured lineages Foralongtime,thephylumThaumarchaeota(former
(Figure 2). The fast-evolving nanosized lineages Group I Crenarchaeota, Table 1) has been identified
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Table1 Newlynamedarchaeallineageswiththeiroriginalacronymsandcorrespondingetymology(whenapplicable)
Originalname/acronym New/Proposedname Reference Etymology
Newphyla
GroupICrenarchaeota Thaumarchaeota Brochier-Armanet θαύμα(thávma)=miracle
etal.,2008
HotWaterCrenarchaeoticGroup(HWCGI) Aigarchaeota Nunouraetal.,2011 [claimed]αυγή(avgí)=dawn/[correct]αίγα
(aíga)=goat
MiscellaneousCrenarchaeotalGroup(MCG) Bathyarchaeota Mengetal.,2014 βαθύς(vathys)=deep
Novelarchaealgroup1(NAG1) Geoarchaeota(basal Kozubaletal.,2013 γαία(gaía)=earth
Crenarchaeota)
DeepSeaArchaealGroup(DSAG) Lokiarchaeota Spangetal.,2015 Loki=Norsetrickstergod
MarineBenthicGroupB(MBG-B) Thorarchaeota Seitzetal.,2016 Thor=Norsegodofthunder
ND Odinarchaeota Zaremba-Niedz- Odin=Germanic/Norsegodwithadiverse
wiedzkaetal.,2017 portfolio
DSAG&AAG-related Heimdallarchaeota Zaremba-Niedz- Heimdallr=Norsegodwhokeepswatchfor
wiedzkaetal.,2017 Ragnarök
TerrestrialMiscellaneousCrenarchaeotaGroup Verstraetearchaeota Vanwonterghemetal., afterProfessorWillyVerstraete
(TMCG) 2016
Newclasses
MarineGroupII(MG-II) Thalassoarchaea Martin-Cuadradoetal., θάλασσα(thálassa)=sea
2015
WSA2/ArcI Ca.Methanofastidiosa Nobuetal.,2016 methane+fastidiosa(=highlycritical)
SouthAfricanGoldMineEuryarchaeotic Hadesarchaea Bakeretal.,2016 Άδης((h)ádis)=Greekgodofthe
Group(SAGMEG) Underworld
MediterraneanSeafloorBrineLakeGroup1 Persephonarchaea Mwirichiaetal.,2016 Περσεφόνη(Persephóni)=Queenofthe
(MSBL-1) (proposed) Underworld,wifeofHades
MarineBenthicGroupD(MBG-D) Izemarchaea(proposed) Lloydetal.,2013 Ίζημα(ízima)=sediment
MarineGroupIII(MG-III) Pontarchaea(proposed) Lietal.,2015 Πόντος(Póntos)=thesea,Greekseadeity,
consortofThálassa
Z7ME43 Theionarchaea Lazaretal.,2017 theion=sulfur
Neworders
RiceClusterI(RC-I) Methanocellales Sakaietal.,2008 Methane+cell
AnaerobicMethanotroph1(ANME-1) Methanophagales Meyerdierksetal., Methane+-phag-(-φαγ-=eater)
(proposed) 2010
RumenClusterC(RCC)/RiceClusterIII(RC-III) Methanomassiliicoccales Iinoetal.,2013 Methane+Massilia(Marseille)+coccus
(κόκκος=grain)
SippenauerMoor1(SM1Euryarchaeon) Altiarchaeales ProbstandMoissl- altus=tall,deep
Eichinger,2015
GoM-Arch87 Syntropharchaeales Laso-Pérezetal.,2016 AftertypegenusSyntrophoarchaeum
(proposed)
Newfamily
RiceClusterII(RC-II) Methanoflorentaceae Mondavetal.,2014 Methane+florens(flowering,blooming)
Newsuperclasses
MG-II,MG-III,DHVE2,RCC/RC-III,TMEG,and Diaforarchaea Petitjeanetal.,2015 διάφορα(diáfora)=various,miscellaneous
Thermoplasmata
Methanopyrales,Methanobacteriales,and Methanomada Petitjeanetal.,2015 Methane+ομάδα(omáda)=team,group
Methanococcales
HadesarchaeaandMSBL-1 Stygia(proposed) Στυξ/Στύγα(Styx/Styga)=theriverbound-
arybetweentheEarthandtheUnderworld
Thermococcales,DG-70,andWSA2/ArcI Acherontia(proposed) Αχέρων(Achéron)=the‘riverofwoe’inthe
Underworld
Methanogensclass2,Halobacteria,ANME-1, Methanotecta(proposed) Methane+τίκτομαι(tíktomai=tobeborn)=
GoM-Arch87,Archaeoglobi thosebornfrom/inmethane
Newsuperphyla
Lokiarchaeota,Thorarchaeota,Heimdallarch- Asgard Zaremba-Niedz- Asgard=InNorsemythology,oneofthe
aeota,Odinarchaeota wiedzkaetal.,2017 NineWorlds.HometotheÆsirgods
Thaumarchaeaota,Aigarchaeota,Crenarch- TACK/Proteoarchaeota GuyandEttema,2011/ Πρωτεύς/Πρωτέας(Protéfs/Protéas):Greek
aeota,GeoarchaeotaandKorarchaeota Petitjeanetal.,2014 shapechangingseagod
Diapherotrites,Parvarchaeota,Aenigmarch- DPANN Rinkeetal.,2013 Acronym
aeota,Nanohaloarchaeota,andNanoarchaeota
Abbreviations:ND,notdetermined;TMEG,TerrestrialMiscellaneousEuryarchaeoticGroup.
Citationsreferspecificallytothearticleswherethenewnameorsystematicsassignmentwasgiven.Somenamesareproposedintheframeofthis
review.Forgrammaticalcorrectness,Greekcompoundwordsintaxonomicnomenclature(neologisms)shouldbeformedusingonlythestemofthe
prefix.Occasionally,alinkingvowelcanbeinsertedforreasonsofeuphonye.g.Hadarchaea/Hadoarchaea.
with the ecologically important aerobic ammonia et al., 2011). Increasing availability of genomic data
oxidizing archaea inhabiting marine (Group I.1a/ from three new thaumarchaeal lineages (Figure 2)
Nitrosopumilales, Nitrosopumilus, Nitrosoarch- has drastically changed this picture and provided
aeum,Cenarchaeum),andsoilenvironments(Group substantial insights into the still largely unexplored
I.1b/Nitrososphaerales, Nitrososphaera) (Pester metabolic versatility of the Thaumarchaeota. These
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genomes correspond to Fn1 (Group I.1c) obtained marine, and subsurface environments (Hedlund
fromdeepanoxicpeatlayers(Linetal.,2015),andto et al., 2015) which robustly branch as the sister
Beowulf (Group I.1d) and Dragon (Group I.1d) clade of Thaumarchaeota (Brochier-Armanet et al.,
obtained from acidic (pH ~3), thermophilic 2011 and Figure 2). Obtained from a subsurface
(65–72°C), iron oxide and sulfur sediments of geothermal water stream, the metagenome of ‘Can-
Yellowstone National Park (Beam et al., 2014; didatus Caldiarchaeum subterraneum’ was the first
Table2).AlthoughFn1ispredicted toobtainenergy to be published (Nunoura et al., 2011), and was
and carbon from β-oxidation of volatile fatty acids, followedbyseveralSAGsfromvarioushydrothermal
either by using fumarate as terminal electron environments(Rinkeetal.,2013).Anothercandidate
acceptor or in syntrophy with methanogens (Lin species named ‘Ca. Caldithenuis aerorheumensis’,
et al., 2015), both Beowulf and Dragon Thaumarch- from an oxic, hot spring streamer microbial commu-
aeota appear to be versatile chemoorganotrophs, nity, has been the target of a metatranscriptomic
potentially growing on diverse carbohydrates, pep- analysis, providing the first insights into the meta-
tides and amino acids (Beam et al., 2014). Surpris- bolic potential of Aigarchaeota in situ (Beam et al.,
ingly, while mostly complete, none of the genomes 2016). They appear as filamentous microorganisms
from these three Thaumarchaeota lineages contains that are capable of chemoorganoheterotrophy by
the amoABC genes for ammonia oxidation (Beam using several organic carbon substrates (Table 2).
etal.,2014).Thisindicatesthattheabilitytooxidize Seemingly,Aigarchaeotaareauxotrophsforvitamins
ammonia is not a general characteristic of the and cofactors, as well as heme, which they might
Thaumarchaeota. In this respect, further genomic obtain from othercommunity members (Beam et al.,
data and exploration of the metabolic potential 2016).
and phylogenetic placement of the three lineages, The phylogenetic placement of Aigarchaeota
in particular Fn1, which appear to be the closest makes them a key lineage to investigate the emer-
relatives of aerobic ammonia oxidizing archaea gence of Thaumarchaeota and their specific meta-
(Figure 2), will provide key information on the bolic adaptations. For example, the presence of an
emergence of ammonia oxidation in the Heme Copper Oxidase, HCO, in the majority of
Thaumarchaeota. available Aigarchaeota and Thaumarchaeota gen-
Fn1, Beowulf and Dragon might also provide omes indicates that the capacity to grow aerobically
significant information on the adaptation of ammo- is a widespread trait of these lineages (Beam et al.,
niaoxidizingThaumarchaeotatoaerobicconditions. 2016).Thisraisesthequestionofwhetheradaptation
Fn1 members were in fact isolated from anaerobic to aerobic environments preceded the divergence of
environments (Lin et al., 2015), Dragon members Aigarchaeota and Thaumarchaeota or instead it
were obtained from hypoxic conditions, and have occurred independently in the two phyla.
genes indicating the ability for elemental sulfur
reduction(Beametal.,2014),whileBeowulfmembers
were isolated from oxic conditions where they might Bathyarchaeota: key players in the global carbon cycle
useoxygenasterminalelectronacceptor(assuggested TheTACKsuperphylumhasrecentlyacquiredanew
bythepresenceofaHemeCopperOxidase,HCO),but member lineage, the Bathyarchaeota (former Mis-
might also be capable of growing anaerobically by cellaneous CrenarchaeotalGroup,MCG,Table1),an
reducing nitrate to nitrite thanks to the presence of a emerging clade of great ecological interest. Bath-
narGHJI gene cluster (Beam et al., 2014). yarchaeota are robustly indicated as the sister line-
Finally, the deep branching of Beowulf and age to the Aigarchaeota/Thaumarchaeota (Figure 2).
Dragon lineages (Figure 2) may support the hypoth- Thisphylogeneticaffiliationisalsosupportedbythe
esis of a thermophilic ancestor for all Thaumarch- fact that many genomes of Bathyarchaeota contain
aeota and a subsequent adaptation to mesophilic homologuesoftheeukaryotic-likeTopoisomeraseIB
environments(Barnsetal.,1996;Emeetal.,2013),a (Meng et al., 2014), a character so far defining the
trend becoming more and more evident for many Thaumarchaeota/Aigarchaeota (Brochier-Armanet
archaeal phyla. Additional genomes and isolation of et al., 2011), pushing the origin of this enzyme
the first members of these lineages, combined with further back in archaeal diversification than pre-
specificphylogeneticanalyseswillclarifytheoverall viously thought. The Bathyarchaeota are ubiquitous
phylogeny of the Thaumarchaeota and allow further in both terrestrial and marine anoxic sediments
assumptions on the diversity and emergence of (surface and subsurface) where they can represent a
various metabolic capacities in this important major fraction of the archaeal community (Kubo
phylum. et al., 2012; Lloyd et al., 2013). The extensive
diversity of this lineage, divided into as many as 17
subgroups (mostly at the family level), suggests a
Aigarchaeota and adaptation to oxygen wide variety of metabolisms and environmental
Genomic coverage has also substantially expanded adaptations (Kubo et al., 2012). The genomic data
for the Aigarchaeota (former Hot Water Crenarch- now available for six subgroups has revealed a
aeotic Group, HWCG I, Table 1), a diverse lineage common capacity to degrade peptides to obtain
widespread in moderate to extremely hot terrestrial, carbon and energy, and a more variable ability to
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S-cycling — Elementalsulfurreduction/thiosul-fatereductionMethylated-thiolreductionElementalsulfurreduction/sulfideoxidation? — ND — ND Elementalsulfur/thiosulfatereduction Methylated-thiolreduction — Sulfitereduction Elementalsulfurreduction
n
o
N-cycling — N-fixation2 — Nitritereduction NitratereductionND — ND — Methylatedaminereducti Nitritereduction Nitrite/nitratereduction —
s,
entlydescribedarchaeallineages C-cycling 13fixation(WLandC)CO2 afixation(partialWL)/peptides,aminoacids&CO2carbohydratesdegradation +R-CH)Methanogenesis(H23 fixation(partialWL)CO2 fixation(partialWL)/peptides,aminoacids&CO2carbohydratesdegradationND fixation(partialWL)CO2 ND aCOfixation(partialWL)/peptides,aminoacids&2carbohydratesdegradation Peptides,aminoacidsdegradation/methanogenesis+R-CH)(H23 afixation(WL)/fattyacids,peptides,aminoacidCO2aromaticcompounds&carbohydratesdegradation/+R-CH?)methanogenesis(H23 Fattyacids,peptides,aminoacids&carbohydratesdegradation Peptides,aminoacids&carbohydratesdegradation
c
e c c c c c c c c c c c c c
yclesofr Aerobic/Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Anaerobi Aerobic Anaerobi
c
distributionandpotentialimplicationinelemental Environment Cold(MuehlbacherSchwefelquelle,Germany)andhot(CristalGeyser,USA)subsurfacewater,estuarinesediment(WOR) Estuarinesediments(WOR) Organic-richenvironments(anaerobicdigestor) Estuarinesediments(WOR,anoxicmethane-richlayer)andhotspring(YNP) Anoxichypersalinesedimentsandwatercolumn(BrinePoolsoftheRedSea)’Marinesediments(AB&LokisCastle) ’Marineandfreshwatersediments(Lokiscastle&Coloradoriveraquifer) High-temperaturehabitats(LowerCulexBasin,YNP&RadiataPool,NZ) –Marine(WOR,sulfatemethanetransitionzone&AB)andfreshwatersediments Freshwatersediments,soil,hydrocarbon/orgnanic-richenvironments(anaerobicdigestor),coalbedmethanewells(SB) Freshwater,estuarine(WOR)&marine(AB&GBs)sediments,coalbedmethanewells(SB) Geothermalwaterstream(YNP),moderatetoextremelyhotterrestrial,marine,andsubsurfaceenvironments(mine,Japan) Elementalsulfurdepositionzoneofahotandacidicspring(DragonSpring,YNP)
al
nt
Table2Environme Lineage Altiarchaeales Theionarchaea Methanofastidiosa Hadesarchaea Persephonarchaea(MSBL-1)Heimdallarchaeota Lokiarchaeota Odinarchaeota Thorarchaeota Verstraetearchaeota Bathyarchaeota Aigarchaeota Dragon
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Table2(Continued) LineageEnvironmentAerobic/C-cyclingN-cyclingS-cyclingAnaerobic BeowulfIronoxidematsofahotandacidicspringAerobicPeptides,aminoacids,aromaticNitrateSulfuroxidation(BeowulfSpring,YNP)compoundandcarbohydratesdegradationreduction ——Fn1Soilandpeat(deepfenlayer,MEF)AnaerobicFattyacidsdegradation —SyntropharchaealesMarinesediments(hydrothermallyAnaerobicShort-chainalkane(butane&propane)degradation(SyntrophicwithheatedGBs)sulfatereducers) ——+CO)MethanoflorentaceaeRicefield&peat(StordalenMire,Sweden)AnaerobicMethanogenesis(H22 ——aIzemarchaea(MBG-D)Freshwater,estuarine(WOR)&marine(AB)AnaerobicFattyacids,peptides,aminoacids&sedimentscarbohydratesdegradation ——a,aminoacids&Pontarchaea(MG-III)Marinewatercolumn(GBw&Caribbeansea)AerobicFattyacids,peptidescarbohydratesdegradation ——aThalassoarchaeaMarinewatercolumn(PugetSound,GBw,Medi-AerobicFattyacids,peptides,aminoacids&terranean&Caribbeansea)carbohydratesdegradation —TMEGMarinesediment,soilandpeat(deepbogAnaerobicFattyacids&carbohydratesdegradationSulfite/organosulfo-layer,MEF)natereduction ——SG8-5Estuarinesediments(WOR)AnaerobicPeptides&aminoacidsdegradation Methylated-thiolMethanomassiliicoccalesAnimaldigestivetract(human,cow&termite),AnaerobicMethanogenesis(H+R-CH)Methylated23reductionsoil,sediments,anaerobicdigestoraminereduc--fixationtion/N2 Abbreviations:AB,AarhusBaysediments,Denmark;GBs/w,Guyamasbasinsediment/watercolumn;MEF,MarcellExperimentalForest,USA;ND,notdeterminedinthestudydescribingthosegenomes;NZ,NewZealand;SB,SuratBasin,Australia;TMEG,TerrestrialMiscellaneousEuryarchaeoticGroup;WOR,WhiteOakRiverestuarysediments,USA;YNP,YellowstoneNationalPark,USA.aIncludingextracellulardegradationofpeptides.Therelationtooxygenispredictedfromtheenvironmentoforiginandfromthepresence/absenceofgenesforaerobicrespiration.RolesinC,N,Scyclesarereportedfrompublishedanalysesofthe‘—’genomes(mainlypredictionfromgenecontent)andmaynotconcerneverymemberofthelineages.symbolssignifynoreportedusageofNorScompoundsaselectrondonors/acceptorsforrespiration.RoleinelementalcyclesthroughassimilatorypathwaysisonlyreportedforCOandNfixation.COfixationwaspredictedbasedonthepresenceofgenescodingfortheWood-22213Ljungdahlpathway(WL),andbyexperimentalmeasurementof13Cinlipids(C).WLcouldalsobeusedinoxidativedirectionforfattyacids,peptides,aminoacidsorcarbohydrates.
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Figure2 PhylogenyoftheArchaea.Bayesianphylogeny(PhyloBayes,CAT+GTR+Γ4)basedona41genesupermatrix(8710aminoacid
positions).Scalebarrepresentstheaveragenumberofsubstitutionspersite.Nodesupportsrefertoposteriorprobabilities,andultrafast
bootstrapvaluesbasedonathousandreplicatescalculatedbymaximumlikelihood(IQTree,LG+C60).The41genesconsistof36genes
fromthePhylosiftmarkergeneslist(Darlingetal.,2014),plusRNApolymerasesubunitsAandB,andthreeuniversalribosomalproteins
(L7-L12,L30,S4)from(Liuetal.,2012).Thetreeisrootedaccordingto(Raymannetal.,2015),butalternativerootsareindicatedwith
numberedreddots(seemaintextfordiscussion).Greyfontindicatesthecladesforwhichnoisolatesareavailable.Currentlyproposed
taxonomicstatus:C=Class;P=Phylum;SC=SuperClass;SP=SuperPhylum.
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use carbohydrates, fatty acids or aromatic com- and the Odinarchaeota (Seitz et al., 2016; Zaremba-
pounds (Lloyd et al., 2013; Meng et al., 2014; Niedzwiedzka et al., 2017). The Thorarchaeota
Evans et al., 2015; He et al., 2016; Lazar et al., (former MBG-B) were described based on partial- to
2016; Table 2). The utilization of a diverse range of near-complete genomes obtained from sediments of
organic compounds for heterotrophic growth is also the White Oak River estuary, in the sulfate–methane
supportedbyincorporationof13C-labelledmolecules transition zone (Seitz et al., 2016). The Odinarch-
(Seyler et al., 2014). In addition, several members of aeota, and the Heimdallarchaeota genomes were
the phylum possess a complete H MPT-type Wood- obtained from high-temperature habitats and marine
4
Ljungdahl (WL) pathway and genes for acetate sediments, respectively (Zaremba-Niedzwiedzka
formation suggesting the possibility of growing et al., 2017). Along with additional metagenomic
autotrophically by acetogenesis from H +CO , a bins of Lokiarchaeota and Thorarchaeota, they were
2 2
capacitypreviouslythoughttobelimitedtoBacteria shown to possess further eukaryotic signature pro-
(He et al., 2016; Lazar et al., 2016). Moreover, some teins, such as eukaryotic-like tubulins, homologues
members possess markers of methanogenesis, sug- of the ε DNA polymerase and membrane-trafficking
gesting a possible role in the methane cycle (Evans components (TRAPP complex, Sec23/24 family
et al., 2015; see below). The potential metabolic proteins), and proposed to form a new superphylum
flexibility between autotrophic and heterotrophic which was named Asgard (Zaremba-Niedzwiedzka
growthonawide rangeofcompoundsrepresentsan et al., 2017, Figure 2). Further evolutionary analysis
ecological advantage for the Bathyarchaeota and ofAsgardlineagesmightprovideimportantinforma-
underlines the importance of this abundant benthic tionontheprocessesthatledtotheemergenceofthe
group in the global carbon cycle. first eukaryotic cell. To confirm and extend these
results,isolationofthefirstrepresentativesofAsgard
members are paramount priorities.
Lokiarchaeum, Asgard and the origin of Asgard lineages are common inhabitants of anae-
eukaryotes robicmarine,estuarineandlakesediments,andthey
might have an important role in the global carbon
Amongthemajoraccomplishmentsoftheexploration cycle(Table2;TeskeandSørensen,2008).Metabolic
of uncultured archaeal diversity is the discovery of prediction suggests that Thorarchaeota are able to
new lineages proposed to be the closest relatives of degrade organic matter, contributing to the carbon
eukaryotes. The phylum Lokiarchaeota was defined cycle,butalsomayhavearoleinintermediatesulfur
following the sequencing of the first metagenomic cycling (Seitz et al., 2016). Based on the presence of
datafromtheunculturedDSAGlineage(Spangetal., analmost-completeH MPT-typeWLpathwayandof
4
2015, Table 1). De novo assembly and binning was some electron-bifurcating hydrogenases coding
applied on DNA extracted from deep marine sedi- genes in its genome, it was proposed that Lokiarch-
ment samples (3283m below sea level) at the Arctic aeummightbeanaerobic,autotrophicandhydrogen-
Mid-Ocean-Ridge, in the vicinities of the hydrother- dependent (Sousa et al., 2016). More in depth
mal Loki’s Castle site (Jorgensen et al., 2012). This genomic analyses and the isolation of representative
resultedinthe reconstruction of onenearlycomplete members will be necessary to clarify further the
(Lokiarchaeum) and two partial (Loki 2 and Loki3) metabolic potential of the Asgard superphylum.
genomesrelatedtothislineage.Thesedatarevealeda
surprisingly large number of eukaryotic signature
proteins previously thought to be absent in Archaea, Methanogens, methanogens everywhere!
in particular genes coding for components related to
membrane remodelling and cytoskeletal functions in Methanogenesis is an important and ancient meta-
eukaryotes (for example, actin, small Ras GTPases, bolism that is specific to the Archaea (Thauer et al.,
extended ESCRT complex; Spang et al., 2015). 2008). For a long time, the known diversity of
Consistent with their genomic content, the inclusion methanogens was known to fall into two large
of the three Lokiarchaeota in a universal tree of life clades, which were called Class I methanogens
indicated them as a sister clade to eukaryotes, (Methanococci, Methanopyri, Methanobacteria) and
suggesting that Lokiarchaeota may represent a ‘miss- Class II methanogens (Methanomicrobia: Methano-
inglink’betweenthetwodomainsoflife(Spangetal., sarcinales and Methanomicrobiales) (Bapteste et al.,
2015). Additional studies have been consistent with 2005). These two clusters have been confirmed and
this hypothesis by analysing the Lokiarchaeum enriched by new genomic data. In particular, the
genome for homologues of a few eukaryotic-like monophylyofClassImethanogenswassupportedby
processes, such as the membrane-trafficking system a large-scale phylogenomic analysis of the archaeal
(Klingeretal.,2016)andtheselenocysteine-encoding domain leading to the proposal of the superclass
system (Mariotti et al., 2016). Methanomada (Table 1 and Figure 2; Petitjean et al.,
Very recently, genomic sequences have been 2015). This additionally stabilized the oft-unclear
obtained from three additional uncultured phyla placementofMethanopyriinthearchaealphylogeny
closely related to Lokiarchaeota (Table 1 and as robustly branching with Methanobacteria, a
Figure 2): the Thorarchaeota, the Heimdallarchaeota relationship also supported by a shared derived
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character,thepresenceofpseudomureinintheircell reliant on methyl-dependent hydrogenotrophic
walls (Albers and Meyer, 2011). methanogenesis in an energy-conservation process
ConcerningClassIImethanogens/Methanomicrobia, that is not completely resolved (Borrel et al., 2014b;
they now firmly include two novel divisions: Metha- Lang et al., 2015). Moreover, the Methanomassilii-
nocellales (former Rice Cluster I) and Methanoflor- coccalesusespecificmethyltransferasesthatcontain
entaceae(formerRiceClusterII;Table1),aswellasthe the rare 22nd proteinogenic amino acid pyrrolysine
non-methanogenic Halobacteria (Figure 2). More spe- (Pyl), which is incorporated during translation by a
cific analyses are, however, necessary to fully resolve sophisticated process involving a specific amber
theinternalrelationshipsofthisclade,inparticular,to non-sense codon suppressor tRNA (Borrel et al.,
clarifywhichlineagerepresentstheclosestoutgroupto 2014a). This genetic code expansion is potentially
the Halobacteria, whose specific amino acid composi- handled by distinct mechanisms compared with
tion might be at the origin of incongruent placements the few other Pyl-containing bacteria and archaea,
indifferentpublishedstudies.Thiswillbeessentialto and even among different Methanomassiliicoccales
understand the process of adaptation to a halophilic, (Borrel et al., 2014a, b).
aerobic and heterotrophic lifestyle from a methano- The discovery of Methanomassiliicoccales under-
genic ancestor (Nelson-Sathi et al., 2015; Groussin linesourstillpoorunderstandingofthediversityand
et al., 2016). Given a possible common origin from a role of archaeal methanogens in human health and
methanogenic ancestor, we propose uniting former disease, an important area of future research (for a
Methanogens Class II with their closely related non- recent review, see Gaci et al., 2014; Bang and
methanogenic lineages (Halobacteria, ANaerobic Schmitz, 2015). Indeed, trimethylamine (TMA),
MEthanotrophic (ANME-1), Syntropharchaeales, which can be depleted into methane by Methano-
Archaeoglobi) into a new superclass called Methano- massiliicoccales, is generated by the gut microbiota
tecta (Figure 2 and Table 1). from nutrients and is further converted in the liver
Recently,importantprogresseshavebeendoneon into the pro-atherogenic compound trimethylamine
the characterization of methanogenesis cofactors N-oxide (Brugère et al., 2014). Analyses of human-
(Zhengetal.,2016;Mooreetal.,2017),andenzymes associated Methanomassiliicoccales have supported
(Wagner,2016).Also,anovelpathwayforutilization their role in trimethylamine utilization in the gut but
of methoxylated compounds (methoxydotrophic alsorevealedthatmembersofthetwo maincladesof
methanogenesis) has been discovered in a member Methanomassiliicoccales have contrasting associa-
of Methanosarcinales, with important implications tions with subject health status and microbiota
fordeepsubsurfacemethanogenesis(Mayumi,2016). (Borrel et al., 2017). Many aspects of the biology of
In addition, the diversity of archaea capable of Methanomassiliicoccales remain largely unknown.
methanogenesis appears much larger than pre- For instance, there are currently no genomic data
viously thought, and among the most exciting and no isolate/enrichment culture from the large
discoveries in the archaeal field is the identification diversity of environmental members. This will pro-
of a large number of new lineages of methanogens. vide important information on the role of Methano-
massiliicoccalesintheenvironmentandonthepaths
that led to their adaptation to the human
Methanomassiliicoccales: from deep sediments to the gastrointestinal tract.
human gut
The Methanomassiliicoccales (former Rumen Cluster
C/Rice Cluster III, Table 1) are a novel order of Methyl-dependent methanogenesis: more widespread
methanogens present in various environments such than previously thought
as marine and lake sediments, sewers, soils and also ThetypeofmethanogenesispresentinMethanomas-
animal digestive systems (insects, ruminants, siliicoccales is not an isolated case and as been
humans; Dridi et al., 2012; Paul et al., 2012; Borrel recentlyinferredinanumberofunculturedlineages.
et al., 2013; Söllinger et al., 2016; Raymann et al., The genome sequences from an uncultured novel
2017;Table2).Importantly,theyrepresentthesecond methanogenic lineage, WSA2/Arc1 (Table 1) were
lineage of methanogens, other than the Methanobac- acquired from a wastewater treatment bioreactor
teriales, to include members consistently adapted to (Nobuetal.,2016;Table2).BecauseWSA2/Arc1did
the human gastrointestinal tract (Gaci et al., 2014). not appear to group with any of the previously
TheanalysisofthefirstgenomesofMethanomassilii- known methanogens, it was proposed that they
coccales isolated/enriched from the human gastro- represent a new class, tentatively called ‘Ca. Metha-
intestinal tract showed that they are unrelated to any nofastidiosa’ (Nobu et al., 2016). This is consistent
previously known Class I and Class II methanogens, with our phylogenetic analysis (Figure 2), where
but are rather affiliated to a large clade of non- Methanofastidiosa are robustly placed within a
methanogenic lineages (Borrel et al., 2013, 2014b). potentialnewsuperclass,theAcherontia(seebelow,
In agreement with their placement, the Methano- Table 1). Interestingly, the metabolism inferred
massiliicoccalesdisplayuniquecharacteristics,such from these genomic data indicates absence of
ascompletelackofgenescodingformethanogenesis CO -reducing or aceticlastic methanogenesis, simi-
2
from H +CO and the MTR complex, making them larly to Methanomassiiicoccales, and a potential
2 2
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specializationonmethylated-thiolreductionwithH allows to break the branch leading to Methanopha-
2
(Nobu et al., 2016; Table 2). gales,sofarrepresentedbyasinglegenome,andmight
Moreover, potential new lineages of methanogens clarify the evolutionary processes that led to loss and
have been reported for the first time within the tinkering of methanogenesis (Borrel et al., 2016).
TACK superphylum. Metagenomic analysis has Based on their phylogenetic proximity with Synthro-
highlighted the presence of methanogenesis phoarchaeales MCR homologues, it has been sug-
markers (for example, McrA) in two members of gestedthatBathyarchaeotaMCRmaybeinvolvedina
the Bathyarchaeota, and it has been proposed that similar metabolism (Laso-Pérez et al., 2016), which
they may proceed through reduction of methyl will require experimental demonstration.
compounds by H , like the Methanomassiliicoccales These new data provide a novel view on the
2
(Evans et al., 2015). Genomic data from a second diversity and evolution of methanogenesis and
lineage of putative methanogens with a similar associated metabolisms (for a recent discussion see
metabolism of reduction of methyl-compounds (Borreletal.,2016)).Inparticular,theyhighlightthe
(methylamines, methanol and methylthiols) was widespread distribution and the likely underesti-
obtained from various anaerobic environments mated environmental importance of methyl-depen-
(Table 2) and proposed to represent a new phylum, dent hydrogenotrophic methanogenesis, and
the Verstraetearchaeota (Vanwonterghem et al., question its potential antiquity (Borrel et al., 2016).
2016; Table 1), which robustly cluster with the In addition, they are consistent with the hypothesis
Crenarchaeota (Figure 2). Interestingly, both Ver- of a methanogenic ancestor for the Archaea, and a
straetearchaeota and the potentially methanogenic scenario whereby multiple independent losses/tin-
Bathyarchaeota are predicted to be able to gain kering of this metabolism occurred during archaeal
energythroughmetabolismsotherthanmethanogen- diversification (Raymann et al., 2015), the details of
esis (for example, fermentation of peptides), an which remain to be fully understood.
observation never reported for any previously
known methanogens.
New emerging clades in the archaeal tree
Beyond methanogenesis: variations on a theme The availability of genomic data from previously
Experimental characterization of members of these uncharacterized lineages has allowed identification
novel putative methanogenic lineages is needed to of several interesting new clades.
clarify their role in methane cycling and more
generally in carbon cycling. Indeed, enzymes tradi-
tionallyconsideredasmarkersofmethanogenesis(for The Diaforarchaea: a model clade to study adaptive
example, MCR) can also be used for anaerobic processes in the Archaea
methane oxidation in several ANME lineages Following the availability of genomic data from
(Timmers et al., 2017) and have even been shown to previously uncharacterized lineages, the new super-
catalyse reactions thatdo not involve methane in two class Diaforarchaea was recently proposed (Petitjean
recently characterized strains of a new genus called et al., 2015; Table 1). All Diaforarchaea members
‘Ca. Syntrophoarchaeum’ (Laso-Pérez et al., 2016; sequenced so far share two common characters: the
Table 2). The two ‘Ca. Syntrophoarchaeum’ strains lack of eukaryotic-like histones otherwise largely
wereenrichedfrom gas-richhydrothermal sediments. presentinarchaeaandthefactthattheir16Sand23S
Their genomes contain MCR-like complexes that are rRNA genes are not clustered in the genome
likely used to activate butane toward butyl-CoM, and (Brochier-Armanet et al., 2011; Borrel et al., 2014b).
this intermediate is further metabolized into acetyl- The Diaforarchaea currently contain at least six
CoA by β-oxidation and finally to CO through the well-defined lineages (Figure 2). Other than the
2
methyl branch of the WL pathway (Laso-Pérez et al., already-mentioned Methanomassiliicoccales, they
2016). To perform this novel anaerobic alkane- include: the Thermoplasmatales, which include the
degradation pathway, the two ‘Ca. Syntrophoarch- only known examples of wall-less archaea and
aeum’ strains are dependent on a syntrophic partner, inhabit extreme acidic, hot, solfataric environments,
the sulfate-reducing bacterium ‘Ca. Desulfofervidus andareimportantcontributorstothereleaseoftoxic
auxilii’ (Laso-Pérez et al., 2016). Direct cell-to-cell acid mine drainage into the environment (Bakerand
electron transfer through nanowire and cytochromes Banfield, 2003); the Deep sea Hydrothermal Vent
may occur between ‘Ca. Desulfofervidus auxilii’ and Euryarchaeota group 2 (DHVE-2, Aciduliprofun-
‘Ca. Syntrophoarchaeum’, similarly to what has been dum), making up 15% of the Archaea at hydro-
observed between ANME and sulfate-reducing bac- thermal vents, where they contribute to sulfur and
teria (Wegener et al., 2015; McGlynn, 2017). The two ironcycling(TakaiandHorikoshi,1999;Reysenbach
‘Ca.Syntrophoarchaeum’arerobustlyplacedassister etal.,2006);theMarineBenthicGroupD(MBG-D),a
group to ANME-1 (proposed Methanophagales, class-level lineage abundant in anoxic deep sedi-
Figure2,Table1),andwethereforeproposethatthey ments (for which we suggest the name Izemarchaea,
represent a new order, the Syntropharchaeales Table 1) that has a key role in the global carbon
(Table 1). This placement is important because it cyclingthroughdegradationoforganicmatter(Lloyd
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