The neomuran origin of archaebacteria, the negibacterial root of the universal tree and bacterial

70 Pages·2002·1.32 MB·English

InternationalJournalofSystematicandEvolutionaryMicrobiology(2002),52,7–76 PrintedinGreatBritain
The neomuran origin of archaebacteria, the
negibacterial root of the universal tree and
bacterial megaclassification
DepartmentofZoology, T.Cavalier-Smith
UniversityofOxford,
SouthParksRoad,Oxford
OX13PS,UK
Tel:›441865281065.Fax:›441865281310.e-mail:tom.cavalier-smith!zoo.ox.ac.uk
Prokaryotesconstituteasinglekingdom,Bacteria,heredividedintotwonew
subkingdoms:Negibacteria,withacellenvelopeoftwodistinctgenetic
membranes,andUnibacteria,comprisingthenewphylaArchaebacteriaand
Posibacteria,withonlyone.Othernewbacterialtaxaareestablishedina
revisedhigher-levelclassificationthatrecognizesonlyeightphylaand29
classes.Morphological,palaeontologicalandmoleculardataareintegratedinto
aunifiedpictureoflarge-scalebacterialcellevolutiondespiteoccasionallateral
genetransfers.Archaebacteriaandeukaryotescomprisethecladeneomura,
withmanycommoncharacters,notablyobligatelyco-translationalsecretionof
N-linkedglycoproteins,signalrecognitionparticlewith7SRNAandtranslation-
arrestdomain,protein-splicedtRNAintrons,eight-subunitchaperonin,
prefoldin,corehistones,smallnucleolarribonucleoproteins(snoRNPs),
exosomesandsimilarreplication,repair,transcriptionandtranslation
machinery.Eubacteria(posibacteriaandnegibacteria)areparaphyletic,
neomurahavingarisenfromPosibacteriawithinthenewsubphylum
Actinobacteria(possiblyfromthenewclassArabobacteria,fromwhich
eukaryoticcholesterolbiosynthesisprobablycame).Replacementof
eubacterialpeptidoglycanbyglycoproteinsandadaptationtothermophilyare
thekeystoneomuranorigins.All19commonneomurancharactersuites
probablyaroseessentiallysimultaneouslyduringtheradicalmodificationof
anactinobacterium.Atleast11werearguablyadaptationstothermophily.
Mostuniquearchaebacterialcharacters(prenyletherlipids;flagellarshaftof
glycoprotein,notflagellin;DNA-bindingprotein10b;speciallymodifiedtRNA;
absenceofHsp90)weresubsequentsecondaryadaptationsto
hyperthermophilyand/orhyperacidity.Theinsertionaloriginofprotein-spliced
tRNAintronsandaninsertioninproton-pumpingATPasealsosupportthe
originofneomurafromeubacteria.Molecularco-evolutionbetweenhistones
andDNA-handlingproteins,andinnovelproteininitiationandsecretion
machineries,causedquantumevolutionaryshiftsintheirpropertiesinstem
neomura.Proteasomesprobablyaroseintheimmediatecommonancestorof
neomuraandActinobacteria.Majorgenelosses(e.g.peptidoglycansynthesis,
hsp90,secA)andgenomicreductionwerecentraltotheoriginof
archaebacteria.Ancestralarchaebacteriawereprobablyheterotrophic,
anaerobic,sulphur-dependenthyperthermoacidophiles;methanogenesisand
halophilyaresecondarilyderived.Multiplelateralgenetransfersfrom
eubacteriahelpedsecondaryarchaebacterialadaptationstomesophilyand
genomere-expansion.Theoriginfromadrasticallyalteredactinobacteriumof
neomura,andtheimmediatelysubsequentsimultaneousoriginsof
archaebacteriaandeukaryotes,arethemostextremeandimportantcasesof
.................................................................................................................................................................................................................................................................................................................
ThispaperisanelaborationofpartofaninvitedpresentationtotheXIIIthmeetingoftheInternationalSocietyforEvolutionaryProtistologyinCCeske!
Bude)jovice,CzechRepublic,31July–4August2000.
Abbreviations: ER, endoplasmic reticulum; GlcNac, N-acetylglucosamine; RuBisCO, ribulose-1,5-bisphosphate carboxylase/oxygenase; snoRNP, small
nucleolarribonucleoprotein;TCA,tricarboxylicacid.
01774#2002IUMS 7
T.Cavalier-Smith
quantumevolutionsincecellsbegan.AllthreestrikinglyexemplifyDeBeer’s
principleofmosaicevolution:thefactthat,duringmajorevolutionary
transformations,someorganismalcharactersarehighlyinnovativeandchange
remarkablyswiftly,whereasothersarelargelystatic,remainingconservatively
ancestralinnature.Thisphenotypicmosaicismcreatescharacterdistributions
amongtaxathatarepuzzlingtothosemistakenlyexpectinguniform
evolutionaryratesamongcharactersandlineages.Themixtureofnovel
(neomuranorarchaebacterial)andancestraleubacteria-likecharactersin
archaebacteriaprimarilyreflectssuchverticalmosaicevolution,notchimaeric
evolutionbylateralgenetransfer.Nosymbiogenesisoccurred.Quantum
evolutionofthebasicneomurancharacters,andbetweensisterparaloguesin
geneduplicationtrees,makesmanysequencetreesexaggerategreatlythe
apparentageofarchaebacteria.Fossilevidenceiscompellingfortheextreme
antiquityofeubacteria[over3500millionyears(My)]but,liketheireukaryote
sisters,archaebacteriaprobablyaroseonly850Myago.Negibacteriaarethe
mostancient,radiatingrapidlyintosixphyla.Evidencefrommolecular
sequences,ultrastructure,evolutionofphotosynthesis,envelopestructureand
chemistryandmotilitymechanismsfitstheviewthatthecenancestralcellwas
aphotosyntheticnegibacterium,specificallyananaerobicgreennon-sulphur
bacterium,andthattheuniversaltreeisrootedatthedivergencebetween
sulphurandnon-sulphurgreenbacteria.Thenegibacterialoutermembrane
waslostonceonlyinthehistoryoflife,whenPosibacteriaaroseabout
2800MyagoaftertheirancestorsdivergedfromCyanobacteria.
Keywords: Unibacteria,Actinobacteria,thermophilyandmolecularco-evolutionof
DNA-handlingenzymes,originofN-linkedglycoproteinsecretion,
microbialfossilsandevolution
Introductionandoverview the cell’s structural integrity and its character as a
growing and reproducing organism depend on these
Recent genome sequencing has fostered a simplistic direct physical interconnections. The ability of mem-
view of organisms as essentially aggregates of genes. branes to sequester food, grow and divide underlies
However, organisms are not simply a sum of their cellgrowthandreproduction.Likechromosomes,but
genesnor,assomebiochemistswereoncewonttosay, unlike ribosomes and the skeleton, membranes show
mere bags of enzymes. Genes and enzymes are both directgeneticcontinuity:allaredescendedbygrowth
fundamental, but play their vital roles as parts of and division from those bounding the first cell
highlyorganizedgrowinganddividingcells.Theirlife (Cavalier-Smith, 1991a,b). Membranes have a her-
dependsonamutualisticsymbiosisofgenes,catalysts, editary role as well as structural and physiological
membranes and cell skeleton (Cavalier-Smith, 1987a, roles (Cavalier-Smith, 2000a, 2001). The unity of life
1991a,b, 2001). Co-adaptation between co-operating stems from the common origin and fundamental
notselfishmoleculesisthekeytounderstandingliving similarity of these processes in all organisms.
organisms. The degree to which different cellular Organismal structural diversity, on the other hand,
macromolecules are co-adapted varies greatly; for arises through variations in membrane topology and
many metabolic enzymes, direct co-adaptation in physico-chemical properties as well as in the shapes
structure is low, integration being mediated through formed by the cell skeleton, for both of which the
non-informational intermediary metabolites, but for genicallyspecifiedcatalystscreatethebuildingblocks.
manyinformationalandstructuralmoleculesitishigh. This means that we cannot understand the evolution
Genetic information is made manifest through physi- of life without elucidating the evolution of cell
cal structure. DNA is physically inert–genes do not organization and reproduction as well as that of the
makeorganisms;theygrowbyphysico-chemicalinter- individual molecules that mediate them.
actionsbetweeneffectormacromoleculeswhosestruc-
ture and physico-chemical properties are genetically The most profound difference within the living world
determined. Membranes of lipids with embedded lies between bacteria and eukaryotes (Stanier & Van
proteins are centrally important: chromosomes, ribo- Niel, 1962; Stanier, 1970; Cavalier-Smith, 1987b,
somesandthecytoskeletonphysicallyattachtothem; 1991a,b, 1998). ‘Bacteria’ in this paper is used in the
8 InternationalJournalofSystematicandEvolutionaryMicrobiology52
EubacterialoriginsoflifeandofArchaebacteria
proper traditional sense to embrace all prokaryotes becomestabilized(Woese &Fox, 1977;Woese, 1998,
(Cavalier-Smith, 1992b, 1998; Mayr, 1998), never as 2000; Graham et al., 2000). The second view is that
a fashionable but highly confusing synonym for archaebacteria are not an ancient group at all (Hori
eubacteria only (Woese et al., 1990). Bacteria and et al., 1982) but arose secondarily from eubacteria
eukaryotes differ fundamentally in the topological relatively recently as an adaptation to hyperther-
relationshipsbetweenmembranes,genomesandribo- mophily (Cavalier-Smith, 1987a,b, 1991a,b, 1998;
somes and in their skeletons. In all bacteria, chromo- Forterre, 1996); although not all archaebacteria are
somal DNA and ribosomes making membrane thermophiles, it is argued that their last common
proteins are attached directly to the cytoplasmic ancestor was a hyperthermophile and that it arose
membrane, which grows by the direct insertion of from a eubacterial ancestor by lipid replacement and
proteins and lipids. In eukaryotes, the chromosomes otheradaptations.Here, Ireview recentevidence and
and ribosomes making membrane proteins are at- argumentsthat,in myview, supportcompellinglythe
tached instead to the endoplasmic reticulum (ER)} secondarilyderivednatureofarchaebacteria.Itisnow
nuclear envelope, which is topologically within, and wellestablishedthatarchaebacteriaareeitherancestral
unconnectedto,theplasmamembrane,whichgrowsby to (Van Valen & Maiorana, 1980) or, more likely
fusion of vesicles budded from endomembranes; the (Cavalier-Smith, 1987b), sisters of eukaryotes, with
ER grows, like the bacterial cytoplasmic membrane, which they share many important characters. When
by the direct insertion of individual lipid molecules first proposing that archaebacteria and eukaryotes
synthesized by proteins embedded within the same weresistertaxa,Icalledthecladethatcomprisedthem
membrane. All eukaryotes have a complex endo- neomura (new walls), because I considered that their
skeleton (the cytoskeleton) of microtubules and actin sharedN-linkedglycoproteinswerederivedcompared
filaments that use attached molecular motors to with the ancestral peptidoglycans of eubacteria, ar-
mediate chromosome segregation and cell division, guingthatthefossilrecordimpliedthatneomurawere
respectively.Bycontrast,bacteriahaveanexoskeleton less than half the age of eubacteria (Cavalier-Smith,
(cell wall) important for DNA segregation and cell 1987b). I also asserted that neomura evolved from
division.Therehasbeenmuchdiscussionofhowthese posibacteria by the replacement of peptidoglycan by
and other profound differences between bacteria and N-linked glycoproteins and tentatively suggested that
eukaryotes have arisen (Margulis, 1970; Cavalier- neomuraaremorecloselyrelatedtohigh-G›CGram-
Smith, 1975, 1980, 1981, 1987b, 1990, 1991a,b,c, positivebacteria(thesubphylumActinobacteria)than
1992c,1993,2000b;deDuve,1996;Faguy&Doolittle, to low-G›C Gram-positives (here collectively
1998), updated in a following paper (Cavalier-Smith, grouped with mycoplasmas and their heliobacterial
2002).Theprimarypurposeofthispaperistodiscuss andthermotogaleanalliesasanewsubphylum,Endo-
theoriginsofthelessprofound,buthighlyimportant bacteria).
differencesbetween the threemajor types of bacteria:
This paper reviews recent evidence that very strongly
the structurally simple archaebacteria (Woese &
supports such an actinobacterial origin for the
Fox, 1977) and posibacteria (Cavalier-Smith, 1987b)
neomura and develops the secondary hyperthermo-
and the topologically more complex negibacteria
phily hypothesis of the origin of archaebacteria
(Cavalier-Smith, 1987b).
(Cavalier-Smith,1987a,b)inmoredetail.Acriticalre-
Archaebacteria and posibacteria are bounded by a evaluation of the fossil record in the present paper
single membrane only and are thus referred to col- indicatesthateukaryotesaremuchyoungerthanoften
lectively as unibacteria (Cavalier-Smith, 1998). Negi- thought(Cavalier-Smith,1990)–probablyonlyabout
bacteria, in sharp contrast, are bounded by two 850millionyears(My)old.Thebacterialfossilrecord
topologically distinct membranes; the cytoplasmic clearly indicates that eubacteria are far more ancient,
membrane,intowhichlipidsandproteinsareinserted atleast3500Myold.Datingarchaebacterialoriginsis
directly, and the relatively porous outer membrane more problematic, but I shall argue that, like
thatgrowsmoreindirectlybytheirsubsequenttransfer eukaryotes, they are probably at least four times
across specific adhesion sites between the two. The younger than eubacteria. The present paper also
biogenesis of the negibacterial envelope is more com- severely criticizes arguments and assumptions that
plexandrequiresextrachaperones.Asthecytoplasmic havebeen usedto suggestthat archaebacteriaand}or
membrane of posibacteria and negibacteria is com- eukaryotes may be more ancient than or as old as
posed of acyl ester lipids,like eukaryotic membranes, eubacteria.Thesomewhatrevisedclassificationofthe
they are grouped together as eubacteria, so as to kingdomBacteriaadoptedhereissummarizedinTable
contrast them with archaebacteria, which are unique 1; my reasons for treating all prokaryotes as a single
inthelivingworldinhavingprenyletherlipidsinstead. kingdomBacteria,andwhyeubacteriaarenotaclade
and are preferably not treated as a taxon, were
Two fundamentally different views have been pro-
explained previously (Cavalier-Smith, 1998).
posed of the significance of this and other striking
differences between archaebacteria and eubacteria. My arguments that neomuran and archaebacterial
One influential school of thought regards them as characteristics are all relatively recently derived
ancientdifferencesthatreflectanearlydivergencesoon characters in no way trivializes the importance of the
aftertheoriginoflife,beforemanycellcharactershad numerous differences between archaebacteria and
http://ijs.sgmjournals.org 9
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Revised from Cavalier-Smith (1992a, 1998); thelatter includes aformal descriptionofthekingdomBacteria: Iherevalidate it undertheBacteriological Code by m
designating Enterobacterialesasthetypeorder. Eubacteriaisauseful grade name,but isnot treatedasataxon here. it
h
Taxon Etymology Description Type
Subkingdom1.NEGIBACTERIA*(Cavalier-Smith, ContractionfromL.negativusnegative,sincemoststain Cellboundedbytwoconcentriclipidbilayers,the OrderEnterobacteriales
1987b)subregnumnov. Gram-negative cytoplasmicmembraneandanoutermembranebearing
porins;ancestrallywithpeptidoglycanandlipoprotein
betweenthemembranes;SRPlackshelices1–4and19p;
proteinsecretionpredominantlypost-translational
Infrakingdom1.Eobacteria(Cavalier-Smith,1992a) Gr.eosdawn,becausetheabsenceoflipopolysaccharide Nolipopolysaccharideorsphingolipids;peptidoglycan OrderChloroflexales
infraregnumnov. suggeststheymaybetheearliestnegibacteria withornithine,notdiaminopimelicacid;usually
thermophilic;flagellaabsent;gasvesiclesabsent
Division1.Eobacteria(Cavalier-Smith,1992a)divisio Asforinfrakingdomabove Asforinfrakingdomabove OrderChloroflexales
nov.
Class1.Chlorobacteria(Cavalier-Smith,1992a) Gr.khlorosyellowgreen,fromthecolourofthe Filamentousgreenbacteria,withbacteriochlorophylla OrderChloroflexales
classisnov. photosyntheticspecies andusuallychlorosomes,glidinggreennon-sulphur
photosyntheticbacteria,withphaeophytinquinone
type-2reactioncentres,withorwithoutchlorosomes
(Chloroflexus,Heliothrix,Roseiflexus,Oscillochloris),
andtheircolourlessrelatives,e.g.Thermomicrobium,
Herpetosiphon,Thermoleiophilum,Dehalococcoides(a
Int halorespirer)
er Class2.Hadobacteria(Cavalier-Smith,1992a; Gr.hadeshell,becausetheycanresistextremesofheat Heterotrophicthermophilesorhighlyradiation-resistant OrderThermales
na emend.1998)classisnov. orradiation bacteriawiththickmureinlayer;withsemi-crystalline
tio S-layer,e.g.Deinococcus,Thermus,Meiothermus;more
n closelyrelatedtoeachotheronrRNAtreesthanto
al Chlorobacteria
Jo Infrakingdom2.Glycobacteria*(Cavalier-Smith,1998) Gr.glukussweet,becausetheyhavesurface Outermembranewithlipopolysaccharideor OrderEnterobacteriales
u infraregnumnov. lipopolysaccharide lipooligosaccharide;peptidoglycanwithdiaminopimelic
r
n acidorornithine;gasvesicleswidespread
a
l Division1.Cyanobacteria(Stanier1974)nom.rev. Gr.kuanosblue-green,becauseoftheircommoncolour Oxygenicphotosynthesiswithchlorophylla;flagella OrderChroococcales
o
f (exStanier&Cohen-Bazire,1977asclass) andthetraditionalnameCyanophyceaeorblue-green absent;oftenglide;ancestrallywithphycobilisomes,
Sy algae sometimeslost
st Subdivision1.Gloeobacteriasubdivisionov. FromGloeobacter,theonlyknowngenus Withoutthylakoids OrderGloeobacterales
em Class1.Gloeobacteria(Cavalier-Smith,1998) Asforsubdivisionabove Asforsubdivisionabove OrderGloeobacterales
a classisnov.
tic Order1.Gloeobacteralesord.nov. Asforsubdivisionabove Havingphycobilisomesbutnothylakoids GenusGloeobacter
a Subdivision2.Phycobacteria(Cavalier-Smith,1998) Gr.phukosseaweed,becauseallthetraditionalblue- Withthylakoids;glidingmotilitybyslimesecretion; OrderChroococcales
n
d subdivisionov. greenalgaeandtheprochlorophytesareincluded classicalCyanophyceaeandprochlorophytes.Thefive
E traditionalcyanobacterialorders,alreadyvalidunder
vo theCodeofBotanicalNomenclature,areherealso
lu formallyvalidatedundertheBacteriological(fl
tio Prokaryotic)Code
n Class1.Chroobacteriaclassisnov. FromthegenusChroococcus Unicellular,palmelloid,colonialorwithfilaments OrderChroococcales
a
r lackingheterocysts
y
M Order1.Chroococcalesord.nov Asforclassabove Unicellularandcolonial(non-filamentous)cyanobacteria GenusChroococcus
ic (withphycobilisomesandprochlorophyteswith
ro chlorophyllbinstead
b
io
lo
g
y
5
2
EubacterialoriginsoflifeandofArchaebacteria
Type Pleurocapsa Oscillatoria Nostocales NostocStigonemaSpirochaetales Spirochaetales Cytophagales Cytophagales Chlorobiales Enterobacteriales Planctomycetales Planctomycetales Verrucomicrobiales Chlamydiales Enterobacteriales Enterobacteriales Enterobacteriales
Genus Genus Order GenusGenusOrder Order Order Order Order Order Order Order Order Order Order Order Order
Description Colonialorfilamentous,reproducingbyintramuralmultiplefissiontoyieldsmallerunicellulardispersalstagesUnbranchedlinearfilamentswithoutheterocysts;cellstypicallyshorterthanbroadFilamentsthatmultiplyvegetativelybyhormogonia;usuallywithheterocystsUnbranchedfilamentsBranchedfilamentsWithspiralflagelladrivenbyarotarymotorhavingshaftswithinperiplasmicspace;cellcorkscrewsthroughsemisolidmedia;outermembraneflexible,withlipooligosaccharideinsteadoflipopolysaccharide;organotrophslackingphotosynthesisTreponemaBorelliaAsfordivisionabove(e.g.,LeptospiraLeptonema,)Cytoplasmicmembranewithsphingolipids;outermembranewithlipopolysaccharide;usuallymesophilic;flagellaabsentAerobicheterotrophse.g.Cytophagales(predatory),FibrobacterFlavobacteriaceae,Bacteroidaceae,.FlavobacteriumIncludesanditsrelativesAnaerobicphototrophswithhomomerictype1reactioncentresandchlorosomes.SoleandtypeorderChlorobiumChlorobiales.IncludesandallothergreensulphurbacteriaNegibacteriawithflagellarshaftsoutsidetheoutermembrane;nosphingolipid NegibacterialackingpeptidoglycanplustheirclosestrelativesWithproteinwallsbutnopeptidoglycan;free-living,oftenflagellate,aquaticheterotrophswithbuddingPirellulaGemmatadivision(e.g.,)Prosthecate,free-livingbacteriawithmureinorintracellularparasiteslackingitObligateintracellularenergyparasitesofeukaryotesthatimportalltheirATP;flagellaabsent;peptidoglycanChlamydiaabsent,wallsofprotein()Alwayswithpeptidoglycanandlipopolysaccharide;multifariousrespiratorypatterns;largeinsertioninRNApolymeraseandHsp70Ancestrallyphototrophswithheterodimerictype2acdreactioncentreswithbacteriochlorophyll,andandcarotenoidslocatedinextensivetubularorflattenedmembraneinvaginations;plustheirorganotrophic(heterotrophicormethylotrophic)descendants;usuallywithubiquinonePurplesulphurbacteriaandtheircolourlessheterotrophicormethylotrophicdescendants;oftenbwithbothubiquinonesandmenaquinones;i.e.-Spirillumproteobacteria,e.g.Neisseriaceae,,cRhodocyclusThiobacillus,,Alcaligenaceae,and-proteobacteria,e.g.Chromatiaceae,Pseudomonadaceae,Methylococcaceae,Vibrionaceae,EnterobacteriaceaeEscherichia(e.g.)
Etymology PleurocapsaFromthegenus OscillatoriaFromthegenus hormosgonoshormogoniaGr.cord;Gr.offspring;N.L.hormogonia,becausetheymultiplybyhormogoniaNostocFromthegenusStigonemaFromthegenusSpirochaetaFromthegenus Asfordivisionabove sphiggoGr.strangle,becausetheyhavesphingolipids FlavobacteriumFromthegenus ChlorobiumFromthegenus exoflagellumGr.outside;L.whip,becausetheyincludeallnegibacteriawithflagellarshaftsoutsidetheoutermembraneFromPlanctomycetales,thetypeandbest-knownfree-livingmembersAsforthedivisionabove VerrucomicrobiumFromthegenus ChlamydiaFromthegenus ProteusL.andGr.aseagodabletoassumemanyshapes,referringtothegreatvarietyofbacteriaincludedrhodonGr.rose,becauseallpurplephotosyntheticRhodobacteria,manywithnamesbeginning-,areincluded ChromatiumFromthegenus
able1(cont.) Taxon Order2.Pleurocapsalesord.nov. Order3.Oscillatorialesord.nov. exClass2.Hormogoneae(Thuret1875)classisnov.Order1.Nostocalesord.nov.Order2.Stigonematalesord.nov.Division2.Spirochaetae ClassSpirochaetes Division3.Sphingobacteria(Cavalier-Smith,1987a)divisionov. Class1.Flavobacteria(Cavalier-Smith,1998)classisnov. Class2.Chlorobeaclassisnov. SuperdivisionExoflagellatasuperdivisionov. Division1.Planctobacteria(Cavalier-Smith,1987)divisionov.Class1.Planctomyceaclassisnov. etalClass2.Verrucomicrobiae(Hedlund.,1997) Class3.Chlamydiaeclassisnov. exetalDivision2.Proteobacteria(Stackebrandt.1986asclass)divisionov. Subdivision1.Rhodobacteria(Cavalier-Smith,1987a)subdivisionov. Class1.Chromatibacteria(Cavalier-Smith,1998)classisnov.
T
http://ijs.sgmjournals.org 11
T.Cavalier-Smith
Type Rickettsiales Myxococcales Myxococcales Aquificales Geovibriales Geovibriales GeovibrioAcidobacteriales AcidobacteriumBacillales Bacillales Bacillales
Order Order Order Order Order Order GenusOrder GenusOrder Order Order
}m A;
Description Non-sulphurpurplebacteriaandtheirheterotrophicdescendants;respirerswithubiquinoneshaving10isoprenoidunits,oftenfacultativeaerobes:e.g.RhodobacterCaulobacterRhodospirillaceae,,,MethylobacteriumRhizobiumBartonellaceae,,,Hyphomicrobium,RickettsialesNon-photosyntheticrelatives,possiblysisters,ofRhodobacteria;sulphate-reducingrespirersandtheirorganotrophicrelatives;withmenaquinonesbutnotubiquinoneAnaerobicsulphatereducersortypicallyaerobicDesulfobacteriumorganotrophsorpredators;e.g.,Bdellovibrio,Myxococcales(typeorder)myxobacteria;fruitingglidersHelicobacterOrganotrophs,oftenparasitice.g.,orhydrogen-oxidizinglithotrophs;hyperthermophileswithalkyletherlipidsorthermophileslackingthem(e.g.AquifexHydrogenobacter,) Non-photosyntheticanaerobicrespirersandtheirfermentingdescendants;ofteniron-reducersoroxidizers;rarelysulphatereducersGeovibrioGeobacteriaphylogeneticallyclosertothanto}}}AcidobacteriumFlexistipesDenitrovibrioDeferribacter.}GeovibrioSynergistesNitrospiraMagnetobacteriugroup;;}LeptospirillumThermodesulfovibriogroupAsforclassaboveAcidobacteriumGeobacteriaphylogeneticallyclosertoGeovibrioAcidobacteriumHolophagathanto:e.g.,,GeothrixAsforclassaboveCellboundedbyonlyasinglecytoplasmicmembrane;commonlywithanexternalproteinaceousSparacrystalline-layer;proteinsecretionpredominantlyco-translationalAcylesterlipids;SRPwithhelices1–4;SRPRNAlackshelix6;lackingSRP19p;ancestrallywithmurein;thick-walled(Gram-positive)orthinwalled(Gram-negative);flagellawithacid-solubleflagellinshafts;proteinswithcleavablesignalpeptidessecretedco-translationallyviaSRPorpost-translationallyviaSecNlacking-linkedglycoproteins–i.e.thetraditionalFirmicutesplusMollicutesandTogobacteria›LowGCcontent;withoutproteasomes;ancestrallywithendospores
Etymology alphaGr.thelettera,soastoformalizetheirearlierainformaldesignationas-proteobacteria thionGr.sulphur,becausesulphatereductionmighthavebeentheirancestralphenotype deltaGr.theletterd,toformalizetheircustomaryddesignationas-proteobacteria epsilonGr.theletterepsilon,toformalizethecustomaryedesignationofmostmembersas-proteobacteria geGr.earth,becausemanyareabundantinsoil ferrumL.iron,asmanyreduceit GeovibrioFromthegenusAcidobacteriumFromthegenus AsforclassaboveunusL.one,referringtothealwayssingleboundingmembrane,incontrasttothetwomembranesofNegibacteria positivusAbbreviationofL.positive,becausefourofthesixclassesstainGram-positive endoGr.within,becausesporesareformedwithinanenvelopingforesporecell
able1(cont.) Taxon Class2.Alphabacteria(Cavalier-Smith,1992a)classisnov. Subdivision2.Thiobacteria(Cavalier-Smith,1998)subdivisionov. Class1.Deltabacteria(Cavalier-Smith,1992a)classisnov. Class2.Epsilobacteriaclassisnov. incertaesedisThermodesulfoThiobacteria:-bacteriumSubdivision3.Geobacteriasubdivisionov. Class1.Ferrobacteriaclassisnov. Order1.Geovibrialesord.nov.Class2.Acidobacteriaclassisnov. Order1.Acidobacterialesord.nov.Subkingdom2.UNIBACTERIA*(Cavalier-Smith,1998)subregnumnov. Division1.Posibacteria*(Cavalier-Smith,1987b)divisionov. Subdivision1.Endobacteria(Cavalier-Smith,1998)subdivisionov.
T
12 InternationalJournalofSystematicandEvolutionaryMicrobiology52
EubacterialoriginsoflifeandofArchaebacteria
Type OrderThermotogales OrderBacillales Notypegiven OrderActinomycetales OrderActinomycetales OrderMycobacteriales ActinoplanesGenusMycobacteriumGenusOrderStreptomycetales StreptomycesGenusOrderMethanococcales
n
Description Teichoicacidabsent,stainGram-negative;Speptidoglycanlayerthin;withathinoutermost-layerortogaeasilyconfusedwiththenegibacterialoutermembraneexceptatveryhighresolution;withorwithoutendospores;heterotrophsnotassignedtoSelenomonasSporomusaDictyoglomusorders,e.g.,,,ThermoanaerovibrioCarboxydobrachium,;anaerobicgphotoheterotrophswithbacteriochlorophyll:HeliorestisHeliobacteriumHeliobacteriales,e.g.,Heliophilum;andhyperthermophileswithacyletherThermotogaPetrotogaFervidobacteriumlipids,e.g.,,Thickrigidmureinwallscontainingteichoicacidsandlipoteichoicacid,stainGram-positive;oftenformendospores;anaerobicoraerobicorganoheterotrophs,BacillusStreptococcusStaphylococcusClostridiume.g.,,,Mycoplasmas:noendospores,peptidoglycanorteichoicUreaplasmaAcholeplasmaacids,e.g.,›HighGCcontentwithproteasomes;sporesifpresentusuallyexospores;oftenwithmycothiolinsteadofglutathione;predominantlyaerobic;oftenwithsnappingdivisionorbranchingfilaments;phosphatidylinositolamajorlipid;Gram-positiveCellwallsvaried,usuallylackingdiaminopimelicacid,}usuallywithornithineandorlysine,neverwitharabinose;usuallynon-filamentous,lackingmycothiolorsterols,oftenfacultativeanaerobes;ancestrallywithtwolayeredwallsandsnappingdivision(e.g.ArthrobacterActinomycesPropionibacterium,,,Bifidobacterium)Cellwallswithmeso-diaminopimelicacid,eitherglycineorarabinoseandeithergalactoseorxylose;non-filamentouscellssometimeswithsnappingdivision,e.g.CorynebacteriumNocardia,fragmentingfilaments,e.g.,orbranchedfilamentslackingaerialhyphaee.g.Actinoplanes;frequentlywithmycolicacid,mycothiolandlipid-richwalls;somemakecholesterolMycobacterium();commonlyhavephosphatidylethanolamineWallswithglycinenotarabinoseWallswitharabinoseandgalactose,notglycineTypicallywithdifferentiatedaerialfilamentsandspores;llmesocellwallswithor-diaminopimelicacid,butnoarabinose,galactoseorxylose;aerobeswithmycothiol,StreptomycesFrankiae.g.,;lackphosphatidylethanolamineAsforclassaboveSyn.Mendosicutes(Gibbons&Murray,1978);etalMetabacteria(Hori.,1982):prenylethermembranelipids;signalrecognitionparticleswith7SSRPRNAhavinghelix6thatbindsSRP19p,usedbothformembraneproteininsertionandforallproteisecretion;mureinpeptidoglycan,SecAandHsp90absent;Nco-translationallysynthesized-linkedglycoproteins;flagellarshaftsofacid-stableglycoprotein
Etymology togaL.alooseoutergarment,referringtotheSsometimeslooseouter-layer teichosGr.wall,becausetheirwallscontainteichoicacids actinoGr.ray,becauseoftheiroftenfilamentouscharacterandinclusionofallactinomycetes arthronGr.joint,becauseoftheiroftensnappingArthrobacterdivisionandtheinclusionofthegenus araboN.L.-combiningformofarabic,because,unlikeotherbacteria,theircellsorwallsalwayscontainarabinose,isolatedoriginallyfromgumarabic ActinoplanesFromthegenusMycobacteriumFromthegenusStreptomycesFrom,thebest-knownmembers AsforclassabovearchaeGr.-ancient
as
ble1(cont.) xon Class1.Togobacteria(Cavalier-Smith,1992a)classisnov. Class2.Teichobacteria(Cavalier-Smith,1998)classisnov. Class3.MollicutesEdwardandFreundt1967 exSubdivision2.Actinobacteria*(Margulis1974class)subdivisionov. Class1.Arthrobacteria*classisnov. Class2.Arabobacteriaclassisnov. Order1.Actinoplanalesord.nov.Order2.Mycobacterialesord.nov.Class3.Streptomycetesclassisnov. Order1.Streptomycetalesord.nov.Division2.Archaebacteria(Woese&Fox,1977)divisionov.
a Ta
T
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Table1(cont.) S
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Taxon Etymology Description Type
Subdivision1.Euryarchaeota(Woeseetal.,1990; Gr.eury-broad;Gr.archae-ancient,becausetheyhave Ancestrallywithcorehistones;cellwallsvaried;with OrderMethanococcales
rankCavalier-Smith,1998)subdivisionov. awiderangeofarchaebacterialphenotypes FtsZandeukaryote-likeoligosaccharyltransferase
Superclass1.Neobacteriasuperclassisnov. Gr.neonew;Gr.bakterionrod LargestRNApolymerasesubunitBsplitintotwo OrderMethanococcales
proteins;predominantlymesophiles;cellwallsvaried;
withhistones
Class1.Methanothermea*classisnov. N.L.methano-combiningformofmethane;Gr.therme Methanogenswithwallsofpseudomurein OrderMethanococcales
heat,becausetheyallgeneratemethaneandsomeare (Methanobacteriales)orprotein(Methanomicrobiales,
hyperthermophiles Methanococcales,Methanopyrales);lackingDNA
gyrase;ancestrallywithreversegyrase;sometimes
hyperthermophiles,usuallymesophiles
Class2.Archaeoglobeaclassisnov. FromtheArchaeoglobales,theonlymember Sulphateornitratereducinghyperthermophileswith OrderArchaeoglobales
glycoproteinwalls;withtetraetherlipids,DNAgyrase
andreversegyrase:soleorderArchaeoglobales
Class3.Halomebacteria(Cavalier-Smith,1986) Gr.halssalt;me-commonscientificabbreviationfor Bietherlipids,DNAgyrase;oftenwithcomplex OrderHalobacteriales
classisnov. methane,sincetheclasscomprisesbothhalophilesand carbohydratewalls;lackreversegyrase;mesophilic
somewhathalophilicmethanogens methanogens,Methanosarcinales,unculturedmarine
euryarchaeotesandhalobacteria,Halobacteriales
Superclass2.Eurythermea*superclassisnov. Gr.eury-broad;Gr.thermeheat,becausetheyare Ancestrallywithcellwallsofglycoproteinorprotein; OrderThermococcales
In euryarchaeotesthataremostlyhyperthermophilicor largestRNApolymerasesubunit(B)unsplit;tetraether
te thermophilic lipids
rn Class1.Protoarchaeaclassisnov. Gr.protofirst;Gr.archae-ancient,becausetheyhave Withhistones,reversegyraseandcellwalls;lacking OrderThermococcales
at allretainedtheputativelyancestralarchaebacterial DNAgyrase;hyperthermophiles,e.g.Pyrococcus,
io phenotypeofhyperthermophily,histonesandsulphur Palaeococcus
n
a reduction
lJ Class2.Picrophileaclassisnov. FromthegenusPicrophilus Hyperacidophiles;membraneglycolipidsandDNA OrderPicrophilales
ou gyrase;lackingmethanogenesis,histones,reversegyrase;
rn withcellwall(Ferroplasma,Picrophilus)orsurfacecoat
a (Thermoplasma);sometimesthermophiles
l
o Order1.Picrophilalesord.nov. FromthegenusPicrophilus Asforclassabove GenusPicrophilus
fS Subdivision2.Crenarchaeota(Woeseetal.,1990; Gr.krenspring,fount;Gr.archae-ancient Sulphur-reducingrespiration;withglycoproteinor OrderThermoproteales
ys syn.eocytesLake)subdivisionov. proteincellwalls,reversegyraseandtetraetherlipids;
te lackingFtsZ,eukaryote-likeoligosaccharyltransferase
m andhistones
a
t Class1.Crenarchaeotaclassisnov. Asforsubdivisionabove Asforsubdivisionabove.Thermoproteales, OrderThermoproteales
ic Sulfolobales–highlyacidophilic,Desulfurococcales;
a
n culturedstrainsallhyperthermophiles
d Cenarchaealesord.nov. Gr.kainosrecent;Gr.archae-ancient,becausetheir Mesophilicorpsychrophiliccrenarchaeotes GenusCenarchaeumPrestonetal.1996
E
v non-thermophilyisaderivedconditionfor
o
lu archaebacteriaandtheyincludeCenarchaeum
t Archaebacteriaincertaesedis:candidategroup(possiblyacrenarchaeoteorder)Korarchaeota(Barnsetal.,1996),recentlyculturedhyperthermophilesthattendtobranchmoredeeplyon16SrRNAtreesthanothers
io
n
ar *Probably paraphyletic. The widespread dogma against paraphyletic taxa is misconceived and harmful (see Cavalier-Smith, 1998). The kingdom Bacteria is itself probably
y
M paraphyletic.
ic
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b
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y
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2
EubacterialoriginsoflifeandofArchaebacteria
Table2.Majorarchaebacterialpropertiesnotfoundineubacteria
(a)Neomuranproperties(i.e.thosesharedwitheukaryotes)
1. Signalrecognitionparticle(SRP)with7SRNAwithahelix6thatbindsSRP19protein;proteinsecretiongenerally
co-translational;SecAabsent
2. Co-translationalglycosylationofsurfaceglycoproteinsbytransferofGlcNAcandmannose-containing
oligosaccharidesfromadolicholisoprenoidcarriertoN-asparagine;homologousoligosaccharyltransferases;murein
absent
3. RibosomalrRNApseudouridylatedbyC}D-boxsnoRNAs
4. Corehistoneswithhistonefold[secondarilylostinsomearchaebacteria(e.g.Thermoplasma)andsomeeukaryotes
(dinoflagellates)]
5. ReplicativeDNApolymerasesBtype;inhibitedbyaphidicolin;replicativeslidingclampisPCNA-type,notpartofa
typeCDNApolymeraseholoenzyme;novelreplicationfactorcomplex
6. FlapendonucleaseandRAD2DNA-repairenzymes
7. SevenormoreRNApolymeraseholoenzymesubunits(notfourasineubacteria)
8. ManysimilaritiesofribosomalRNAandproteins;amoresubstantialprojectingbillonthesmallribosomalsubunit;
ribosomesinsensitivetochloramphenicol;anisomycininhibitspeptidyltransferasebybindingto23S}28SrRNA
9. CCT-typegroupIIchaperoninswitheightfoldsymmetry,notsevenfoldsymmetryasintheirdistanteubacterialHsp60
relatives;withbuilt-incap;co-chaperoninHsp10absent;prefoldin(GimC)channelsnascentproteinstothechaperonin
lumen
10. SomesimilartRNAmodification
11. Exosomes;complexof11–16proteinsinvolvedinexonucleolyticdigestionofRNA;exonucleases,helicasesandRNA-
bindingproteins(Kooninetal.,2001)
12. Moresimilarproteinsynthesiselongationfactors(e.g.sensitivetoADPribosylationbydiphtheriatoxin)
13. Co-translationalselenocysteineinsertionrequiresaSECIS-bindingproteininadditiontoaselenocysteine-specific
elongationfactor
14. CCA3«terminusoftRNAaddedpost-translationally,notencodedbythegene
15. ProteinsynthesisinitiatedbymethioninenotN-formylmethionine;severalextrainitiationfactors(eIF-2,2A,2Band
5A)
16. 5«-OH}3«-phosphateprotein-splicedtRNAintronswithhomologousendonucleases
17. NoveltypeIIDNAtopoisomeraseVI}meioticprotein
18. Insertionincatalyticsubunitofthevacuolar-typeproton-pumpingATPase
19. HexamericreplicativeDNAhelicaseMcminsteadofeubacterialDnaB(Poplawskietal.,2001)
(b)Uniquearchaebacterialproperties
1. Prenyletherinsteadofacylesterlipids
2. Flagellarshaftofacid-insolubleglycoproteinsrelatedtopilin,notacid-solubleflagellin
3. DNA-bindingprotein10b
4. UniquetRNAmodifications,includingarchaeosineind-loopandabsenceofqueuine
5. Atinylargesubunitribosomalprotein,LX
6. AbsenceofHsp90chaperone
7. RNApolymeraseAsplitintotwoproteins
8. Glutamatesynthetasesplitintothreeseparateproteins
eubacteria.Althoughthedifferencesinorganizationof that all 19 features listed in Table 2(a) arose in the
the replication, transcription and translation machin- commonancestorofeukaryotesandarchaebacteriain
eryofarchaebacteriaarewellknown(Doolittle,1998; association with the loss of eubacterial peptidoglycan
Graham et al., 2000), the full extent of other major anditsfunctionalreplacementbyneomuranN-linked
differences between archaebacteria and eubacteria in glycoproteins. This part of the neomuran theory is
cell organization is still insufficiently widely appreci- identical to the original, except that the number of
ated, some having only become apparent recently. uniquely shared neomuran character suites has
Table2liststhekeydifferencesbetweenarchaebacteria doubled since the theory was originally proposed
andeubacteria.Thescale of theseis sogreat that this (Cavalier-Smith, 1987b), placing the relationship be-
paper,whichattemptstoexplainthemall,isnecessarily tweeneukaryotesandarchaebacteriabeyondquestion.
longanddetailed.Tohelpthereaderseethewoodfor Tosavespace,Ireferreaderstotheoriginalpaperfor
thetrees,letmeoutlineitsbasicstructure.Ishallargue more details of the basic rationale of the neomuran
http://ijs.sgmjournals.org 15
T.Cavalier-Smith
theory, including the sister relationship of archae- ution of photosynthesis strongly supports earlier
bacteria and eukaryotes (rather than an ancestor arguments that the root of the tree of life lies within
descendant one, as suggested by Van Valen & the negibacteria (Cavalier-Smith, 1987a,b, 1991a,b,
Maiorana,1980;Rivera&Lake,1992;Baldaufetal., 1992b). Although the precise position of the root
1996), the much more ancient ancestral character of remains uncertain, it very likely lies within or im-
eubacteriaandthechangeoverfrompeptidoglycanto mediatelyadjacenttothegreenbacteria,as suggested
glycoproteins,aswellasfordiagramssummarizingthe previously(Cavalier-Smith,1985a,1987a).Ipointout
cellular transformations (Cavalier-Smith, 1987b). thatmanycurrentinterpretationsofcellandmolecular
evolution are fundamentally flawed by the serious
I concentrate here on six things. First are the key misrooting of molecular trees and the misplacing of
innovations of the present paper: the arguments that somelongbranches.Mysixthconcernistoshowthat,
themajorityofthenovelneomurancharactersaroseas although lateral gene transfer is more frequent and
adaptationsoftheneomuranancestortothermophily confusing in bacteria than in eukaryotes, we can still
andthatnearlyallneomurancharacterscanbeusedto constructsensibleorganismalphylogeniesforbacteria,
polarize unambiguously the direction of evolution provided we emphasize organismal features that
fromposibacteriatoneomura,notthereverse.Second depend on strong co-adaptation between macro-
is the argument that, after the neomuran common molecules and do not overemphasize the evidence
ancestor adapted thus to thermophily, the archae- from any single molecule.
bacterial ancestor alone underwent a more extreme
I emphasize that, for most of the history of life,
adaptationtohyperthermophilyandhyperaciditythat
immenselylongperiodsofrelativestasishavefollowed
produced almost all the uniquely archaebacterial
two explosive radiations or ‘biological big bangs’,
characters listed in Table 2(b). About a third of the
each stimulated by revolutionary innovations in cell
paper discusses the origin of each of these neomuran
biology: (i) the origin about 3700My ago of the first
and archaebacterial characters. Having provided ex-
eubacterial cell with peptidoglycan walls and photo-
tensive evidence from comparative biology that neo-
synthesis (Cavalier-Smith, 2001) and (ii) the origin
mura are derived compared with eubacteria, I then
about 850My ago of the ancestral neomuran cell,
discuss the fossil record for all three domains of life,
when N-linked glycoproteins replaced peptidoglycan
which shows exactly the same thing and indicates
and the pre-eukaryote neomurans evolved phago-
that neomura are about four times younger than
trophy, internal skeletons and the endomembrane
eubacteria. Central to my re-evaluation of the fossil
system. The neomuran theory of the origin of
recordisrecentevidencethatsomeactinobacteria,the
eukaryotes is further developed in another paper,
probableancestorsofeukaryotes,makesterols(Lamb
published separately because of space constraints
etal.,1998),whichinvalidatesearlierpalaeontological
(Cavalier-Smith,2002);however,thetwopapersneed
interpretations of fossil steranes as eukaryotic
tobereadtogetherfullytoappreciateandevaluatethis
markers; this and other recent discoveries of mor-
revised neomuran theory of the simultaneous actino-
phologicalfossilsmakemyearlierestimateof850My
bacterial origins of archaebacteria and eukaryotes. A
for the origin of eukaryotes (Cavalier-Smith, 1980)
thirdpaper,ontheoriginofthenegibacterialcelland
more accurate than more recent ones giving an older
the genetic code (Cavalier-Smith, 2001), is com-
date(Cavalier-Smith,1987a,1990).Myfourthtopicis
plementarytoboth,sinceitshowsthatitismucheasier
the application of the ideas of quantum and mosaic
to understand the origin of life if we root the tree
evolution to the interpretation of molecular sequence
among photosynthetic negibacteria, rather than be-
trees. These principles explain many of the puzzling
tween archaebacteria and eubacteria as suggested by
conflicts between different trees. Still more import-
most reciprocally rooted protein paralogue trees.
antly, in conjunction with my discussion of the
evidence for temporarily accelerated evolution I also discuss the early diversification of negibacteria
affecting all the characters of Table 2 at the time of that constituted the first big bang, integrating both
origin of neomura, but not other more ancestral fossil and recent evidence and arguing that the
characters,theytellusthatreciprocallyrootedprotein differences between the six phyla arose primarily as
paralogue trees and single-gene trees (e.g. for rRNA) divergent adaptations within the microlayers of early
basedonthemaresodimensionallydistortedastobe microbialmats.Inadditiontothesephylogeneticand
highly misleading about the temporal history of life; evolutionary questions, I discuss briefly the higher
thishascausedthemisrootingoftheuniversaltreeof classification of bacteria and how it may be improved.
life.Onceweunderstandthesedistortions,wecansee
thatthereisnogenuineconflictbetweenanymolecular
trees and the fossil evidence that neomura are very Secondaryhyperthermophilyandacidophily
recent.Myfifthtopicistousethisnewunderstanding
andtheoriginofarchaebacteria
ofthestrengthsandweaknessesofdifferentmolecular
trees to integrate their evidence with the fossil record Ithas longbeen argued thatthe prenylether lipidsof
andcell-biologicalconsiderationssoastopinpointthe archaebacteria evolved as replacements for the acyl
rootofthetreeasaccuratelyasiscurrentlypossible.I esterlipidsofeubacteria(Cavalier-Smith,1987a,b)as
shall argue that recent evidence concerning the evol- a secondary adaptation to hot, acid environments
16 InternationalJournalofSystematicandEvolutionaryMicrobiology52