Comparative biochemistry of Archaea and Bacteria Wolfram Zillig M a x Planck Institut f~r Biochemie, Martinsried, G e r m a n y This review compares exemplary molecular and metabolic features of Archaea and Bacteria in terms of phylogenetic aspects. The results of the comparison confirm the coherence of the Archaea as postulated by Woese. Archaea and Bacteria share many basic features of their genetic machinery
and their central metabolism. Similarities and distinctions allow projections regarding the nature of the common ancestor and the process of lineage diversification. Current Opinion in Genetics and Development 1991, 1:544--551
Introduction Comparative analysis of 16S rRNA sequences led Woese and collaborators to divide the 'prokaryotic domain' into two 'urkingdoms of life', originally termed eubacteria and archaebacteria. Phylogenetic dendrogrzmls of not only 16S ,and 23S rRNAs but :dso of large components of DNAdependent RNA pol}qllerases, translation factors, and ATPases indicated that each of these two major groups of prokaryotes is coherent and that they are distinct from each other. This distinction between both archaebacteria and eubacteria, and between them and the third group of organisms, the eukaryotes, was confirmed by the groupspecific shaping of homologous features (summarized in Table 1). To emphasize that archaebacteria and eubacteria are ft, ndanmntally different from each other rather than merely two branches of a coherent prokaryotic entity, Woese el al. [1"] recently proposed that the highest taxon level be termed 'domain', rather than 'urMngdom', and that the terms archaebacteria, eubacteria and eukaryotes be replaced by the ,systematic designations Archaea, Bacteria and EttcaD,a.
The Archaea are a holophyletic domain This division of the IMng world as proposed by Woese el al. [1o.], who postulated the holophyletic nature of the Archaea, was questioned by Lake [2-4], who separated the archaebacteria into three phyla: the extreme halophiles, which he combines with the eubacteria tem~ing the combination'photocTtes'; the archaebacteria (this name being reserved exclusively for the methanogens) [2]; and the 'eocytes', which comprised the extremely thermophilic, often sulfur-dependent organisms that were recently temmd Crenarchaeola by Woese et al. [1 °o] and which Lake claimed to be linked to the eukaryotes [3]. The essence of this phylogenetic scheme is the derivation of eubacteria and eukaryotes from different subgroups of Woese's archaebacteria,
which then would have to be considered paraphyletic, that is, not including all their descendants [4]. The validity of the data supporting these claims has been questioned [5-7]. Table 1 shows that the 'photocyte' Halobacterium, the archaebacterium Methanococcus and the 'eocyte' SulJb/obus corresponding to each other in 24 out of 26 sufficiently analyzed homologous features. One of the two exceptions, the RNA polymerase (RNAP) component B split, is a branch character of methanogens and extreme halophiles and does not support Lake's claim. Even the second exception, the gene order in rRNA operons, in which the 'photocyte' lqalobacterium resembles the eubacteria and the 'eocyte' Sulfolobus is grouped with the eukaryotes, does not support bake's assertion because it also links the archaebacterium Methanococcua with Halobacterium. As Lake [7] points out, relating five taxa in a parsimony tree requires 'three and two patterns' (two of the live phyla differ from the other three). Seven of the first eight features listed in Table 1 confront the three Archaea with both the Eucar3pa and the Bacteria and thus yield the archaeal tree. The linkage of the three Archaea to each other in all but two of the listed features, strongly supports the archaeal case by the rules of numeric taxonomy (although each feature by itself does not support construction of a tree). The concept of three domains of life and the coherence of the Archaea is thus not only based on an increasing number of phylogenetic dendrograms but also on the distribution of a growing body of single molecular and biochemical characters.
Archaea, Bacteria and the origin of the Eucarya Of the 26 features listed in Table 1 only the first eight show a domain-specific shaping for the Archaea. The next 14 features link the Archaea to the EucaDpa and only two, genome organization and the occurrence of ribosome binding sites, are shared between Archaea and Bacteria.
Abbreviations GAPDH--glyceraldehyde phosphate dehydrogenase;pol--polymerase; RNAP--RNA polymerase.
544
(~) Current Biolobn/ Ltd ISSN 0959-437X
C o m p a r a t i v e b i o c h e m i s t r y of Archaea a n d Bacteria Zillig
Table 1. Distribution of discrete characters between Bacteria, Eucarya and three phyla of Archaea.
Bacteria E. coli Acylester lipids Fatty acid synthetase Flagellins Isopranyl ether lipids A ' + A" split of RNAP component A(13') RNAP gene order rpoHBA1A2-X-rpsLG Unique modified nucleotides in tRNA Unique sequences flanking rRNA genes 7S RNA RNAP component H corresponds to yeast ABC 27 Kd subunit EF10~ ADP ribosylatable DNAP0~ aphidicolin sensitive Promoter type RNAP type ATP synthase (ATPase) Protein splicing of tRNAs Translation starts with N-formylmethionyl-tRNA CCA end of tRNA encoded RNAP gene order rplKAJLrpoBC Mureine RNAP rifampicin sensitive Ribosome streptomycin sensitive Transcription units Shine Dalgarno sequences B " + B' split of RNAP component B(13) Gene order in rRNA operonl
+ + b
b b F
+ + + + ' + + + + b
Archaea Halobacterium
Eucarya
Methanococcus
Sullolobus
(Eukaryotes)
References
a + +
-a + +
-? + +
+ + e -
[25",62] [25"',62] [631 [25"',62] [12",13"1
+
+
+
-
[12"" 13"']
+
+
+
-
[64"']
+
+
+
-
[65.1
+
+
+
+
[15oi
+
+
+
+
[13"]
+ + d c V (+ )
+ + d c V ?
+ + d c V +
+ + d c V (+ )
[66] [67] [14"] ll 2"'l
-
-
-
168--1 [69,701
. . .
. . .
. . .
. . .
[46] [461 [46]
. . + +
. .
. . + +
. .
[46] [46] [46] [46] [12"'l
+ b
+ b
+ +
-
c
e
[461
"Except myocoplasma, tb = rrs, ala, rrl, rrf; c = rrs, rrl (rff unlinked), a, Archaeal; b, bacterial; c, complex; d, box A--boxB; e, eucaryal.
Most of the features listed in Table 1 are associated with the genetic machinery. Amino acid sequences of archaeal ribosomal proteins [8°'], a histone of Methanothennus fervidus [9..], translation factors [10--,11.], RNAP components [12..,13.-], standard promoters [14.-], and also ATP synthase, the central enzyme of energy conservation by electron transport phosphorylation [15",16"], often show striking sequence similarities to their eucaryal rather than to their bacterial counterparts. In contrast, Bacteria and Eucarya strongly resemble each other in the sequences of several enzymes of glycolysis and central metabolism, for example, glyceraldehyde phosphate dehydrogenase (GAPDH) [17], phosphoglycerate kinase [18.] and malate dehydrogenase [19"], whereas the archaeal versions of these enzymes show less similarity, both to their bacterial and to their eucaryal homologs. The large components of the singular archaeal RNAPs exhibit high similarity to the corresponding subunits of two of the three specialized eucaryal RNAPs, polymerase (pol)2 and po13, but only low similarity to the third, poll [20]. Phylogenetic trees constructed using various algorithms show po12 and po13 in the immediate neighbor-
hood of the Archaea, but poll at a significant distance, sharing a bifurcation with the Bacteria [12.',21]. A possible explanation for the absence of a stem shared by the three eucaryal RNAPs is that the urkaryote, the ancestor of the Eucar3,a, arose by some sort of fusion event between an archaeal and one or several (possibly bacterial) ancestors, such that the po12 and po13 large-component genes were derived from a prearchaeal ancestor and the poll genes from another (possibly prebacterial) gene donor (Fig. 1) [12"]. The presence of 'bacterial' genes beside 'archaeal' ones in Eucar)pa would thus be explained by the chimaeric nature of the eucaryal nuclear genome. As the GAPDH of Giardia lamblia, a eukaryote devoid of mitochondria, and which is presumed to be primitive, also resembles bacterial GAPDHs [17], these 'bacterial' genes should logically have been acquired earlier than the ancestors of the mitochondria. One of the most remarkable recent achievements in molecular phylogeny is the rooting of phylogenetic trees of ATPase components and translation factors by determining the intersection of dendrograms of genes that
545
546
Gene organization and evolution
(a)
Eucarya
Archaea
' ~~
X
Bacteria
y-Mit°ch°ncl'rina Primary oisuf
Common ancestor
(b)
(b') Archaea
Eucarya
Bacteria
Archaea
Common ancestor
Eucarya X
Bacteria
Common ancestor
arose by duplication/diversification, presumably before first interdomain ramification (i.e. pairs of paralogous genes present in all three domains) [10.o,22,23]. In both the case of ATPase components and the case of elongation factors EFI~ and EFII, the Bacteria branched off first, followed by a ramification of Archaea and Eucarya. One should keep in mind, however, that this is the phylogeny of genes rather than organisms, and that this result could be compatible with the occurrence of the opposite branching order for 'bacterial' genes of Eucarya, in which the Archaea branch off before a bifurcation of Bacteria and Eucarya. Superposition of both types of single gene phylogenies would yield the fusion tree represented in Figure 1.
Features shared by Archaea and Bacteria
The distinct nature of the Archaea is characterized by aspects of the genetic machinery, electron transport phosphorytation, and lipid structure and biosynthesis. Although the presence of straight chain fatty acids and of
Fig. 1. (a) Schematic representation of the genesisof the Eucarya by a fusion of Archaea and Bacteria. The dendrograms in the lower part of the figure are typical phylogenetic trees of (b) archaebacterial and (b') eubacterial genes of Eucarya,the superposition of which yields the upper dendrogram. Where one fusion partner arose from an already diversified bacterial lineage, X denotes extant representatives of that lineage, which appear on the lowest branch of the Eucarya,rather than among the other Bacteria.
fatty acid synthetase has been reported in Archaea [24], the small enzymatic activity associated with Halobacterium is salt sensitive and recent attempts to prove the presence of fatty acids in Archaea failed completely (M De Rosa and A Gambacorta, personal communication) [25"]. As discussed by Danson [26], many other metabolic capacities are shared either by Archaea and Bacteria, or by certain phyla in either domain. Thus, methanogens, like many Bacteria, appear to use the Embden-Meyerhof pathway of glycolysis in both directions. Extreme halophiles, Sulfolobus and Tbermoplasma use a version of the early steps of the Entner-Doudoroff pathway of glucose catabolism, employing non-phosphorylated rather than phosphorylated intermediates. Again, certain Bacteria follow the same path. It has been found that different versions (aerobic/anaerobic, oxidative/reductive, complete/interrupted) and parts of the citric-acid cycle are expressed in different Archaea and Bacteria. In both Archaea and anaerobic Bacteria 2-oxo-acid oxidoreductases occur. Although the 2-oxo-acid dehydrogenase multi- enzyme complexes present in aerobic Bao
Comparative biochemistry of Archaea and Bacteria Zillig 547 teria have not been found in Archaea, their component dihydrolipoamide dehydrogenase has been found in extreme halophiles.
lishing several complex features of this type in different Arcbaea and Bacteria is needed to elucidate whether horizontal gene transfer occurred.
Principles and components of electron transport phosphorylation have been discovered in Arcbaea, although their respiratory chains appear primitive [27°.]. Both the Archaeum Sulfolobus and the Bacterium Thiobacil/us oxidize sulfur. Both the Archaeum Archaeoglo&us [28] and certain Bacteria reduce sulfate for energy conservation. Representatives of the ¢t-group of purple bacteria and certain methanogens [29,30"] are able to fix molecular nitrogen. Like sulfur-dependent, extremely thermophilic Archaea of the branch Crenarchaeota and the order Thermococcales, certain Bacteria use sulfur as the terminal electron acceptor, although in contrast to some Archaea [31"'] they do not seem to be able to couple this to autotrophic CO x fixation. Reverse gyrase has not only been found in extremely thermophilic Archaea [32], Crenarchaeota and Euryarchaeota, but also in the extremely thermophilic Bacterium Thermotoga [33"'].
In both Archaea and Bacteria, many genes are organized in transcription units of often similar gene composition (for review see [46])[47"-49,50"-53"]. The similarity of this organization between the two domains indicates a common origin. Operons certainly alleviate the control of expression of correlated genes. Linkage of such genes could, however, also be advantageous in genome evolution. Highly similar transcription units map in different contexts in the chromosomes of Archaea and Bacteria (for example, see [12"]), indicating independent arrangement or extensive rearrangement of gene clusters within coherent circular genomes during the diversification of the domains. Different single genes are absent in corresponding gene clusters of different Archaea, for example in archaeal 'strep operons' (cited in [12.-] ). Complete separation of rRNA genes has been found in Therrnoplasma [54"]. These data are in line with the hypothesis that genomes were originally composed, and later under certain conditions supplemented, by the recombinative joining and addition, respectively, of sets of genes once or still available. For example, the genes could be donated by a common pool of plasmids in a manner similar to the virus modules of Campbell and Botstein [55], or they could occur as accessory DNA elements able to enter the chromosome [56]. The unique metabolic capacities found in isolated bacterial and archaeal phyla could thus have been acquired from this unidentified pool by unknown modes of transfer and recombination.
Gas vacuoles exist in Halobacteria and several Bacteria. The structural proteins of these organelles in I-L. halobium and Cyanobacteria are strikingly similar [34"]. Homologous superoxide dismutases have been discovered in Bacteria and Archaea [35], including the anaerobic archaebacterium Methanobacterium thermoautotrophicum [36"]. The ability of a particular group of Archaea, the methanogens, to exist autotrophically by gaining energy through methanogenesis appears to be unique, although the mode of energy conservation in this pathway resembles in principle other ATP synthesis processes that are membrane associated and proton driven [37"',38",39"']. In contrast, however, 13-galactosidases discovered in Sulfolobus [40] appear to be unrelated to the enzyme of E. coli. The gene described by CubeUis et al. [41.] has been isolated from S. solfataricua strain MT4. The homologous, yet strikingly different, gene described by Little et al. [40] could stem from a contamination of DSM 1616 by S. acidocaldarius [42°]. Capacities shared by isolated phyla in both domains could have belonged to the repertoire of the common ancestor of Archaea and Bacteria and were possibly lost during lineage diversification in all but the particular taxa still possessing them. As several of these features are complex, the genome of the common ancestor should have been significantly larger than those of present members of both domains, the genomes of which range around 3 x 96bp [43]; (Klenk, Diploma thesis, Eberhard-Karls-UniversRy, Tf~ingen, 1986). Alternatively, it is possible that the sharing of such metabolic capacities by particular phyla in both domains could at least, in some cases, have resulted from horizontal gene transfer. In the case of the nlfgenes, where sequences for comparison are available, the phylo genetic tree appears to contradict this hypothesis [44]. Because for ferredoxins [45] and gas vacuole proteins [34"] the sequences of only two phyla (Halobacteria and Cyanobacteria), one from each domain, were compared, phylogenetic dendrograms could not be constructed. The cloning and sequencing of genes involved in estab-
The nature of the common ancestor The features shared by Arcbaea and Bacteria testify to the existence of a highly developed intermediary metabolism including glycolysis, gluconeogenesis, the citric acid cycle [26], electron transport phosphorylation (for example, see [37"]) and even elements of respiratory chains [19"'] in the common ancestor of both domains. This ancestor should thus have possessed a large set of enzymes sufficient for autonomous existence and also the molecular components necessary for their accurate manufacture (e.g. a DNA genome, RNA polymerase, and ribosome-binding sites for the initiation of translation) [46]. It was thus not the progenote of Woese and Fox [57], in which inaccurate (not yet fully developed) gene expression and genome replication should have excluded the synthesis of large specific enzymes [67], but rather an already strikingly perfect genote, that is, an organism equipped with a fully developed gene replication and expression system. Even the organization of transcription units was principally complete, although their context (linkage) within a single circular genome was possibly not yet established (see above). By possessing a genome consisting of unlinked gene clusters, the common ancestor would conform to a second important characteristic ascribed to the progenote by Woese [58]. As exemplified by characteristic differences, for example in the transcription apparatus (including the structure of RNAP and promoters and their interaction [14-,]) parts
548
Gene organization and evolution of the genetic machinery were, however, not yet fully established. Among other domain specific features, the apparently absolute inability of Archaea to synthesize fatty acids and fatty acid ester lipids (see above) is most conspicuous. In contrast, the basic biosynthetic pathways of polyisoprenoid compounds are shared by Bacteria and Arcbaea [25"'], although Bacteria cannot synthesize ether lipids because they lack the ability to join isopranyl residues to glycerol [59,60], to completely reduce the linked residues and to condense the heads of two C20 chains to fore1 a C40 compound. The primeval membrane was therefore probably neither of the isopranyl-ether nor of the fatty-acid-ester type, but was rather, for example, a membrane of protein. The capacity, to s'ynthesize fatty-acid-ester lipids would then have been an achievement of the ancestral Bacteria, which donated it to the Eucaopa; the ancestral Ardaaea inventing isopranyl-ether lipids instead. The absence of lineages going back to transitional fomas between Archaea and Bacteria indicates that starting lineages probably required irreversible changes, possibly isolation of individuals, ending the phase of transition from the conmaon ancestor to the already distinctly diversified ancestral Archaea and Bacteria. It seems that extensive gene sharing, already postulated as a third characteristic of the progenote suggested by Woese [61], prevented lineage separation in two isolated, rapidly evolving populations of progenotes that finally became separated by the increasing incompatibility of their transcription systems. The fomaation of strong barriers between individuals within each population, for example by changes in the quality of their membranes, could then have ended the phase of ancestral communication, thus preparing the stage for speciation. This ancestral communication should have effected rapid joint evolution by making rare or nmtatect gene clusters (plasmids?) available as a common gene pool to all individuals throughout the progenote population. This pool should have consisted of two fractions: a set of house-keeping genes required for the autonomous existence of each individual; and a fraction of rare gene clusters encoding special capacities present only in small subpopulations. The transfer of the latter would have ensured survival in a changing environment. The genetic fixation of the genes should have occurred by the development of the communication barriers discussed above, concomitant with the linkage of gene clusters into coherent genomes. The superiority of the resulting true genotes, for example in maintaining their gene stocks, would then have ended the age of progenotes. Although the details of these ideas are still speculative, aspects of them appear as rather compelling interpretations of the comparative biochemistry/molecular genetics of the domains. The details may unfold with the growing understanding of the molecular similarities and differences between the domains.
three domains of life, enables extrapolations to the early evolution of organisms and the nature of the common ancestor. The Arcbaea have facilitated our understanding of evolution, both by being distinct in certain features as well as by sharing fundamental capacities with the Bacteria. Their coherent circular genomes are composed of gene clusters resembling those found in Bacteria, although the order in which these clusters are linked appears to differ, indicating two independent processes of chromosome formation. This implies that the common ancestor of Arcbaea and Bacteria, "although possessing an almost fully developed metabolic and genetic machinery, did not initially have a coherent genome. That and other projections, for ex~unple, the differences of transcription signalling and lipid structure, bring early biotic evolution in the progenote state into focus.
Acknowledgements Due to limitations of space this review' is unable to reference the literature prior to 1990 in flail. 1 would like to apologise to those whose work I have not been able to acknowledge.
References and recommended reading Papers of speci:d interest, published within the annual peri(x.t of review, have been highlighted -ts: • of interest • ,, of ot, tstanding interest 1. .,
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4.
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5,
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Conclusion The discovery of the Arcbaea by Woese and collaborators and the comparison of corresponding features in the
ee
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SANDMANK, KRZYCK] JA, DOBRINSK] B, LtmZ R, REEVE JN: HMf, a DNA-binding Protein Isolated from the Hyperthermophilic Archaeon M e t h a n o t h e r m u s fervidus, is Most Closely Related to Histones. Proc Natl Acad Sci U~Cel 1990, 87:5788-5791. Demonstrates that Ard2aea contain DNA-binding proteins homologous to eucaryal histones. 10. ••
HASEGAWAM, IWABEN, MIIKOHATAY, MIYATAT: Close Evolutionary Relatedness of Archaebacteria. Methanococcus and Halobacterium, to Eukaryotes Demonstrated by Composite Phylogenetic Trees of Elongation Factors EF-Tu and EF-G. Eocyte Tree is Unlikely..lpn .1 Genet 1990, 65:109-114. One of two phylogenetic dendrognmls of genes rooted by intersection of the trees of pandogous proteins. The other case was reported independently byJP Gogarten el al. and N lwabe el al., in 1989. CRt-.'TIR, CITAREIJA F, TIBONI O, SANANGEIANTONIA, PALM P, CAMbkkRANOP: Nucleotide Sequence of a DNA Region Comprising the Gene for Elongation Factor let (EF-100 from the Ultrathermophilic Archaeote Pyrococcus woesei: PbyIogenetic Implications. J Mol Evol 1991, in press. The phylogenetic tree of EFI cc confimls the coherence of the Arcbaea.
19. ••
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11.
•
12. **
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KLENKH-P, PA~t P, [D'I=I'SIq'.'ICHF, ZIIJJG W: Component of the DNA-dependent RNA Polymerases of A r c h a e a is Homologous to a Subunit Shared by the Three Eukaryal Nuclear RNA Polymerases. Proc Natl Acad Sci USA 1991, in press. Demonstrates that archael RNA pob,merases resenable the eucaryal enzymes not only in their large component, hut also in a small subunit. 14. •,
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18. •
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25. .•
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27. ..
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30. •
StBou) L, HENRIQUETM, POSSOT O, AUBERTJ-P: Nucleotide Sequence of niflt Regions from M e t h a n o b a c t e r i u m i v a n o v i i and M e t h a n o s a r c i n a b a r k e r i 227 and Characterization of glnB.Like Genes. Res Microbiol 1991, 142:5-12. Only certain methanogenic Arcbaea and certain Bacteria share m f genes, which are not present in the other Arc&tea and Bacteria. 31. ••
AI).~Is MWW: The Metabolism of Hydrogen by Extremely Thermophilic, Sulfur-dependent Bacteria. FEMS Microbiol Revs 1990, 75:219--238. The first thorough treatise of a fundanmntal life style of a group of Archaea. 32.
BOtrI'HIER DE LA TOUR C, PORTEMER C, NADAL M, STETTER KO, FORTERRE P, DUGUET M: Reverse Gyrase, a Hallmark of the Hyperthermophilic Archaebacteria. J Bact 1990, 172:6803-6808.
33. ••
BOUTHIERDE LA TOUR, PORTEMER C, HUBER R, FORTERRE P, DUGUETM: Reverse Gyrase in Thermophilic Eubacteria. J Bact 1991, 173:3921-3923.
549
550
Gene organization and evolution A hallmark of hyperthermophilic Archaea is a general feature of hyperthermophiles including the Bacterium 7bemnotogct ENGLERTC, HORNE M, PFEn:ER F: Expression of the Major Gas Vesicle Protein Gene in the Halophilic Archaebacterium Haloferax mediterranei is Modulated by Salt. Mol Gen Genet 1990, 222:225-232. Describes the control of gas vesicle .synthesis in extreme halophiles.
48.
34. •
35.
MAY BP, DENNIS PP: Unusual Evolution of a Superoxide Dismutase-like Gene from t h e Extremely Halophilic Archaebacterium Halobacterium cutirubrum. J Bact 1990, 172:372%3729.
36. •
TAKAO M, OIKAWA A, Y,Lc,UI A: Characterization of a Superoxide Dismutase Gene from the Archaebacterium Methanobacterium thermoautotrophicurrL Arch Biocbem Biopt2vs 1990, 283:210-216. Shows that the anaerobic M. thermoautotropbicum contains superoxide dismutase.
ARNDTE, KROMERW, HATAKEWAMAT: Organization and Nucleotide Sequence of a Gene Cluster Coding for Eight Ribosomal Proteins in the Archaebacterium Halobactertum marismortui. J Biol Chem 1990 265:3034-3039.
49.
ARNm"E, WEIGEL C: Nucleotide Sequence of the G e n e s Encoding the LII, L1, LIO and LI2 Equivalent Ribosomal proteins from the Archaebacterium Halobacterium marismortui. Nucleic Acids Res 1990, 18:1285. An archaeal gene cluster comprising the ribosomal protein genes linked in E colt in tile L7 operon. 50. ..
AUERJ, SPICKER G, MAYERHOFER L, POHLER G, BOCK A: Organization and Nucleotide Sequence of a Gene Cluster Comprising the Translation Elongation Factor 10t From Sulfolobu$ acidocaldarius. S),tem Appl Microbiol 1991, 14:14-22. Thorough analysis of :m example of an archaeal transcription unit. This excellent piece of work comes from one of the leading groups in the field.
37. **
DEPPENMEIERU, BLAUT M, MAHI2dANNA, GOTTSCHALKG: Reduced Coenzyme 1:42o: Heterodisulfide Oxidoreductase, a Proton-translocated Redox System in Methanogenic Bacteria. Proc Nail Acad Sci USA 1990, 87:9449-9453. The breakthrough in understanding how methanogenesis and proton translocation for energy conservation are coupled.
DENDAK, KONISHIJ, FIAJIRO K, OSHINIA T, DATE T, YOSHIDA M: Structure of an ATPase O p e r o n of an Acidothermophilic Archaebacterium, Sulfolobus acidocaldarius. J Biol Cbem 1990, 265:21509-21513. The first analysis of an archaeal ATPase operon. This operon from Sulfolobus resembles that of E. colt in composition and context.
38. •
52. ..
DEPPENMEIER U, BLAUT M, MAHLMANN A, GOTIBCHAI~ G: Membrane-bound F420H2-Dependent Heterodisulfide Reductase in Methanogenic Bacterium Strain GO 1 and Methanolobus tindarius. FEBS Lett 1990, 261:199-203. Describes a proton tmnslocating redox system coupled to methanogenesis. 39. ••
DEPPENMEtERU, Bbxtrr M, GO'I'rSCHALKG: H2: Heterodisultide Oxidoreductase, a Second Energy-Conserving System in the Methanogenic Strain G61. Arch Microbiol 1991, 155:272-277. Describes in detail a second proton translocating redox system coupled to methanogenesis (also see [38•*]). 40.
LITTLES, CARTWRIGHTP, CAMPBELLC, PRENNETAA, MCCHESNtD" J, MOUNTAINA, ROBINSON M: Nucleotide Sequence of a Thermostable ~-Galactosidase from Sulfolobus solfataricus, Nucleic Acids Res 1989, 17:7980.
41. •
CUBELIaSMV, ROZZO C, MONTECUCCHIP, ROSSt M: Isolation and Sequencing of a N e w [3-Galactosidase-encoding Archaebacterial Gene. Gene 1990, 94:89-94. Shows that a [3-G-alactosidase from the Arcbaeum S. solfataricu.~ is not homologous to the enzyme from E. colt.
GROGAND, PALM P, ZILL/G W: Isolate B12, w h i c h Harbours a Virus-like Element, Represents a New Species of the Archaebacterial G e n u s Sulfolobus, Sulfolobus shibatae sp. nov. Arch Microbiol 1990, 154:594-599. Description of lysogeneic Archaeum S. shibatae, which harbours the virus SSV1 as a prophage.
51. ..
HORNE M, ENGLERT C, WIMMER C, PFEIFER F: A DNA Region of 9 kbp Contains all G e n e s Necessary for Gas Vesicle Synthesis in Halophilic Archaebacteria. Mol Microbiol 1991, 5:1159-1174. A thorough analysis of this complex gene cluster, which is involved in gas vesicle synthesis and contains three transcription units comprising 14 genes. 53. ..
PALM P, SCHLEPER C, GRAMPP B, YEATS S, MCWILLIAMP, REITER W-D, ZILLIG W: Complete Nucleotide Sequence of the Virus SSV1 of t h e Archaebacterium Sulfolobus sbibatae. Virolog), 1991, 185, in press. First completely sequenced genome of an archaeal virus that is organized in transcription units. 54. •
REE HK, ZIMME~tANN RA: Organization and Expression of the 165,235 and 55 Ribosomal RNA G e n e s from the Arc h a e b a c t e r i u m Thermoplasma acidophilum. Nucleic Acids Res, 18:45, 44171-4478. Shows that the rRNA genes of T. acidophilum are not linked. 55.
CAMPBELLA, BOTSTEIN D: Evolution of the Lamboid Phages. In Lambda 11 edited by Hendrix RW, Roberts JW, Stahl FW, Waisberg RA [book]. New York: Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press, 1983.
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CAMPBELLA: Evolutionary Significance of Accessory DNA Ele m e n t s in Bacteria. Annu Rev Microbiol 1981, 35:55-83.
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WOESE CR, FOX GE: T h e C o n c e p t of Cellular Evolution. J Mol Et,ol 1977, 10:1-6.
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WOESE CR: 51:263-264.
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KAKINUNIAK, YAMAGISHI M, FUJIMOTO Y, IKEKAWAN, OSHIMA T: Biosynthetic Mechanism of sn-2,3-Di-O-phytanylglycerol, Core Membrane Lipid of the Archaebacterium Halobacterium halobtum. J Am Cbem Soc 1990, 112:2740-2745.
60.
KAKINUMAK, OBATAY, MATSUZAWAT, UZAWAT, OSHIMAT: T h e Stereochemical Fate of Glycerol During t h e Biosynthesis of Membrane Lipids in Thermoacidophilic Archaebacteria Sulfolobus acidocaldartus. J Cbem Soc Cbem Commun 1990, pp 92%927.
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WOESE CA: Archaebacteria and Cellular Overview. Zbl Bakt Hyg I. Abt Orig C3:1-17.
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KATESM, KUSHWAHA:In Energetics a n d Structure of Halophilic Microorganisms edited by Caplan SR, Ginsburg M [book]. Amsterdam/New York: Elsevier/North-Holland Biochemical Press, 1978, pp 461-480.
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SAPIENZAC, DOOLrI'n.E WF: Unusual Physical Organization o f the Halobacterium G e n o m e . Nature 1982, 295:384--389.
44.
HENNECKE H, KALUZA K, THONY B, FUHRMANN M, LUDWIG W, STACKEBRANDTE: C o n c u r r e n t Evolution of Nitrogenase G e n e s and 16S rRNA in R h i z o b i u m Species and o t h e r nitrogen Fixing Bacteria. Arch Microbiol 1985, 142:342-348.
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HASE T, WAKABAYASHIS, MATSUBARAH: Halobacterium halob i u m ferredoxin. An H o m o l o g o u s Protein to Chloroplasttype Ferredoxins. FEBS Lett 1977, 77:308-310. ZILUGW, PAInt P, REITERW-D, GROPP F, PUHLER G, KLE.NKH-P: Comparative Evaluation of Gene Expression in Archaebacteria. Eur J Biochem 1988, 173:473--482.
ARNDTE: Nucleotide Sequence of Four G e n e s Encoding Ribosomal Proteins from the 'SlO and Spectinomycin' O p e r o n Equivalent Region in t h e Archaebacterium Halobacterium marismortui. FEBS Lett 1990, 267:193-198. Archaeal gene clusters comprising ribosomal protein genes linked in E. colt in the $10 and the spc operons.
Bacterial
Evolution.
Microbiol
Revs
1987,
Origins:
an
Comparative biochemistry of Archaea and Bacteria Zillig 63.
KALMOKOFFME, KARNAUCHOWTM, JARRELL KF: Conserved NTerminal Sequences in the Flagellins of ArchaebacteriaBiochem Biophys Res Commun 1990, 167:154--160.
67.
EDMONDSCG, CP,AIN PF, GUPTA R, HASHmUMET, HOCART CH, KOWAIAKJA, POMERAN'IT.SC, STEWI'ERKO, McCLOSKEYJA: Posttranscriptional Modification of tRNA in Thermophilic Archaea (Archaebacteria). J Bact 1991, 173:3138-3148. A thorough comparative analysis of the patterns of modified nucleotides present in tRNAs of tile three domains of life, showing few unique feanares of Arcbaea, and s o m e modifications typical for life at high tempemnare. The first comparison of this feature in the three domains of life.
68. .•
64. ,,.
65. •
KJEMSJ, GARRE'rr RA: secondary Structure Elements Exclusive to the s e q u e n c e s Flanking Ribosomal RNAs Lend Support to the Monophyletic Nature o f the Archaebacteri:L J Mol Evol 1990, 31:25-32. Further evidence supporting the coherence fo the Ardmea. 66.
GEHRMANNR, HENSCHEN A, POSTULKAW, KLINK F: Comparative Studies on Structure and Function of Archaebacterial Elongation Factors Indicate the Phylogenetic Diversity of the Urkingdom. Sl*tem Appl Microbiol 1986, 7:115-122.
ZABEL H-P, HOLLER E, WINTER J: Mode of Inhibition o f t h e DNA Polymerase of Methanococcus vannielii by Aphidicolin. Eur J Biocbem 1987, 165:171-175.
IHARAK, MUKOHATAY: T h e ATP Synthase of Halobactertum s a l i n a r i u m ( h a l o b t u m ) is an Archaebacteria/ Type as Revealed from the Amino Acid S e q u e n c e s of its T w o Major Subunits. Arch Biochem Biopbys 1991, 286:111-116. Another argument for the phylogenetic position of Halobacterium v~thin the Arcdmea. 69.
K2dNEBP: Intron-containing tRNA G e n e s o f Sulfolobus solfataricu£ J Mol Evol 1987, 25:248--254.
70.
WICH G, LEINFELDER W, BOCK A: G e n e s for Stable RNA in the Extreme Thermophfle Thermoproteus tena• lntrons and Transcription S i g n a l s . . ~ I B O J 1987, 6:523-528.
W Zillig, Max-Planck-lnstitut fOr Biochemie, 138033 Martinsried, Germany.
551
and their central metabolism. Similarities and distinctions allow projections regarding the nature of the common ancestor and the process of lineage diversification. Current Opinion in Genetics and Development 1991, 1:544--551
Introduction Comparative analysis of 16S rRNA sequences led Woese and collaborators to divide the 'prokaryotic domain' into two 'urkingdoms of life', originally termed eubacteria and archaebacteria. Phylogenetic dendrogrzmls of not only 16S ,and 23S rRNAs but :dso of large components of DNAdependent RNA pol}qllerases, translation factors, and ATPases indicated that each of these two major groups of prokaryotes is coherent and that they are distinct from each other. This distinction between both archaebacteria and eubacteria, and between them and the third group of organisms, the eukaryotes, was confirmed by the groupspecific shaping of homologous features (summarized in Table 1). To emphasize that archaebacteria and eubacteria are ft, ndanmntally different from each other rather than merely two branches of a coherent prokaryotic entity, Woese el al. [1"] recently proposed that the highest taxon level be termed 'domain', rather than 'urMngdom', and that the terms archaebacteria, eubacteria and eukaryotes be replaced by the ,systematic designations Archaea, Bacteria and EttcaD,a.
The Archaea are a holophyletic domain This division of the IMng world as proposed by Woese el al. [1o.], who postulated the holophyletic nature of the Archaea, was questioned by Lake [2-4], who separated the archaebacteria into three phyla: the extreme halophiles, which he combines with the eubacteria tem~ing the combination'photocTtes'; the archaebacteria (this name being reserved exclusively for the methanogens) [2]; and the 'eocytes', which comprised the extremely thermophilic, often sulfur-dependent organisms that were recently temmd Crenarchaeola by Woese et al. [1 °o] and which Lake claimed to be linked to the eukaryotes [3]. The essence of this phylogenetic scheme is the derivation of eubacteria and eukaryotes from different subgroups of Woese's archaebacteria,
which then would have to be considered paraphyletic, that is, not including all their descendants [4]. The validity of the data supporting these claims has been questioned [5-7]. Table 1 shows that the 'photocyte' Halobacterium, the archaebacterium Methanococcus and the 'eocyte' SulJb/obus corresponding to each other in 24 out of 26 sufficiently analyzed homologous features. One of the two exceptions, the RNA polymerase (RNAP) component B split, is a branch character of methanogens and extreme halophiles and does not support Lake's claim. Even the second exception, the gene order in rRNA operons, in which the 'photocyte' lqalobacterium resembles the eubacteria and the 'eocyte' Sulfolobus is grouped with the eukaryotes, does not support bake's assertion because it also links the archaebacterium Methanococcua with Halobacterium. As Lake [7] points out, relating five taxa in a parsimony tree requires 'three and two patterns' (two of the live phyla differ from the other three). Seven of the first eight features listed in Table 1 confront the three Archaea with both the Eucar3pa and the Bacteria and thus yield the archaeal tree. The linkage of the three Archaea to each other in all but two of the listed features, strongly supports the archaeal case by the rules of numeric taxonomy (although each feature by itself does not support construction of a tree). The concept of three domains of life and the coherence of the Archaea is thus not only based on an increasing number of phylogenetic dendrograms but also on the distribution of a growing body of single molecular and biochemical characters.
Archaea, Bacteria and the origin of the Eucarya Of the 26 features listed in Table 1 only the first eight show a domain-specific shaping for the Archaea. The next 14 features link the Archaea to the EucaDpa and only two, genome organization and the occurrence of ribosome binding sites, are shared between Archaea and Bacteria.
Abbreviations GAPDH--glyceraldehyde phosphate dehydrogenase;pol--polymerase; RNAP--RNA polymerase.
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(~) Current Biolobn/ Ltd ISSN 0959-437X
C o m p a r a t i v e b i o c h e m i s t r y of Archaea a n d Bacteria Zillig
Table 1. Distribution of discrete characters between Bacteria, Eucarya and three phyla of Archaea.
Bacteria E. coli Acylester lipids Fatty acid synthetase Flagellins Isopranyl ether lipids A ' + A" split of RNAP component A(13') RNAP gene order rpoHBA1A2-X-rpsLG Unique modified nucleotides in tRNA Unique sequences flanking rRNA genes 7S RNA RNAP component H corresponds to yeast ABC 27 Kd subunit EF10~ ADP ribosylatable DNAP0~ aphidicolin sensitive Promoter type RNAP type ATP synthase (ATPase) Protein splicing of tRNAs Translation starts with N-formylmethionyl-tRNA CCA end of tRNA encoded RNAP gene order rplKAJLrpoBC Mureine RNAP rifampicin sensitive Ribosome streptomycin sensitive Transcription units Shine Dalgarno sequences B " + B' split of RNAP component B(13) Gene order in rRNA operonl
+ + b
b b F
+ + + + ' + + + + b
Archaea Halobacterium
Eucarya
Methanococcus
Sullolobus
(Eukaryotes)
References
a + +
-a + +
-? + +
+ + e -
[25",62] [25"',62] [631 [25"',62] [12",13"1
+
+
+
-
[12"" 13"']
+
+
+
-
[64"']
+
+
+
-
[65.1
+
+
+
+
[15oi
+
+
+
+
[13"]
+ + d c V (+ )
+ + d c V ?
+ + d c V +
+ + d c V (+ )
[66] [67] [14"] ll 2"'l
-
-
-
168--1 [69,701
. . .
. . .
. . .
. . .
[46] [461 [46]
. . + +
. .
. . + +
. .
[46] [46] [46] [46] [12"'l
+ b
+ b
+ +
-
c
e
[461
"Except myocoplasma, tb = rrs, ala, rrl, rrf; c = rrs, rrl (rff unlinked), a, Archaeal; b, bacterial; c, complex; d, box A--boxB; e, eucaryal.
Most of the features listed in Table 1 are associated with the genetic machinery. Amino acid sequences of archaeal ribosomal proteins [8°'], a histone of Methanothennus fervidus [9..], translation factors [10--,11.], RNAP components [12..,13.-], standard promoters [14.-], and also ATP synthase, the central enzyme of energy conservation by electron transport phosphorylation [15",16"], often show striking sequence similarities to their eucaryal rather than to their bacterial counterparts. In contrast, Bacteria and Eucarya strongly resemble each other in the sequences of several enzymes of glycolysis and central metabolism, for example, glyceraldehyde phosphate dehydrogenase (GAPDH) [17], phosphoglycerate kinase [18.] and malate dehydrogenase [19"], whereas the archaeal versions of these enzymes show less similarity, both to their bacterial and to their eucaryal homologs. The large components of the singular archaeal RNAPs exhibit high similarity to the corresponding subunits of two of the three specialized eucaryal RNAPs, polymerase (pol)2 and po13, but only low similarity to the third, poll [20]. Phylogenetic trees constructed using various algorithms show po12 and po13 in the immediate neighbor-
hood of the Archaea, but poll at a significant distance, sharing a bifurcation with the Bacteria [12.',21]. A possible explanation for the absence of a stem shared by the three eucaryal RNAPs is that the urkaryote, the ancestor of the Eucar3,a, arose by some sort of fusion event between an archaeal and one or several (possibly bacterial) ancestors, such that the po12 and po13 large-component genes were derived from a prearchaeal ancestor and the poll genes from another (possibly prebacterial) gene donor (Fig. 1) [12"]. The presence of 'bacterial' genes beside 'archaeal' ones in Eucar)pa would thus be explained by the chimaeric nature of the eucaryal nuclear genome. As the GAPDH of Giardia lamblia, a eukaryote devoid of mitochondria, and which is presumed to be primitive, also resembles bacterial GAPDHs [17], these 'bacterial' genes should logically have been acquired earlier than the ancestors of the mitochondria. One of the most remarkable recent achievements in molecular phylogeny is the rooting of phylogenetic trees of ATPase components and translation factors by determining the intersection of dendrograms of genes that
545
546
Gene organization and evolution
(a)
Eucarya
Archaea
' ~~
X
Bacteria
y-Mit°ch°ncl'rina Primary oisuf
Common ancestor
(b)
(b') Archaea
Eucarya
Bacteria
Archaea
Common ancestor
Eucarya X
Bacteria
Common ancestor
arose by duplication/diversification, presumably before first interdomain ramification (i.e. pairs of paralogous genes present in all three domains) [10.o,22,23]. In both the case of ATPase components and the case of elongation factors EFI~ and EFII, the Bacteria branched off first, followed by a ramification of Archaea and Eucarya. One should keep in mind, however, that this is the phylogeny of genes rather than organisms, and that this result could be compatible with the occurrence of the opposite branching order for 'bacterial' genes of Eucarya, in which the Archaea branch off before a bifurcation of Bacteria and Eucarya. Superposition of both types of single gene phylogenies would yield the fusion tree represented in Figure 1.
Features shared by Archaea and Bacteria
The distinct nature of the Archaea is characterized by aspects of the genetic machinery, electron transport phosphorytation, and lipid structure and biosynthesis. Although the presence of straight chain fatty acids and of
Fig. 1. (a) Schematic representation of the genesisof the Eucarya by a fusion of Archaea and Bacteria. The dendrograms in the lower part of the figure are typical phylogenetic trees of (b) archaebacterial and (b') eubacterial genes of Eucarya,the superposition of which yields the upper dendrogram. Where one fusion partner arose from an already diversified bacterial lineage, X denotes extant representatives of that lineage, which appear on the lowest branch of the Eucarya,rather than among the other Bacteria.
fatty acid synthetase has been reported in Archaea [24], the small enzymatic activity associated with Halobacterium is salt sensitive and recent attempts to prove the presence of fatty acids in Archaea failed completely (M De Rosa and A Gambacorta, personal communication) [25"]. As discussed by Danson [26], many other metabolic capacities are shared either by Archaea and Bacteria, or by certain phyla in either domain. Thus, methanogens, like many Bacteria, appear to use the Embden-Meyerhof pathway of glycolysis in both directions. Extreme halophiles, Sulfolobus and Tbermoplasma use a version of the early steps of the Entner-Doudoroff pathway of glucose catabolism, employing non-phosphorylated rather than phosphorylated intermediates. Again, certain Bacteria follow the same path. It has been found that different versions (aerobic/anaerobic, oxidative/reductive, complete/interrupted) and parts of the citric-acid cycle are expressed in different Archaea and Bacteria. In both Archaea and anaerobic Bacteria 2-oxo-acid oxidoreductases occur. Although the 2-oxo-acid dehydrogenase multi- enzyme complexes present in aerobic Bao
Comparative biochemistry of Archaea and Bacteria Zillig 547 teria have not been found in Archaea, their component dihydrolipoamide dehydrogenase has been found in extreme halophiles.
lishing several complex features of this type in different Arcbaea and Bacteria is needed to elucidate whether horizontal gene transfer occurred.
Principles and components of electron transport phosphorylation have been discovered in Arcbaea, although their respiratory chains appear primitive [27°.]. Both the Archaeum Sulfolobus and the Bacterium Thiobacil/us oxidize sulfur. Both the Archaeum Archaeoglo&us [28] and certain Bacteria reduce sulfate for energy conservation. Representatives of the ¢t-group of purple bacteria and certain methanogens [29,30"] are able to fix molecular nitrogen. Like sulfur-dependent, extremely thermophilic Archaea of the branch Crenarchaeota and the order Thermococcales, certain Bacteria use sulfur as the terminal electron acceptor, although in contrast to some Archaea [31"'] they do not seem to be able to couple this to autotrophic CO x fixation. Reverse gyrase has not only been found in extremely thermophilic Archaea [32], Crenarchaeota and Euryarchaeota, but also in the extremely thermophilic Bacterium Thermotoga [33"'].
In both Archaea and Bacteria, many genes are organized in transcription units of often similar gene composition (for review see [46])[47"-49,50"-53"]. The similarity of this organization between the two domains indicates a common origin. Operons certainly alleviate the control of expression of correlated genes. Linkage of such genes could, however, also be advantageous in genome evolution. Highly similar transcription units map in different contexts in the chromosomes of Archaea and Bacteria (for example, see [12"]), indicating independent arrangement or extensive rearrangement of gene clusters within coherent circular genomes during the diversification of the domains. Different single genes are absent in corresponding gene clusters of different Archaea, for example in archaeal 'strep operons' (cited in [12.-] ). Complete separation of rRNA genes has been found in Therrnoplasma [54"]. These data are in line with the hypothesis that genomes were originally composed, and later under certain conditions supplemented, by the recombinative joining and addition, respectively, of sets of genes once or still available. For example, the genes could be donated by a common pool of plasmids in a manner similar to the virus modules of Campbell and Botstein [55], or they could occur as accessory DNA elements able to enter the chromosome [56]. The unique metabolic capacities found in isolated bacterial and archaeal phyla could thus have been acquired from this unidentified pool by unknown modes of transfer and recombination.
Gas vacuoles exist in Halobacteria and several Bacteria. The structural proteins of these organelles in I-L. halobium and Cyanobacteria are strikingly similar [34"]. Homologous superoxide dismutases have been discovered in Bacteria and Archaea [35], including the anaerobic archaebacterium Methanobacterium thermoautotrophicum [36"]. The ability of a particular group of Archaea, the methanogens, to exist autotrophically by gaining energy through methanogenesis appears to be unique, although the mode of energy conservation in this pathway resembles in principle other ATP synthesis processes that are membrane associated and proton driven [37"',38",39"']. In contrast, however, 13-galactosidases discovered in Sulfolobus [40] appear to be unrelated to the enzyme of E. coli. The gene described by CubeUis et al. [41.] has been isolated from S. solfataricua strain MT4. The homologous, yet strikingly different, gene described by Little et al. [40] could stem from a contamination of DSM 1616 by S. acidocaldarius [42°]. Capacities shared by isolated phyla in both domains could have belonged to the repertoire of the common ancestor of Archaea and Bacteria and were possibly lost during lineage diversification in all but the particular taxa still possessing them. As several of these features are complex, the genome of the common ancestor should have been significantly larger than those of present members of both domains, the genomes of which range around 3 x 96bp [43]; (Klenk, Diploma thesis, Eberhard-Karls-UniversRy, Tf~ingen, 1986). Alternatively, it is possible that the sharing of such metabolic capacities by particular phyla in both domains could at least, in some cases, have resulted from horizontal gene transfer. In the case of the nlfgenes, where sequences for comparison are available, the phylo genetic tree appears to contradict this hypothesis [44]. Because for ferredoxins [45] and gas vacuole proteins [34"] the sequences of only two phyla (Halobacteria and Cyanobacteria), one from each domain, were compared, phylogenetic dendrograms could not be constructed. The cloning and sequencing of genes involved in estab-
The nature of the common ancestor The features shared by Arcbaea and Bacteria testify to the existence of a highly developed intermediary metabolism including glycolysis, gluconeogenesis, the citric acid cycle [26], electron transport phosphorylation (for example, see [37"]) and even elements of respiratory chains [19"'] in the common ancestor of both domains. This ancestor should thus have possessed a large set of enzymes sufficient for autonomous existence and also the molecular components necessary for their accurate manufacture (e.g. a DNA genome, RNA polymerase, and ribosome-binding sites for the initiation of translation) [46]. It was thus not the progenote of Woese and Fox [57], in which inaccurate (not yet fully developed) gene expression and genome replication should have excluded the synthesis of large specific enzymes [67], but rather an already strikingly perfect genote, that is, an organism equipped with a fully developed gene replication and expression system. Even the organization of transcription units was principally complete, although their context (linkage) within a single circular genome was possibly not yet established (see above). By possessing a genome consisting of unlinked gene clusters, the common ancestor would conform to a second important characteristic ascribed to the progenote by Woese [58]. As exemplified by characteristic differences, for example in the transcription apparatus (including the structure of RNAP and promoters and their interaction [14-,]) parts
548
Gene organization and evolution of the genetic machinery were, however, not yet fully established. Among other domain specific features, the apparently absolute inability of Archaea to synthesize fatty acids and fatty acid ester lipids (see above) is most conspicuous. In contrast, the basic biosynthetic pathways of polyisoprenoid compounds are shared by Bacteria and Arcbaea [25"'], although Bacteria cannot synthesize ether lipids because they lack the ability to join isopranyl residues to glycerol [59,60], to completely reduce the linked residues and to condense the heads of two C20 chains to fore1 a C40 compound. The primeval membrane was therefore probably neither of the isopranyl-ether nor of the fatty-acid-ester type, but was rather, for example, a membrane of protein. The capacity, to s'ynthesize fatty-acid-ester lipids would then have been an achievement of the ancestral Bacteria, which donated it to the Eucaopa; the ancestral Ardaaea inventing isopranyl-ether lipids instead. The absence of lineages going back to transitional fomas between Archaea and Bacteria indicates that starting lineages probably required irreversible changes, possibly isolation of individuals, ending the phase of transition from the conmaon ancestor to the already distinctly diversified ancestral Archaea and Bacteria. It seems that extensive gene sharing, already postulated as a third characteristic of the progenote suggested by Woese [61], prevented lineage separation in two isolated, rapidly evolving populations of progenotes that finally became separated by the increasing incompatibility of their transcription systems. The fomaation of strong barriers between individuals within each population, for example by changes in the quality of their membranes, could then have ended the phase of ancestral communication, thus preparing the stage for speciation. This ancestral communication should have effected rapid joint evolution by making rare or nmtatect gene clusters (plasmids?) available as a common gene pool to all individuals throughout the progenote population. This pool should have consisted of two fractions: a set of house-keeping genes required for the autonomous existence of each individual; and a fraction of rare gene clusters encoding special capacities present only in small subpopulations. The transfer of the latter would have ensured survival in a changing environment. The genetic fixation of the genes should have occurred by the development of the communication barriers discussed above, concomitant with the linkage of gene clusters into coherent genomes. The superiority of the resulting true genotes, for example in maintaining their gene stocks, would then have ended the age of progenotes. Although the details of these ideas are still speculative, aspects of them appear as rather compelling interpretations of the comparative biochemistry/molecular genetics of the domains. The details may unfold with the growing understanding of the molecular similarities and differences between the domains.
three domains of life, enables extrapolations to the early evolution of organisms and the nature of the common ancestor. The Arcbaea have facilitated our understanding of evolution, both by being distinct in certain features as well as by sharing fundamental capacities with the Bacteria. Their coherent circular genomes are composed of gene clusters resembling those found in Bacteria, although the order in which these clusters are linked appears to differ, indicating two independent processes of chromosome formation. This implies that the common ancestor of Arcbaea and Bacteria, "although possessing an almost fully developed metabolic and genetic machinery, did not initially have a coherent genome. That and other projections, for ex~unple, the differences of transcription signalling and lipid structure, bring early biotic evolution in the progenote state into focus.
Acknowledgements Due to limitations of space this review' is unable to reference the literature prior to 1990 in flail. 1 would like to apologise to those whose work I have not been able to acknowledge.
References and recommended reading Papers of speci:d interest, published within the annual peri(x.t of review, have been highlighted -ts: • of interest • ,, of ot, tstanding interest 1. .,
WOESI'." CR, KANDLER O, WHEEl.IS ML: Towards a Natu. ral System of Organisms: Proposal for the Domains Archaea, Bacteria and Eucarya. Proc Natl Acad Sci USA 1990, 87:4576~579. A novel proposal for the nomenclature of the taxa of the living world that accounts for their phylogeny. JA, C t . ~ MW, HENDERSON E, FAY SP, tAKES M, SCHF.INMAN A, THORNBER JP, MM-! RA: Eubacteria, Halobacteria, and the Origin of Photosynthesis: T h e Photocytes. Proc Natl Acad Sci USA 1985, 82:3716-3720. LAKEJA, HENDRSON E, tAKES M, CLARK MW: Eocytes: A New Ribosome Structure Indicates a Kingdom with a Close Relationship to Eukaryotes. Proc Natl Acad Sci LISA 1984, 81:3786-3790.
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LAKE JAz Prokaryotes and Archaebacteria are Not Monophyletic: Rate Invariant Analysis of rRNA G e n e s Indicates that Eukaryotes and Eocytes form a Monophyletic Taxon. Cold Spring Harbor Syrup Quant Biol 1987, 52:839-846.
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Conclusion The discovery of the Arcbaea by Woese and collaborators and the comparison of corresponding features in the
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Comparative biochemistry of Archaea and Bacteria Zillig Ribosome. Structure, Function a n d Evohaion cxlited by Hill WE Ibook]. Washington DC: American Sex:let3, for Microbiology, 1990, pp 598-616. This is an up to date and concise review on the topic by the group which did most of the work. 9. °°
SANDMANK, KRZYCK] JA, DOBRINSK] B, LtmZ R, REEVE JN: HMf, a DNA-binding Protein Isolated from the Hyperthermophilic Archaeon M e t h a n o t h e r m u s fervidus, is Most Closely Related to Histones. Proc Natl Acad Sci U~Cel 1990, 87:5788-5791. Demonstrates that Ard2aea contain DNA-binding proteins homologous to eucaryal histones. 10. ••
HASEGAWAM, IWABEN, MIIKOHATAY, MIYATAT: Close Evolutionary Relatedness of Archaebacteria. Methanococcus and Halobacterium, to Eukaryotes Demonstrated by Composite Phylogenetic Trees of Elongation Factors EF-Tu and EF-G. Eocyte Tree is Unlikely..lpn .1 Genet 1990, 65:109-114. One of two phylogenetic dendrognmls of genes rooted by intersection of the trees of pandogous proteins. The other case was reported independently byJP Gogarten el al. and N lwabe el al., in 1989. CRt-.'TIR, CITAREIJA F, TIBONI O, SANANGEIANTONIA, PALM P, CAMbkkRANOP: Nucleotide Sequence of a DNA Region Comprising the Gene for Elongation Factor let (EF-100 from the Ultrathermophilic Archaeote Pyrococcus woesei: PbyIogenetic Implications. J Mol Evol 1991, in press. The phylogenetic tree of EFI cc confimls the coherence of the Arcbaea.
19. ••
HONKAE, FABRYS, NIERblPuNNT, PAl.~l P, HENSELR: Properties and Primary Structure of the L-Malate Dehydrogenase from the Extremely Thermophilic Archaebacterium Methanothe r m u s fervidus. Eur J Biocbem 1990, 188:623-632. A.s ff)r reference [18••], a particular b, strong case for the resemblance of the bacterial and eucaryal versions of an enzyme, with the archaeal version differing from these two. 20.
PUtlU'R G, LEFFERSY H, GROI'P F, PAI.M P, KLENK H-P, IxOTrSPEIClt F, GARRETr RA, ZIt.UG W: Archaebacterial DNAdependent RNA Polymerases Testify to the Evolution of the Eukaryotic Nuclear Genome. Proc Natl Acad Sci LISA 1989, 86:4569-4573.
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C~,tLR'I'EN JP, KIBAK H, DITI'RICH P. TAIZ L, BOWMAN EJ, BOWMAN BJ, MANOLSON MF, POOLE RJ, DATE T, OSHIMA T, KONISHI J, DENDA K, YOSHIDA M: Evolution of the Vacuolar H + -ATPases: Implications for the Origin of Eukaryotes. Proc Nail Acad Sci lISA 1989, 86:6661~o665.
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KLENKH-P, PA~t P, [D'I=I'SIq'.'ICHF, ZIIJJG W: Component of the DNA-dependent RNA Polymerases of A r c h a e a is Homologous to a Subunit Shared by the Three Eukaryal Nuclear RNA Polymerases. Proc Natl Acad Sci USA 1991, in press. Demonstrates that archael RNA pob,merases resenable the eucaryal enzymes not only in their large component, hut also in a small subunit. 14. •,
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Gene organization and evolution A hallmark of hyperthermophilic Archaea is a general feature of hyperthermophiles including the Bacterium 7bemnotogct ENGLERTC, HORNE M, PFEn:ER F: Expression of the Major Gas Vesicle Protein Gene in the Halophilic Archaebacterium Haloferax mediterranei is Modulated by Salt. Mol Gen Genet 1990, 222:225-232. Describes the control of gas vesicle .synthesis in extreme halophiles.
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37. **
DEPPENMEIERU, BLAUT M, MAHI2dANNA, GOTTSCHALKG: Reduced Coenzyme 1:42o: Heterodisulfide Oxidoreductase, a Proton-translocated Redox System in Methanogenic Bacteria. Proc Nail Acad Sci USA 1990, 87:9449-9453. The breakthrough in understanding how methanogenesis and proton translocation for energy conservation are coupled.
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38. •
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