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Archaeal and Bacterial Hyperthermophiles Archaeal and Bacterial Hyperthermophiles Horizontal Gene Exchange Or Common Ancestry?

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Archaeal and Bacterial Hyperthermophiles Archaeal and Bacterial Hyperthermophiles Horizontal Gene Exchange Or Common Ancestry? Outlook GENOME ANALYSIS Archaeal and bacterial hyperthermophiles Archaeal and bacterial hyperthermophiles horizontal gene exchange or common ancestry? ravind and colleagues1 recently concluded that massive thermal tolerance to the archaeal hyperthermophiles and Agene transfer has occurred from Archaea to the bac- Aquifex by vertical inheritance. Consistent with this, we terial ancestors of the hyperthermophile Aquifex aeolicus. have identified presumptive homologs of at least a third of Their analyses were based primarily on similarity searches these genes in the incomplete genome of another deeply of all complete bacterial genomes against the non- diverging bacterial hyperthermophile, Thermotoga redundant protein sequence database, showing that the maritima (see below). genome of A. aeolicus2 has a much larger fraction of pro- We also find methodological problems in the analysis teins with best hits to archaeal proteins than any other of Aravind et al.1 The 246 Aquifex proteins reported as bacterium. In particular, they reported that 246 Aquifex ‘reliable best hits’ with their archaeal homologs were proteins are most similar to archaeal proteins, with 26 of defined by having an E-value (expected number of these proteins belonging to families found only in Archaea matches at least this good in random data) of at least 100 and Aquifex. Thus, the authors suggested that at least times lower than that obtained with any bacterial or 10% of the Aquifex genes have been horizontally trans- eukaryotic protein, which is not a particularly stringent ferred from Archaea. Although we agree that gene transfer criterion. In reality there is no simple relationship between has played an important role in the history of life3,4, we do differences in expectation and being significantly more not agree with the conclusions that Aravind et al.1 reach. related. Nor is there any translation of this measure into In particular, limitations imposed by their assumptions relative phylogenetic distances (amino acid replacements and flaws in the analyses and conclusions drawn will be per position), or even into a difference in percentage discussed. amino acid identity. Because they did not compare all The two most fundamental problems with the con- pairs of sequences within a family, these data are not even clusions of the work cited of Aravind et al.1 are that the sufficient for a cluster analysis, but the authors have authors (1) ignore the evidence that Aquifex is the most drawn conclusions about the histories of genes (phylo- deeply branching eubacterium with a complete genome genetic analyses). For statements about the histories of sequence5 (Fig. 1) and (2) assume that hyperthermophilic- these genes, it would be more appropriate to use explicit ity in Bacteria and Archaea are independent inventions. phylogenetic analysis, supported by bootstrap analysis of Firstly, ancestral genes passed vertically through the bac- confidence. Of the 60 protein families (27% of the 220 terial lineage could be transmitted to Aquifex (and poss- families that go beyond Archaea and Aquifex) for which ibly to other early diverging bacterial lineages) but are Aravind et al.1 report such analyses, they find bootstrap lost in the common ancestor of the more recently diverg- support for an Aquifex–Archaea grouping in only 26 ing bacterial lineages for which genome sequences are families. Thus, only 43% of the cases they examined available. Neither the data nor the discussion of Aravind (12% of these 220 ‘reliable best hits’ with the Archaea) are et al.1 deals with this simple explanation of genes that are actually demonstrated to support their suggestion. shared by Aquifex and the Archaea but are absent in other Finally, because of our own interest in the set of pro- bacterial genomes. teins uniquely shared between Aquifex and Archaea, we *Nikos C. Kyrpides Secondly, hyperthermophiles are represented among all repeated this analysis comparing our results with those of 1 [email protected]. of the deepest and least diverged lineages both in Bacteria Aravind et al. Although there were a number of differ- 6 6,7 uiuc.edu and Archaea (Fig. 1), leading many workers but not ences in the genes identified, the real importance of this all8 to argue that the last universal common ancestor analysis lies in the fact that the majority of these genes are Gary J. Olsen (cenancestor) was a hyperthermophile. Aravind et al.1 found in only one or two of the four complete archaeal [email protected]. uiuc.edu ignored this possibility when they interpreted their data. genomes. Thus, even if these genes have been horizontally Regardless of whether the root of the tree of life is placed transferred, we cannot possibly infer whether the transfer Department of in the bacterial branch9,10 or in the eukaryotic branch11, occurred from Archaea to Aquifex (as the authors sug- Microbiology, University and regardless of whether life originated at a hot environ- gested) or vice versa. In addition, we identified homologs of Illinois at Urbana- ment or started cool and later adapted to high tempera- of at least a third of these genes in the partial genome of Champaign, IL 61801, tures12, it is possible – even likely – that hyperthermo- Thermotoga maritima, another bacterial hyperthermo- USA. *Also at the Mathematics philicity was invented once (prior to the last prokaryotic phile, suggesting that vertical inheritance via a thermo- and Computer Science common ancestor stage; Fig. 1), and not independently at philic lineage from the archaeal–bacterial common ances- Division, Argonne two or more later times (as explicitly assumed by Aravind tor (Fig. 1) will be a more parsimonious explanation National Laboratory, et al.1). If the cenancestor was a hyperthermophile, it than independent lateral transfers as suggested by IL 60439, USA. would be natural for it to pass genes contributing to Aravind et al.1 298 TIG August 1999, volume 15, No. 8 0168-9525/99/$ – see front matter © 1999 Elsevier Science All rights reserved. PII: S0168-9525(99)01811-9 Archaeal and bacterial hyperthermophiles GENOME ANALYSIS Outlook FIGURE 1. A rooted phylogenetic tree of Bacteria, Eukarya and Archaea In summary, we find the ideas expressed by Aravind et al.1 to be very Escherichia interesting, but we also argue that these Agrobacterium authors have made assumptions (with- Planctomyces out offering justification) that led them Flavobacterium to conclusions that do not follow from Chlamydia the data per se. In particular, alternative Leptonema hypotheses on the history of extreme Synechocystis thermophilicity would suggest (regard- Bacillus less of the rooting of the tree) that sub- Thermomicrobium Thermus stantial numbers of the genes discussed Thermotoga could be vertically inherited from the Aquifex cenancestor. Giardia Tritrichomonas Physarum References Entamoeba 1 Aravind, L. et al. (1998) Evidence for massive gene Dictyostelium exchange between archaeal and bacterial Trypanosoma hyperthermophiles. Trends Genet. 14, 442–444 2 Deckert, G. et al. (1998) The complete genome of the Paramecium hyperthermophilic bacterium Aquifex aeolicus. Nature Zea 392, 353–358 Coprinus 3 Médigue, C. et al. (1991) Evidence for horizontal gene transfer in Escherichia coli speciation. J. Mol. Biol. Homo 222, 851–856 Desulfurococcus 4 Woese, C.R. (1998) The universal ancestor. Proc. Natl. Sulfolobus Acad. Sci. U. S. A. 95, 6854–6859 5 Burggraf, S. et al. (1992) A phylogenetic analysis of Pyrococcus Aquifex pyrophilus. Syst. Appl. Microbiol. 15, 352–356 Thermoproteus 6 Stetter, K.O. (1996) Hyperthermophilic prokaryotes. Thermophilum FEMS Microbiol. Rev. 18, 149–158 Methanopyrus 7 Pace, N.R. (1991) Origin of life-facing up to the Methanobacterium formicicum physical setting. Cell 65, 531–533 8 Galtier, N. et al. (1999) A nonhyperthermophilic common Methanothermus ancestor to extant life forms. Science 283, 220–221 Thermococcus 9 Iwabe, N. et al. (1989) Evolutionary relationship of Methanococcus vannielii archaebacteria, eubacteria and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc. Methanococcus jannaschii Natl. Acad. Sci. U. S. A. 86, 9355–9359 Archaeoglobus 10 Brown, J.R. and Doolittle, W.F. (1995) Root of the Thermoplasma universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc. Natl. Acad. Sci. 0.10 Haloferax Methanospirillum U. S. A. 92, 2441–2445 11 Forterre, P. (1995) Thermoreduction, a hypothesis for the origin of prokaryotes. C. R. Acad. Sci. 318, This Maximum Likelihood tree was inferred essentially as described in Ref. 5, and rooted as in Ref. 9. 415–422 The heavy lines trace the evolution of extreme thermophilicity under the assumption that it originated 12 Forterre, P. (1996) A hot topic: the origin of only once. Scale bar: 0.10 amino acid substitutions per site. hyperthermophiles. Cell 85, 789–792 Reply e welcome the discussion of the evolutionary mecha- tral origin of the archaeal genes in Aquifex. The main L. Aravind Wnism(s) underlying the special relationship between reasons for this are simple and have little to do with the [email protected] archaeal and bacterial hyperthermophiles. First of all, to details of the phylogenetic methods used by us, or others, Roman L. Tatusov our satisfaction, we find that Kyrpides and Olsen1 agree but rather stem directly from the nature of the special tatusov@ with us on the critically important issue: such a special relationship. We discuss these reasons briefly below. ncbi.nlm.nih.gov relationship does exist – something that was not at all With respect to the majority of its genes, Aquifex looks Yuri I. Wolf obvious from the original publication on the Aquifex like a ‘garden-variety’ bacterium and does not show any [email protected] genome sequence2. In fact, this was the principal point specific affinity with the Archaea. A significant subset of D. Roland Walker that we tried to convey, as convincingly as we could, in the the Aquifex genes, however, appears to be very different in walker@ 3 article that is discussed . Perhaps we should have been that they show a much greater similarity to archaeal ncbi.nlm.nih.gov more explicit about distinguishing between these basic orthologs than to bacterial ones, and some are (so far) Eugene V.
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