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Early evolutionary relationships among known life forms inferred from elongation factor EF-2/EF-G sequences: Phylogenetic coherence and structure of the archaeal domain

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Phylogenies were inferred from both the gene and the protein sequences of the translational elongation factor termed EF-2 (for Archaea and Eukarya) and EF-G (for Bacteria). All treeing methods used (distance-matrix, maximum likelihood, and parsimony), including evolutionary parsimony, support the archaeal tree and disprove the “eocyte tree” (i.e., the polyphyly and paraphyly of the Archaea). Distance-matrix trees derived from both the amino acid and the DNA sequence alignments (first and second codon positions) showed the Archaea to be a monophyletia-holophyletic grouping whose deepest bifurcation divides a Sulfolobus branch from a branch comprising Methanococcus, Halobacterium, and Thermoplasma. Bootstrapped distance-matrix treeing confirmed the monophyly-holophyly of Archaea in 100% of the samples and supported the bifurcation of Archaea into a Sulfolobus branch and a methanogen-halophile branch in 97% of the samples. Similar phylogenies were inferred by maximum likelihood and by maximum (protein and DNA) parsimony. DNA parsimony trees essentially identical to those inferred from first and second codon positions were derived from alternative DNA data sets comprising either the first or the second position of each codon. Bootstrapped DNA parsimony supported the monophyly-holophyly of Archaea in 100% of the bootstrap samples and confirmed the division of Archaea into a Sulfolobus branch and a methanogen-halophile branch in 93% of the bootstrap samples. Distance-matrix and maximum likelihood treeing under the constraint that branch lengths must be consistent with a molecular clock placed the root of the universal tree between the Bacteria and the bifurcation of Archaea and Eukarya. The results support the division of Archaea into the kingdoms Crenarchaeota (corresponding to the Sulfolobus branch and Euryarchaeota). This division was not confirmed by evolutionary parsimony, which identified Halobacterium rather than Sulfolobus as the deepest offspring within the Archaea.

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References

  • Achenbach-Richter L, Stetter KO, Woese CR (1987) A possible missing link among archaebacteria. Nature 327:348–349

    Google Scholar 

  • Amann R, Ludwig W, Schleifer KH (1988) β-subunit of ATP-synthase: a useful marker for studying the phylogenetic relationships of Eubacteria. J Gen Microbiol 134:2815–2821

    Google Scholar 

  • Auer J, Spicker G, Mayerhofer L, Pühler G, Böck A (1991) Organisation and nucleotide sequence of a gene cluster comprising the translation elongation factor 1α from Sulfolobus acidocaldarius. Syst Appl Microbiol 14:14–22

    Google Scholar 

  • Bachleitner M, Ludwig W, Stetter KO, Schleifer KH (1989) Nucleotide sequence of the gene coding for the elongation factor Tu from the extremely thermophylic eubacterium Thermotoga maritima. FEMS Microbiol Lett 57:115–120

    Google Scholar 

  • Bernardi G, Bernardi G (1986) Compositional constraints and genome evolution. J Mol Evol 24:1–11

    Google Scholar 

  • Burggraf S, Stetter KO, Rouviere P, Woese CR (1991) Methanopyrus kandleri: an archaeal methanogen unrelated to all other known methanogens. System Appl Microbiol (in press)

  • Corpet F (1988) Multiple sequence alignment with hierarchical clustering. Nucleic Acids Res 16:10881–10890

    Google Scholar 

  • Creti R, Citarella F, Tiboni O, Sanangelantoni AM, Palm P, Cammarano P (1991) Nucleotide sequence of a DNA region comprising the gene for elongation factor 1α (EF-1α) from the ultrathermophilic Archaeote Pyrococcus woesei. Phylogenetic implications. J Mol Evol 33:332–342

    Google Scholar 

  • Devereux I, Haeberli P, Smithies O (1984) A comprehensive set of sequence programs for the VAX. Nucleic Acids Res 12: 387–395

    Google Scholar 

  • Diaconis P, Efron B (1983) Computer-intensive methods in statistics. Sci Am 248:116–130

    Google Scholar 

  • Felsenstein J (1985) Confidence limits in phylogenies: an approach using the bootstrap. Evolution 39:783–791

    Google Scholar 

  • Felsenstein J (1990) Phylogenetic inference program (PHYLIP) manual version 3.3. University of Washington, Seattle

    Google Scholar 

  • Feng DF, Johnson MS, Doolittle RF (1985) Aligning amino acid sequences: comparison of commonly used methods. J Mol Evol 21:112–125

    Google Scholar 

  • Fitch WM, Margoliash E (1967) Construction of phylogenetic trees. Science 15:279–284

    Google Scholar 

  • Gogarten JP, Kibak H, Dittrrich P, Lincoln T, Bowman E, Bowmman H, Manolson MF, Poole RJ, Date T, Oshima T, Konishi J, Denda K, Yoshida M (1989a) Evolution of the vacuolar H+-ATPase: implications for the origin of eukaryotes. Proc Natl Acad Sci USA 86:6661–6665

    Google Scholar 

  • Gogarten JP, Rausch T, Bernasconi P, Kibak H, Taiz L (1989b) Molecular evolution of H+ATPases. I. Methanococcus and Sulfolobus are monophyletic with respect to eukaryotes and eubacteria. Z Naturforsch 44:97–105

    Google Scholar 

  • Gouy M, Li W-H (1989) Phylogenetic analysis based on rRNA sequences supports the archaebacterial rather than the eocyte tree. Nature 339:145–147

    Google Scholar 

  • Grinblat Y, Brown N, Kafatos F (1989) Isolation and characterization of the Drosophila translational elongation factor 2 gene. Nucleic Acids Res 17:7303–7314

    Google Scholar 

  • Hasegawa M, Kishino H, Saitou N (1991) On the maximum likelihood method in molecular phylogenetics. J Mol Evol 32:443–445

    Google Scholar 

  • Higgins DG, Sharp PM (1988) Clustal: a package for performing multiple sequence alignments on a microcomputer. Gene 73: 237–244

    Google Scholar 

  • Holmquist R, Miyamoto MM, Goodman M (1988) Analysis of higher primate phylogeny from transversional distances in nuclear and mitochondrial DNA by Lake's method of evolutionary parsimony and operator metrics. Mol Biol Evol 5:217–236

    Google Scholar 

  • Itoh T (1989) Sequence analysis of the peptide-elongation factor EF-2 gene downstream from those of ribosomal protein H-S12 and H-S7, from the archaebacterial extreme halophile, Halobacterium halobium. Eur J Biochem 186:213–219

    Google Scholar 

  • Iwabe N, Kuma KI, Hasegawa M, Osawa S, Miyata T (1989) Evolutionary relationship of archaebacteria, eubacteria and eukaryotes inferred from phylogenetic trees of duplicated genes. Proc Natl Acad Sci USA 86:9355–9359

    Google Scholar 

  • Jukes TH, Cantor CR (1969) Evolution of protein molecules. In: Munro HN (ed) Mammalian protein metabolism, vol 3. Academic Press, New York, pp 21–132

    Google Scholar 

  • Khono K, Uchida T, Ohkubo H, Nakanishi S, Nakanishi T, Fukui T, Ohtuka E, Ikehara M, Okada Y (1986) Amino acid sequence of mammalian elongation factor 2 deduced from the cDNA sequence: homology with GTP binding proteins. Proc Natl Acad Sci USA 83:4978–4982

    Google Scholar 

  • Kimura M (1980) A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol 16:111–120

    Google Scholar 

  • Lake JA (1987a) A rate-independent technique for analysis of nucleic acid sequences: evolutionary parsimony. Mol Biol Evol 4:167–191

    Google Scholar 

  • Lake JA (1987b) Determining evolutionary distances from highly diverged nucleic acid sequences: operator metrics. J Mol Evol 26:59–73

    Google Scholar 

  • Lake JA (1988) Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331: 184–186

    Google Scholar 

  • Lake JA (1991a) Tracing origins with molecular sequences: metazoan and eukaryotic beginnings. Trends Biochem Sci 16: 46–50

    Google Scholar 

  • Lake JA (1991b) The order of alignment can bias the selection of tree topology. Mol Biol Evol 8:378–385

    Google Scholar 

  • Lechner K, Heller G, Böck A (1988) Gene for the diphtheria toxin susceptible elongation factor 2 from Methanococcus vannielii. Nucleic Acids Res 16:7817–7826

    Google Scholar 

  • Leffers H, Kjems J, Ostergaard L, Larsen N, Garrett RA (1987) Evolutionary relationships amongst archaebacteria: a comparative study of 23S rRNAs of a sulfur-dependent extreme thermophile, extreme halophile and a thermophile methanogen. J Mol Biol 195:43–61

    Google Scholar 

  • Linkkila TP, Gogarten JP (1991) Tracing origins with molecular sequences: rooting the universal tree of life. Trends Biochem Sci 16:287–288

    Google Scholar 

  • Ohama T, Yamaho A, Muto A, Osawa S (1987) Organization and codon usage of the streptomycin operon in Micrococcus luteus, a bacterium with a high genomic G+C content. J Bacteriol 169:4770–4777

    Google Scholar 

  • Olsen G (1987) Earliest phylogenetic branchings: comparing rRNA-based evolutionary trees inferred with various techniques. Cold Spring Harb Symp Quant Biol 52:825–837

    Google Scholar 

  • Pechmann H, Tesch A, Klink F (1991) Cloning and sequencing of the fus-gene encoding elongation factor 2 in the archae-bacterium Thermoplasma acidophilum. FEMS Microbiol Lett 79:51–56

    Google Scholar 

  • Pühler G, Leffers H, Gropp F, Palm P, Klenk H, Lottspeich HP, Garrett R, Zillig W (1989) Archaebacterial DNA-dependent RNA polymerases testify to the evolution of the eukaryotic nuclear genome. Proc Natl Acad Sci USA 86:4569–4573

    Google Scholar 

  • Saitou N, Nei M (1987) The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4:406–425

    Google Scholar 

  • Schröder H, Klink F (1991) Gene for the ADP-ribosylatable elongation factor 2 from the extreme thermoacidophilic archaebacterium Sulfolobus acidocaldarius. Cloning, sequencing, comparative analysis. Eur J Biochem 195:321–327

    Google Scholar 

  • Sydow A, Wilson AC (1990) Compositional statistics: an improvement of evolutionary parsimony and its application to deep branches in the tree of life. J Mol Evol 31:51–68

    Google Scholar 

  • Tiboni O, Cantoni R, Creti R, Cammarano P, Sanangelantoni AM (1991) Phylogenetic depth of Thermotoga maritima inferred from analysis of the fus gene: amino acid sequence of elongation factor G and organization of the Thermotoga str operon. J Mol Evol 33:142–151

    Google Scholar 

  • Toda K, Tasaka M, Mashima K, Khono K, Uchida T, Takeuchi I (1989) Structure and expression of elongation factor 2 gene during the development of Dictyostelium discoideum. J Biol Chem 264:15489–15493

    Google Scholar 

  • Woese CR (1987) Bacterial evolution. Microbiol Rev 51:221–271

    Google Scholar 

  • Woese CR, Kandler O, Wheelis M (1990) Towards a natural system of organisms: proposal for the domains of Archaea, Bacteria and Eucarya. Proc Natl Acad Sci USA 87:4576–4579

    Google Scholar 

  • Zengel JM, Archer RH, Lindhal L (1984) The nucleotide sequence of Escherichia coli fus gene coding for elongation factor G. Nucleic Acids Res 12:2181–2192

    Google Scholar 

  • Zillig W, Holz I, Klenk HP, Trent J, Wunderl S, Janekovic D, Insel E, Haas B (1987) Pyrococcus woesei sp. nov., an ultrathermophilic marine archaebacterium representing a novel order, Thermococcales. Syst Appl Microbiol 9:62–70

    Google Scholar 

  • Zillig W, Klenk HP, Palm P, Leffers H, Pühler G, Gropp F, Garrett R (1989) Did eukaryotes originate by a fusion event? Endocytobiosis Cell Res 6:1–25

    Google Scholar 

  • Zuckerkandl E (1987) On the molecular evolutionary clock. J Mol Evol 26:36–46

    Google Scholar 

Download references

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Cammarano, P., Palm, P., Creti, R. et al. Early evolutionary relationships among known life forms inferred from elongation factor EF-2/EF-G sequences: Phylogenetic coherence and structure of the archaeal domain. J Mol Evol 34, 396–405 (1992). https://doi.org/10.1007/BF00162996

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  • DOI: https://doi.org/10.1007/BF00162996

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