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Early branchings in the evolution of eukaryotes: Ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data

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Summary

Phylogenetic analyses of ribosomal RNA sequences have played an important role in the study of early evolution of life. However, Loomis and Smith suggested that the ribosomal RNA tree is sometimes misleading—especially when G+C content differs widely among lineages—and that a protein tree from amino acid sequences may be more reliable. In this study, we analyzed amino acid sequence data of elongation factor-1α by a maximum likelihood method to clarify branching orders in the early evolution of eukaryotes. Contrary to Sogin et al.'s tree of small-subunit ribosomal RNA, a protozoan species, Entamoeba histolytica, that lacks mitochondria was shown to have diverged from the line leading to eukaryotes with mitochondria before the latter separated into several kingdoms. This indicates that Entamoeba is a living relic of the earliest phase of eukaryotic evolution before the symbiosis of protomitochondria occurred. Furthermore, this suggests that, among eukaryotic kingdoms with mitochondria, Fungi is the closest relative of Animalia, and that a cellular slime mold, Dictyostelium discoideum, had not diverged from the line leading to Plantae-Fungi-Animalia before these three kingdoms separated.

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References

  • Adachi J, Hasegawa M (1992) Computer science monographs, No. 27, MOLPHY: Programs for molecular phylogenetics I—PROTML: maximum likelihood inference of protein phylogeny. Institute of Statistical Mathematics, Tokyo

    Google Scholar 

  • Alarcon CM, Donelson JE (1991) Translational elongation factor 1α (EF-1α) of Onchocerca volvulus. Mol Biochem Parasitol 48:105–108

    Article  CAS  PubMed  Google Scholar 

  • Auer J, Spicker G, Böck A (1990) Nucleotide sequence of the gene for the translation elongation factor 1α from the extreme thermophilic archaebacterium Thermococcus celer. Nucleic Acids Res 18:3989–3989

    Google Scholar 

  • Baldacci G, Guinet F, Tillit J, Zaccai G, de Recondo AM (1990) Functional implications related to the gene structure of the elongation factor EF-Tu from Halobacterium marismortui. Nucleic Acids Res 18:507–511

    CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326:332–333

    Article  CAS  PubMed  Google Scholar 

  • Cavalier-Smith T (1991) The evolution of cells. In: Osawa S, Honjo T (eds) Evolution of life: fossils, molecules, and culture. Springer-Verlag, Tokyo, pp 271–304

    Google Scholar 

  • Dayhoff MO, Schwartz RM, Orcutt BC (1978) A model of evolutionary change in proteins. In: Dayhoff MO (ed) Atlas of protein sequence and structure, vol 5, suppl 3. National Biomedical Research Foundation, Washington DC, pp 345–352

    Google Scholar 

  • De Meester F, Bracha R, Huber M, Keren Z, Rozenblatt S, Mirelman D (1991) Cloning and characterization of an unusual elongation factor-1α cDNA from Entamoeba histolytica. Mol Biochem Parasitol 44:23–32

    Google Scholar 

  • Douglas SE, Murphy CA, Spencer DF, Gray MW (1991) Cryptomonad algae are evolutionary chimaeras of two phylogenetically distinct unicellular eukaryotes. Nature 350:148–151

    Google Scholar 

  • Felsenstein J (1978a) The number of evolutionary trees. Syst Zool 27:27–33

    Google Scholar 

  • Felsenstein J (1978b) Cases in which parsimony and compatibility methods will be positively misleading. Syst Zool 27:401–410

    Google Scholar 

  • Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376

    CAS  PubMed  Google Scholar 

  • Fukami-Kobayashi K, Tateno Y (1991) Robustness of maximum likelihood tree estimation against different patterns of base substitutions. J Mol Evol 32:79–91

    Google Scholar 

  • Gouy M, Li W-H (1989) Molecular phylogeny of the kingdoms Animalia, Plantae, and Fungi. Mol Biol Evol 6:109–122

    Google Scholar 

  • Hasegawa M, Cao Y, Adachi J, Yano T (1992) Rodent polyphyly? Nature 355:595

    Google Scholar 

  • Hasegawa M, Fujiwara M (1993) Relative efficiencies of the maximum likelihood, maximum parsimony, and neighbor joining methods for estimating protein phylogeny. Mol Phyl Evol (in press)

  • Hasegawa M, Iida Y, Yano T, Takaiwa F, Iwabuchi M (1985) Phylogenetic relationships among eukaryotic kingdoms inferred from ribosomal RNA sequences. J Mol Evol 22:32–38

    Google Scholar 

  • Hasegawa M, Kishino H, Hayasaka K, Horai S (1990) Mitochondrial DNA evolution in primates: transition rate has been extremely low in lemur. J Mol Evol 31:113–121

    Google Scholar 

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

    Google Scholar 

  • Hayashi Y, Urade R, Utsumi S, Kito M (1989) Anchoring of peptide elongation factor EF-1α by phosphatidylinositol at the endoplasmic reticulum membrane. J Biochem 106:560–563

    Google Scholar 

  • Hendriks L, De Baere R, Van de Peer Y, Neefs J, Goris A (1991) The evolutionary position of rhodophyte Porphyra umbilicalis and the basidiomycete Leucosporidium scottii among other eukaryotes as deduced from complete sequences of small ribosomal subunit RNA. J Mol Evol 32:167–177

    Google Scholar 

  • Herzog M, Maroteaux L (1986) Dinoflagellate 17S rRNA sequence inferred from the gene sequence: evolutionary implications. Proc Natl Acad Sci USA 83:8644–8648

    Google Scholar 

  • Hovemann B, Richer S (1988) Two genes encode related cytoplasmic elongation factors 1-α (EF-1) in Drosophila melanogaster with continuous and stage specific expression. Nucleic Acids Res 16:3175–3194

    Google Scholar 

  • Iwabe N, Kuma K, 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 

  • Iwabe N, Kuma K, Kishino H, Hasegawa M, Miyata T (1991) Evolution of RNA polymerases and branching patterns of the three major groups of archaebacteria. J Mol Evol 32:70–78

    Google Scholar 

  • Kimura M, Ohta T (1973) Eukaryote-prokaryote divergence estimated by 5S ribosomal RNA sequences. Nature New Biol 243:199–200

    Google Scholar 

  • Kishino H, Hasegawa M (1989) Evaluation of the maximum like-lihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179

    CAS  PubMed  Google Scholar 

  • Kishino H, Hasegawa M (1990) Converting distance to time: an application to human evolution. Methods Enzymol 183:550–570

    Google Scholar 

  • Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–160

    Google Scholar 

  • Krieg PA, Varnum SM, Wormington WM, Melton DA (1989) The mRNA encoding elongation factor 1α (EF-1α) is a major transcript at the midblastula transition in Xenopus. Dev Biol 133:93–100

    Google Scholar 

  • Lechner K, Böck A (1987) Cloning and nucleotide sequence of the gene for an archaebacterial protein synthesis elongation factor Tu. Mol Gen Genet 208:523–528

    Google Scholar 

  • Li W-H (1989) A statistical test of phylogenies estimated from sequence data. Mol Biol Evol 6:424–435

    Google Scholar 

  • Liboz T, Bardet C, Le Van Thai A, Axelos M, Lescure B (1989) The four members of the gene family encoding the A. thaliana translation elongation factor. Plant Mol Biol 14:107–110

    Google Scholar 

  • Linz JE, Lira LM, Sypherd PS (1986) The primary structure and the functional domains of an elongation factor-1α from Mucor racemosus. J Biol Chem 261:15022–15029

    Google Scholar 

  • Loomis WF, Smith DW (1990) Molecular phylogeny of Dictyostelium discoideum by protein sequence comparison. Proc Natl Acad Sci USA 87:9093–9097

    Google Scholar 

  • McCarroll R, Olsen GJ, Stahl YD, Woese CR, Sogin ML (1983) Nucleotide sequence of the Dictyostelium discoideum small-subunit ribosomal ribonucleic acid inferred from the gene sequence: evolutionary implications. Biochemistry 22:5858–5868

    Google Scholar 

  • Miyata T, Iwabe N, Kuma K, Kawanishi Y, Hasegawa M, Kishino H, Mukohata Y, Ihara K, Osawa S (1991) Evolution of archaebacteria: Phylogenetic relationships among archaebacteria, eubacteria, and eukaryotes. In: Osawa S, Honjo T (eds) Evolution of life: fossils, molecules, and culture. Springer-Verlag, Tokyo, pp 337–351

    Google Scholar 

  • Montandon PE, Stutz E (1990) Structure and expression of the Euglena gracilis nuclear gene coding for the translation elongation factor EF-1a. Nucleic Acids Res 18:75–82

    Google Scholar 

  • Nagashima K, Kasai M, Nagata S, Kaziro Y (1986) Structure of the two genes coding for polypeptide chain elongation factor 1-α (EF-1-α) from Saccharomyces cerevisiae. Gene 45:265–273

    Google Scholar 

  • Pokalsky AR, Hiatt WR, Ridge N, Rasmussen R, Houck CM, Shewmaker CK (1989) Structure and expression of elongation factor 1α in tomato. Nucleic Acids Res 17:4661–4673

    Google Scholar 

  • Sakamoto Y, Ishiguro M, Kitagawa G (1986) Akaike information criterion statistics. D Reidel Publ Comp, Dordrecht

    Google Scholar 

  • Schwartz RM, Dayhoff MO (1978) Origins of prokaryotes, eukaryotes, mitochondria, and chloroplasts. Science 199:395–403

    Google Scholar 

  • Sogin ML, Elwood HJ, Gunderson JH (1986) Evolutionary diversity of eukaryotic small-subunit rRNA genes. Proc Natl Acad Sci USA 83:1383–1387

    Google Scholar 

  • Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989a) Phylogenetic meaning of the kingdom concept: An unusual ribosomal RNA from Giardia lamblia. Science 243: 75–77

    CAS  PubMed  Google Scholar 

  • Sogin ML, Edman U, Elwood H (1989b) A single kingdom of eukaryotes. In: Fernholm B, Bremer K, Jörnvall H (eds) The hierarchy of life. Elsevier, Amsterdam, pp 133–143

    Google Scholar 

  • Sundstrom P, Smith D, Sypherd PS (1990) Sequence analysis and expression of the two genes for elongation factor 1-α from the dimorphic yeast Candida albicans. J Bacteriol 172: 2036–2045

    Google Scholar 

  • Tesch A, Klink F (1990) Cloning and sequencing of the gene coding for the elogation factor 1α from the archaebacterium Thermoplasma acidophilum. FEMS Microbiol Lett 71:293–298

    Google Scholar 

  • Uetsuki T, Naito A, Nagata S, Kaziro Y (1989) Isolation and characterization of the human chromosomal gene for polypeptide chain elongation factor 1-α. J Biol Chem 264:5791–5798

    Google Scholar 

  • van Hemert FJ, Amons R, Pluijms WJM, van Ormondt H, Möller W (1984) The primary structure of elongation factor EF-1α from the brine shrimp Artemia. EMBO J 3:1109–1113

    Google Scholar 

  • Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CR (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411–414

    Article  CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Yang F, Demma M, Warren V, Dharmawardhane S, Condeelis J (1990) Identification of an actin-binding protein from Dictyostelium as elongation factor 1a. Nature 347:494–496

    Google Scholar 

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Hasegawa, M., Hashimoto, T., Adachi, J. et al. Early branchings in the evolution of eukaryotes: Ancient divergence of entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36, 380–388 (1993). https://doi.org/10.1007/BF00182185

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  • DOI: https://doi.org/10.1007/BF00182185

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