Advertisement

Journal of Molecular Evolution

, Volume 42, Issue 2, pp 257–263 | Cite as

Protein phylogeny of translation elongation factor EF-1α suggests microsporidians are extremely ancient eukaryotes

  • Takashi Kamaishi
  • Tetsuo Hashimoto
  • Yoshihiro Nakamura
  • Fuminori Nakamura
  • Shigenori Murata
  • Norihiro Okada
  • Ken-ichi Okamoto
  • Makoto Shimizu
  • Masami Hasegawa
Articles

Abstract

Partial regions of the mRNA encoding a major part of translation elongation factor 1α (EF-1α) from a mitochondrion-lacking protozoan,Glugea plecoglossi, that belongs to microsporidians, were amplified by polymerase chain reaction (PCR) and their primary structures were analyzed. The deduced amino acid sequence was highly divergent from typical EF-1α's of eukaryotes, although it clearly showed a eukaryotic feature when aligned with homologs of the three primary kingdoms. Maximum likelihood (ML) analyses on the basis of six different stochastic models of amino acid substitutions and a maximum parsimony (MP) analysis consistently suggest that among eukaryotic species being analyzed,G. plecoglossi is likely to represent the earliest offshoot of eukaryotes. Microsporidians might be the extremely ancient eukaryotes which have diverged before an occurrence of mitochondrial symbiosis.

Key words

Microsporidians Glugea plecoglossi Eukaryotes Mitochondrion-lacking protozoa Elongation factor 1α Protein phylogeny 

Abbreviations

EF-1α

translation elongation factor 1α

EF-Tu

translation elongation factor Tu

SrRNA

small subunit ribosomal RNA

ML

maximum likelihood

MP

maximum parsimony

PCR

polymerase chain reaction

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 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, TokyoGoogle Scholar
  2. Auer J, Spicker G, Mayerhofer L, Pühler G, Böck A (1990) Organization and nucleotide sequence of a gene cluster comprising the translation elongation factor 1α from the extreme thermophilic archaebacteriumSulfolobus acidocaldarius. Syst Appl Microbiol 14:14–22Google Scholar
  3. Axelos M, Bardet C, Liboz T, Le Van Thai A, Curie C, Lescure B (1989) The gene family encoding theArabidopsis thaliana translation elongation factor EF-1α: molecular cloning, characterization and expression. Mol Gen Genet 219:106–112Google Scholar
  4. 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 fromHalobacterium marismortui. Nucleic Acids Res 18:507–511Google Scholar
  5. Baldauf SL, Palmer JD (1993) Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA 90:11558–11562Google Scholar
  6. Brands JHGM, Maassen JA, van Hemert FJ, Amons R, Möller W (1986) The primary structure of the α subunit of human elongation factor 1. Structural aspects of guanine-nucleotide-binding sites. Eur J Biochem 155:167–171Google Scholar
  7. Brown JR, Doolittle WF (1995) The root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc Natl Acad Sci USA 92:2441–2445Google Scholar
  8. Cao Y, Adachi J, Yano T, Hasegawa M (1994a) Phylogenetic place of guinea pigs: no support of the rodent-polyphyly hypothesis from maximum-likelihood analyses of multiple protein sequences. Mol Biol Evol 11:593–604Google Scholar
  9. Cao Y, Adachi J, Janke A, Pääbo S, Hasegawa M (1994b) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J Mol Evol 39:519–527Google Scholar
  10. Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326:332–333Google Scholar
  11. Cavalier-Smith T (1989) Archaebacteria and archezoa. Nature 339:100–101Google Scholar
  12. 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 271–304Google Scholar
  13. De Meester F, Bracha R, Huber M, Keren Z, Rozenblatt S, Mirelman D (1991) Cloning and characterization of an unusual elongation factor-1α cDNA fromEntamoeba histolytica. Mol Biochem Parasitol 44:23–32Google Scholar
  14. Hanahan D (1983) Studies on transformation ofEscherichia coli with plasmids. J Mol Biol 166:557–580Google Scholar
  15. Hasegawa M, Fujiwara M (1993) Relative efficiencies of maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol Phylogenet Evol 2:1–5Google Scholar
  16. Hasegawa M, Hashimoto T (1993) Ribosomal RNA trees misleading? Nature 361:23–23Google Scholar
  17. Hasegawa M, Hashimoto T, Adachi J (1992a) Origin and evolution of eukaryotes as inferred from protein sequence data. In: Hartman H, Matsuno K (eds) The origin and evolution of the cell. World Scientific, SingaporeGoogle Scholar
  18. Hasegawa M, Cao Y, Adachi J, Yano T (1992b) Rodent polyphyly? Nature 355:595–595Google Scholar
  19. Hasegawa M, Hashimoto T, Adachi J, Iwabe N, Miyata T (1993) Early branchings in the evolution of eukaryotes: ancient divergence of Entamoeba that lacks mitochondria revealed by protein sequence data. J Mol Evol 36:380–388Google Scholar
  20. Hasegawa M, Kishino H (1994) Accuracies of the simple methods for estimating the bootstrap probability of a maximum-likelihood tree. Mol Biol Evol 11:142–145Google Scholar
  21. Hashimoto T, Adachi J, Hasegawa M (1992) Phylogenetic place of Giardia lamblia, a protozoan that lacks mitochondria. Endocytobiosis Cell Res 9:59–69Google Scholar
  22. Hashimoto T, Nakamura Y, Nakamura F, Shirakura T, Adachi J, Goto N, Okamoto K, Hasegawa M (1994) Protein phylogeny gives a robust estimation for early divergences of eukaryotes: phylogenetic place of a mitochondria-lacking protozoan,Giardia lamblia. Mol Biol Evol 11:65–71Google Scholar
  23. Hashimoto T, Nakamura Y, Kamaishi T, Adachi J, Nakamura F, Okamoto K, Hasegawa M (1995a) Phylogenetic place of kinetoplastid protozoa inferred from protein phylogeny of elongation factor 1α. Mol Biochem Parasitol 70:181–185Google Scholar
  24. Hashimoto T, Nakamura Y, Kamaishi T, Nakamura F, Adachi J, Okamoto K, Hasegawa M (1995b) Phylogenetic place of a mitochondrion-lacking protozoan,Giardia lamblia, inferred from amino acid sequences of elongation factor 2. Mol Biol Evol 12:782–793Google Scholar
  25. Hoshina T (1951) On a new microsporidian,Pleistophora anguillarum n.sp., from the muscle of the eel,Anguilla Japonica. J Tokyo Univ Fish 38:35–49Google Scholar
  26. Hovemann B, Richer S (1988) Two genes encode related cytoplasmic elongation factors 1-α (EF-1) inDrosophila melanogaster with continuous and stage specific expression. Nucleic Acids Res 16:3175–3194Google Scholar
  27. 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 86:9355–9359Google Scholar
  28. Kishino H, Hasegawa M (1989) Evaluation of the maximum likelihood estimate of the evolutionary tree topologies from DNA sequence data, and the branching order in Hominoidea. J Mol Evol 29:170–179Google Scholar
  29. Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–160Google Scholar
  30. Kurasawa Y, Numata O, Katoh M, Hirano H, Chiba J, Watanabe Y (1992) Identification ofTetrahymena 14-nm filament-associated protein as elongation factor 1α. Exp Cell Res 203:251–258Google Scholar
  31. Lechner K, Böck A (1987) Cloning and nucleotide sequence of the gene for an archaebacterial protein synthesis elongation factor Tu. Mol Gen Genet 208:523–528Google Scholar
  32. Leipe DD, Gunderson JH, Nerad TA, Sogin ML (1993) Small subunit ribosomal RNA+ ofHexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 59:41–48Google Scholar
  33. Linz JE, Lira LM, Sypherd PS (1986) The primary structure and the functional domains of an elongation factor-1α fromMucor racemosus. J Biol Chem 261:15022–15029Google Scholar
  34. Lom J, Dyková I (1992) Protozoan parasites of fishes. Elsevier Science, AmsterdamGoogle Scholar
  35. 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 337–351Google Scholar
  36. Montandon PE, Stutz E (1990) Structure and expression of theEuglena gracilis nuclear gene coding for the translation elongation factor EF-1a. Nucleic Acids Res 18:75–82Google Scholar
  37. Nagashima K, Kasai M, Nagata S, Kaziro Y (1986) Structure of the two genes coding for polypeptide chain elongation factor 1-α (EF-1α) fromSaccharomyces cerevisiae. Gene 45:265–273Google Scholar
  38. 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 17:4661–4673Google Scholar
  39. Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257:74–76Google Scholar
  40. Sakamoto Y, Ishiguro M, Kitagawa G (1986) Akaike information criterion statistics. D Reidel, DordrechtGoogle Scholar
  41. Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, 2nd ed. Cold Spring Harbor Laboratory Press, New YorkGoogle Scholar
  42. Shirakura T, Hashimoto T, Nakamura Y, Kamaishi T, Cao Y, Adachi J, Hasegawa M, Yamamoto A, Goto N (1994) Phylogenetic place of a mitochondria-lacking protozoan,Entamoeba histolytica, inferred from amino acid sequences of elongation factor 2. Jpn J Genet 69:119–135Google Scholar
  43. Sogin ML (1991) Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1:457–463Google Scholar
  44. Sogin ML, Edman U, Elwood H (1989a) A single kingdom of eukaryotes. In: Fernholm B, Bremer K, Jörnvall H (eds) The hierarchy of life. Elsevier Science, Amsterdam, pp 133–143Google Scholar
  45. Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989b) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA fromGiardia lamblia. Science 243:75–77Google Scholar
  46. Takahashi S, Egusa S (1977) Studies onGlugea infection of the ayu,Plecoglossus altivelis—I. Description of theGlugea and a proposal of a new species,Glugea plecoglossi (in Japanese). Fish Path 11:175–182Google Scholar
  47. Takvorian PM, Cali A (1994) Enzyme histochemical identification of the Golgi apparatus in the microsporidian,Glugea stephani. J Euk Microbiol 41(Suppl):63S-64SGoogle Scholar
  48. Vossbrinck CR, Maddox JV, Friedman S, Debrunner-Vossbrinck BA, Woese CR (1987) Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411–414Google Scholar
  49. Yang F, Demma M, Warren V, Dharmawardhane S, Condeelis J (1990) Identification of an actin-binding protein fromDictyostelium as elongation factor 1a. Nature 347:494–496Google Scholar

Copyright information

© Springer-Verlag New York Inc. 1996

Authors and Affiliations

  • Takashi Kamaishi
    • 1
    • 5
  • Tetsuo Hashimoto
    • 2
  • Yoshihiro Nakamura
    • 3
  • Fuminori Nakamura
    • 1
  • Shigenori Murata
    • 4
  • Norihiro Okada
    • 4
  • Ken-ichi Okamoto
    • 1
  • Makoto Shimizu
    • 5
  • Masami Hasegawa
    • 2
  1. 1.Department of Medical Biology, School of MedicineShowa UniversityTokyoJapan
  2. 2.The Institute of Statistical MathematicsTokyoJapan
  3. 3.Laboratory of Gene ManipulationShowa UniversityTokyoJapan
  4. 4.Faculty of Bioscience and BiotechnologyTokyo Institute of TechnologyYokohamaJapan
  5. 5.Department of Fisheries, Faculty of AgricultureThe University of TokyoTokyoJapan

Personalised recommendations