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.
Article PDF
Similar content being viewed by others
Avoid common mistakes on your manuscript.
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
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
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 14:14–22
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 219:106–112
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 18:507–511
Baldauf SL, Palmer JD (1993) Animals and fungi are each other's closest relatives: congruent evidence from multiple proteins. Proc Natl Acad Sci USA 90:11558–11562
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 155:167–171
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 92:2441–2445
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 11:593–604
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 39:519–527
Cavalier-Smith T (1987) Eukaryotes with no mitochondria. Nature 326:332–333
Cavalier-Smith T (1989) Archaebacteria and archezoa. Nature 339:100–101
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
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 44:23–32
Hanahan D (1983) Studies on transformation ofEscherichia coli with plasmids. J Mol Biol 166:557–580
Hasegawa M, Fujiwara M (1993) Relative efficiencies of maximum likelihood, maximum parsimony, and neighbor-joining methods for estimating protein phylogeny. Mol Phylogenet Evol 2:1–5
Hasegawa M, Hashimoto T (1993) Ribosomal RNA trees misleading? Nature 361:23–23
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, Singapore
Hasegawa M, Cao Y, Adachi J, Yano T (1992b) Rodent polyphyly? Nature 355:595–595
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 36:380–388
Hasegawa M, Kishino H (1994) Accuracies of the simple methods for estimating the bootstrap probability of a maximum-likelihood tree. Mol Biol Evol 11:142–145
Hashimoto T, Adachi J, Hasegawa M (1992) Phylogenetic place of Giardia lamblia, a protozoan that lacks mitochondria. Endocytobiosis Cell Res 9:59–69
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 11:65–71
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 70:181–185
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 12:782–793
Hoshina T (1951) On a new microsporidian,Pleistophora anguillarum n.sp., from the muscle of the eel,Anguilla Japonica. J Tokyo Univ Fish 38:35–49
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 16:3175–3194
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
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 29:170–179
Kishino H, Miyata T, Hasegawa M (1990) Maximum likelihood inference of protein phylogeny and the origin of chloroplasts. J Mol Evol 30:151–160
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 203:251–258
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
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 59:41–48
Linz JE, Lira LM, Sypherd PS (1986) The primary structure and the functional domains of an elongation factor-1α fromMucor racemosus. J Biol Chem 261:15022–15029
Lom J, Dyková I (1992) Protozoan parasites of fishes. Elsevier Science, Amsterdam
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
Montandon PE, Stutz E (1990) Structure and expression of theEuglena gracilis nuclear gene coding for the translation elongation factor EF-1a. Nucleic Acids Res 18:75–82
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 45:265–273
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
Rivera MC, Lake JA (1992) Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257:74–76
Sakamoto Y, Ishiguro M, Kitagawa G (1986) Akaike information criterion statistics. D Reidel, Dordrecht
Sambrook J, Fritsch EF, Maniatis T (1989) Molecular cloning, 2nd ed. Cold Spring Harbor Laboratory Press, New York
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 69:119–135
Sogin ML (1991) Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1:457–463
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 133–143
Sogin ML, Gunderson JH, Elwood HJ, Alonso RA, Peattie DA (1989b) Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA fromGiardia lamblia. Science 243:75–77
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 11:175–182
Takvorian PM, Cali A (1994) Enzyme histochemical identification of the Golgi apparatus in the microsporidian,Glugea stephani. J Euk Microbiol 41(Suppl):63S-64S
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
Yang F, Demma M, Warren V, Dharmawardhane S, Condeelis J (1990) Identification of an actin-binding protein fromDictyostelium as elongation factor 1a. Nature 347:494–496
Author information
Authors and Affiliations
Additional information
Sequence availability: The nucleotide sequence data reported here appear in the GSDB, DDBJ, EMBL, and NCBI databases with the accession number D32139
Rights and permissions
About this article
Cite this article
Kamaishi, T., Hashimoto, T., Nakamura, Y. et al. Protein phylogeny of translation elongation factor EF-1α suggests microsporidians are extremely ancient eukaryotes. J Mol Evol 42, 257–263 (1996). https://doi.org/10.1007/BF02198852
Received:
Accepted:
Issue Date:
DOI: https://doi.org/10.1007/BF02198852