Mitochondrial connection to the origin of the eukaryotic cell

European Journal of Biochemistry

Volumn 270, Issue 8, 2003, Pages 1599-1618

  Emelyanov, Victor V ^a  

^a GAMALEYA RESEARCH INSTITUTE OF EPIDEMIOLOGY AND MICROBIOLOGY   (Russian Federation)

Author keywords

Endosymbiotic origin; Energy metabolism; Eukaryogenesis; Fusion hypothesis; Mitochondrial ancestor; Paralogous protein family; Phylogenetic analysis; Respiration; Rickettsiae

Indexed keywords

AMINO ACID TRANSFER RNA LIGASE; GLYCERALDEHYDE 3 PHOSPHATE DEHYDROGENASE; GLYCOLYTIC ENZYME; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; MITOCHONDRIAL PROTEIN; PHOSPHOLIPASE; RIBOSOME RNA;

AMINO ACID SEQUENCE; ARCHAEBACTERIUM; BACTERIAL GENOME; CELL MEMBRANE; CELL ORGANELLE; ENERGY METABOLISM; ENZYME ACTIVITY; EUBACTERIUM; EUKARYOTIC CELL; FERMENTATION; FLAGELLATE; GENOMICS; GLYCOLYSIS; MITOCHONDRION; MOLECULAR EVOLUTION; MOLECULAR PHYLOGENY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROKARYOTE; PROTEIN FAMILY; REVIEW; RICKETTSIACEAE; SEQUENCE ANALYSIS; UNINDEXED SEQUENCE;

AMINO ACID SEQUENCE; ANIMALS; CONSERVED SEQUENCE; ENERGY METABOLISM; EUKARYOTIC CELLS; GLYCOLYSIS; HUMANS; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; SEQUENCE ALIGNMENT; VALINE-TRNA LIGASE;

ARCHAEA; ARCHEZOA; BACTERIA (MICROORGANISMS); EUKARYOTA; MASTIGOPHORA (FLAGELLATES); PROKARYOTA; PROTOZOA; RICKETTSIA; RICKETTSIACEAE;

EID: 0037733985     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1033.2003.03499.x     Document Type: Review

References (159)

1. Brown, J.R. & Doolittle, W.F. (1997) Archaea and prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456-502.
2. Feng, D.-F., Cho, G. & Doolittle, R.F. (1997) Determining divergence times with a protein clock: update and reevaluation. Proc. Natl Acad. Sci. USA 94, 13028-13033.
3. Gupta, R.S. & Golding, G.B. (1996) The origin of the eukaryotic cell. Trends Biochem. Sci. 21, 166-171.
4. Horiike, T., Hamada, K., Kanaya, S. & Shinozawa, T. (2001) Origin of eukaryotic cell nuclei by symbiosis of Archaea in Bacteria is revealed by homology-hit analysis. Nat. Cell Biol. 3, 210-214.
5. Lake, J.A. & Rivera, M.C. (1994) Was the nucleus the first endosymbiont? Proc. Natl Acad. Sci. USA 91, 2880-2881.
6. Ribeiro, S. & Golding, G.B. (1998) The mosaic nature of eukaryotic nucleus. Mol. Biol. Evol. 15, 779-788.
7. Rivera, M.C., Jain, R., Moore, J.E. & Lake, J.A. (1998) Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239-6244.
8. Adams, K.L., Daley, D.O., Qiu, Y.L., Whelan, J. & Palmer, J.D. (2000) Repeated, recent and diverse transfers of a mitochondrial gene to the nucleus in flowering plants. Nature (London) 408, 354-357.
9. Andersson, S.G.E., Zomorodipour, A., Andersson, J.O., Sicheritz-Ponten, T., Alsmark, U.C.M., Podowski, R.M., Näslund, A.K., Eriksson, A.-S., Winkler, H.H. & Kurland, C.G. (1998) The genome sequence of Rickettsia prowazekii and the origin of mitochondria. Nature (London) 396, 133-140.
10. Gray, M.W., Burger, G. & Lang, B.F. (1999) Mitochondrial evolution. Science 283, 1476-1481.
11. Lang, B.F., Gray, M.W. & Burger, G. (1999) Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33, 351-397.
12. Gray, M.W. (2000) Mitochondrial genes on the move. Nature (London) 408, 302-305.
13. Kurland, C.G. & Andersson, S.G.E. (2000) Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786-820.
14. Marcotte, E.M., Xenarios, I., van der Bliek, A.M. & Eisenberg, D. (2000) Localizing proteins in the cell from their phylogenetic profiles. Proc. Natl Acad. Sci. USA 97, 12115-12120.
15. Embley, T.M. & Hirt, R.P. (1998) Early branching eukaryotes? Curr. Opin. Genet. Dev. 8, 624-629.
16. Keeling, P.J. (1998) Kingdom's progress: Archezoa and the origin of eukaryotes. Bioessays 20, 87-95.
17. Roger, A.J. (1999) Reconstructing early events in eukaryotic evolution. Am. Nat. 152, S146-S163.
18. Hashimoto, T., Sanchez, L.B., Shirakura, T., Müller, M. & Hasegawa, M. (1998) Secondary absence of mitochondria in Giardia lamblia and Trichomonas vaginalis revealed by valyl-tRNA synthetase phylogeny. Proc. Natl Acad. Sci. USA 95, 6860-6865.
19. Martin, W. & Müller, M. (1998) The hydrogen hypothesis for the first eukaryote. Nature (London) 392, 37-41.
20. Schnarrenberger, C. & Martin, W. (2002) Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants. A case study of endosymbiotic gene transfer. Eur. J. Biochem. 269, 868-883.
21. Gupta, R.S., Aitken, K., Falah, M. & Singh, B. (1994) Cloning of Giardia lamblia heat shock protein HSP70 homologs: implications regarding origin of eukaryotic cells and of endoplasmic reticulum. Proc. Natl Acad. Sci. USA 91, 2895-2899.
22. Gupta, R.S. (1995) Evolution of the chaperonin families (Hsp60, Hsp10 and Tcp-1) of proteins and the origin of eukaryotic cells. Mol. Microbiol. 15, 1-11.
23. Gupta, R.S. (1998) Protein phylogenies and signature sequences: a reappraisal of evolutionary relationships among archaebacteria, eubacteria, and eukaryotes. Microbiol. Mol. Biol. Rev. 62, 1435-1491.
24. Gupta, R.S. (1999) Origin of eukaryotic cells: was metabolic symbiosis based on hydrogen driving force? Trends Biochem. Sci. 24, 423.
25. Cavalier-Smith, T. (1998) A revised six-kingdom system of life. Biol. Rev. 73, 203-266.
26. Cavalier-Smith, T. (2002) The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297-354.
27. Doolittle, R.F. (2000) Searching for the common ancestor. Res. Microbiol. 151, 85-89.
28. Doolittle, W.F. (1998) You are what you eat: a gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307-311.
29. Doolittle, W.F. (1998) A paradigm gets shifty. Nature (London) 392, 15-16.
30. Margulis, L., Dolan, M.F. & Guerrero, R. (2000) The chimeric eukaryote: origin of the nucleus from karyomastigont in amitochondriate protists. Proc. Natl Acad. Sci. USA 97, 6954-6959.
31. Bui, E.T., Bradley, P.J. & Johnson, P.J. (1996) A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl Acad. Sci. USA 93, 9651-9656.
32. Clark, C.G. & Roger, A.J. (1995) Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl Acad. Sci. USA 92, 6518-6521.
33. Duncan, R., Faggart, M.A., Roger, A.J. & Cornell, N.W. (1999) Phylogenetic analysis of the 5-aminolevulinate synthase. Mol. Biol. Evol. 16, 383-396.
34. Emelyanov, V.V. (2001) Evolutionary relationship of rickettsiae and mitochondria. FEBS Lett. 501, 11-18.
35. Germot, A., Philippe, H. & LeGuyader, H. (1996) Presence of a mitochondrial-type 70-kDa heat shock protein in Trichomonas vaginalis suggests a very early mitochondrial endosymbiosis in eukaryotes. Proc. Natl Acad. Sci. USA 93, 14614-14617.
36. Germot, A., Philippe, H. & LeGuyader, H. (1997) Evidence for loss of mitochondria in Microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol. Biochem. Parasitol. 87, 159-168.
37. Gray, M.W. (1998) Rickettsia, typhus and the mitochondrial connection. Nature (London) 396, 109-110.
38. Horner, D.S., Hirt, R.P., Kilvington, S., Lloyd, D. & Embley, T.M. (1996) Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc. R. Soc. London Ser. B 263, 1053-1059.
39. Olsen, G.J., Woese, C.R. & Overbeek, R. (1994) The winds of (evolutionary) change: breathing new life into microbiology. J. Bacteriol. 176, 1-6.
40. Peyretaillade, E., Broussolle, V., Peyret, P., Metenier, G., Gouy, M. & Vivares, C.P. (1998) Microsporidia, amitochondrial profists, possess a 70-kDa heat shock protein gene of mitochondrial origin. Mol. Biol. Evol. 15, 683-689.
41. Roger, A.J., Clark, C.G. & Doolittle, W.F. (1996) A possible mitochondrial gene in the early branching amitochondriate protist Trichomonas vaginalis. Proc. Natl Acad. Sci. USA 93, 14618-14622.
42. Roger, A.J., Svärd, S.G., Tovar, J., Clark, C.G., Smith, M.W., Gillin, F.D. & Sogin, M.L. (1998) A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to progenitor of mitochondria. Proc. Natl Acad. Sci. USA 95, 229-234.
43. Tachezy, J., Sanchez, L.B. & Müller, M. (2001) Mitochondrial type iron-sulfur cluster assembly in the amitochondriate eukaryotes Trichomonas vaginalis and Giardia intestinalis, as indicated by the phylogeny of IscS. Mol. Biol. Evol. 18, 1919-1928.
44. Viale, A.M. & Arakaki, A.K. (1994) The chaperone connection to the origins of the eukaryotic organelles. FEBS Lett. 341, 146-151.
45. Palmer, J.D. (1997) Organelle genomes: going, going, gone! Science 275, 790-791.
46. Field, J., Rosenthal, B. & Samuelson, J. (2000) Early lateral transfer of genes encoding malic enzyme, acetyl-CoA synthetase and alcohol dehydrogenase from anaerobic prokaryotes to Entamoeba histolytica. Mol. Microbiol. 38, 446-455.
47. Figge, R.M., Schubert, M., Brinkmann, H. & Cerff, R. (1999) Glyceraldehyde-3-phosphate dehydrogenase gene diversity in eubacteria and eukaryotes: evidence for intra- and interkingdom gene transfer. Mol. Biol. Evol. 16, 429-440.
48. Gerbod, D., Edgcomb, V.P., Noel, C., Vanacova, S., Wintjens, R., Tachezy, J., Sogin, M.L. & Viscogliosi, E. (2001) Phylogenetic relationships of class II fumarase genes from trichomonad species. Mol. Biol. Evol. 18, 1574-1584.
49. Hannaert, V., Brinkmann, H., Nowitzki, U., Lee, J.A., Albert, M.-A., Sensen, C.W., Gaasterland, T., Müller, M., Michels, P. & Martin, W. (2000) Enolase from Trypanosoma brucei, from the amitochondriate protist Mastigamoeba balamuthi, and from the chloroplast and cytosol of Euglena gracilis: pieces in the evolutionary puzzle of the eukaryotic glycolytic pathway. Mol. Biol. Evol. 17, 989-1000.
50. Henze, K., Horner, D.S., Suguri, S., Moore, D.V., Sanchez, L.B., Müller, M. & Embley, T.M. (2001) Unique phylogenetic relationships of glucokinase and glucose phosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis. Gene 281, 123-131.
51. Horner, D.S., Foster, P.G. & Embley, T.M. (2000) Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 17, 1695-1709.
52. de Koning, A.P., Brinkman, F.J., Jones, S.J. & Keeling, P.J. (2000) Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol. Biol. Evol. 17, 1769-1773.
53. Qian, Q. & Keeling, P.J. (2001) Diplonemid glyceraldehyde-3-phosphate dehydrogenase (GAPDH) and prokaryote-to-eukaryote lateral gene transfer. Protist 152, 193-201.
54. Wu, G., Henze, K. & Müller, M. (2001) Evolutionary relationships of the glucokinase from the amitochondriate protist, Trichomonas vaginalis. Gene 264, 265-271.
55. Doolittle, R.F. (1998) Microbial genomes opened up. Nature (London) 392, 339-342.
56. Faguy, D.M. & Doolittle, W.F. (1998) Cytoskeletal proteins: the evolution of cell division. Curr. Biol. 8, R338-R341.
57. van den Ent, F., Amos, L.A. & Löwe, J. (2001) Prokaryotic origin of the actin cytoskeleton. Nature (London) 413, 39-44.
58. Capela, D., Barloy-Hubler, F., Gouzy, J., Bothe, G., Ampe, F., Batut, J., Boistard, P., Becker, A., Boutry, M., Cadieu, E., Dreano, S., Gloux, S., Godrie, T., Goffeau, A., Kahn, D., Kiss, E., Lelaure, V., Masuy, D., Pohl, T., Portetelle, D., Puhler, A., Purnelle, B., Ramsperger, U., Renard, C., Thebault, P., Vandenbol, M., Weidner, S. & Galibert, F. (2001) Analysis of the chromosome sequence of the legume symbiont Sinorhizobium meliloti strain 1021. Proc. Natl Acad. Sci. USA 98, 9877-9882.
59. DelVecchio, V.G., Kapatral, V., Redkar, R.J., Patra, G., Mujer, C., Los, T., Ivanova, N., Anderson, I., Bhattacharyya, A., Lykidis, A., Reznik, G., Jablonski, L., Larsen, N., D'Souza, M., Bernal, A., Mazur, M., Goltsman, E., Selkov, E., Elzer, P.H., Hagius, S., O'Callaghan, D., Letesson, J.J., Haselkorn, R., Kyrpides, N. & Overbeek, R. (2002) The genome sequence of the facultative intracellular pathogen Brucella melitensis. Proc. Natl Acad. Sci. USA 99, 443-448.
60. Goodner, B., Hinkle, G., Gattung, S., Miller, N., Blanchard, M., Qurollo, B., Goldman, B.S., Cao, Y., Askenazi, M., Halling, C., Mullin, L., Houmiel, K., Gordon, J., Vaudin, M., Iartchouk, O., Epp, A., Liu, F., Woliam, C., Allinger, M., Doughty, D., Scott, C., Lappas, C., Markelz, B., Flanagan, C., Crowell, C., Gurson, J., Lomo, C., Sear, C., Strub, G., Cielo, C. & Slater, S. (2001) Genome sequence of the plant pathogen and biotechnology agent Agrobacterium tumefaciens C58. Science 294, 2323-2331.
61. Kaneko, T., Nakamura, Y., Sato, S., Asamizu, E., Kato, T., Sasamoto, S., Watanabe, A., Idesawa, K., Ishikawa, A., Kawashima, K., Kimura, T., Kishida, Y., Kiyokawa, C., Kohara, M., Matsumoto, M., Matsuno, A., Mochizuki, Y., Nakayama, S., Nakazaki, N., Shimpo, S., Sugimoto, M., Takeuchi, C., Yamada, M. & Tabata, S. (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res. 7, 331-338.
62. Nierman, W.C., Feldblyum, T.V., Laub, M.T., Paulsen, I.T., Nelson, K.E., Eisen, J.A., Heidelberg, J.F., Alley, M.R., Ohta, N., Maddock, J.R., Potocka, I., Nelson, W.C., Newton, A., Stephens, C., Phadke, N.D., Ely, B., DeBoy, R.T., Dodson, R.J., Durkin, A.S., Gwinn, M.L, Haft, D.H., Kolonay, J.F., Smit, J., Craven, M.B., Khouri, H., Shetty, J., Berry, K., Utterback, T., Tran, K., Wolf, A., Vamathevan, J., Ermolaeva, M., White, O., Salzberg, S.L., Venter, J.C., Shapiro, L., Fraser, C.M. & Eisen, J. (2001) Complete genome sequence of Caulobacter crescentus. Proc. Natl Acad. Sci. USA 98, 4136-4141.
63. Ogata, H., Audic, S., Renesto-Audiffren, P., Fournier, P.-E., Barbe, V., Samson, D., Roux, V., Cossart, P., Weissenbach, J., Claverie, J.-M. & Raoult, D. (2001) Mechanisms of evolution in Rickettsia conorii and Rickettsia prowazekii. Science 293, 2093-2098.
64. Adachi, J. & Hasegawa, M. (1996) MOLPHY, Version 2.3. Comput. Sci. Monogr. 28.
65. Felsenstein, J. (1999) PHYLIP, Phylogeny Inference Package, Version 3.6. University of Washington, Seattle, WA.
66. Strimmer, K. & von Haeseler, A. (1997) Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl Acad. Sci. USA 94, 6815-6819.
67. Swofford, D.L. (1998) PAUP*, Phylogenetic Analysis Using Parsimony (*and other methods), Version 4.0. Sinauer Associates, Sunderland, MA.
68. Brinkmann, H. & Philippe, H. (1999) Archaea sister group of bacteria? Indications from tree reconstruction artifacts in ancient phylogenies. Mol. Biol. Evol. 16, 817-825.
69. Philippe, H., Lopez, P., Brinkmann, H., Budin, K., Germot, A., Laurent, J., Moreira, D., Müller, M. & Le Guyader, H. (2000) Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc. R. Soc. London Ser. B 267, 1213-1221.
70. Archibald, J.M., Logsdon, J.M. jr. & Doolittle, W.F. (2000) Origin and evolution of eukaryotic chaperonins: phylogenetic evidence for ancient duplications in CCT genes. Mol. Biol. Evol. 17, 1456-1466.
71. 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.
72. +-ATPase: implications for the origin of eukaryotes. Proc. Natl Acad. Sci. USA 86, 6661-6665.
73. Gribaldo, S. & Cammarano, P. (1998) The root of the universal tree of life inferred from anciently duplicated genes encoding components of the protein-targeting machinery. J. Mol. Evol. 47, 508-516.
74. Boucher, Y. & Doolittle, W.F. (2000) The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol. Microbiol. 37, 703-716.
75. Doolittle, W.F. (1999) Phylogenetic classification and the universal tree. Science 284, 2124-2129.
76. Martin, W. (1999) Mosaic bacterial chromosomes: a challenge en route to a tree of genomes. Bioessays 21, 99-104.
77. Philippe, H., Germot, A. & Moreira, D. (2000) The new phylogeny of eukaryotes. Curr. Opin. Genet. Dev. 10, 596-601.
78. Reyes, A., Pesole, G. & Saccone, C. (2000) Long-branch attraction phenomenon and the impact of among-site rate variation on rodent phylogeny. Gene 259, 177-187.
79. Kumar, S. (1996) PHYLTEST: a program for testing phylogenetic hypotheses. Pennsylvania State University.
80. Shimodaira, H. & Hasegawa, M. (2001) CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17, 1246-1247.
81. Baughn, A.D. & Malamy, M.H. (2002) A mitochondrial-like aconitase in the bacterium Bacteroides flagilis: implications for the evolution of the mitochondrial Krebs cycle. Proc. Natl Acad. Sci. USA 99, 4662-4667.
82. Henze, K., Morrison, H.G., Sogin, M.L. & Müller, M. (1998) Sequence and phylogenetic position of a class II aldolase gene in the amitochondriate protist, Giardia lamblia. Gene 222, 163-168.
83. Horner, D.S., Hirt, R.P. & Embley, T.M. (1999) A single eubacterial origin of eukaryotic pyruvate:ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 16, 1280-1291.
84. Horner, D.S., Heil, B., Happe, T. & Embley, T.M. (2002) Iron hydrogenases: ancient enzymes in modern eukaryotes. Trends Biochem. Sci. 27, 148-153.
85. Liaud, M.-F., Lichtle, C., Apt, K., Martin, W. & Cerff, R. (2000) Compartment-specific isoforms of TPI and GAPDH are imported into diatom mitochondria as a fusion protein: evidence in favor of a mitochondrial origin of the eukaryotic glycolytic pathway. Mol. Biol. Evol. 17, 213-223.
86. Nowitzki, U., Flechner, A., Kellermann, J., Hasegawa, M., Schnarrenberger, C. & Martin, W. (1998) Eubacterial origin of nuclear genes for chloroplast and cytosolic glucose-6-phosphate isomerase from spinach: sampling eubacterial gene diversity in eukaryotic chromosomes through symbiosis. Gene 214, 205-213.
87. Voncken, F.G., Boxma, B., van Hoek, A.H., Akhmanova, A.S., Vogels, G.D., Huynen, M., Veenhuis, M. & Hackstein, J.H. (2002) A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp. L2. Gene 284, 103-112.
88. Graham, D.E., Overbeek, R., Olsen, G.J. & Woese, C.R. (2000) An archaeal genomic signature. Proc. Natl Acad. Sci. USA 97, 3304-3308.
89. Müller, M. & Martin, W. (1999) The genome of Rickettsia prowazekii and some thoughts on the origin of mitochondria and hydrogenosomes. Bioessays 21, 377-381.
90. Keeling, P.J. & Doolittle, W.F. (1997) Evidence that eukaryotic triosephosphate isomerase is of alpha-proteobacterial origin. Proc. Natl Acad. Sci. USA 94, 1270-1275.
91. Page, R.D.M. (1996) TREEVIEW: an application to display phylogenetic trees on personal computers. Comput. Appl. Biosci. 12, 357-358.
92. Hirt, R.P., Logsdon, J.M. jr., Healy, B., Dorey, M.W., Doolittle, W.F. & Embley, T.M. (1999) Microsporidia are related to fungi: evidence from the largest subunit of RNA polymerase II and other proteins. Proc. Natl Acad. Sci. USA 96, 580-585.
93. Suguri, S., Henze, K., Sanchez, L.B., Moore, D.V. & Müller, M. (2001) Archaebacterial relationships of the phosphoenolpyruvate carboxykinase gene reveal mosaicism of Giardia intestinalis core metabolism. J. Euk. Microbiol. 48, 493-497.
94. Viscogliosi, E. & Müller, M. (1998) Phylogenetic relationships of the glycolytic enzyme, glyceraldehyde-3-phosphate hydrogenase, from parabasalid flagellates. J. Mol. Evol. 47, 190-199.
95. Canbäck, B., Andersson, S.G.E. & Kurland, C.G. (2002) The global phylogeny of glycolytic enzymes. Proc. Natl Acad. Sci. USA 99, 6097-6102.
96. Emelyanov, V.V. (2001) Rickettsiaceae, rickettsia-like endosymbionts, and the origin of mitochondria. Biosci. Rep. 21, 1-17.
97. + oxidoreductase from the mitochondrion of Euglena gracilis and from the apicomplexan Cryptosporidium parvum: a biochemical relic linking pyruvate metabolism in mitochondriate and amitochondriate protists. Mol. Biol. Evol. 18, 710-720.
98. + oxidoreductase in mitochondria of Euglena gracilis. FEBS Lett. 479, 155-157.
99. Chatton, B., Walter, P., Ebel, J.-P., Lacroute, F. & Fasiolo, F. (1988) The yeast VAS1 gene encodes both mitochondrial and cytoplasmic valyl-tRNA synthetases. J. Biol. Chem. 263, 52-57.
100. Hsieh, S.-L. & Campbell, R.D. (1991) Evidence that gene G7a in the human major histocompatibility complex encodes valyl-tRNA synthetase. Biochem. J. 278, 809-816.
101. Souciet, G., Menand, B., Ovesna, J., Cosset, A., Dietrich, A. & Wintz, H. (1999) Characterization of two bifunctional Arabidopsis thaliana genes coding for mitochondrial and cytosolic forms of valyl-tRNA synthetase and threonyl-tRNA synthetase by alternative use of two in-frame AUGs. Eur. J. Biochem. 266, 848-854.
102. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W. & Lipman, D.J. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25, 3389-3402.
103. Karlberg, O., Canbäck, B., Kurland, C.G. & Andersson, S.G.E. (2000) The dual origin of the yeast mitochondrial proteome. Yeast 17, 170-187.
104. Scotti, P.A., Urbanus, M.L., Brunner, J., de Gier, J.-W., von Heijne, G., van der Does, Driessen, A.J.M., Oudega, B. & Luirink, J. (2000) YidC, the Escherichia coli homologue of mitochondrial Oxa1p, is a component of the Sec translocase. EMBO J. 19, 542-549.
105. Wolf, Y.I., Aravind, L. & Koonin, E.V. (1999) Rickettsiae and chlamydiae: evidence of horizontal gene transfer and gene exchange. Trends Genet. 15, 173-175.
106. Castresana, J., Lübben, M., Saraste, M. & Higgins, D.G. (1994) Evolution of cytochrome oxidase, an enzyme older than atmospheric oxygen. EMBO J. 13, 2516-2525.
107. Saraste, M. & Walker, J.E. (1982) Internal sequence repeats and the path of polypeptide in mitochondrial ADP/ATP translocase. FEBS Lett. 144, 250-254.
108. Matsuoka, Y., Li, X. & Bennett, V. (2000) Adducin: structure, function and regulation. Cell. Mol. Life Sci. 57, 884-895.
109. Gupta, R.S. (1995) Phylogenetic analysis of the 90 kD heat shock family of protein sequences and an examination of the relationship among animals, plants, and fungi species. J. Mol. Evol. 12, 1063-1073.
110. Gupta, R.S. (2000) The phylogeny of proteobacteria: relationships to other eubacterial phyla and eukaryotes. FEMS Microbiol. Rev. 24, 367-402.
111. Gribaldo, S., Lumia, V., Creti, R., de Macario, E.C., Sanangelantoni, A. & Cammarano, P. (1999) Discontinuous occurrence of the hsp70 (dnaK) gene among Archaea and sequence features of HSP70 suggest a novel outlook on phylogenies inferred from this protein. J. Bacteriol. 181, 434-443.
112. Emelyanov, V.V. (2002) Phylogenetic relationships of organellar Hsp90 homologs reveal fundamental difference to organellar Hsp70 and Hsp60 evolution. Gene 299, 125-133.
113. McArthur, A.G., Knodler, L.A., Silberman, J.D., Davids, B.J., Gillin, F.D. & Sogin, M.L. (2001) The evolutionary origins of eukaryotic protein disulfide isomerase domains: new evidence from the amitochondriate protist Giardia lamblia. Mol. Biol. Evol. 18, 1455-1463.
114. Culligan, K.M., Meyer-Gauen, G., Lyons-Weiler, J. & Hays, J.B. (2000) Evolutionary origin, diversification and specialization of eukaryotic MutS homolog mismatch repair proteins. Nucleic Acids Res. 28, 463-471.
115. Pont-Kingdon, G., Okada, N.A., Macfarlane, J.L., Beagley, C.T., Watkins-Sims, C.D., Cavalier-Smith, T., Clark-Walker, G.D. & Wolstenholme, D.R. (1998) Mitochondrial DNA of the coral Sarcophyton glaucum contains a gene for a homologue of bacterial MutS: a possible case of gene transfer from the nucleus to the mitochondrion. J. Mol. Evol. 46, 419-431.
116. Augusto-Pinto, L., Bartholomeu, D.C., Teixeira S.M., Pena, S.D. & Machado, C.R. (2001) Molecular cloning and characterization of the DNA mismatch repair gene class 2 from the Trypanosoma cruzi. Gene 272, 323-333.
117. Walter, T.C. & Kennell, J.C. (1999) Linear mitochondrial plasmids of Fusarium oxysporum are novel, telomere-like retro-elements. Mol. Cell 4, 229-238.
118. Cavalier-Smith, T. (1987) Eukaryotes with no mitochondria. Nature (London) 326, 332-333.
119. Embley, T.M., Horner, D.S. & Hirt, R.P. (1997) Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria. Trends Ecol. Evol. 12, 437-441.
120. Fast, N.M. & Keeling, P.J. (2001) Alpha and beta subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Mol. Biochem. Parasitol. 117, 201-209.
121. Baldauf, S.L., Roger, A.J., Wenk-Siefert, I. & Doolittle, W.F. (2000) A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290, 972-977.
122. Katinka, M.D., Duprat, S., Cornillot, E., Metenier, G., Thomarat, F., Prensier, G., Barbe, V., Peyretaillade, E., Brottier, P., Wincker, P., Delbac, F., El Alaoui, H., Peyret, P., Saurin, W., Gouy, M., Weissenbach, J. & Vivares, C.P. (2001) Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature (London) 414, 450-453.
123. Keeling, P.J., Luker, M.A. & Palmer, J.D. (2000) Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17, 23-31.
124. Van de Peer, Y., Ben Ali, A. & Meyer, A. (2000) Microsporidia: accumulating molecular evidence that a group of amitochondriate and suspectedly primitive eukaryotes are just curious fungi. Gene 246, 1-8.
125. Hackstein, J.H., Akhmanova, A., Boxma, B., Harhangi, H.R. & Voncken, F.G. (1999) Hydrogenosomes: eukaryotic adaptations to anaerobic environments. Trends Microbiol. 7, 441-447.
126. Müller, M. (1993) The hydrogenosome. J. Gen. Microbiol. 139, 2879-2889.
127. Akhmanova, A., Voncken, F., van Alen, T., van Hoek, A., Boxma, B., Vogels, G., Veenhuis, M. & Hackstein, J.H. (1998) A hydrogenosome with a genome. Nature (London) 396, 527-528.
128. Akhmanova, A., Voncken, F.G., Harhangi, H., Hosea, K.M., Vogels, G.D. & Hackstein, J.H. (1998) Cytosolic enzymes with a mitochondrial ancestry from the anaerobic chytrid Piromyces sp. E2. Mol. Microbiol. 30, 1017-1027.
129. Bradley, P.J., Lahti, C.J., Plumper, E. & Johnson, P.J. (1997) Targeting and translocation of proteins into the hydrogenosome of the protist Trichomonas: similarities with mitochondrial protein import. EMBO J. 16, 3484-3493.
130. Dyall, S.D. & Johnson, P.J. (2000) Origins of hydrogenosomes and mitochondria: evolution and organelle biogenesis. Curr. Opin. Microbiol. 3, 404-411.
131. Embley, T.M., Finlay, B.J., Dyal, P.L., Hirt, R.P., Wilkinson, M. & Williams, A.G. (1995) Multiple origins of anaerobic ciliates with hydrogenosomes within the radiation of aerobic ciliates. Proc. R. Soc. London Ser. B 23, 87-93.
132. Embley, T.M. & Martin, W. (1998) A hydrogen-producing mitochondrion. Nature (London) 396, 517-519.
133. van der Giezen, M., Sjollema, K.A., Artz, R.R., Alkema, W. & Prins, R.A. (1997) Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS Lett. 408, 147-150.
134. van der Giezen, M., Slotboom, D.J., Horner, D.S., Dyal, P.L., Harding, M., Xue, G.P., Embley, T.M. & Kunji, E.R. (2002) Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: a common origin for both organelles. EMBO J. 21, 572-579.
135. Hausler, T., Stierhof, Y.D., Blattner, J. & Clayton, C. (1997) Conservation of mitochondrial targeting sequence function in mitochondrial and hydrogenosomal proteins from the early-branching eukaryotes Crithidia, Trypanosoma and Trichomonas. Eur. J. Cell Biol. 73, 240-251.
136. van Hoek, A.H., Akhmanova, A.S., Huynen, M.A. & Hackstein, J.H. (2000) A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol. Biol. Evol. 17, 202-206.
137. Plumper, E., Bradley, P.J. & Johnson, P.J. (2000) Competition and protease sensitivity assays provide evidence for the existence of a hydrogenosomal protein import machinery in Trichomonas vaginalis. Mol. Biochem. Parasitol. 106, 11-20.
138. Rotte, C., Henze, K., Müller, M. & Martin, W. (2000) Origins of hydrogenosomes and mitochondria. Curr. Opin. Microbiol. 3, 481-486.
139. Van Hellemond, J.J., Opperdoes, F.R. & Tielens, A.G.M. (1998) Trypanosomatidae produce acetate via a mitochondrial acetate:succinate CoA transferase. Proc. Natl Acad. Sci. USA 95, 3036-3041.
140. Bunjun, S., Stathopoulos, C., Graham, D., Min, B., Kitabatake, M., Wang, A.L., Wang, C.C., Vivares, C.P., Weiss, L.M. & Söll, D. (2000) A dual-specificity aminoacyl-tRNA synthetase in the deep-rooted eukaryote Giardia lamblia. Proc. Natl Acad. Sci. USA 97, 12997-13002.
141. Chihade, J.W., Brown, J.R., Schimmel, P.R. & Ribas de Pouplana, L. (2000) Origin of mitochondria in relation to evolutionary history of eukaryotic alanyl-tRNA synthetase. Proc. Natl Acad. Sci. USA 97, 12153-12157.
142. Woese, C.R., Olsen, G.J., Ibba, M. & Söll, D. (2000) Aminoacyl-tRNA synthetases, the genetic code, and the evolutionary process. Microbiol. Mol. Biol. Rev. 64, 202-236.
143. Morrison, H.G., Roger, A.J., Nystul, T.G., Gillin, F.D. & Sogin, M.L. (2001) Giardia lamblia expresses a proteobacterial-like DnaK homolog. Mol. Biol. Evol. 18, 530-541.
144. Sogin, M.L. (1997) History assignment: when was the mitochondrion founded? Curr. Opin. Genet. Dev. 7, 792-799.
145. Sogin, M.L. (1997) Organelle origins: energy-producing symbionts in early eukaryotes? Curr. Biol. 7, R315-R317.
146. Germot, A. & Philippe, H. (1999) Critical analysis of eukaryotic phylogeny: a case study based on the HSP70 family. J. Euk. Microbiol. 46, 116-124.
147. Arisue, N., Sanchez, L.B., Weiss, L.M., Müller, M. & Hashimoto, T. (2002) Mitochondrial-type hsp70 genes of the amitochondriate protists, Giardia intestinalis, Entamoeba histolytica and two microsporidians. Parasitol. Int. 51, 9-16.
148. Homer, D.S. & Embley, T.M. (2001) Chaperonin 60 phylogeny provides further evidence for secondary loss of mitochondria among putative early-branching eukaryotes. Mol. Biol. Evol. 18, 1970-1975.
149. Ghosh, S., Field, J., Rogers, R., Hickman, M. & Samuelson, J. (2000) The Entamoeba histolytica mitochondrion-derived organelle (crypton) contains double-stranded DNA and appears to be bound by a double membrane. Infect. Immun. 68, 4319-4322.
150. Tovar, J., Fischer, A. & Clark, C.G. (1999) The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32, 1013-1021.
151. Roger, A.J., Morrison, H.G. & Sogin, M.L. (1999) Primary structure and phylogenetic relationships of a malate dehydrogenase gene from Giardia lamblia. J. Mol. Evol. 48, 750-755.
152. Keeling, P.J. & Palmer, J.D. (2000) Parabasalian flagellates are ancient eukaryotes. Nature (London) 405, 635-637.
153. Vellai, T., Takacs, K. & Vida, G. (1998) A new aspect to the origin and evolution of eukaryotes. J. Mol. Evol. 46, 499-507.
154. Castresana, J. & Saraste, M. (1995) Evolution of energetic metabolism: the respiration-early hypothesis. Trends Biochem. Sci. 20, 443-448.
155. Knoll, A.H. (1992) The early evolution of eukaryotes: a geological perspective. Science 256, 622-627.
156. Lopez-Garcia, P. & Moreira, D. (1999) Metabolic symbiosis at the origin of eukaryotes. Trends Biochem. Sci. 24, 88-93.
157. Winkler, H.H. (1990) Rickettsia species (as organisms). Annu. Rev. Microbiol. 44, 131-153.
158. von Dohlen, C.D., Kohler, S., Alsop, S.T. & McManus, W.R. (2001) Mealybug beta-proteobacterial endosymbionts contain gamma-proteobacterial symbionts. Nature (London) 412, 433-435.
159. Emelyanov, V.V. (1990) A simple method for counting ricket-tsiae. Mikrobiol. Z. (USSR) 52, 91-95.