Eukaryotic evolution, changes and challenges

Nature

Volumn 440, Issue 7084, 2006, Pages 623-630

  Embley, T Martin ^a   Martin, William ^b  

^a NEWCASTLE UNIVERSITY   (United Kingdom)

^b HEINRICH HEINE UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOLOGY;

EUKARYOTES; EVOLUTIONARY GAP; PROKARYOTE-TO-EUKARYOTE TRANSITION;

CELL CULTURE;

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; DIHYDROFOLATE REDUCTASE; DNA DIRECTED RNA POLYMERASE; ELONGATION FACTOR; HEAT SHOCK PROTEIN 60; HEAT SHOCK PROTEIN 70; HYDROGEN; IRON SULFUR PROTEIN; MITOCHONDRIAL PROTEIN; NICOTINAMIDE ADENINE DINUCLEOTIDE; PYRUVATE SYNTHASE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SMALL SUBUNIT RIBOSOMAL RNA; THYMIDYLATE SYNTHASE;

EUKARYOTE; MITOCHONDRION; ORIGIN OF LIFE; PROKARYOTE;

ALPHAPROTEOBACTERIA; ASCARIS; BIOGENESIS; CATALYSIS; CHIMERA; COEVOLUTION; CRYPTOSPORIDIUM; ELECTRON MICROSCOPY; ELECTRON TRANSPORT; ENDOSYMBIONT; ENTAMOEBA HISTOLYTICA; EUGLENA; EUKARYOTE EVOLUTION; FASCIOLA; GIARDIA; HORIZONTAL GENE TRANSFER; METHANOBACTERIUM; MICROSPORUM; MITOCHONDRION; NONHUMAN; PHOSPHORYLATION; PHYLOGENETIC TREE; PLASTID; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PYROCOCCUS; REVIEW; RIBOSOME; SULFOLOBUS; THERMOPLASMA; TRICHOMONAS;

ALPHAPROTEOBACTERIA; ASCARIS; CRYPTOSPORIDIUM; ENTAMOEBA HISTOLYTICA; EUGLENA; EUKARYOTA; FASCIOLA; GIARDIA; METHANOBACTERIUM; MICROSPORUM; PROKARYOTA; PYROCOCCUS; SULFOLOBUS; THERMOPLASMA; TRICHOMONAS;

EID: 33645456207     PISSN: 00280836     EISSN: 14764687     Source Type: Journal    
DOI: 10.1038/nature04546     Document Type: Review

References (93)

1. Woese, C. R., Kandler, O. & Wheelis, M. L. Towards a natural system of organisms: Proposal for the domains Archaea, Bacteria, and Eucarya. Proc. Natl Acad. Sci. USA 87, 4576-4579 (1990).
2. Leipe, D. D., Gunderson, J. H., Nerad, T. A. & Sogin, M. L. Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol. Biochem. Parasitol. 59, 41-48 (1993).
3. Hashimoto, T., Nakamura, Y., Kamaishi, T. & Hasegawa, M. Early evolution of eukaryotes inferred from the amino acid sequences of elongation factors 1α and 2. Arch. Protistenkd. 148, 287-295 (1997).
4. Cavalier-Smith, T. in Endocytobiology II (eds Schwemmler, W. & Schenk, H. E. A.) 1027-1034 (De Gruyter, Berlin, 1983).
5. Gray, M. W., Lang, B. F. & Burger, G. Mitochondria of protists. Annu. Rev. Genet. 38, 477-524 (2004).
6. Cavalier-Smith, T. in Endocytobiology II (eds Schwemmler, W. & Schenk, H. E. A.) 265-279 (De Gruyter, Berlin, 1983).
7. Pfanner, N. & Geissler, A. Versatility of the mitochondrial protein import machinery. Nature Rev. Mol. Cell Biol. 2, 339-349 (2001).
8. Esser, C. et al. A genome phylogeny for mitochondria among α-proteobacteria and a predominantly eubacterial ancestry of yeast nuclear genes. Mol. Biol. Evol. 21, 1643-1660 (2004).
9. Timmis, J. N., Ayliffe, M. A., Huang, C. Y. & Martin, W. Endosymbiotic gene transfer: Organelle genomes forge eukaryotic chromosomes. Nature Rev. Genet. 5, 123-135 (2004).
10. Clark, C. G. & Roger, A. J. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl Acad. Sci. USA 92, 6518-6521 (1995).
11. Roger, A. J. Reconstructing early events in eukaryotic evolution. Am. Nat. 154, S146-S163 (1999).
12. Abrahamsen, M. S. et al. Complete genome sequence of the apicomplexan, Cryptosporidium parvum. Science 304, 441-445 (2004).
13. Boxma, B. et al. An anaerobic mitochondrion that produces hydrogen. Nature 434, 74-79 (2005).
14. Müller, M. in Molecular Medical Parasitology (eds Marr, J. J., Nilsen, T. W. & Komuniecki, R. W.) 125-139 (Academic, Amsterdam, 2003).
15. Katinka, M. D. et al. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414, 450-453 (2001).
16. Tielens, A. G., Rotte, C., van Hellemond, J. J. & Martin, W. Mitochondria as we don't know them. Trends Biochem. Sci. 27, 564-572 (2002).
17. Komuniecki, R. W. & Tielens, A. G. M. in Molecular Medical Parasitology (eds Marr, J. J., Nilsen, T. W. & Komuniecki, R.) 339-358 (Academic, Amsterdam, 2003).
18. Darwin, C. The Origin of Species Reprint edn (Penguin Books, London, 1968).
19. Müller, M. The hydrogenosome. J. Gen. Microbiol. 139, 2879-2889 (1993).
20. van der Giezen, M. et al. Conserved properties of hydrogenosomal and mitochondrial ADP/ATP carriers: A common origin for both organelles. EMBO J. 21, 572-579 (2002).
21. Tjaden, J. et al. A divergent ADP/ATP carrier in the hydrogenosomes of Trichomonas gallinae argues for an independent origin of these organelles. Mol. Microbiol. 51, 1439-1446 (2004).
22. Embley, T. M. et al. Hydrogenosomes, mitochondria and early eukaryotic evolution. IUBMB Life 55, 387-395 (2003).
23. Dyall, S. D. et al. Presence of a member of the mitochondrial carrier family in hydrogenosomes: Conservation of membrane-targeting pathways between hydrogenosomes and mitochondria. Mol. Cell. Biol. 20, 2488-2497 (2000).
24. Sutak, R. et al. Mitochondrial-type assembly of FeS centers in the hydrogenosomes of the amitochondriate eukaryote Trichomonas vaginalis. Proc. Natl Acad. Sci. USA 101, 10368-10373 (2004).
25. Hrdy, I. et al. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432, 618-622 (2004).
26. Schnarrenberger, C. & Martin, W. 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 (2002).
27. Fenchel, T. & Finlay, B. J. Ecology and Evolution in Anoxic Worlds (eds May, R. M. & Harvey, P. H.) (Oxford Univ. Press, Oxford, 1995).
28. Roger, A. J. & Silberman, J. D. Cell evolution: Mitochondria in hiding. Nature 418, 827-829 (2002).
29. Whatley, J. M., John, P. & Whatley, F. R. From extracellular to intracellular: The establishment of mitochondria and chloroplasts. Proc. R. Soc. Lond. B 204, 165-187 (1979).
30. Dyall, S. D., Brown, M. T. & Johnson, P. J. Ancient invasions: From endosymbionts to organelles. Science 304, 253-257 (2004).
31. Dyall, S. D. et al. Non-mitochondrial complex I proteins in a hydrogenosomal oxidoreductase complex. Nature 431, 1103-1107 (2004).
32. Tovar, J., Fischer, A. & Clark, C. G. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32, 1013-1021 (1999).
33. Tovar, J. et al. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426, 172-176 (2003).
34. Williams, B. A., Hirt, R. P., Lucocq, J. M. & Embley, T. M. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865-869 (2002).
35. Regoes, A. et al. Protein import, replication and inheritance of a vestigial mitochondrion. J. Biol. Chem. 280, 30557-30563 (2005).
36. Chan, K. W. et al. A Novel ADP/ATP transporter in the mitosome of the microaerophilic human parasite Entamoeba histolytica. Curr. Biol. 15, 737-742 (2005).
37. Dolezal, P. et al. Giardia mitosomes and trichomonad hydrogenosomes share a common mode of protein targeting. Proc. Natl Acad. Sci. USA 102, 10924-10929 (2005).
38. Lill, R. & Muhlenhoff, U. Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30, 133-141 (2005).
39. Ali, V., Shigeta, Y., Tokumoto, U., Takahashi, Y. & Nozaki, T. An intestinal parasitic protist, Entamoeba histolytica, possesses a non-redundant nitrogen fixation-like system for iron-sulfur cluster assembly under anaerobic conditions. J. Biol. Chem. 279, 16863-16874 (2004).
40. Penny, D., McComish, B. J., Charleston, M. A. & Hendy, M. D. Mathematical elegance with biochemical realism: The covarion model of molecular evolution. J. Mol. Evol. 53, 711-723 (2001).
41. Ho, S. Y. W. & Jermiin, L. S. Tracing the decay of the historical signal in biological sequence data. Syst. Biol. 53, 623-637 (2004).
42. Felsenstein, J. Cases in which parsimony or incompatibility methods will be positively misleading. Syst. Zool. 25, 401-410 (1978).
43. Stiller, J. W. & Hall, B. D. Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol. Biol. Evol. 16, 1270-1279 (1999).
44. Philippe, H. et al. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc. R. Soc. Lond. B 267, 1213-1221 (2000).
45. Hirt, R. P. et al. 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 (1999).
46. Keeling, P. J., Luker, M. A. & Palmer, J. D. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17, 23-31 (2000).
47. Arisue, N., Hasegawa, M. & Hashimoto, T. Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. Mol. Biol. Evol. 22, 409-420 (2005).
48. Penny, D. Criteria for optimising phylogenetic trees and the problem of determining the root of a tree. J. Mol. Evol. 8, 95-116 (1976).
49. Stechmann, A. & Cavalier-Smith, T. The root of the eukaryote tree pinpointed. Curr. Biol. 13, R665-R666 (2003).
50. Steenkamp, E. T., Wright, J. & Baldauf, S. L. The protistan origins of animals and fungi. Mol. Biol. Evol. 23, 93-106 (2006); published online 8 September 2005 (doi:10.1093/molbev/msj011).
51. Richards, T. A. & Cavalier-Smith, T. Myosin domain evolution and the primary divergence of eukaryotes. Nature 436, 1113-1118 (2005).
52. Adl, S. M. et al. The new higher level classification of eukaryotes with emphasis on the taxonomy of protists. J. Eukaryot. Microbiol. 52, 399-451 (2005).
53. Graybeal, A. Is it better to add taxa or characters to a difficult phylogenetic problem? Syst. Biol. 47, 9-17 (1998).
54. Philippe, H. & Adoutte, A. in Evolutionary Relationships Among Protozoa (eds Coombs, G. H., Vickerman, K., Sleigh, M. A. & Warren, A.) 25-56 (Kluwer Academic, Dordrecht, 1998).
55. Forterre, P. & Philippe, H. Where is the root of the universal tree of life? Bioessays 21, 871-879 (1999).
56. Knoll, A. H. Life on a Young Planet: The First Three Billion Years of Evolution on Earth (Princeton Univ. Press, 2003).
57. Margulis, L., Dolan, M. F. & Whiteside, J. H. "Imperfections and oddities" in the origin of the nucleus. Paleobiology 31, 175-191 (2005).
58. Moreira, D. & Lopez Garcia, P. Symbiosis between methanogenic archaea and δ-proteobacteria as the origin of eukaryotes: The syntrophic hypothesis. J. Mol. Evol. 47, 517-530 (1998).
59. Lake, J., Moore, J., Simonson, A. & Rivera, M. in Microbial Phylogeny and Evolution Concepts and Controversies (ed. Sapp, J.) 184-206 (Oxford Univ. Press, Oxford, 2005).
60. Cavalier-Smith, T. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52, 297-354 (2002).
61. Cavalier-Smith, T. Only six kingdoms of life. Proc. R. Soc. Lond. B 271, 1251-1262 (2004).
62. Martin, W. & Müller, M. The hydrogen hypothesis for the first eukaryote. Nature 392, 37-41 (1998).
63. Vellai, T., Takacs, K. & Vida, G. A new aspect to the origin and evolution of eukaryotes. J. Mol. Evol. 46, 499-507 (1998).
64. Searcy, D. G. in The Origin and Evolution of the Cell (eds Matsuno, H. H. & Matsuno, K.) 47-78 (World Scientific, Singapore, 1992).
65. von Dohlen, C. D., Kohler, S., Alsop, S. T. & McManus, W. R. Mealybug β-proteobacterial endosymbionts contain γ-proteobacterial symbionts. Nature 412, 433-436 (2001).
66. Zillig, W., Schnabel, R. & Stetter, K. O. Archaeabacteria and the origin of the eukaryotic cytoplasm. Curr. Top. Microbiol. Immunol. 114, 1-18 (1985).
67. Rivera, M. C., Jain, R., Moore, J. E. & Lake, J. A. Genomic evidence for two functionally distinct gene classes. Proc. Natl Acad. Sci. USA 95, 6239-6244 (1998).
68. Ribeiro, S. & Golding, G. B. The mosaic nature of the eukaryotic nucleus. Mol. Biol. Evol. 15, 779-788 (1998).
69. Lake, J. A. Origin of the eukaryotic nucleus determined by rate-invariant analysis of rRNA sequences. Nature 331, 184-186 (1988).
70. Rivera, M. C. & Lake, J. A. Evidence that eukaryotes and eocyte prokaryotes are immediate relatives. Science 257, 74-76 (1992).
71. Baldauf, S. L., Palmer, J. D. & Doolittle, W. F. The root of the universal tree and the origin of eukaryotes based upon elongation factor phylogeny. Proc. Natl Acad. Sci. USA 93, 7749-7754 (1996).
72. Brown, J. R. & Doolittle, W. F. Archaea and the prokaryote-to- eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456-502 (1997).
73. Tourasse, N. J. & Gouy, M. Accounting for evolutionary rate variation among sequence sites consistently changes universal phylogenies deduced from rRNA and protein-coding genes. Mol. Phylogenet. Evol. 13, 159-168 (1999).
74. Brown, J. R. et al. Universal trees based on large combined protein sequence data sets. Nature Genet. 28, 281-285 (2001).
75. Daubin, V., Gouy, M. & Perriere, G. A phylogenomic approach to bacterial phylogeny: Evidence of a core of genes sharing a common history. Genome Res. 12, 1080-1090 (2002).
76. Rivera, M. C. & Lake, J. A. The ring of life provides evidence for a genome fusion origin of eukaryotes. Nature 431, 152-155 (2004).
77. Horiike, T., Hamada, K., Miyata, D. & Shinozawa, T. The origin of eukaryotes is suggested as the symbiosis of Pyrococcus into γ- proteobacteria by phylogenetic tree based on gene content. J. Mol. Evol. 59, 606-619 (2004).
78. Margulis, L., Dolan, M. F. & Guerrero, R. The chimeric eukaryote: Origin of the nucleus from the karyomastigont in amitochondriate protists. Proc. Natl Acad. Sci. USA 97, 6954-6959 (2000).
79. Gabaldon, T. & Huynen, M. A. Reconstruction of the proto-mitochondrial metabolism. Science 301, 609 (2003).
80. Martin, W. et al. Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus. Proc. Natl Acad. Sci. USA 99, 12246-12251 (2002).
81. Doolittle, W. F. You are what you eat: A gene transfer ratchet could account for bacterial genes in eukaryotic nuclear genomes. Trends Genet. 14, 307-311 (1998).
82. Loftus, B. et al. The genome of the protist parasite Entamoeba histolytica. Nature 433, 865-868 (2005).
83. Doolittle, W. F. Lateral genomics. Trends Cell Biol. 9, M5-M8 (1999).
84. Kunin, V., Goldovsky, L., Darzentas, N. & Ouzounis, C. A. The net of life - reconstruction of the microbial phylogenetic network. Genome Res. 15, 954-959 (2005).
85. Javaux, E. J., Knoll, A. H. & Walter, M. R. Morphological and ecological complexity in early eukaryotic ecosystems. Nature 412, 66-69 (2001).
86. Butterfield, N. J. Bangiomorpha pubescens n. gen., n. sp.: implications for the evolution of sex, multicellularity, and the Mesoproterozoic/ Neoproterozoic radiation of eukaryotes. Paleobiology 26, 386-404 (2000).
87. Benton, M. J. & Ayala, F. J. Dating the tree of life. Science 300, 1698-1700 (2003).
88. Kurland, C. G. & Andersson, S. G. Origin and evolution of the mitochondrial proteome. Microbiol. Mol. Biol. Rev. 64, 786-820 (2000).
89. Shen, Y., Knoll, A. H. & Walter, M. R. Evidence for low sulphate and anoxia in a mid-Proterozoic marine basin. Nature 423, 632-635 (2003).
90. Poulton, S. W., Fralick, P. W. & Canfield, D. E. The transition to a sulphidic ocean ∼1.84 billion years ago. Nature 431, 173-177 (2004).
91. Rodriguez-Ezpeleta, N. et al. Monophyly of primary photosynthetic eukaryotes: green plants, red algae, and glaucophytes. Curr. Biol. 15, 1325-1330 (2005).
92. Pace, N. R. A molecular view of microbial diversity and the biosphere. Science 276, 734-740 (1997).
93. Keithly, J. S., Langreth, S. G., Buttle, K. F. & Mannella, C. A. Electron tomographic and ultrastructural analysis of the Cryptosporidium parvum relict mitochondrion, its associated membranes, and organelles. J. Eukaryot. Microbiol. 52, 132-140 (2005).