Comprehensive multigene phylogenies of excavate protists reveal the evolutionary positions of "primitive" eukaryotes

Molecular Biology and Evolution

Volumn 23, Issue 3, 2006, Pages 615-625

  Simpson, Alastair G B ^a   Inagaki, Yuji ^b   Roger, Andrew J ^a,c  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF TSUKUBA   (Japan)

^c DALHOUSIE UNIVERSITY   (Canada)

Author keywords

Eukaryote evolution; Giardia; Mitochondria; Protozoa; Tubulin

Indexed keywords

NUCLEAR PROTEIN; RNA POLYMERASE;

ARTICLE; BACTERIOPHAGE TYPING; CARPEDIEMONAS; CELL LINEAGE; CLADISTICS; DISCICRISTATA; EUGLENOZOA; EUKARYOTE; FLAGELLATE; GENETIC CODE; HETEROLOBOSEA; JAKOBIDS; MALAWIMONAS; MITOCHONDRION; MOLECULAR PHYLOGENY; MONOPHYLY; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXYMONADS; PARABASALIDS; PROTOZOON; SAMPLING; TRIMASTIX; TRYPANOSOMA;

ANIMALS; DNA-DIRECTED RNA POLYMERASES; EUKARYOTIC CELLS; EVOLUTION; MODELS, GENETIC; MULTIGENE FAMILY; PHYLOGENY; PROTOZOA; RNA;

ARCHEZOA; BACTERIA (MICROORGANISMS); CARPEDIEMONAS; DIPLOMONADIDA; DISCICRISTATA; EUGLENOZOA; EUKARYOTA; GIARDIA; HETEROLOBOSEA; JAKOBIDAE; MALAWIMONAS; MASTIGOPHORA (FLAGELLATES); OXYMONADIDA; PARABASALIDEA; PROTISTA; PROTOZOA; RECLINOMONAS; TRICHOMONAS; TRIMASTIX; TRYPANOSOMA;

EID: 33244466796     PISSN: 07374038     EISSN: None     Source Type: Journal    
DOI: 10.1093/molbev/msj068     Document Type: Article

References (76)

1. Adams, K. L., and J. D. Palmer. 2003. Evolution of mitochondrial gene content: gene loss and transfer to the nucleus. Mol. Phylogenet. Evol. 29:380-395.
2. Andersson, J. O., S. W. Sarchfield, and A. J. Roger. 2005. Gene transfers from Nanoarchaeota to an ancestor of diplomonads and parabasalids. Mol. Biol. Evol. 22:85-90.
3. Archibald, J. M., C. J. O'Kelly, and W. F. Doolittle. 2002. The chaperonin genes of jakobid and jakobid-like flagellates: implications for eukaryotic evolution. Mol. Biol. Evol. 19: 422-431.
4. Arisue, N., M. Hasegawa, and T. Hashimoto. 2005. Root of the Eukaryota tree as inferred from combined maximum likelihood analyses of multiple molecular sequence data. Mol. Biol. Evol. 22:409-420.
5. Baldauf, S. L. 2003. The deep roots of eukaryotes. Science 300:1703-1706.
6. Baldauf, S. L., A. J. Roger, I. Wenk-Siefert, and W. F. Doolittle. 2000. A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290:972-977.
7. Bapteste, E., H. Brinkmann, J. A. Lee et al. (11 co-authors). 2002. The analysis of 100 genes supports the grouping of three highly divergent amoebae: Dictyostelium, Entamoeba, and Mastigamoeba. Proc. Natl. Acad. Sci. USA 99:1414-1419.
8. Bergthorsson, U., K. L. Adams, B. Thomason, and J. D. Palmer. 2003. Widespread horizontal transfer of mitochondrial genes in flowering plants. Nature 424:197-201.
9. Bergthorsson, U., A. O. Richardson, G. J. Young, L. R. Goertzen, and J. D. Palmer. 2004. Massive horizontal transfer of mitochondrial genes from diverse land plant donors to the basal angiosperm Amborella. Proc. Natl. Acad. Sci. USA 101: 17747-17752.
10. Berney, C., J. F. Fahrni, and J. Pawlowski. 2004. How many novel eukaryotic 'kingdoms'? Pitfalls and limitations of environmental DNA surveys. BMC Biol. 2:13.
11. Burger, G., M. W. Gray, and B. F. Lang. 2003. Mitochondrial genomes: anything goes. Trends Genet. 19:709-716.
12. Cavalier-Smith, T. 1998. A revised six-kingdom system of life. Biol. Rev. 73:203-266.
13. _. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of Protozoa. Int. J. Syst. Evol. Microbiol. 52:297-354.
14. _. 2003. The excavate protozoan phyla Metamonada Grasse emend. (Anaeromonadea, Parabasalia, Carpediemonas, Eopharyngia) and Loukozoa emend. (Jakobea, Malawimonas): their evolutionary affinities and new higher taxa. Int. J. Syst. Evol. Microbiol. 53:1741-1758.
15. _. 2004. Only six kingdoms of life. Proc. R. Soc. Lond. B 271:1251-1262.
16. Cermakian, N., T. M. Ikeda, R. Cedergren, and M. W. Gray. 1996. Sequences homologous to yeast mitochondrial and bacteriophage T3 and T7 RNA polymerases are widespread throughout the eukaryotic lineage. Nucleic Acids Res. 24: 648-654.
17. Chihade, J. W., J. R. Brown, P. R. Schimmel, and L. Ribas de Pouplana. 2000. Origin of mitochondria in relation to evolutionary history of eukaryotic alanyl-tRNA synthetase. Proc. Natl. Acad. Sci. USA 97:12153-12157.
18. Clark, C. G., and L. S. Diamond. 1991. The Laredo strain and other 'Entamoeba histolytica-like' amoebae are Entamoeba moshkovskii. Mol. Biochem. Parasitol. 46:11-18.
19. Clement, S. L., and D. J. Koslowsky. 2001. Unusual organization of a developmentally regulated mitochondrial RNA polymerase (TBMTRNAP) gene in Trypanosoma brucei. Gene 272:209-218.
20. Cummings, M. P., S. A. Handley, D. S. Myers, D. L. Reed, A. Rokas, and K. Winka. 2003. Comparing bootstrap and posterior probability values in the four-taxon case. Syst. Biol. 52:477-487.
21. Dacks, J. B., J. D. Silberman, A. G. B. Simpson, S. Moruya, T. Kudo, M. Ohkuma, and R. Redfield. 2001. Oxymonads are closely related to the excavate taxon Trimastix. Mol. Biol. Evol. 18:1034-1044.
22. Davis, C. C., and K. J. Wurdack. 2004. Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676-677.
23. Douady, C. J., F. Delsuc, Y. Boucher, W. F. Doolittle, and E. J. P. Douzery. 2003. Comparison of Bayesian and maximum likelihood bootstrap measures of phylogenetic reliability. Mol. Biol. Evol. 20:248-254.
24. Dyall, S. D., D. M. Brown, and P. J. Johnson. 2004. Ancient invasions: from endosymbionts to organelles. Science 304: 253-257.
25. Edgcomb, V. P., A. J. Roger, A. G. B. Simpson, D. Kysela, and M. L. Sogin. 2001. Evolutionary relationships among "jakobid" flagellates as indicated by alpha- and beta-tubulin phylogenies. Mol. Biol. Evol. 18:514-522.
26. Embley, T. M., and R. P. Hirt. 1998. Early branching eukaryotes? Curr. Opin. Genet. Dev. 8:624-629.
27. Erixon, P., B. Svennblad, T. Britton, and B. Oxelman. 2003. Reliability of Bayesian posterior probabilities and bootstrap frequencies in phylogenies. Syst. Biol. 52:665-673.
28. Felsenstein, J. 2004. PHYLIP (phylogeny inference package), version 3.6b. Distributed by the author, University of Washington, Seattle.
29. Gillin, F. D., D. S. Reiner, and J. M. McCaffery. 1996. Cell biology of the primitive eukaryote Giardia lamblia. Annu. Rev. Microbiol. 50:679-705.
30. Gray, M. W., G. Burger, and B. F. Lang. 1999. Mitochondrial evolution. Science 283:1476-1481.
31. Gray, M. W., B. F. Lang, and G. Burger. 2004. Mitochondria of protists. Annu. Rev. Genet. 38:477-524.
32. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
33. Hampl, V., D. S. Horner, P. Dyal, J. Kulda, J. Flegr, P. Foster, and T. M. Embley. 2005. Inference of the phylogenetic position of oxymonads based on nine genes: support for Metamonada and Excavata. Mol. Biol. Evol. 22:2508-2518.
34. Harper, J. T., E. Waanders, and P. J. Keeling. 2005. On the monophyly of chromalveolates using a six-protein phylogeny of eukaryotes. Int. J. Syst. Evol. Microbiol. 55:487-496.
35. Hashimoto, T., Y. Nakamura, F. Nakamura, T. Shirakura, J. Adachi, N. Goto, K. Okamoto, and M. Hasegawa. 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.
36. Henze, K., D. S. Horner, S. Suguri, D. V. Moore, L. B. Sanchez, M. Müller, and T. M. Embley. 2001. Unique phylogenetic relationships of glucokinase and glucosephosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis. Gene 281: 123-131.
37. Inagaki, Y., E. Susko, N. M. Fast, and A. J. Roger. 2004. Covarion shifts cause a long-branch attraction artifact that unites microsporidia and archaebacteria in EF-1α phylogenies. Mol. Biol. Evol. 21:1340-1349.
38. Keeling, P. J., and W. F. Doolittle. 1996. Alpha-tubulin from early-diverging eukaryotic lineages and the evolution of the tubulin family. Mol. Biol. Evol. 13:1297-1305.
39. Keeling, P. J., and B. S. Leander. 2003. Characterisation of a non-canonical genetic code in the oxymonad Streblomastix strix. J. Mol. Biol. 326:1337-1349.
40. Lang, B. F., G. Burger, C. J. O'Kelly, R. Cedergren, G. B. Golding, C. Lemieux, D. Sankoff, M. Turmel, and M. W. Gray. 1997. An ancestral mitochondrial DNA resembling a eubacterial genome in miniature. Nature 387:493-497.
41. Lang, B. F., C. J. O'Kelly, T. A. Nerad, M. W. Gray, and G. Burger. 2002. The closest unicellular relatives of animals. Curr. Biol. 12:1773-1778.
42. McArthur, A., H. Morrison, J. Nixon et al. 2000. The Giardia genome project database. FEMS Microbiol. Lett. 189: 271-273.
43. Nikolaev, S. I., C. Berney, J. F. Fahrni, I. Bolivar, S. Polet, A. P. Mylnikov, V. V. Aleshin, N. B. Petrov, and J. Pawlowski. 2004. The twilight of Heliozoa and rise of Rhizaria, an emerging supergroup of amoeboid eukaryotes. Proc. Natl. Acad. Sci. USA 101:8066-8071.
44. Nylander, J. A. A., F. Ronquist, J. P. Huelsenbeck, and J. L. Nieves-Aldrey. 2004. Bayesian phylogenetic analysis of combined data. Syst. Biol. 53:47-67.
45. O'Kelly, C. J. 1993. The jakobid flagellates: structural features of Jakoba, Reclinomonas and Histiona and implications for the early diversification of eukaryotes. J. Eukaryot. Microbiol. 40:627-636.
46. O'Kelly, C. J., and T. A. Nerad. 1999. Malawimonas jakobiformis n. gen., n. sp. (Malawimonadidae fam. nov.): a Jakoba-like heterotrophic nanoflagellate with discoidal mitochondrial cristae. J. Eukaryot. Microbiol. 46:522-531.
47. Paquin, B., M.-J. Laforest, and B. F. Lang. 1994. Interspecific transfer of mitochondrial genes in fungi and creation of a homologous hybrid gene. Proc. Natl. Acad. Sci. USA 91: 11807-11810.
48. Patterson, D. J. 1994. Protozoa: evolution and systematics. Pp. 1-14 in K. Hausmann and N. Hülsmann, eds. Progress in protozoology. Gustav Fischer Verlag, Berlin, Germany.
49. Philippe, H., P. Lopez, H. Brinkmann, K. Budin, A. Germot, J. Laurent, D. Moreira, M. Müller, and H. Le Guyader. 2000. Early-branching or fast-evolving eukaryotes? An answer based on slowly evolving positions. Proc. R. Soc. Lond. B 267: 1213-1221.
50. Philippe, H., E. A. Snell, E. Bapteste, P. Lopez, P. W. H. Holland, and D. Casane. 2004. Phylogenomics of eukaryotes: impact of missing data on large alignments. Mol. Biol. Evol. 21: 1740-1752.
51. Pont-Kingdon, G., N. A. Okada, J. L. Macfarlane, C. T. Beagley, C. D. Watkins-Sims, T. Cavalier-Smith, G. D. Clark-Walker, and D. R. Wolstenholme. 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.
52. Pupko, T., D. Huchon, Y. Cao, N. Okada, and M. Hasegawa. 2002. Combining multiple data sets in a likelihood analysis: which models are the best? Mol. Biol. Evol. 19:2294-2307.
53. Roger, A. J. 1999. Reconstructing early events in eukaryotic evolution. Am. Nat. 154:S146-S163.
54. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixture models. Bioinformatics 19:1572-1574.
55. Schmidt, H. A., K. Strimmer, M. Vingron, and A. von Haeseler. 2002. TREE-PUZZLE: maximum likelihood phylogenetic analysis using quartets and parallel computing. Bioinformatics 18:502-504.
56. Shimodaira, H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51:492-508.
57. Shimodaira, H., and M. Hasegawa. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247.
58. Silberman, J. D., A. G. B. Simpson, J. Kulda, I. Cepicka, V. Hampl, P. J. Johnson, and A. J. Roger. 2002. Retortamonad flagellates are closely related to diplomonads - implications for the history of mitochondrial function in eukaryote evolution. Mol. Biol. Evol. 19:777-786.
59. Simpson, A. G. B. 2003. Cytoskeletal organisation, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). Int. J. Syst. Evol. Microbiol. 53:1759-1777.
60. Simpson, A. G. B., J. Lukeš, and A. J. Roger. 2002. The evolutionary history of kinetoplastids and their kinetoplasts. Mol. Biol. Evol. 19:2071-2083.
61. Simpson, A. G. B., E. K. MacQuarrie, and A. J. Roger. 2002. Early origin of canonical introns. Nature 419:270.
62. Simpson, A. G. B., and D. J. Patterson. 1999. The ultrastructure of Carpediemonas membranifera (Eukaryota) with reference to the excavate hypothesis. Eur. J. Protistol. 35:353-370.
63. Simpson, A. G. B., R. Radek, J. B. Dacks, and C. J. O'Kelly. 2002a. How oxymonads lost their groove: an ultrastructural comparison of Monocercomonoides and excavate taxa. J. Eukaryot. Microbiol. 49:239-248.
64. Simpson, A. G. B., and A. J. Roger. 2004. Excavata and the origin of amitochondriate eukaryotes. Pp. 27-53 in R. P. Hirt and D. S. Horner, eds. Organelles, genomes and eukaryote phylogeny: an evolutionary synthesis in the age of genomics. CRC Press, Boca Raton, Fla.
65. Simpson, A. G. B., A. J. Roger, J. D. Silberman, D. Leipe, V. P. Edgcomb, L. S. Jermiin, D. J. Patterson, and M. L. Sogin. 2002b. Evolutionary history of 'early diverging' eukaryotes: the excavate taxon Carpediemonas is closely related to Giardia. Mol. Biol. Evol. 19:1782-1791.
66. Sogin, M. L. 1989. Evolution of eukaryotic microorganisms and their small subunit ribosomal RNAs. Am. Zool. 29:487-499.
67. Sogin, M. L., J. H. Gunderson, H. J. Elwood, R. A. Alonso, and D. A. Peattie. 1989. Phylogenetic significance of the kingdom concept: an unusual eukaryotic 16S-like ribosomal RNA from Giardia lamblia. Science 243:75-77.
68. Stechmann, A., and T. Cavalier-Smith. 2002. Rooting the eukaryote tree by using a derived gene fusion. Science 297: 89-91.
69. _. 2003. The root of the eukaryote tree pinpointed. Curr. Biol. 13:R665-R666.
70. Stiller, J. W., and B. D. Hall. 2002. Evolution of the RNA polymerase II C-terminal domain. Proc. Natl. Acad. Sci. USA 99:6091-6096.
71. Sullivan, J., and D. L. Swofford. 2001. Should we use model-based methods of phylogenetic inference when we know that assumptions about among-site rate variation and nucleotide substitution pattern are violated? Syst. Biol. 50:723-729.
72. Suzuki, Y., G. V. Glazko, and M. Nei. 2002. Overcredibility of molecular phylogenies obtained by Bayesian phylogenetics. Proc. Natl. Acad. Sci. USA 99:16138-16143.
73. Taylor, F. J. R. 1976. Flagellate phylogeny: a study in conflicts. J. Protozool. 23:28-40.
74. Tovar, J., G. Leon-Avila, L. B. Sanchez, R. Sutak, J. Tachezy, M. Van Der Giezen, M. Hernandez, M. Muller, and J. M. Lucocq. 2003. Mitochondrial remnant organelles of Giardia function in iron-sulphur protein maturation. Nature 426:172-176.
75. Yamamoto, A., T. Hashimoto, E. Asaga, M. Hasegawa, and N. Goto. 1997. Phylogenetic position of the mitochondrion-lacking protozoan Trichomonas tenax, based on amino acid sequences of elongation factors 1-alpha and 2. J. Mol. Evol. 44:98-105.
76. Yoon, H. S., J. D. Hackett, and D. Bhattacharya. 2002. A single origin of the peridinin- and fucoxanthin-containing plastids in dinoflagellates through tertiary endosymbiosis. Proc. Natl. Acad. Sci. USA 99:11724-11729.