Inference of the phylogenetic position of oxymonads based on nine genes: Support for metamonada and Excavata

Molecular Biology and Evolution

Volumn 22, Issue 12, 2005, Pages 2508-2518

  Hampl, Vladimír ^a   Horner, David S ^b   Dyal, Patricia ^c   Kulda, Jaroslav ^a   Flegr, Jaroslav ^a   Foster, Peter G ^c,d   Embley, T Martin ^c,d  

^a CHARLES UNIVERSITY   (Czech Republic)

^b UNIVERSITY OF MILAN   (Italy)

^c DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

^d NEWCASTLE UNIVERSITY   (United Kingdom)

Author keywords

Concatenation; Excavata; Metamonada; Monocercomonoides; Oxymonads; Phylogeny

Indexed keywords

ALPHA TUBULIN; BETA TUBULIN; CONCATENATED DNA; GAMMA TUBULIN; HEAT SHOCK PROTEIN 70; HEAT SHOCK PROTEIN 90; UBIQUITIN;

AMINO ACID SEQUENCE; ANALYTIC METHOD; ARTICLE; EUKARYOTE; FLAGELLATE; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; SEQUENCE ANALYSIS;

ANIMALS; BASE SEQUENCE; CLASSIFICATION; EUKARYOTIC CELLS; EVOLUTION, MOLECULAR; FLAGELLA; GENES, RRNA; PEPTIDE ELONGATION FACTOR 1; PEPTIDE ELONGATION FACTOR 2; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; TUBULIN;

CARPEDIEMONAS; DIPLOMONADIDA; EUGLENOZOA; EUKARYOTA; EXCAVATA; HETEROLOBOSEA; JAKOBIDAE; MALAWIMONAS; MASTIGOPHORA (FLAGELLATES); MONOCERCOMONOIDES; OXYMONADIDA; PARABASALIDEA; RETORTAMONADIDAE; TRIMASTIX;

EID: 27844547962     PISSN: 07374038     EISSN: 15371719     Source Type: Journal    
DOI: 10.1093/molbev/msi245     Document Type: Article

References (60)

1. Andersson, J. O., S. W. Sarchfield, and A. J. Roger. 2004. Gene transfer from Nanoarchaeota to an ancestor of diplomonads and parabasalids. Mol. Biol. Evol. 21:1-6.
2. Arisue, N., M. Hasegawa, and T. Hashimoto. 2005. Root of the eukaryota tree as inferred from combined likelihood analyses of multiple molecular sequence data. Mol. Biol. Evol. 22:409-420.
3. Ausubel, F. M., R. Brent, R. E. Kingston, D. D. More, J. G. Seidman, J. A. Smith, and K. Struhl. 2001. Current protocols in molecular biology. John Wiley & Sons Inc., Stafford, Australia.
4. 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.
5. Bapteste, E., H. Brinkmann, J. A. Lee, D. V. Moore, C. W. Sensen, P. Gordon, L. Durufle, T. Gaasterland, P. Lopez, M. Muller, and H. Philippe. 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.
6. Brugerolle, G. 1991. Flagellar and cytoskeletal systems in amitochondrial flagellates - Archamoeba, Metamonada and Parabasala. Protoplasma 164:70-90.
7. Brugerolle, G., and J. J. Lee. 2000. Order Oxymonadida. Pp. 1186-1195 in J. Lee, G. F. Leedale, and P. Bradbury, eds. The illustrated guide to the Protozoa. J Allen Press Inc., Lawrence, Kans.
8. Cavalier-Smith, T. 1983. Endosymbiotic origin of the mitochondrial envelope. Pp. 265-279 in W. Schwemmler and H. E. A. Schenk, eds. Endocytobiology II. de Gruyter, Berlin, Germany.
9. _. 1998. A revised six-kingdom system of life. Biol. Rev. Camb. Philos. Soc. 73:203-266.
10. _. 1999. Principles of protein and lipid targeting in secondary symbiogenesis: euglenoid, dinoflagellate, and sporozoan plastid origins and the eukaryote family tree. J. Eukaryot. Microbiol. 46:347-366.
11. _. 2002. The phagotrophic origin of eukaryotes and phylogenetic classification of protozoa. Int. J. Syst. Evol. Microbiol. 52:297-354.
12. _. 2003a. 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.
13. _. 2003b. Protist phylogeny and the high-level classification of Protozoa. Eur. J. Protistol. 39: 338-348.
14. Clark, C. G., and A. J. Roger. 1995. Direct evidence for secondary loss of mitochondria in Entamoeba histolytica. Proc. Natl. Acad. Sci. USA 92:6518-6521.
15. Dacks, J., and A. J. Roger. 1999. The first sexual lineage and the relevance of facultative sex. J. Mol. Evol. 48:779-783.
16. Dacks, J. B., A. Marinets, W. F. Doolittle, T. Cavalier-Smith, and J. M. Logsdon. 2002. Analyses of RNA polymerase II genes from free-living protists: phylogeny, long branch attraction, and the eukaryotic big bang. Mol. Biol. Evol. 19:830-840.
17. Dacks, J. B., J. D. Silberman, A. G. B. Simpson, S. Moriya, T. Kudo, M. Ohkuma, and R. J. Redfield. 2001. Oxymonads are closely related to the excavate taxon Trimastix. Mol. Biol. Evol. 18:1034-1044.
18. Edgcomb, V. P., A. J. Roger, A. G. B. Simpson, D. T. 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.
19. Felsenstein, J. 1993. PHYLIP (phylogeny inference package). Version 3.6a2. Distributed by the author, Department of Genetics, University of Washington, Seattle.
20. Foster, P.G. 2004. Modeling compositional heterogeneity. Syst. Biol. 53:485-495.
21. Germot, A., H. Philippe, and H. Le Guyader. 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.
22. Guindon, S., and O. Gascuel. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 52:696-704.
23. Hall, T. A. 1999. BioEdit: a user-friendly biological sequence alignment editor and analysis program for Windows 95/98/NT. Nucleic Acids Symp. Ser. 41:95-98.
24. Henze, K., D. S. Horner, S. Suguri, D. V. Moore, L. B. Sánchez, 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.
25. Hirt, R. P., J. M. Logsdon, B. Healy, M. W. Dorey, W. F. Doolittle, and T. M. Embley. 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.
26. Horner, D. S., R. P. Hirt, S. Kilvington, D. Lloyd, and T. M. Embley. 1996. Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc. R. Soc. Lond. B Biol. Sci. 263:1053-1059.
27. Hrdy, I., R. P. Hirt, P. Dolezal, L. Bardonová, P. G. Foster, J. Tachezy, and T. M. Embley. 2004. Trichomonas hydrogenosomes contain the NADH dehydrogenase module of mitochondrial complex I. Nature 432:618-622.
28. Keeling, P. J., and W. F. Doolitle. 1996. A non-canonical genetic code in an early diverging eukaryotic lineage. EMBO J. 15:2285-2290.
29. 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.
30. Lang, B. F., M. W. Gray, and G. Burger. 1999. Mitochondrial genome evolution and the origin of eukaryotes. Annu. Rev. Genet. 33:351-397.
31. Mai, Z. M., S. Ghosh, M. Frisardi, B. Rosenthal, R. Rogers, and J. Samuelson. 1999. Hsp60 is targeted to a cryptic mitochondrion-derived organelle ("crypton") in the microaerophilic protozoan parasite Entamoeba histolytica. Mol. Cell. Biol. 19:2198-2205.
32. McFadden, G. I., and G. G. van Dooren. 2004. Evolution: red algal genome affirms a common origin of all plastids. Curr. Biol. 14:R514-R516.
33. Medlin, L., H. J. Elwood, S. Stickel, and M. L. Sogin. 1988. The characterisation of enzymatically amplified eukaryotic 16S-like rRNA-coding regions. Gene 71:491-499.
34. Moriya, S., J. B. Dacks, A. Takagi, S. Noda, M. Ohkuma, W. F. Doolittle, and T. Kudo. 2003. Molecular phylogeny of three oxymonad genera: Pyrsonympha, Dinenympha and Oxymonas. J. Eukaryot. Microbiol. 50:190-197.
35. Moriya S., M. Ohkuma, and T. Kudo. 1998. Phylogenetic position of symbiotic protist Dinenympha [correction of Dinemympha] exilis in the hindgut of the termite Reticulitermes speratus inferred from the protein phylogeny of elongation factor-1α. Gene 210:221-227.
36. Moriya, S., K. Tanaka, M. Ohkuma, S. Sugano, and T. Kudo. 2001. Diversification of the microtubule system in the early stage of eukaryote evolution: elongation factor-1α and α-tubulin protein phylogeny of termite symbiotic oxymonad and hypermastigote protists. J. Mol. Evol. 52:6-16.
37. 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.
38. Philippe, H. 2000. Opinion: long branch attraction and protist phylogeny. Protist 151:307-316.
39. Posada, D., and K. A. Crandall. 1998. Modeltest: testing the model of DNA substitution. Bioinformatics 14:817-818.
40. Roger, A. J., S. G. Svard, J. Tovar, C. G. Clark, M. W. Smith, F. D. Gillin, and M. L. Sogin. 1998. A mitochondrial-like chaperonin 60 gene in Giardia lamblia: evidence that diplomonads once harbored an endosymbiont related to the progenitor of mitochondria. Proc. Natl. Acad. Sci. USA 95:229-234.
41. Ronquist, F., and J. P. Huelsenbeck. 2003. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19:1572-1574.
42. Shimodaira, H. 2002. An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51:492-508.
43. Shimodaira, H., and M. Hasegawa. 2001. CONSEL: for assessing the confidence of phylogenetic tree selection. Bioinformatics 17:1246-1247.
44. 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.
45. Simpson, A. G. B. 2003. Cytoskeletal organization, phylogenetic affinities and systematics in the contentious taxon Excavata (Eukaryota). Int. J. Syst. Evol. Microbiol. 53:1759-1777.
46. 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.
47. 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.
48. Simpson, A. G. B., and A. J. Roger. 2004. Excavata and the origin of amitochondriate eukaryotes. Pp. 27-53 in R. Hirt and D. S. Horner, eds. Organelles, genomes and eukaryote phylogeny. CRC Press, London, UK.
49. Simpson, A. G. B., A. J. Roger, J. D. Silberman, D. 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 a close relative of Giardia. Mol. Biol. Evol. 19:1782-1791.
50. Sogin, M. L., and J. D. Silberman. 1998. Evolution of the protists and protistan parasites from the perspective of molecular systematics. Int. J. Parasitol. 28:11-20.
51. Stechmann, A., and T. Cavalier-Smith. 2003. The root of the eukaryote tree pinpointed. Curr. Biol. 13: R665-R666.
52. Stiller, J. W., and B. D. Hall. 1999. Long-branch attraction and the rDNA model of early eukaryotic evolution. Mol. Biol. Evol. 16:1270-1279.
53. Strimmer, K., and A. vonHaeseler. 1996. Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13:964-969.
54. _. 1997. Likelihood-mapping: a simple method to visualize phylogenetic content of a sequence alignment. Proc. Natl. Acad. Sci. USA 94:6815-6819.
55. Swofford, D. L. 1998. PAUP*: Phylogenetic analysis using parsimony (*and other methods). Version 4. Sinauer Associates, Sunderland, Mass.
56. Tachezy, J., L. B. Sánchez, and M. Müller. 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.
57. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 24:4876-4882.
58. Tovar, J., A. Fischer, and C. G. Clark. 1999. The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32:1013-1021.
59. 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.
60. Williams, B. A. P., R. P. Hirt, J. M. Lucocq, and T. M. Embley. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869.