Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes

Current Biology

Volumn 13, Issue 2, 2003, Pages 94-104

  Andersson, Jan O ^a   Sjögren, Åsa M ^a   Davis, Lesley A M ^a   Embley, T Martin ^b   Roger, Andrew J ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ADAPTATION, PHYSIOLOGICAL; ALDEHYDE OXIDOREDUCTASES; ALDEHYDE-LYASES; AMINO ACYL-TRNA SYNTHETASES; ANAEROBIOSIS; ANIMALS; DIPLOMONADIDA; DNA, PROTOZOAN; EVOLUTION, MOLECULAR; GENE TRANSFER, HORIZONTAL; GENES, PROTOZOAN; GIARDIA LAMBLIA; MOLECULAR SEQUENCE DATA; PHYLOGENY; PROTOZOAN PROTEINS; THREONINE DEHYDRATASE; TRANSAMINASES;

DIPLOMONADIDA; EUKARYOTA; GIARDIA; GIARDIA INTESTINALIS; LANGAT VIRUS; PROKARYOTA; PROTISTA; PROTOZOA; SALMO SALAR; SPIRONUCLEUS; SPIRONUCLEUS BARKHANUS; VERTEBRATA;

EID: 0037458124     PISSN: 09609822     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0960-9822(03)00003-4     Document Type: Article

References (54)

1. Doolittle, W.F. (1999). Phylogenetic classification and the universal tree. Science 284, 2124-2129.
2. Boucher, Y., and Doolittle, W.F. (2000). The role of lateral gene transfer in the evolution of isoprenoid biosynthesis pathways. Mol. Microbiol. 37, 703-716.
3. Suguri, S., Henze, K., Sánchez, L.B., Moore, D.V., and Müller, M. (2001). Archaebacterial relationships of the phosphoenolpyruvate carboxykinase gene reveal mosaicism of Giardia intestinalis core metabolism. J. Eukaryot. Microbiol. 48, 493-497.
4. Wu, G., Henze, K., and Müller, M. (2001). Evolutionary relationships of the glucokinase from the amitochondriate protist, Trichomonas vaginalis. Gene 264, 265-271.
5. Field, J., Rosenthal, B., and Samuelson, J. (2000). Early lateral transfer of genes encoding malic enzyme, acetyl-CoA synthetase and alcohol dehydrogenases from anaerobic prokaryotes to Entamoeba histolytica. Mol. Microbiol. 38, 446-455.
6. Henze, K., Horner, D.S., Suguri, S., Moore, D.V., Sánchez, L.B., Müller, M., and Embley, T.M. (2001), Unique phylogenetic relationship of glucokinase and glucosephosphate isomerase of the amitochondriate eukaryotes Giardia intestinalis, Spironucleus barkhanus and Trichomonas vaginalis. Gene 281, 123-131.
7. Striepen, B., White, M.W., Li, C., Guerini, M.N., Malik, S.-B., Logsdon, J.M., Jr., Liu, C., and Abrahamsen, M.S. (2002). Genetic complementation in apicomplexan parasites. Proc. Natl. Acad. Sci. USA 99, 6304-6309.
8. Nixon, J.E.J., Wang, A., Field, J., Morrison, H.G., McArthur, A.G., Segin, M.L., Loftus, B.J., and Samuelson, J. (2002). Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase, and alcohol dehydregenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Eukaryot. Cell 1, 181-190.
9. Andersson, J.O., and Roger, A.J. (2002). Evolutionary analyses of the small subunit of glutamate synthase: gene order conservation, gene fusions and prokaryote-to-eukaryote lateral gene transfers. Eukaryot. Cell 1, 304-310.
10. 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.
11. Sogin, M.L., Gunderson, J.H., Elwood, H.J., Alonso, R.A., and Peattie, D.A. (1989). Phylogenetic meaning of the kingdom concept: an unusual ribosomal RNA from Giardia lamblia. Science 243, 75-77.
12. Upcroft, J., and Upcroft, P. (1998). My favorite cell: Giardia. Bioessays 20, 256-263.
13. Roger, A.J., Svärd, S.G., Tovar, J., Clark, C.G., Smith, M.W., Gillin, F.D., and Sogin, M.L. (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.
14. Simpson, A.G.B., Roger, A.J., Silberman, J.D., Leipe, D.D., Edgcomb, V.P., Jermiin, L.S., Patterson, D.J., and Sogin, M.L. (2002). Evolutionary history of 'early diverging' eukaryotes: the excavate taxon Carpediemonas is a close relative of Giardia. Mol. Biol. Evol. 19, 1782-1791.
15. Tachezy, J., Sánchez, L.B., and 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.
16. Horner, D.S., and 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.
17. Embley, T.M., and Hirt, R.P. (1998). Early branching eukaryotes? Curr. Opin. Genet. Dev. 8, 624-629.
18. Roger, A.J. (1999). Reconstructing early events in eukaryotic evolution. Am. Nat. 154, S146-S163.
19. Stechmann, A., and Cavalier-Smith, T. (2002). Rooting the eukaryote tree by using a derived gene fusion. Science 297, 89-91.
20. McArthur, A.G., Morrison, H.G., Nixon, J.E., Passamaneck, N.Q., Kim, U., Hinkle, G., Crocker, M.K., Holder, M.E., Farr, R., Reich, C.I., et al. (2000). The Giardia genome project database. FEMS Microbiol. Lett. 189, 271-273.
21. Silberman, J.D., Simpson, A.G.B., Kulda, J., Cepicka, I., Hampl, V., Johnson, P.J., and Roger, A.J. (2002). Retortamonad flagellates are closely related to diplomonads - implications for the history of mitochondrial function in eukaryote evolution. Mol. Biol. Evol. 19, 777-786.
22. Bunjun, S., Stathopoulos, C., Graham, D., Min, B., Kitabatake, M., Wang, A.L., Wang, C.C., Vivares, C.P., Weiss, L.M., and Soll, D. (2000). A dual-specificity aminoacyl-tRNA synthetase in the deep-rooted eukaryote Giardia lamblia. Proc. Natl. Acad. Sci. USA 97, 12997-13002.
23. Chihade, J.W., Brown, J.R., Schimmel, P.R., and 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.
24. Felsenstein, J. (1978). Cases in which parsimony or compatibility methods will be positively misleading. Syst. Zool. 27, 401-410.
25. Bapteste, E., Brinkmann, H., Lee, J.A., Moore, D.V., Sensen, C.W., Gordon, P., Durufle, L., Gaasterland, T., Lopez, P., Müller, M., et al. (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.
26. Arisue, N., Hashimoto, T., Lee, J.A., Moore, D.V., Gordon, P., Sensen, C.W., Gaasterland, T., Hasegawa, M., and Müller, M. (2002). The phylogenetic position of the pelobiont Mastig-amoeba balamuthi based on sequences of rRNA and translation elongation factors EF-1α and EF-2. J. Eukaryot. Microbiol. 49, 1-10.
27. Baldauf, S.L., Roger, A.J., Wenk-Siefert, I., and Doolittle, W.F. (2000). A kingdom-level phylogeny of eukaryotes based on combined protein data. Science 290, 972-977.
28. Shimodaira, H. (2002). An approximately unbiased test of phylogenetic tree selection. Syst. Biol. 51, 492-508.
29. Dan, M., and Wang, C.C. (2000). Role of alcohol dehydrogenase E (ADHE) in the energy metabolism of Giardia lamblia. Mol. Biochem. Parasitol. 109, 25-36.
30. van den Berg, W.A., Hagen, W.R., and van Dongen, W.M. (2000). The hybrid-cluster protein ('prismane protein') from Escherichia coli. Characterization of the hybrid-cluster protein, redox properties of the [2Fe-2S] and [4Fe-2S-2O] clusters and identification of an associated NADH oxidoreductase containing FAD and [2Fe-2S]. Eur. J. Biochem. 267, 666-676.
31. Wasserfallen, A., Ragettli, S., Jouanneau, Y., and Leisinger, T. (1998). A family of flavoproteins in the domains Archaea and Bacteria. Eur. J. Biochem. 254, 325-332.
32. Das, A., Coulter, E.D., Kurtz, D.M., Jr., and Ljungdahl, L.G. (2001). Five-gene cluster in Clostridium thermoaceticum consisting of two divergent operons encoding rubredoxin oxidore-ductase-rubredoxin and rubrerythrin-type A flavoproteinhigh-molecular-weight rubredoxin. J. Bacteriol. 183, 1560-1567.
33. Hausladen, A., Gow, A., and Stamler, J.S. (2001). Flavohemo-globin denitrosylase catalyzes the reaction of a nitroxyl equivalent with molecular oxygen. Proc. Natl. Acad. Sci. USA 98, 10108-10112.
34. Williams, B.A.P., Hirt, R.P., Lucocq, J.M., and Embley, T.M. (2002). A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418, 865-869.
35. Roger, A.J., and Silberman, J.D. (2002). Cell evolution: mitochondria in hiding. Nature 418, 827-829.
36. Sicheritz-Pontén, T., Kurland, C.G., and Andersson, S.G.E. (1998). A phylogenetic analysis of the cytochrome b and cytochrome c oxidase I genes supports an origin of mitochondria from within the Rickettsiaceae. Biochim. Biophys. Acta 1365, 545-551.
37. Henze, K., Morrison, H.G., Sogin, M.L., and Müller, M. (1998). Sequence and phylogenetic position of a class II aldolase gene in the amitochondriate protist, Giardia lamblia. Gene 222, 163-168.
38. Sánchez, L.B., Galperin, M.Y., and Müller, M. (2000). Acetyl-CoA synthetase from the amitochondriate eukaryote Giardia lamblia belongs to the newly recognized superfamily of acyl-CoA synthetases (nucleoside diphosphate-forming). J. Biol. Chem. 275, 5794-5803.
39. Tovar, J., Fischer, A., and Clark, C.G. (1999). The mitosome, a novel organelle related to mitochondria in the amitochondrial parasite Entamoeba histolytica. Mol. Microbiol. 32, 1013-1021.
40. Martin, W., and Müller, M. (1998). The hydrogen hypothesis for the first eukaryote. Nature 392, 37-41.
41. Rotte, C., Henze, K., Müller, M., and Martin, W. (2000). Origins of hydrogenosomes and mitochondria. Curr. Opin. Microbiol. 3, 481-486.
42. Keeling, P.J., and Palmer, J.D. (2001). Lateral transfer at the gene and subgenic levels in the evolution of eukaryotic enolase. Proc. Natl. Acad. Sci. USA 98, 10745-10750.
43. McFadden, G.I. (1999). Plastids and protein targeting. J. Eukaryot. Microbiol. 46, 339-346.
44. Stanhope, M.J., Lupas, A., Italia, M.J., Koretke, K.K., Volker, C., and Brown, J.R. (2001). Phylogenetic analyses do not support horizontal gene transfers from bacteria to vertebrates. Nature 411, 940-944.
45. Andersson, J.O., Doolittle, W.F., and Nesbo, C.L. (2001). Are there bugs in our genome? Science 292, 1848-1850.
46. Hartman, H., and Fedorov, A. (2002). The origin of the eukaryotic cell: a genomic investigation. Proc. Natl. Acad. Sci. USA 99, 1420-1425.
47. Gupta, R.S., and Golding, G.B. (1996). The origin of the eukaryotic cell. Trends Biochem. Sci. 21, 166-171.
48. 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.
49. Horiike, T., Hamada, K., Kanaya, S., and 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.
50. Ribeiro, S., and Golding, G.B. (1998). The mosaic nature of the eukaryotic nucleus. Mol. Biol. Evol. 15, 779-788.
51. Brown, J.R., and Doolittle, W.F. (1997). Archaea and the prokaryote-to-eukaryote transition. Microbiol. Mol. Biol. Rev. 61, 456-502.
52. Rivera, M.C., Jain, R., Moore, J.E., and Lake, J.A. (1998), Genomic evidence for two functionally distinct gene classes. Proc. Natl. Acad. Sci. USA 95, 6239-6244.
53. Rotte, C., and Martin, W. (2001). Does endosymbiosis explain the origin of the nucleus? Nat. Cell Biol. 3, E173-E174.
54. Katz, L.A. (1999). The tangled web: gene genealogies and the origin of eukaryotes. Am. Nat. 154, S137-S145.