Iron-dependent hydrogenases of Entamoeba histolytica and Giardia lamblia: Activity of the recombinant entamoebic enzyme and evidence for lateral gene transfer

Biological Bulletin

Volumn 204, Issue 1, 2003, Pages 1-9

  Nixon, Julie E J ^a   Field, Jessica ^a   McArthur, Andrew G ^b   Sogin, Mitchell L ^b   Yarlett, Nigel ^c   Loftus, Brendan J ^d   Samuelson, John ^a,e  

^a HARVARD SCHOOL OF PUBLIC HEALTH   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c PACE UNIVERSITY   (United States)

^d J CRAIG VENTER INSTITUTE   (United States)

^e BOSTON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENZYME; GENE TRANSFER;

BACTERIA (MICROORGANISMS); DIPLOMONADIDA; ENTAMOEBA HISTOLYTICA; GIARDIA INTESTINALIS; GIARDIA LAMBLIA; PROTISTA; PROTOZOA; SPIRONUCLEUS BARKHANUS;

EID: 0037329339     PISSN: 00063185     EISSN: None     Source Type: Journal    
DOI: 10.2307/1543490     Document Type: Article

References (52)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer, J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25: 3389-3402.
2. Andersson, S. G., and C. G. Kurland. 1999. Origins of mitochondria and hydrogenosomes. Curr. Opin. Microbiol. 2: 535-541.
3. Bapteste, E., H. Brinkmann, J. A. Lee, D. V. Moore, C. W. Sensen, P. Gordon, L. Durufle, T. Gaasterland, P. Lopez, M. Müller, 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.
4. Bradley, P. J., C. J. Lahti, E. Plumper, and P. J. Johnson. 1997. Targeting and translocation of proteins into the hydrogenosome of the protist Trichomonas: similarities with mitochondrial protein import. EMBO J. 16: 3484-3493.
5. Brown, D. M., J. A. Upcroft, M. R. Edwards, and P. Upcroft. 1998. Anaerobic bacterial metabolism in the ancient eukaryote Giardia duodenalis. Int. J. Parasitol. 28: 149-164.
6. Bui, E. T., and P. J. Johnson. 1996. Identification and characterization of [Fe]-hydrogenases in the hydrogenosome of Trichomonas vaginalis. Mol. Biochem. Parasitol. 76: 305-310.
7. Bui, E. T., P. J. Bradley, and P. J. Johnson. 1996. A common evolutionary origin for mitochondria and hydrogenosomes. Proc. Natl. Acad. Sci. USA 93: 9651-9656.
8. Cammark, R. 1992. Iron-sulfur clusters in enzymes: themes and variations. Adv. Inorg. Chem. 38: 281-322.
9. Choczynski, P., and N. Sacchi. 1987. Single-step method of RNA isolation by acid guanidinium-thiocyanate-phenol-chloroform extraction. Anal. Biochem. 162: 156-159.
10. 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.
11. Claros, M. G., and P. Vincens. 1996. Computational method to predict mitochondrially imported proteins and their targeting sequences. Eur. J. Biochem. 241: 779-786.
12. Dayhoff, M. O., R. M. Schwartz, and B. C. Orcutt. 1978. Pp. 345-352 in Atlas of Protein Sequence and Structure, Vol. 5, suppl. 3. National Biomedical Research Foundation, Silver Spring, MD.
13. de Koning, A. P., F. S. Brinkman, S. J. Jones, and P. J. Keeling. 2000. Lateral gene transfer and metabolic adaptation in the human parasite Trichomonas vaginalis. Mol. Biol. Evol. 17: 1769-1773.
14. 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.
15. Doolittle, W. F. 1999. Phylogenetic classification and the universal tree. Science 284: 2124-2129.
16. Dyall, S. D., C. M. Koehler, M. G. Delgadillo-Correa, P. J. Bradley, E. Plumper, D. Leuenberger, C. W. Turck, and P. J. Johnson. 2000. 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.
17. Felsenstein, J. 1989. PHYLIP-phylogeny inference package (version 3.2). Cladistics 5: 164-166.
18. Field, J., B. Rosenthal, and J. Samuelson. 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.
19. Fitch, W. M., and E. Margoliash. 1967. Construction of phylogenetic trees. Science 155: 279-284.
20. Ghosh, S., J. Field, R. Rogers, M. Hickman, and J. Samuelson. 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.
21. Gray, M. W., G. Burger, and B. F. Lang. 1999. Mitochondrial evolution. Science 283: 1476-1481.
22. 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.
23. Horner, D. S., R. P. Hirt, and T. M. Embley. 1999. A single eubacterial origin of eukaryofic pyruvate: ferredoxin oxidoreductase genes: implications for the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 16: 1280-1291.
24. Horner, D. S., P. G. Foster, and T. M. Embley. 2000. Iron hydrogenases and the evolution of anaerobic eukaryotes. Mol. Biol. Evol. 17: 1695-1709.
25. Hrdy, I., and M. Müller. 1995a. Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote Trichomonas vaginalis. J. Mol. Evol. 41: 388-396.
26. Hrdy, I., and M. Müller. 1995b. Primary structure of the hydrogenosomal malic enzyme of Trichomonas vaginalis and its relationship to homologous enzymes. J. Eukaryot. Microbiol. 42: 593-603.
27. Huston, C. D., and W. A. Petri. 2001. Emerging and reemerging intestinal protozoa. Curr. Opin. Gastroenterol. 17: 17-23.
28. Johnson, P. J., C. E. d'Oliveira, T. E. Gorrell, and M. Müller. 1990. Molecular analysis of the hydrogenosomal ferrédoxin of the anaerobic protist Trichomonas vaginalis. Proc. Natl. Acad. Sci. USA 87: 6097-6101.
29. Lindmark, D. G., and M. Müller. 1973. Hydrogenosome, a cytoplasmic organelle of the anaerobic flagellate Trichomonas foetus, and its role in pyruvate metabolism. J. Biol. Chem. 248: 7724-7728.
30. Lloyd, D., and J. C. Harris. 2002. Giardia: highly evolved parasite or early branching eukaryote? Trends Microbiol. 10: 122-127.
31. Mai, Z., 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. Martin, W., and M. Müller. 1998. The hydrogen hypothesis for the first eukaryote. Nature 392: 37-41.
33. McArthur, A. G., H. G. Morrison, J. E. Nixon, N. Q. Passamaneck, U. Kim, G. Hinkle, M. K. Crocker, M. E. Holder, R. Farr, C. I. Reich, G. E. Olsen, S. B. Aley, R. D. Adam, F. D. Gillin, and M. L. Sogin. 2000. The Giardia genome project database. FEMS Microbiol. Lett. 189: 271-273.
34. Müller, M. 1993. The hydrogenosome. J. Gen. Microbiol. 139: 2879-2889.
35. Müller, M. 1998. Enzymes and compartmentation of core energy metabolism of anaerobic protist - a special case in eukaryotic evolution. Pp. 109-127 in Evolutionary Relationships among Protozoa, G. H. Coombs, K. Vickerman, M. A. Sleigh, and A. Warren, eds. Kluwer Academic, London.
36. Nicolet, Y., C. Piras, P. Legrand, C. E. Hatchikian, and J. C. Fontecilia-Camps. 1999. Desulfovibrio desulfuricans iron hydrogenase: the structure shows unusual coordination to an active site Fe binuclear center. Struct. Fold. Des. 7: 13-23.
37. Nixon, J. E. J., A. Wang, J. Field, H. G. Morrison, A. G. McArthur, M. L. Sogin, B. Loftus, and J. Samuelson. 2002. Evidence for lateral transfer of genes encoding ferredoxins, nitroreductases, NADH oxidase and alcohol dehydrogenase 3 from anaerobic prokaryotes to Giardia lamblia and Entamoeba histolytica. Euk. Cell 1: 181-190.
38. Payne, M. J., A. Chapman, and R. Cammack. 1993. Evidence for an [Fe]-type hydrogenase in the parasitic protozoan Trichomonas vaginalis. FEBS Lett. 317: 101-104.
39. Peters, J. W., W. N. Lanzilotta, B. J. Lemon, and L. C. Seefeldt. 1998. X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282: 1853-1858.
40. Reeves, R. E. 1984. Metabolism of Entamoeba histolytica Scaudinn, 1903. Adv. Parasitol. 23: 105-142.
41. 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.
42. Rosenthal, B., Z. Mai, D. Caplivski, S. Ghosh, H. de la Vega, T. Graf, and J. Samuelson. 1997. Evidence for the bacterial origin of genes encoding fermentation enzymes of the amitochondriate protozoan parasite Entamoeba histolytica. J. Bacteriol. 179: 3736-3745.
43. Rotte, C., K. Henze, M. Müller, and W. Martin. 2000. Origins of hydrogenosomes and mitochondria. Curr. Opin. Microbiol. 3: 481-486.
44. Searcy, D. G. 1992. Origins of mitochondria and chloroplasts from sulfur based symbiosis. Pp. 47-78 in The Origin and Evolution of the Cell, H. Hartman and K. Matsuna, eds. World Scientific, London.
45. Smith, D. B., and K. S. Johnson. 1988. Single-step purification of polypeptides expressed in Escherichia coli as fusions with glutathione S-transferase. Gene 67: 31-40.
46. 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.
47. Strimmer, K., and A. von Haeseler. 1996. Quartet puzzling: a quarter maximum likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13: 964-969.
48. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22: 4673-4680.
49. 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.
50. van Hoek, A. H., A. S. Akhmanova, M. A. Huynen, and J. H. Hackstein. 2000. A mitochondrial ancestry of the hydrogenosomes of Nyctotherus ovalis. Mol. Biol. Evol. 17: 202-206.
51. Voncken, F. G., B. Boxma, A. H. van Hoek, A. S. Akhmanova, G. D. Vogels, M. Huynen, M. Veenhuis, and J. H. Hackstein. 2002. A hydrogenosomal [Fe]-hydrogenase from the anaerobic chytrid Neocallimastix sp. L2. Gene 284: 103-112.
52. Wunschiers, R., K. Stangier, H. Senger, and R. Schulz. 2001. Molecular evidence for a Fe-hydrogenase in the green alga Scenedesmus obliquus. Curr. Microbiol. 42: 353-360.