Sawyeria marylandensis (heterolobosea) has a hydrogenosome with novel metabolic properties

Eukaryotic Cell

Volumn 9, Issue 12, 2010, Pages 1913-1924

  Barberà, Maria José ^a   Ruiz Trillo, Iñaki ^a,b   Tufts, Julia Y A ^a   Bery, Amandine ^b   Silberman, Jeffrey D ^a,c   Roger, Andrew J ^a  

^a DALHOUSIE UNIVERSITY   (Canada)

^b UNIVERSITY OF BARCELONA   (Spain)

^c UNIVERSITY OF ARKANSAS   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CILIOPHORA; FUNGI; HETEROLOBOSEA; NAEGLERIA GRUBERI; PARABASALIDEA; PROTISTA; SAWYERIA MARYLANDENSIS;

EID: 78649917623     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.00122-10     Document Type: Article

References (59)

1. Ali, V., Y. Shigeta, U. Tokumoto, Y. Takahashi, and T. Nozaki. 2004. 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.
2. Anderson, I. J., and B. J. Loftus. 2005. Entamoeba histolytica: observations on metabolism based on the genome sequence. Exp. Parasitol. 110:173-177.
3. Andreoli, C., H. Prokisch, K. Hortnagel, J. C. Mueller, M. Munsterkotter, C. Scharfe, and T. Meitinger. 2004. MitoP2, an integrated database on mitochondrial proteins in yeast and man. Nucleic Acids Res. 32:D459-D462.
4. Badidi, E., C. De Sousa, B. F. Lang, and G. Burger. 2003. AnaBench: a Web/CORBA-based workbench for biomolecular sequence analysis. BMC Bioinform. 4:63.
5. Barber, M. J., I. Ruiz-Trillo, J. Leigh, L. A. Hug, and A. J. Roger. 2007. The diversity of mitochondrion-related organelles amongst eukaryotic microbes, p. 239-275. In W. F. Martin and M. Müller (ed.), Origin of mitochondria and hydrogenosomes. Springer-Verlag, Berlin, Germany.
6. Biagini, G. A., and C. Bernard. 2000. Primitive anaerobic protozoa: a false concept? Microbiology 146:1019-1020.
7. Boxma, B., R. M. de Graaf, G. W. van der Staay, T. A. van Alen, G. Ricard, T. Gabaldon, A. H. van Hoek, S. Y. Moon-van der Staay, W. J. Koopman, J. J. van Hellemond, A. G. Tielens, T. Friedrich, M. Veenhuis, M. A. Huynen, and J. H. Hackstein. 2005. An anaerobic mitochondrion that produces hydrogen. Nature 434:74-79.
8. Burri, L., B. A. Williams, D. Bursac, T. Lithgow, and P. J. Keeling. 2006. Microsporidian mitosomes retain elements of the general mitochondrial targeting system. Proc. Natl. Acad. Sci. U. S. A. 103:15916-15920.
9. Carlton, J. M., R. P. Hirt, J. C. Silva, A. L. Delcher, M. Schatz, Q. Zhao, J. R. Wortman, S. L. Bidwell, U. C. Alsmark, S. Besteiro, T. Sicheritz-Ponten, C. J. Noel, J. B. Dacks, P. G. Foster, C. Simillion, Y. Van de Peer, D. Miranda-Saavedra, G. J. Barton, G. D. Westrop, S. Muller, D. Dessi, P. L. Fiori, Q. Ren, I. Paulsen, H. Zhang, F. D. Bastida-Corcuera, A. Simoes- Barbosa, M. T. Brown, R. D. Hayes, M. Mukherjee, C. Y. Okumura, R. Schneider, A. J. Smith, S. Vanacova, M. Villalvazo, B. J. Haas, M. Pertea, T. V. Feldblyum, T. R. Utterback, C. L. Shu, K. Osoegawa, P. J. de Jong, I. Hrdy, L. Horvathova, Z. Zubacova, P. Dolezal, S. B. Malik, J. M. J. Logsdon, K. Henze, A. Gupta, C. C. Wang, R. L. Dunne, J. A. Upcroft, P. Upcroft, O. White, S. L. Salzberg, P. Tang, C. H. Chiu, Y. S. Lee, T. M. Embley, G. H. Coombs, J. C. Mottram, J. Tachezy, C. M. Fraser-Liggett, and P. J. Johnson. 2007. Draft genome sequence of the sexually transmitted pathogen Trichomonas vaginalis. Science 315:207-212.
10. Claros, M. G. 1995. MitoProt, a Macintosh application for studying mitochondrial proteins. Comput. Appl. Biosci. 11:441-447.
11. Clements, A., D. Bursac, X. Gatsos, A. J. Perry, S. Civciristov, N. Celik, V. A. Likic, S. Poggio, C. Jacobs-Wagner, R. A. Strugnell, and T. Lithgow. 2009. The reducible complexity of a mitochondrial molecular machine. Proc. Natl. Acad. Sci. U. S. A. 106:15791-15795.
12. de Graaf, R. M., I. Duarte, T. A. van Alen, J. W. Kuiper, K. Schotanus, J. Rosenberg, M. A. Huynen, and J. H. Hackstein. 2009. The hydrogenosomes of Psalteriomonas lanterna. BMC Evol. Biol. 9:287.
13. Dolezal, P., A. Dancis, E. Lesuisse, R. Sutak, I. Hrdy, T. M. Embley, and J. Tachezy. 2007. Frataxin, a conserved mitochondrial protein, in the hydrogenosome of Trichomonas vaginalis. Eukaryot. Cell 6:1431-1438.
14. Dolezal, P., V. Likic, J. Tachezy, and T. Lithgow. 2006. Evolution of the molecular machines for protein import into mitochondria. Science 313:314-318.
15. Douce, R., J. Bourguignon, M. Neuburger, and F. Rebeille. 2001. The glycine decarboxylase system: a fascinating complex. Trends Plant Sci. 6:167-176.
16. Embley, T. M., and W. Martin. 2006. Eukaryotic evolution, changes and challenges. Nature 440:623-630.
17. Embley, T. M. 2006. Multiple secondary origins of the anaerobic lifestyle in eukaryotes. Philos. Trans. R. Soc. Lond. B Biol. Sci. 361:1055-1067.
18. Ewing, B., and P. Green. 1998. Base-calling of automated sequencer traces using phred. II. Error probabilities. Genome Res. 8:186-194.
19. Fritz-Laylin, L. K., S. E. Prochnik, M. L. Ginger, J. B. Dacks, M. L. Carpenter, M. C. Field, A. Kuo, A. Paredez, J. Chapman, J. Pham, S. Shu, R. Neupane, M. Cipriano, J. Mancuso, H. Tu, A. Salamov, E. Lindquist, H. Shapiro, S. Lucas, I. V. Grigoriev, W. Z. Cande, C. Fulton, D. S. Rokhsar, and S. C. Dawson. 2010. The genome of Naegleria gruberi illuminates early eukaryotic versatility. Cell 140:631-642.
20. Gelius-Dietrich, G., M. Ter Braak, and K. Henze. 2007. Mitochondrial steps of arginine biosynthesis are conserved in the hydrogenosomes of the chytridiomycete Neocallimastix frontalis. J. Eukaryot. Microbiol. 54:42-44.
21. Gill, E. E., S. Diaz-Trivino, M. J. Barbera, J. D. Silberman, A. Stechmann, D. Gaston, I. Tamas, and A. J. Roger. 2007. Novel mitochondrion-related organelles in the anaerobic amoeba Mastigamoeba balamuthi. Mol. Microbiol. 66:1306-1320.
22. Goldberg, A. V., S. Molik, A. D. Tsaousis, K. Neumann, G. Kuhnke, F. Delbac, C. P. Vivares, R. P. Hirt, R. Lill, and T. M. Embley. 2008. Localization and functionality of microsporidian iron-sulphur cluster assembly proteins. Nature 452:624-628.
23. Hackstein, J. H. P., J. Tjaden, W. Koopman, and M. Huynen. 2007. Hydrogenosomes (and related organelles, either) are not the same, p. 135-159. In W. F. Martin and M. Müller (ed.), Origin of mitochondria and hydrogenosomes. Springer-Verlag, Berlin, Germany.
24. Hampl, V., L. Hug, J. W. Leigh, J. B. Dacks, B. F. Lang, A. G. Simpson, and A. J. Roger. 2009. Phylogenomic analyses support the monophyly of Excavata and resolve relationships among eukaryotic "supergroups." Proc. Natl. Acad. Sci. U. S. A. 106:3859-3864.
25. Hampl, V., J. D. Silberman, A. Stechmann, S. Diaz-Trivino, P. J. Johnson, and A. J. Roger. 2008. Genetic evidence for a mitochondriate ancestry in the 'amitochondriate' flagellate trimastix pyriformis. PLoS One 3:e1383.
26. Hampl, V., and A. G. B. Simpson. 2008. Possible mitochondria-related organelles in poorly-studied "amitochondriate" eukaryotes, p. 265-282. In J. Tachezy (ed.), Hydrogenosomes and mitosomes: mitochondria of anaerobic eukaryotes. Springer Science Business Media, Berlin, Germany.
27. Hrdy, I., R. P. Hirt, P. Dolezal, L. Bardonova, 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. Hrdy, I., and M. Muller. 1995. Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote Trichomonas vaginalis. J. Mol. Evol. 41:388-396.
29. Hug, L. A., A. Stechmann, and A. J. Roger. 2010. Phylogenetic distributions and histories of proteins involved in anaerobic pyruvate metabolism in eukaryotes. Mol. Biol. Evol. 27:311-324.
30. Lill, R., and U. Muhlenhoff. 2005. Iron-sulfur-protein biogenesis in eukaryotes. Trends Biochem. Sci. 30:133-141.
31. Lloyd, D., J. R. Ralphs, and J. C. Harris. 2002. Giardia intestinalis, a eukaryote without hydrogenosomes, produces hydrogen. Microbiology (Reading, England) 148:727-733.
32. Loftus, B., I. Anderson, R. Davies, U. C. Alsmark, J. Samuelson, P. Amedeo, P. Roncaglia, M. Berriman, R. P. Hirt, B. J. Mann, T. Nozaki, B. Suh, M. Pop, M. Duchene, J. Ackers, E. Tannich, M. Leippe, M. Hofer, I. Bruchhaus, U. Willhoeft, A. Bhattacharya, T. Chillingworth, C. Churcher, Z. Hance, B. Harris, D. Harris, K. Jagels, S. Moule, K. Mungall, D. Ormond, R. Squares, S. Whitehead, M. A. Quail, E. Rabbinowitsch, H. Norbertczak, C. Price, Z. Wang, N. Guillen, C. Gilchrist, S. E. Stroup, S. Bhattacharya, A. Lohia, P. G. Foster, T. Sicheritz-Ponten, C. Weber, U. Singh, C. Mukherjee, N. M. El- Sayed, W. A. Petri, Jr., C. G. Clark, T. M. Embley, B. Barrell, C. M. Fraser, and N. Hall. 2005. The genome of the protist parasite Entamoeba histolytica. Nature 433:865-868.
33. Mentel, M., V. Zimorski, P. Haferkamp, W. Martin, and K. Henze. 2008. Protein import into hydrogenosomes of Trichomonas vaginalis involves both N-terminal and internal targeting signals: a case study of thioredoxin reductases. Eukaryot. Cell 7:1750-1757.
34. Miichi, F., M. Abu Yousuf, K. Nakada-Tsukui, and T. Nozaki. 2009. Mitosomes in Entamoeba histolytica contain a sulfate activation pathway. Proc. Natl. Acad. Sci. U. S. A. 106:21731-21736.
35. Mukherjee, M., M. T. Brown, A. G. McArthur, and P. J. Johnson. 2006. Proteins of the glycine decarboxylase complex in the hydrogenosome of Trichomonas vaginalis. Eukaryot. Cell 5:2062-2071.
36. Muller, M. 1993. The hydrogenosome. J. Gen. Microbiol. 139:2879-2889.
37. Nakai, K., and P. Horton. 1999. PSORT: a program for detecting sorting signals in proteins and predicting their subcellular localization. Trends Biochem. Sci. 24:34-36.
38. O'brien, E. A., L. B. Koski, Y. Zhang, L. Yang, E. Wang, M. W. Gray, G. Burger, and B. F. Lang. 2007. TBestDB: a taxonomically broad database of expressed sequence tags (ESTs). Nucleic Acids Res. 35:D445-D451.
39. O'Kelly, C. J., J. D. Silberman, L. A. Amaral Zettler, T. A. Nerad, and M. L. Sogin. 2003. Monopylocystis visvesvarai n. gen., n. sp. and Sawyeria marylandensis n. gen., n. sp.: two new amitochondrial heterolobosean amoebae from anoxic environments. Protist 154:281-290.
40. Page, F. C., and R. L. Blanton. 1985. The heterolobosea(Sarcodina: Rhizopoda), a new class uniting the Schizopyrenida and the Acrasidae(Acrasida). Protistologica 21:121-132.
41. Posewitz, M. C., P. W. King, S. L. Smolinski, R. D. Smith, A. R. Ginley, M. L. Ghirardi, and M. Seibert. 2005. Identification of genes required for hydrogenase activity in Chlamydomonas reinhardtii. Biochem. Soc Trans. 33:102-104.
42. Posewitz, M. C., P. W. King, S. L. Smolinski, L. Zhang, M. Seibert, and M. L. Ghirardi. 2004. Discovery of two novel radical S-adenosylmethionine proteins required for the assembly of an active [Fe] hydrogenase. J. Biol. Chem. 279:25711-25720.
43. Putz, S., P. Dolezal, G. Gelius-Dietrich, L. Bohacova, J. Tachezy, and K. Henze. 2006. Fe-hydrogenase maturases in the hydrogenosomes of Trichomonas vaginalis. Eukaryot. Cell 5:579-586.
44. Reeves, R. E., L. G. Warren, B. Susskind, and H. S. Lo. 1977. An energyconserving pyruvate-to-acetate pathway in Entamoeba histolytica. Pyruvate synthase and a new acetate thiokinase. J. Biol. Chem. 252:726-731.
45. Rodriguez-Ezpeleta, N., H. Brinkmann, B. Roure, N. Lartillot, B. F. Lang, and H. Philippe. 2007. Detecting and overcoming systematic errors in genome- scale phylogenies. Syst. Biol. 56:389-399.
46. Schirch, V., and D. M. Szebenyi. 2005. Serine hydroxymethyltransferase revisited. Curr. Opin. Chem. Biol. 9:482-487.
47. Schneider, G., S. Sjoling, E. Wallin, P. Wrede, E. Glaser, and G. von Heijne. 1998. Feature-extraction from endopeptidase cleavage sites in mitochondrial targeting peptides. Proteins 30:49-60.
48. Silberman, J. D., A. G. 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.
49. Smith, S. W., R. Overbeek, C. R. Woese, W. Gilbert, and P. M. Gillevet. 1994. The genetic data environment an expandable GUI for multiple sequence analysis. Comput. Appl. Biosci. 10:671-675.
50. Stamatakis, A. 2006. RAxML-VI-HPC: maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690.
51. Stechmann, A., K. Hamblin, V. Perez-Brocal, D. Gaston, G. S. Richmond, M. van der Giezen, C. G. Clark, and A. J. Roger. 2008. Organelles in blastocystis that blur the distinction between mitochondria and hydrogenosomes. Curr. Biol. 18:580-585.
52. Taylor, S. W., E. Fahy, B. Zhang, G. M. Glenn, D. E. Warnock, S. Wiley, A. N. Murphy, S. P. Gaucher, R. A. Capaldi, B. W. Gibson, and S. S. Ghosh. 2003. Characterization of the human heart mitochondrial proteome. Nat. Biotechnol. 21:281-286.
53. Tielens, A. G., K. W. van Grinsven, K. Henze, J. J. van Hellemond, and W. Martin. 2010. Acetate formation in the energy metabolism of parasitic helminths and protists. Int. J. Parasitol. 40:387-397.
54. Tovar, J. 2007. Mitosomes of parasitic protozoa: biology and evolutionary significance, p. 276-300. In W. F. Martin and M. Müller (ed.), Origin of mitochondria and hydrogenosomes. Springer-Verlag, Berlin, Germany.
55. 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.
56. Townson, S. M., J. A. Upcroft, and P. Upcroft. 1996. Characterisation and purification of pyruvate:ferredoxin oxidoreductase from Giardia duodenalis. Mol. Biochem. Parasitol. 79:183-193.
57. van der Giezen, M., J. Tovar, and C. G. Clark. 2005. Mitochondrion-derived organelles in protists and fungi. Int. Rev. Cytol. 244:175-225.
58. van Grinsven, K. W., S. Rosnowsky, S. W. van Weelden, S. Putz, M. van der Giezen, W. Martin, J. J. van Hellemond, A. G. Tielens, and K. Henze. 2008. Acetate:succinate CoA-transferase in the hydrogenosomes of Trichomonas vaginalis: identification and characterization. J. Biol. Chem. 283:1411-1418.
59. 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.