Bacterial catalase in the microsporidian Nosema locustae: Implications for microsporidian metabolism and genome evolution

Eukaryotic Cell

Volumn 2, Issue 5, 2003, Pages 1069-1075

  Fast, Naomi M ^a   Law, Joyce S ^a   Williams, Bryony A P ^a   Keeling, Patrick J ^a  

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

ANIMALS; BACTERIA; CATALASE; EVOLUTION, MOLECULAR; GENE LIBRARY; GENE TRANSFER, HORIZONTAL; GENOME; NOSEMA; PHYLOGENY; SPORES, PROTOZOAN;

ANIMALIA; ANTONOSPORA LOCUSTAE; BACTERIA (MICROORGANISMS); ENCEPHALITOZOON CUNICULI; EUKARYOTA; FUNGI; INSERTION SEQUENCES; MICROSPORIDIA; NOSEMA; PROTEOBACTERIA;

EID: 0142153849     PISSN: 15359778     EISSN: None     Source Type: Journal    
DOI: 10.1128/EC.2.5.1069-1075.2003     Document Type: Article

References (45)

1. Aitchinson, J. D., W. W. Murray, and R. A. Rachubinski. 1991 The carboxyl-terminal tripeptide Ala-Lys-Ile is essential for targeting Candida tropicalis trifunctional enzyme to yeast peroxisomes. J. Biol. Chem. 266:23197-23203.
2. Andersson, J. O., A. M. Sjögren, L. A. M. Davis, T. M. Embley, and A. J. Roger. 2003. Phylogenetic analyses of diplomonad genes reveal frequent lateral gene transfers affecting eukaryotes. Curr. Biol. 13:94-104.
3. Brown, J. R., and W. F. Doolittle. 1999. Gene descent, duplication, and horizontal transfer in the evolution of glutamyl- and glutaminyl-tRNA synthetases. J. Mol. Evol. 49:485-495.
4. Brown, J. R., and W. F. Doolittle. 1995. Root of the universal tree of life based on ancient aminoacyl-tRNA synthetase gene duplications. Proc. Natl. Acad. Sci. USA 92:2441-2445.
5. Bruno, W. J., N. D. Soeei, and A. L. Halpern. 2000. Weighted neighbor joining: a likelihood-based approach to distance-based phylogeny reconstruction. Mol. Biol. Evol. 17:189-197.
6. Busslnk, H. J., and R. Oliver. 2001. Identification of two highly divergent catalase genes in the fungal tomato pathogen, Cladosporium fulvum. Eur. J. Biochem. 268:15-24.
7. Cavalier-Smith, T. 1983. A 6-kingdom classification and a unified phylogeny, p. 1027-1034. In H. E. A. Schenk and W S. Schwemmler (ed.), Endocytobiology II: intracellular space as oligogenetic. Walter de Gruyter & Co., Berlin, Germany.
8. Chary, P., and D. O. Natvig. 1989. Evidence for three differentially regulated catalase genes in Neurospora crassa: effects of oxidative stress, heat shock, and development. J. Bacteriol. 171:2646-2652.
9. Curgy, J. J., J. Vávra, and C. P. Vivarès. 1980. Presence of ribosomal RNAs with prokaryotic properties in microsporidia, eukaryotic organisms. Biol. Cell. 38:49-51.
10. 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. 7:1769-1773.
11. Didion, T., and R. Roggenkamp. 1992. Targeting signal of the peroxisomal catalase in the methylotrophic yeast Hansenuda polymorpha. FEBS Lett. 303:113-116.
12. Fast, N. M., and P. J. Keeling. 2001. Alpha and beta subunits of pyruvate dehydrogenase E1 from the microsporidian Nosema locustae: mitochondrion-derived carbon metabolism in microsporidia. Mol. Biochem. Parasitol. 117:201-209.
13. Fast, N. M., J. M. Logsdon, Jr., and W. F. Doolittle. 1999. Phylogenetic analysis of the TATA box binding protein (TBP) gene from Nosema locustae: evidence for a microsporidia-fungi relationship and spliceosomal intron loss. Mol. Biol. Evol. 16:1415-1419.
14. Germot, A., H. Philippe, and H. Le Guyader. 1997. Evidence for loss of mitochondrJa in microsporidia from a mitochondrial-type HSP70 in Nosema locustae. Mol. Biochem. Parasitol. 87:159-168.
15. Hansen, H., T. DJdion, A. Thiemann, M. Veenhuis, and R. Roggenkamp. 1992. Targeting sequences of the two major peroxisomal proteins in the methylotrophic yeast Hansenula polymorpha. Mol. Gen. Genet. 235:269-278.
16. Henlde-Duhrsen, K., V. H. O. Eekelt, G. Wildenhurg, M. Blaxter, and R. D. Walter. 1998. Gene structure, activity and localization of a catalase from intracellular bacteria in Onchocerca volvulus. Mol. Biochem. Parasitol. 96:69-81.
17. Hirt, R. P., B. Healy, C. R. Vosshrinck, E. U. Canning, and T. M. Embley. 1997. A mitochondrlal Hsp70 orthologue in Vairimorpha necatrix: molecular evidence that microsporidia once contained mitochondria. Curr. Biol. 7:995-998.
18. Hirt, R. P., J. M. Logsdon, Jr., 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.
19. Holroyd, C., and R. Erdmann. 2001. Protein translocation machineries of peroxisomes. FEBS Lett. 501:6-10.
20. Ishihara, R., and Y. Hayashi. 1968. Some properties of ribosomes from the sporoplasm of Nosema bombycis. J. Invertebr. Pathol. 11:377-385.
21. Johnson, C. H., M. G. Klotz, J. L York, V. Kruft, and J. E. McEwen. 2002. Redundancy, phylogeny and differential expression of Histoplasma capsulatum catalases. Microbiology 148:1129-1142.
22. Kamaishi, T. T. Hashimoto, Y. Nakamura, Y. Masuda, F. Nakamura, K. Okamoto, M. Shimizu, and M. Hasegawa. 1996. Complete nucleotide sequences of the genes encoding translation elongation factors 1 alpha and 2 from a microsporidian parasite, Glugea plecoglossi: implications for the deepest branching of eukaryotes. J. Biochem. (Tokyo) 120:1095-1103.
23. Kamaishi, T., T. Hashimoto, Y. Nakamura, F. Nakamura, S. Murata, N. Okada, K.-I. Okamoto, M. Shimzu, and M. Hasegawa. 1996. Protein phylogeny of translation elongation factor EF-1α suggests microsporidians are extremely ancient eukaryotes. J. Mol. Evol. 42:257-263.
24. Katinka, M. D., S. Duprat, E. Cornillot, G. Méténier, F. Thomarat, G. Prensier, V. Barbe, E. Peyretaillade, P. Brottier, P. Wincker, F. Delbac, H. El Alaoui, P. Peyret, W. Saurin, M. Gouy, J. Weissenbach, and C. P. Vivariès. 2001. Genome sequence and gene compaction of the eukaryote parasite Encephalitozoon cuniculi. Nature 414:450-453.
25. Kawasaki, L., and J. Aguirre. 2001. Multiple catalase genes are differentially regulated in Aspergillus nidulans. J. Bacteriol 183:1434-1440
26. Keeling, P. J. 2003. Congruent evidence from alpha-tubulin and beta-tubulin phylogenies for a zygomycete origin of microsporidia. Fungal Genet. Biol. 38:298-309.
27. 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.
28. Keeling, P. J., and N. M. Fast. 2002. Microsporidia: biology and evolution of highly reduced intracellular parasites. Annu. Rev. Microbiol. 56:93-116.
29. Keeling, P. J., M. A. Luker, and J. D. Palmer. 2000. Evidence from beta-tubulin phylogeny that microsporidia evolved from within the fungi. Mol. Biol. Evol. 17:23-31.
30. Klotz, M. G., G. R. Klassen, and P. C. Loewen. 1997. Phylogenetic relationships among prokaryotic and eukaryotic catalases. Mol. Biol. Evol. 14:951-958.
31. Klotz, M. G., and P. C. Loewen. 2003. The molecular evolution of catalatic hydroperoxidases: evidence for multiple lateral transfer of genes between prokaryota and from bacteria into eukaryota. Mol. Biol. Evol. 20:1098-1112.
32. Loewen, P. C., J. Switala, and B. L. Triggs-Raine. 1985. Catalases HPI and HPII in Escherichia coli are induced independently. Arch. Biochem. Biophys 243:144-149
33. Müller, M. 1998. Enzymes and compartmentation of core energy metabolism of anaerobic eukaryotes - a special case in eukaryotic evolution?, p. 109-132. In G. H. Coombs, K. Vickerman, M A. Sleigh, and A. Warren (ed.), Evolutionary relationships among protozoa. Chapman & Hall, New York, N.Y.
34. Navarro, R. E., M. A. Stringer, W. Hansberg, W. E. Timberlake, and J. Aguirre. 1996. catA, a new Aspergillus nidulans gene encoding a developmentally regulated catalase Curr. Genet. 29:352-359.
35. Peyretaillade, E., V. Broussolle, P. Peyret, G. Méténier, M. Gouy, and C. P. Vivarès. 1998. Microsporidia, amitochondrial protists, possess a 70-kDa heat shock protein gene of mitochondrial evolutionary origin. Mol. Biol. Evol. 15:683-689.
36. Strimmer, K., and A. von Haeseler. 1996. Quartet puzzling: a quartet maximum-likelihood method for reconstructing tree topologies. Mol. Biol. Evol. 13:964-969.
37. Switala, J., and P. C. Loewen. 2002. Diversity of properties among catalases. Arch. Biochem. Biophys. 401:145-154.
38. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: improving sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
39. Vávra, J., and J. I. R. Larsson. 1999. Structure of the microsporidia, p. 7-84. In M. Wittner and L. M. Weiss (ed.), The microsporidia and microsporidiosis. ASM Press, Washington, D.C.
40. von Ossowski, I., G. Hausner, and P. C. Loewen. 1993. Molecular evolutionary analysis based on the amino acid sequence of catalase. J. Mol. Evol. 37:71-76.
41. Vossbrinck, C. R., J. V. Maddox, S. Friedman, B. A. Dehrunner-Vossbrinck, and C. R. Woese. 1987. Ribosomal RNA sequence suggests microsporidia are extremely ancient eukaryotes. Nature 326:411-414.
42. Vossbrinck, C. R., and C. R. Woese. 1986. Eukaryotic ribosomes that lack a 5.8S RNA. Nature 320:287-288.
43. Williams, B. A., R. P. Hirt, J. M. Lucocq, and T. M. Embley. 2002. A mitochondrial remnant in the microsporidian Trachipleistophora hominis. Nature 418:865-869.
44. Witteveen, C. F. B., M. Veenhuis, and J. Visser. 1992. Localization of glucose oxidase-and catalase activities in Aspergillus niger. Appl. Environ. Microbiol. 58:1190-1194.
45. Zancopé-Oliveira, R. M., E. Reiss, T. J. Lott, L. W. Mayer, and G. S. Deepe, Jr. 1999. Molecular cloning, characterization, and expression of the M antigen of Histoplasma capsulatum. Infect. Immun. 67:1947-1953.