Cytosolic enzymes with a mitochondrial ancestry from the anaerobic chytrid Piromyces sp. E2

Molecular Microbiology

Volumn 30, Issue 5, 1998, Pages 1017-1027

  Akhmanova, Anna ^a,b   Voncken, Frank G J ^a   Harhangi, Harry ^a   Hosea, Ken M ^a   Vogels, Godfried D ^a   Hackstein, Johannes H P ^a  

^a RADBOUD UNIVERSITY NIJMEGEN   (Netherlands)

^b ERASMUS MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

ACETOHYDROXYACID REDUCTOISOMERASE; ACONITATE HYDRATASE; BACTERIAL ENZYME; CELL ENZYME; ISOMERASE; MALATE DEHYDROGENASE; MITOCHONDRIAL ENZYME; UNCLASSIFIED DRUG;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ANAEROBIC GROWTH; ARTICLE; CARBOXY TERMINAL SEQUENCE; CYTOSOL; DNA LIBRARY; DNA SEQUENCE; ENZYME LOCALIZATION; GENE ISOLATION; MOLECULAR EVOLUTION; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; PRIORITY JOURNAL;

5' UNTRANSLATED REGIONS; ACONITATE HYDRATASE; ALCOHOL OXIDOREDUCTASES; AMINO ACID SEQUENCE; ANAEROBIOSIS; BASE SEQUENCE; CYTOSOL; DNA, COMPLEMENTARY; DNA, FUNGAL; GENE DOSAGE; GENE EXPRESSION; KETOL-ACID REDUCTOISOMERASE; MALATE DEHYDROGENASE; MITOCHONDRIA; MOLECULAR SEQUENCE DATA; PIROMYCES; RNA, FUNGAL; RNA, MESSENGER;

BACTERIA (MICROORGANISMS); EUKARYOTA; PIROMYCES SP.;

EID: 0031739880     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1998.01130.x     Document Type: Article

References (64)

1. Bergmeyer, H.U., Grassl, M., and Walter, H.-E. (1983) Enzymes. In Methods of Enzymatic Analysis. Bergmeyer, H.U., Bergmeyer, J., and Grassl, M. (eds). Weinheim: Verlag Chemie, pp. 126-328.
2. Biagini, G.A., Finlay, B.J., and Lloyd, D. (1997) Evolution of the hydrogenosome. FEMS Microbiol Lett 155: 133-140.
3. Bowman, B.H., Taylor, J.W., Brownlee, A.G., Lee, J., Lu, S.D., and White, T.J. (1992) Molecular evolution of the fungi: relationship of the Basidiomycetes, Ascomycetes, and Chytridiomycetes. Mol Biol Evol 9: 285-296.
4. Brondijk, T.H., Durand, R., van der Giezen, M., Gottschal, J.C., Prins, R.A., and Fevre, M. (1996) scsB, a cDNA encoding the hydrogenosomal beta subunit of succinyl-CoA synthetase from the anaerobic fungus Neocallimastix frontalis. Mol Gen Genet 253: 315-323.
5. Brownlee, A.G. (1994) The nucleic acids of anaerobic fungi. In Anaerobic Fungi. Biology, Ecology, and Function. Mountfort, D.O., and Orpin, C.G. (eds). New York, Basel, Hong Kong: Marcel Dekker, pp. 241-256.
6. Cendrin, F., Chroboczek, J., Zaccai, G., Eisenberg, H., and Mevarech, M. (1993) Cloning, sequencing, and expression in Escherichia coli of the gene coding for malate dehydrogenase of the extremely halophilic archaebacterium Haloarcula marismortui. Biochemistry 32: 4308-4313.
7. Chirgwin, J.M., Przybyla, A.E., MacDonald, R.J., and Rutter, W.J. (1979) Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18: 5294-5299.
8. Danpure, C.J. (1997) Variable peroxisomal and mitochondrial targeting of alanine:glyoxylate aminotransferase in mammalian evolution and disease. BioEssays 19: 317-326.
9. Devereux, J., Haeberli, P., and Smithies, O. (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12: 387-395.
10. Dijkerman, R., Ledeboer, J., Verhappen, A.B.M., den Camp, H.J.M.O., der Drift, C.V., and Vogels, G.D. (1997) The anaerobic fungus Piromyces sp. strain E2: nitrogen requirement and enzymes involved in primary nitrogen metabolism. Arch Microbiol 166: 399-404.
11. Dore, J., and Stahl, D.A. (1991) Phylogeny of anaerobic rumen Chytridiomycetes inferred from small subunit ribosomal RNA sequence comparisons. Can J Bot 69: 1964-1971.
12. Durand, R., Fischer, M., Rascle, C., and Fevre, M. (1995) Neocallimastix frontalis enolase gene, enol: first report of an intron in an anaerobic fungus. Microbiology 141: 1301-1308.
13. Embley, T.M., Horner, D.A., and Hirt, R.P. (1997) Anaerobic eukaryote evolution: hydrogenosomes as biochemically modified mitochondria? Trends Ecol Evol 12: 437-441.
14. Fanutti, C., Ponyi, T., Black, G.W., Hazlewood, G.P., and Gilbert, H.J. (1995) The conserved noncatalytic 40-residue sequence in cellulases and hemicellulases from anaerobic fungi functions as a protein docking domain. J Biol Chem 270: 29314-29322.
15. Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package). Seattle, USA: Department of Genetics, University of Washington.
16. van der Giezen, M., Sjollema, K.A., Artz, R.R., Alkema, W., and Prins, R.A. (1997a) Hydrogenosomes in the anaerobic fungus Neocallimastix frontalis have a double membrane but lack an associated organelle genome. FEBS Lett 408: 147-150.
17. van der Giezen, M., Rechinger, K.B., Svendsen, I., Durand, R., Hirt, R.P., Fevre, M., et al. (1997b) A mitochondrial-like targeting signal on the hydrogenosomal malic enzyme from the anaerobic fungus Neocallimastix frontalis: support for the hypothesis that hydrogenosomes are modified mitochondria. Mol Microbiol 23: 11-21.
18. van der Giezen, M., Kiel, J.A.K.W., Sjollema, K.A., and Prins, R.A. (1998) The hydrogenosomal malic enzyme from the anaerobic fungus Neocallimastix frontalis is targeted to mitochondria of the methylotrophic yeast Hansenula polymorpha. Curr Genet 33: 131-135.
19. Gruer, M.J., Artymiuk, P.J., and Guest, J.R. (1997) The aconitase family: three structural variations on a common theme. Trends Biochem Sci 22: 3-6.
20. Gutteridge, W.E., Dave, D., and Richards, W.H.G. (1979) Conversion of dihydroorotate to orotate in parasitic protozoa. Biochim Biophys Acta 582: 390-401.
21. Hackstein, J.H.P., Rosenberg, J., Broers, C.A.M., Voncken, F.G.J., Matthijs, H.C.P., Stumm, C.K., et al. (1997) Biogenesis of hydrogenosomesin Psalteriomonas lanterna: no evidence for an exogenosomal ancestry. In Eukaryotism and Symbiosis. Intertaxonic Combination versus Symbiotic Adaptation. Schenk, H.E.A., Herrmann, R.G., Jeon, K.W., Müller, N.E., and Schwemmler, W. (eds). Berlin: Springer-Verlag, pp. 63-70.
22. Hackstein, J.H.P., Voncken, F.G.J., Vogels, G.D., Rosenberg, J., and Mackenstedt, U. (1998) Hydrogenosomes and plastid-like organelles in amoebomastigotes, chytrids, and apicomplexan parasites. In Evolutionary Relationships among Protozoa. The Systematics Association, special volume. Coombs, G.H., Vickerman, K., Sleigh, M.A., and Warren, A. (eds). London: Chapman & Hall, pp. 149-168.
23. von Heijne, G., Steppuhn, J., and Herrmann, R.G. (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535-545.
24. Hendrick, J.P., Hodges, P.E., and Rosenberg, L.E. (1989) Survey of amino-terminal proteolytic cleavage sites in mitochondrial precursor proteins: leader peptides cleaved by two matrix proteases share a three-amino acid motif. Proc Natl Acad Sci USA 86: 4056-4060.
25. Joh, T., Takeshima, H., Tsuzuki, T., Setoyama, C., Shimada, K., Tanase, S., et al. (1987) Cloning and sequence analysis of cDNAs encoding mammalian cytosolic malate dehydrogenase. Comparison of the amino acid sequences of mammalian and bacterial malate dehydrogenase. J Biol Chem 262: 15127-15131.
26. Knoll, A.H. (1992) The early evolution of eukaryotes: a geological perspective. Science 256: 622-627.
27. Kremer, D.R., Nienhuis-Kuiper, H.E., Timmer, C.J., and Hansen, T.A. (1989) Catabolism of malate and related dicarboxylic acids in various Desulfovibrio strains and the involvement of an oxygen labile NADPH dehydrogenase. Arch Microbiol 151: 34-39.
28. Krungkrai, J., Cerami, A., and Henderson, G.B. (1991) Purification and characterization of dihydroorotate dehydrogenase from the rodent malarias parasite Plasmodium berghei. Biochemistry 30: 1934-1939.
29. Li, J., and Heath, I.B. (1992) The phylogenetic relationships of the anaerobic chytridiomycetous gut fungi (Neocallimasticaceae) and the chytridiomycota. I. Cladistic analysis of rRNA sequences. Can J Bot 70: 1738-1746.
30. Li, J., Heath, I.B., and Packer, L. (1993) The phylogenetic relationships of the anaerobic chytridiomycetous gut fungi (Neocallimasticaceae) and the chytridiomycota. II. Cladistic analysis of structural data and description of Neocallimasticales ord. nov. Can J Bot 71: 393-407.
31. McAlister-Henn, L., Steffan, J.S., Minard, K.I., and Anderson, S.L. (1995) Expression and function of a mislocalized form of peroxisomal malate dehydrogenase (MDH3) in yeast. J Biol Chem 270: 21220-21225.
32. McAlister-Henn, L., and Small, W.C. (1997) Molecular genetics of yeast TCA cycle isozymes. Prog Nucleic Acid Res Mol Biol 57: 317-339.
33. Magee, P.T., and Hereford, L.M. (1969) Multivalent repression of isoleucine-valine biosynthesis in Saccharomyces cerevisiae. J Bacteriol 98: 857-862.
34. Margulis, L. (1993) Symbiosis in Cell Evolution. Microbial Communities in the Archean and Proterozoic Eons. New York: W.H. Freeman.
35. Martin, W., and Müller, M. (1998) The hydrogen hypothesis for the first eukaryote. Nature 392: 37-41.
36. Marvin-Sikkema, F.D., Pedro Gomes, T.M., Grivet, J.P., Gottschal, J.C., and Prins, R.A. (1993a) Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch Microbiol 160: 388-396.
37. Marvin-Sikkema, F.D., Kraak, M.N., Veenhuis, M., Gottschal, J.C., and Prins, R.A. (1993b) The hydrogenosomal enzyme hydrogenase from the anaerobic fungus Neocallimastix sp. L2 is recognized by antibodies, directed against the C-terminal microbody protein targeting signal SKL. Eur J Cell Biol 61: 86-91.
38. Marvin-Sikkema, F.D., Driessen, A.J., Gottschal, J.C., and Prins, R.A. (1994) Metabolic energy generation in hydrogenosomes of the anaerobic fungus Neocallimastix: evidence for a functional relationship with mitochondria. Mycol Res 98: 205-212.
39. Mountfort, D.O. (1994) Regulatory constraints in the degradation and fermentation of carbohydrate by anaerobic fungi. In Anaerobic Fungi. Biology, Ecology and Function. Mountfort, D.O., and Orpin, C.G. (eds). New York: Marcel Dekker, pp. 147-168.
40. Müller, M. (1993) The hydrogenosome. J Gen Microbiol 139: 2879-2889.
41. Müller, M. (1997) Evolutionary origins of trichomonad hydrogenosomes. Parasitol Today 13: 166-167.
42. Ocheretina, O., and Scheibe, R. (1997) Cloning and sequence analysis of cDNAs encoding plant cytosolic malate dehydrogenase. Gene 199: 145-148.
43. O'Fallon, J.V., Wright, R.W., and Calza, R.E. (1991) Glucose metabolic pathways in the anaerobic fungus Neocallimastix frontalis. Biochem J 274: 595-599.
44. Orpin, C.G. (1994) Anaerobic fungi: taxonomy, biology, and distribution in nature. In Anaerobic Fungi. Biology, ecology, and function. Mountfort, D.O., and Orpin, C.G. (eds). New York, Basel, Hong Kong: Marcel Dekker, pp. 1-45.
45. Paquin, B., and Lang, B.F. (1996) The mitochondrial DNA of Allomyces macrogynus: the complete genomic sequence from an ancestral fungus. J Mol Biol 255: 688-701.
46. Paquin, B., Forget, L., Roewer, I., and Lang, B.F. (1995) Molecular phylogeny of Allomyces macrogynus: congruency between nuclear ribosomal RNA- and mitochondrial protein-based trees. J Mol Evol 41: 657-665.
47. Park, H.S., Xing, R., and Whitman, W.B. (1995) Nonenzymatic acetolactate oxidation to diacetyl by flavin, nicotinamide and quinone coenzymes. Biochim Biophys Acta 1245: 366-370.
48. Petersen, J.G., and Holmberg, S. (1986) The ILV5 gene of Saccharomyces cerevisiae is highly expressed. Nucleic Acids Res 14: 9631-9651.
49. Peyret, P., Perez, P., and Alric, M. (1995) Structure, genomic organization, and expression of the Arabidopsis thaliana aconitase gene. Plant aconitase shows significant homology with mammalian iron-responsive element-binding protein. J Biol Chem 270: 8131-8137.
50. Prapunwattana, P., O'Sullivan, W.J., and Yuthavong, Y. (1988) Depression of Plasmodium falciparum dihydroorotate dehydrogenase activity in in vitro culture by tetracycline. Mol Biochem Parasitol 27: 119-124.
51. Ragan, M.A., and Chapman, D.J. (1978) A Biochemical Phylogeny of the Protists. New York: Academic Press.
52. Reeves, H.C., Rabin, R., Wegener, W.S., and Ajl, S.J. (1971) In Methods in Microbiology. Norris, J.R., and Ribbons, D.W. (eds). New York and London: Academic Press, pp. 425.
53. Reymond, P., Geourjon, C., Roux, B., Durand, R., and Fevre, M. (1992) Sequence of the phosphoenolpyruvate carboxykinase-encoding cDNA from the rumen anaerobic fungus Neocallimastix frontalis: comparison of the amino acid sequence with animals and yeast. Gene 110: 57-63.
54. Ryan, E.D., and Kohlhaw, G.B. (1974) Subcellular localization of isoleucine-valine biosynthetic enzymes in yeast. J Bacteriol 120: 631-637.
55. Small, W.C., and McAlister-Henn, L. (1997) Metabolic effects of altering redundant targeting signals for yeast mitochondrial malate dehydrogenase. Arch Biochem Biophys 344: 53-60.
56. Sogin, M. (1991) Early evolution and the origin of eukaryotes. Curr Opin Genet Dev 1: 457-463.
57. Sogin, M. (1997) Organelle origins: energy-producing symbionts in early eukaryotes? Curr Biol 7: R315-R317.
58. Stams, A.J.M., Kremer, D.R., Nicolay, K., and Hansen, T.A. (1984) Pathway of propionate formation in Desulfobulbus propionicus. Arch Microbiol 139: 167-173.
59. Teunissen, M.J., Smits, A.A., Op den Camp, H.J., Huis in 't Veld, J.H., and Vogels, G.D. (1991) Fermentation of cellulose and production of cellulolytic and xylanolytic enzymes by anaerobic fungi from ruminant and non-ruminant herbivores. Arch Microbiol 156: 290-296.
60. Thompson, L.M., and McAlister-Henn, L. (1989) Dispensable presequence for cellular localization and function of mitochondrial malate dehydrogenase from Saccharomyces cerevisiae. J Biol Chem 264: 12091-12096.
61. Trinci, A.P., Davies, D.R., Gull, K., Lawrence, M.I., Bonde Nielsen, B., Rickers, A., et al. (1994) Anaerobic fungi in herbivorous animals. Mycol Res 98: 129-152.
62. Yarlett, N. (1994) Fermentation product generation in rumen chytridiomycetes. In Anaerobic Fungi. Biology, Ecology and Function. Mountfort, D.O., and Orpin, C.G. (eds). New York: Marcel Dekker, pp. 129-146.
63. Yarlett, N., Orpin, C.G., Munn, E.A., Yarlett, N.C., and Greenwood, C.A. (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236: 729-739.
64. Zhou, Y.H., and Ragan, M.A. (1995) Characterization of the nuclear gene encoding mitochondrial aconitase in the marine red alga Gracilaria verrucosa. Plant Mol Biol 28: 635-646.