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

Molecular Microbiology

Volumn 23, Issue 1, 1997, Pages 11-21

  Van Der Giezen, Mark ^a   Rechinger, K Björn ^b   Svendsen, Ib ^b   Durand, Roger ^c   Hirt, Robert P ^d   Fèvre, Michel ^c   Embley, T Martin ^d   Prins, Rudolf A ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b CARLSBERG LABORATORY   (Denmark)

^c CENTRE DE GÉNÉTIQUE MOLÉCULAIRE ET CELLULAIRE   (France)

^d DEPARTMENT OF LIFE SCIENCES   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

MALATE DEHYDROGENASE (DECARBOXYLATING);

ANAEROBIC METABOLISM; ARTICLE; CELL ORGANELLE; CONTROLLED STUDY; FUNGUS CULTURE; MITOCHONDRION; NONHUMAN; OXIDATION REDUCTION POTENTIAL; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; SIGNAL TRANSDUCTION;

BACTERIA (MICROORGANISMS); EUKARYOTA; FUNGI; METAZOA; NEOCALLIMASTIX FRONTALIS; PROTISTA;

EID: 0031023807     PISSN: 0950382X     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-2958.1997.1891553.x     Document Type: Article

References (85)

1. Adachi, J., and Hasegawa, M. (1992) MOLPHY version 2.2: programs for molecular phylogenetics. Tokyo: Institute of Statistical Mathematics.
2. Bagchi, S., Wise, L.S., Brown, M.L., Bregman, D., Sul, H.S., and Rubin, C.S. (1987) Structure and expression of murine malic enzyme mRNA: differentiation-dependent accumulation of two forms of malic enzyme mRNA in 3T3-L1 cells. J Biol Chem 262: 1558-1565.
3. Billon-Grand, G., Fiol, J.B., Breton, A., Bruyère, A., and Oulhaj, Z. (1991) DNA of some anaerobic fungi: G + C content determination. FEMS Microbiol Lett 82: 267-270.
4. Borsch, D., and Westhoff, P. (1990) Primary structure of NADP-dependent malic enzyme in the dictyledonous C4 plant Flaveria trinervia. FEBS Lett 273: 111-115.
5. Brondijk, T.H.C., Durand, R., van der Giezen, M., Gottschal, J.C., Prins, R.A., and Fèvre, M. (1996) scsB, a cDNA encoding the hydrogenosomal protein β-succinyl-CoA synthetase from the anaerobic fungus Neocallimastix frontalis. Mol Gen Genet, in press.
6. Brownlee, A.G. (1988) A rapid DNA isolation procedure applicable to many refractory filamentous fungi. Fungal Genetics Newsletter 35: 8-9.
7. Brownlee, A.G. (1989) Remarkably AT-rich genomic DNA from the anaerobic fungus Neocallimastix. Nucl Acids Res 17: 1327-1335.
8. Bruns, T.D., Vilgalis, R., Barns, S.M., Gonzalez, D., Hibbett, D.S., Lane, D.J., Simon, L, Stickel, S., Szaro, T.M., Weisburg, W.G., and Sogin, M.L. (1992) Evolutionary relationships within the fungi: analyses of nuclear small subunit rRNA sequences. Mol Phylogenet Evol 1: 231-241.
9. Cao, Y., Adachi, J., Janke, A., Pääbo, S., and Hasegawa, M. (1994) Phylogenetic relationships among eutherian orders estimated from inferred sequences of mitochondrial proteins: instability of a tree based on a single gene. J Mol Evol 39: 519-527.
10. Cavalier-Smith, T. (1987) The simultaneous symbiotic origin of mitochondria, chloroplasts, and microbodies. Ann N Y Acad Sci 503: 55-71.
11. Cavalier-Smith, T. (1993) Kingdom Protozoa and its 18 phyla. Microbiol Rev 57: 953-994.
12. +-dependent malic enzyme cDNA and some of its abortive mutants. Arch Biochem Biophys 310: 158-166.
13. Corliss, J.C. (1994) An interim utilitarian ('user-frendly') hierarchial classification and characterisation of the protists. Acta Protozoologica 33: 1-51.
14. Cushman, J.C. (1992) Characterization and expression of a NADP-malic enzyme cDNA induced by salt stress from the facultative crassulacean acid metabolism plant, Mesembryanthemum crystallinum. Eur J Biochem 208: 259-266.
15. Danpure, C.J. (1995) How can the products of a single gene be localized to more than one intracellular compartment? Trends Cell Biol 5: 230-238.
16. Denayrolles, M., Aigle, M., and Lonvaud-Funel, A. (1994) Cloning and sequence analysis of the gene encoding Lactococcus lactis malolactic enzyme: relationships with malic enzymes. FEMS Microbiol Lett 116: 79-86.
17. van Doorselaere, J., Villaroel, R., van Montagu, M., and Inzé, D. (1991) Nucleotide sequence of a cDNA encoding enzyme from poplar. Plant Physiol 96: 1385-1386.
18. 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.
19. Durand, R., Reymond-Cotton, P., Fischer, M., Rascle, C., and Fèvre, M. (1994) Cloning and expression of genes encoding enzymes of the glycolytic pathway in Neocallimastix frontalis. In Microorganisms in Ruminant Nutrition. Prins, R.A., and Stewart, C.S. (eds). Nottingham, UK: Nottingham University Press, pp. 137-151.
20. Durand, R., Fischer, M., Rascle, C., and Fèvre, M. (1995) Neocallimastix frontalis enolase gene, enol: first report of an intron in an anaerobic fungus. Microbiology 141: 1301-1308.
21. de Duve, C. (1983) Microbodies in the living cell. Scientific American 248: 52-62.
22. Elgersma, Y., van Roermond, C.W.T., Wanders, R.J.A., and Tabak, H.F. (1995) Peroxisomal and mitochondrial carnitine acetyltransferase of Saccharomyces cerevisiae are encoded by a single gene. EMBO J 14: 3472-3479.
23. Embley, T.M., Finlay, B.J., Dyal, P.L., Hirt, R.P., Wilkinson, M., and Williams, A.G. (1995) Multiple origins of anaerobic ciliates with hydrogenosomes within radiation of aerobic ciliates. Proc R Soc Lond B Biol Sci 262: 87-93.
24. Felsenstein, J. (1993) PHYLIP (Phylogeny Inference Package). Department of Genetics, University of Washington, Seattle, USA. Distributed by the author.
25. Fenchel, T., and Finlay, B.J. (1995) Ecology and Evolution In Anoxic Worlds. New York: Oxford University Press.
26. Fernandez, J., DeMott, M., Atherton, D., and Mische, S.M. (1992) Internal protein sequence analysis: enzymatic digestion from less than 10 μg of protein bound to polyvinylidene difluoride or nitrocellulose membranes. Anal Biochem 201: 255-265.
27. Finlay, B.J., and Fenchel, T. (1989) Hydrogenosomes in some anaerobic protozoa resemble mitochondria. FEMS Microbiol Lett 65: 311-314.
28. Franke, K.E., and Adams, D.O. (1995) Cloning of a full-length cDNA for malic enzyme (EC 1.1.1.40) from grape berries. Plant Physiol 107: 1009-1010.
29. Fushimi, T., Umeda, M., Shimazaki, T., Kato, A., Toriyama, K., and Uchimiya, H. (1994) Nucleotide sequence of a rice cDNA similar to a maize NADP-dependent malic enzyme. Plant Mol Biol 24: 965-967.
30. van der Giezen, M., Gottschal, J.C., and Prins, R.A. (1994) The evolutionary origin of hydrogenosomes from anaerobic fungi. In Microorganisms in Ruminant Nutrition. Prins, R.A., and Stewart, C.S. (eds). Nottingham, UK: Nottingham University Press, pp. 195-208.
31. González-Manchón, C., Ferrer, M., Ayuso, M.S., and Parrilla, R. (1995) Cloning, sequencing and functional expression of a cDNA encoding a NADP-dependent malic enzyme from human liver. Gene 159: 255-260.
32. Gould, S.J., Keller, G.-A., Hosken, N., Wilkinson, J., and Subramani, S. (1989) A conserved tripeptide sorts proteins to peroxisomes. J Cell Biol 108: 1657-1664.
33. Gurr, S.J., Unkles, S.E., and Kinghorn, J.R. (1987) The structure and organization of nuclear genes of filamentous fungi. In Gene Structure in Eukaryotic Microbes. Kinghorn, J.R. (ed.). Oxford: IRL Press, pp. 93-139.
34. von Heijne, G., Steppuhn, J., and Herrmann, R.G. (1989) Domain structure of mitochondrial and chloroplast targeting peptides. Eur J Biochem 180: 535-545.
35. Hoop, M.J.D., and AB, G. (1992) Import of proteins into peroxisomes and other microbodies. Biochem J 286: 657-669.
36. Horner, D.S., Hirt, R.P., Kilvington, S., Lloyd, D., and Embley, T.M. (1996) Molecular data suggest an early acquisition of the mitochondrion endosymbiont. Proc R Soc Lond B Biol Sci 263: 1053-1059.
37. Hrdý, I., and Müller, M. (1995a) Primary structure and eubacterial relationships of the pyruvate:ferredoxin oxidoreductase of the amitochondriate eukaryote Trichomonas vaginalis. J Mol Evol 41: 388-396.
38. Hrdý, I., and Müller, M. (1995b) Primary structure of the hydrogenosomal malic enzyme of Trichomonas vaginalis and its relationship to homologous enzymes. J Euk Microbiol 42: 593-603.
39. Hsu, R.Y., Glynias, M.J., Satterlee, J., Feeney, R., Clarke, A.R., Emery, D.C., Roe, B.A., Wilson, R.K., Goodridge, A.G., and Holbrooke, J J. (1992) Duck liver 'malic' enzyme: expression in Escherichia coli and characterization of the wild-type enzyme and site-directed mutants. Biochem J 284: 869-876.
40. Johnson, P.J., D'Oliveira, C.E., Gorrell, T.E., and Müller, M. (1990) Molecular analysis of the hydrogenosomal ferredoxin of the anaerobic protist Trichomonas vaginalis. Proc Natl Acad Sci USA 87: 6097-6101.
41. Johnson, P.J., Lahti, C.J., and Bradley, P.J. (1993) Biogenesis of the hydrogenosome in the anaerobic protist Trichomonas vaginalis. J Parasitol 79: 664-670.
42. Johnston, M. (1996) Genome sequencing: the complete code for a eukaryotic cell. Curr Biol 6: 500-503.
43. Kishino, H., and Hasegawa, M. (1989) Evaluation of the maximum likelihood estimate of evolutionary tree topologies from DNA sequence data, and the branching order in huminoidea. J Mol Evol 29: 170-179.
44. Kochan, Z., Karbowska, J., Bukato, G., Zydowo, M.M., Bertoli, E., Tanfani, F., and Swierczynski, J. (1995) A comparison of the secondary structure of human brain mitochondrial and cytosolic 'malic' enzyme investigated by Fourier-transform infrared spectroscopy. Biochem J 309: 607-611.
45. 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.
46. Kulkarni, L.P., Cook, P.F., and Harris, B.G. (1993) Cloning and nucleotide sequence of a full-length cDNA encoding Ascaris suum malic enzyme. Arch Biochem Biophys 300: 231-237.
47. Kyhse-Anderson, J. (1984) Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Meth 10: 203-209.
48. Laemmli, U.K. (1987) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227: 680-685.
49. Lahti, C.J., D'Oliveira, C.E., and Johnson, P.J. (1992) β-Succinyl-coenzyme A synthetase from Trichomonas vaginalis is a soluble hydrogenosomal protein with an amino-terminal sequence that resembles mitochondrial pre-sequences. J Bacteriol 174: 6822-6830.
50. Lahti, C.J., Bradley, P.J., and Johnson, P.J. (1994) Molecular characterization of the α-subunit of Trichomonas vaginalis hydrogenosomal succinyl CoA synthetase. Mol Biochem Parasitol 66: 309-318.
51. Länge, S., Rozario, C., and Müller, M. (1994) Primary structure of the hydrogenosomal adenylate kinase of Trichomonas vaginalis and its phylogenetic relationships. Mol Biochem Parasitol 66: 297-308.
52. Leipe, D.D., Gunderson, J.H., Nerad, T.A., and Sogin, M.L. (1993) Small subunit ribosomal RNA of Hexamita inflata and the quest for the first branch in the eukaryotic tree. Mol Biochem Parasitol 59: 41-48.
53. Lipka, B., Steinmuller, K., Rosche, E., Borsch, D., and Westhoff, P. (1994) The C3 plant Flaveria pringlei contains a plastidic NADP-malic enzyme which is orthologous to the C4 isoform of the C4 plant Flaveria trinervia. Plant Mol Biol 26: 1775-1783.
54. +-dependent mitochondrial malic enzyme: cDNA cloning, primary structure, and expression in Escherichia coli. J Biol Chem 266: 3016-3021.
55. Long, J.J., Wang, J., and Berry, J.O. (1994) Cloning and analysis of the C4 photosynthetic NAD-dependent malic enzyme of Amaranth mitochondria. J Biol Chem 269: 2827-2833.
56. Magnuson, M.A., Morioka, H., Tecce, M.F., and Nikodem, V.M. (1986) Coding nucleotide sequence of rat liver malic enzyme mRNA. J Biol Chem 261: 1183-1186.
57. Mahajan, S.K., Chu, C.C., Willis, D.K., Templin, A., and Clark, A.J. (1990) Physical analysis of spontaneous and mutagen-induced mutants of Escherichia coli K-12 expressing DNA exonuclease VIII activity. Genetics 125: 261-273.
58. Maidak, B.L., Olsen, G.J., Larsen, N., Overbeek, R., McCaughey, M.J., and Woese, C.R. (1996) The ribosomal database project (RDP). Nucl Acids Res 24: 82-85.
59. Marvin-Sikkema, F.D., Richardson, A.J., Stewart, C.S., Gottschal, J.C., and Prins, R.A. (1990) Influence of hydrogen-consuming bacteria on cellulose degradation by anaerobic fungi. Appl Environ Microbiol 56: 3793-3797.
60. Marvin-Sikkema, F.D., Kraak, M.N., Veenhuis, M., Gottschal, J.C., and Prins, R.A. (1993a) 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.
61. Marvin-Sikkema, F.D., Pedro Gomes, T.M., Grivet, J., Gottschal, J.C., and Prins, R.A. (1993b) Characterization of hydrogenosomes and their role in glucose metabolism of Neocallimastix sp. L2. Arch Microbiol 160: 388-396.
62. Morioka, H., Magnuson, M.A., Mitsuhashi, T., Song, M.K., Rail, J.E., and Nikodem, V.M. (1989) Structural characterization of the rat malic enzyme gene. Proc Natl Acad Sci USA 86: 4912-4916.
63. 4 plants. Plant Cell Physiol 30: 429-437.
64. Müller, M. (1980) The hydrogenosome. In The Eukaryotic Microbial Cell. 30th Symposium of the Society for General Microbiology, University of Cambridge. Gooday, G.W., Lloyd, D., and Trinci, A.P.J. (eds). London: Cambridge University Press, pp. 127-142.
65. Müller, M. (1988) Energy metabolism of protozoa without mitochondria. Ann Rev Microbiol 42: 465-488.
66. Müller, M. (1993) The hydrogenosome. J Gen Microbiol 139: 2879-2889.
67. Ochoa, S., Mehler, A.H., and Kornberg, A. (1948) Biosynthesis of dicarboxylic acids by carbon dioxide fixation. I. Isolation and properties of an enzyme from pigeon liver catalyzing the reversible oxidative decarboxylation of L-malic acid. J Biol Chem 174: 979-1000.
68. + oxidoreductase (decarboxylating), EC 1.1.1.39. Meth Enzymol 3: 176-183.
69. Reymond, P., Durand, R., Hebraud, M., and Fèvre, M. (1991) Molecular cloning of genes from the rumen anaerobic fungus Neocallimastix frontalis: expression during hydrolase induction. FEMS Microbiol Lett 77: 107-112.
70. Reymond, P., Geourjon, C., Roux, B., Durand, R., and Fèvre, M. (1992) Sequence of the phosphoenolpyruvate carboxy-kinase-encoding cDNA from the rumen anaerobic fungus Neocallimastix frontalis: comparison of the amino acid sequence with animals and yeast. Gene 110: 57-63.
71. Rothermel, B.A., and Nelson, T. (1989) Primary structure of the maize NADP-dependent malic enzyme. J Biol Chem 264: 19587-19592.
72. Sambrook, J., Fritsch, E., and Maniatis, T. (1987) Molecular Cloning: A Laboratory Manual. Vol. 2. Cold Spring Harbor, New York: Cold Spring Harbor Laboratory Press.
73. Scrutton, N.S., Berry, A., and Perham, R.N. (1990) Redesign of the coenzyme specificity of a dehydrogenase by protein engineering. Nature 343: 38-43.
74. Swofford, D.L. (1993) PAUP version 3.1.1: phylogenetic analysis using parsimony. Champagne, Illinois: Illinois Natural History Survey.
75. Tamblyn Lee, J.M., Hu, Y., Zhu, H., Cheng, K.J., Krell, P.J., and Forsberg, C.W. (1993) Cloning of a xylanase gene from the ruminai fungus Neocallimastix patriciarum 27 and its expression in Escherichia coli. Can J Microbiol 39:134-139.
76. Thompson, J.D., Higgins, D.G., and Gibson, T.J. (1994) CLUSTAL W: improving the sensitivity of progressive multiple alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl Acids Res 22: 4673-4680.
77. Veenhuis, M., Van der Klei, I.J., Titorenko, V., and Harder, W. (1992) Hansenula polymorpha: an attractive model organism for molecular studies of peroxisome biogenesis and function. FEMS Microbiol Lett 100: 393-404.
78. Viljoen, M., Subden, R.E., Krizus, A., and Van Vuuren, H.J.J. (1994) Molecular analysis of the malic enzyme gene (mae2) of Schizosaccharomyces pombe. Yeast 10: 613-624.
79. Walter, M.H., Grima-Pettenati, J., Grand, C., Boudet, A.M., and Lamb, C.J. (1990) Extensive sequence similarity of the bean CAD4 (cinnamyl-alcohol dehydrogenase) to a maize malic enzyme. Plant Mol Biol 15: 525-526.
80. Wieringa, R.K., De Maeyer, M.C.H., and Hol, W.G.J. (1985) Interaction of pyrophosphate moieties with a-helixes in dinucleotide binding proteins. Biochemistry 24: 1346-1357.
81. Wilson, C.M. (1983) Staining of proteins on gels: comparisons of dyes and procedures. Meth Enzymol 91: 236-247.
82. +-dependent malic enzyme. J Biol Chem 269: 4780-4786.
83. Yarlett, N., Orpin, G.G., Munn, E.A., Yarlett, N., and Greenwood, C. (1986) Hydrogenosomes in the rumen fungus Neocallimastix patriciarum. Biochem J 236: 729-739.
84. Young, R.A., and Davis, R.W. (1983) Efficient isolation of genes by using antibody probes. Proc Natl Acad Sci USA 80: 1194.
85. Zhou, L., Xue, G., Orpin, C.G., Black, G.W., Gilbert, H.J., and Hazlewood, G.P. (1994) Intronless celB from the anaerobic fungus Neocallimastix patriciarum encodes a modular family A endoglucanase. Biochem J 297: 359-364.