Molecular analysis of a novel methanesulfonic acid monooxygenase from the methylotroph Methylosulfonomonas methylovora

Journal of Bacteriology

Volumn 181, Issue 7, 1999, Pages 2244-2251

  De Marco, Paolo ^a   Moradas Ferreira, Pedro ^a   Higgins, Timothy P ^b,c   Mcdonald, Ian ^b   Kenna, Elizabeth M ^b   Murrell, J Colin ^b  

^a UNIVERSITY OF PORTO   (Portugal)

^b UNIVERSITY OF WARWICK   (United Kingdom)

^c UNIVERSITY OF READING   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FERREDOXIN; MESYLIC ACID; OXYGENASE; STEROID 5ALPHA REDUCTASE; UNSPECIFIC MONOOXYGENASE;

ARTICLE; BINDING AFFINITY; ENZYME ACTIVITY; ENZYME ANALYSIS; GENE EXPRESSION; GENE SEQUENCE; GRAM NEGATIVE BACTERIUM; NUCLEOTIDE SEQUENCE; OXIDATION; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL;

BACTERIA (MICROORGANISMS); MARINOSULFONOMONAS METHYLOTROPHA; METHYLOSULFONOMONAS; METHYLOSULFONOMONAS METHYLOVORA; NEGIBACTERIA; PROKARYOTA;

EID: 0032936735     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/jb.181.7.2244-2251.1999     Document Type: Article

References (66)

1. Altshul, S. F., T. L. Madden, A. A. Schäffer, 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. Andreae, M. O. 1986. The ocean as a source of atmospheric sulfur compounds, p. 331-362. In P. Buat-Menard (ed.), The role of air-sea exchange in geochemical cycling. Reidel, New York, N.Y.
3. Asturias, J. A., E. Diaz, and K. N. Timmis. 1995. The evolutionary relationship of biphenyl dioxygenase from Gram-positive Rhodococcus globerulus P6 to multicomponent dioxygenases from Gram-negative bacteria. Gene 156: 11-18.
4. Bairoch, A., and R. Apweiler. 1998. The SWISS-PROT protein sequence data bank and its supplement TrEMBL in 1998. Nucleic Acids Res. 26: 38-42.
5. Baker, S. C., D. P. Kelly, and J. C. Murrell. 1991 Microbial degradation of methanesulphonic acid: a missing link in the biogeochemical sulphur cycle. Nature 350:627-628.
6. Blattner, F. R., G. Plunkett III, C. A. Bloch, N. T. Perna, V. Burland, M. Riley, J. Collado-Vides, J. D. Glasner, C. K. Rode, G. F. Mayhew, J. Gregor, N. W. Davis, H. A. Kirkpatrick, M. A. Goeden, D. J. Rose, B. Mau, and Y. Shao. 1997. The complete genome sequence of Escherichia coli K-12. Science 277:1453-1474.
7. Bruce, K. D., A. M. Osborn, A. J. Pearson, P. Strike, and D. A. Ritchie. 1995. Genetic diversity within mer genes directly amplified from communities of noncultivated soil and sediment bacteria. Mol. Ecol. 4:605-612.
8. Brunel, P., and J. Davison. 1988. Cloning and sequencing of Pseudomonas genes encoding vanillate demethylase. J. Bacteriol. 170:4924-4930.
9. Byrne, A. M., J. J. Kukor, and R. H. Olsen. 1995. Sequence analysis of the gene cluster encoding toluene-3-monooxygenase from Pseudomonas pickettii PK01. Gene 154:65-70.
10. Cardy, D. L. N., V. Laidler, G. P. C. Salmond, and J. C. Murrell. 1991. Molecular analysis of the methane monooxygenase (MMO) gene cluster of Methylosinus trichosporium OB3b. Mol. Microbiol. 5:335-342.
11. Danganan, C. E., R. W. Ye, D. L. Daubaras, L. Xun, and A. M. Chakrabarty. 1994. Nucleotide sequence and functional analysis of the genes encoding 2,4,5-trichlorophenoxyacetic acid oxygenase in Pseudomonas cepacia AC1100. Appl. Environ. Microbiol. 60:4100-4106.
12. Davey, M. 1996. Ph.D. thesis. University of Warwick, Coventry, United Kingdom.
13. De Marco, P. 1996. Ph.D. thesis. University of Warwick. Coventry, United Kingdom.
14. De Marco, P., A. A. Bordalo e Sá, P. Moradas-Ferreira, and J. C. Murrell. Unpublished data.
15. Eaton, R. W. 1996. p-Cumate catabolic pathway in Pseudomonas putida F1: cloning and characterization of DNA carrying the cmt operon. J. Bacteriol. 178:1351-1362.
16. Eaton, R. W., and K. N. Timmis. 1986. Characterization of a plasmid-specified pathway for catabolism of isopropylbenzene in Pseudomonas putida RE204. J. Bacteriol. 168:123-131.
17. Erb, R. W., and I. Wagner-Döbler. 1993. Detection of polychlorinated byphenyl degradation genes in polluted sediments by direct DNA extraction and polymerase chain reaction. Appl. Environ. Microbiol. 59:4065-4073.
18. Felsenstein, J. 1995. Phylogeny inference package, version 3.57c. University of Washington, Seattle.
19. Haak, B., S. Fetzner, and F. Lingens. 1995. Cloning, nucleotide sequence, and expression of the plasmid-encoded genes for the two-component 2-halobenzoate 1,2-dioxygenase from Pseudomonas cepacia 2CBS. J. Bacteriol. 177:667-675.
20. Harayama, S., M. Kok, and E. L. Neidle. 1992. Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 46:565-601.
21. Harayama, S., M. Rekik, A. Bairoch, E. L. Neidle, and L. N. Ornston. 1991. Potential DNA slippage structures acquired during evolutionary divergence of Acinetobacter calcoaceticus chromosomal benABC and Pseudomonas putida TOL pWW0 plasmid xylXYZ, genes encoding benzoate dioxygenases. J. Bacteriol. 173:7540-7548.
22. Higgins, T. P., P. De Marco, and J. C. Murrell. 1997. Purification and molecular characterization of the electron transfer protein of methanesulfonic acid monooxygenase. J. Bacteriol. 179:1974-1979.
23. Higgins, T. P., M. Davey, J. Trickett, D. P. Kelly, and J. C. Murrell. 1996. Metabolism of methanesulfonic acid involves a multicomponent monooxygenase system. Microbiology 124:251-260.
24. Holmes, A. J., D. P. Kelly, S. C. Baker, A. S. Thompson, P. De Marco, E. M. Kenna, and J. C. Murrell. 1997. Methylosulfonomonas methylovora gen. nov., sp. nov., and Marinosulfonomonas methylotropha gen. nov., sp. nov.: novel methylotrophs able to grow on methanesulfonic acid. Arch. Microbiol. 167: 46-53.
25. Horinouchi, M., K. Kasuga, H. Nojiri, H. Yamane, and T. Omori. 1997. Cloning and characterization of genes encoding an enzyme which oxidizes dimethyl sulfide in Acinetobacter sp. strain 20B. FEMS Microbiol. Lett. 155: 99-105.
26. Irie, S., S. Doi, T. Yorifuji, M. Takagi, and K. Yano. 1987. Nucleotide sequencing and characterization of the genes encoding benzene oxidation enzymes of Pseudomonas putida. J. Bacteriol. 169:5174-5179.
27. Junker, F., R. Kiewitz, and A. M. Cook. 1997. Characterization of the p-toluenesulfonate operon tsaMBCD and tsaR in Comamonas testosteroni T-2. J. Bacteriol. 179:919-927.
28. Kelly, D. P., and S. C. Baker. 1990. The organosulphur cycle: aerobic and anaerobic processes leading to turnover of organic C1-sulphur compounds. FEMS Microbiol. Rev. 87:241-246.
29. Kelly, D. P., S. C. Baker, J. Trickett, M. Davey, and J. C. Murrell. 1994. Methanesulphonate utilization by a novel methylotrophic bacterium involves an unusual monooxygenase. Microbiology 140:1419-1426.
30. Kelly, D. P., and N. A. Smith. 1990. Organic sulfur compounds in the environment. Biogeochemistry, microbiology and ecological aspects. Adv. Microb. Ecol. 11:345-385.
31. Kesseler, M., E. R. Dabbs, B. Averhoff, and G. Gottschalk. 1996 Studies on the isopropylbenzene 2,3-dioxygenase and the 3-iso-propylcatechol 2,3-dioxygenase genes encoded by the linear plasmid of Rhodococcus erythropolis BD2. Microbiology 142:3241-3251.
32. Kurkela, S., H. Lehvaslaiho, E. T. Palva, and T. H. Teeri. 1988 Cloning, nucleotide sequence and characterization of genes encoding naphthalene dioxygenase of Pseudomonas putida strain NCIB9816. Gene 73:355-362.
33. Masai, E., A. Yamada, J. M. Healy, T. Hatta, K. Kimbara, M. Fukuda, and K. Yano. 1995. Characterization of biphenyl catabolic genes of gram-positive polychlorinated biphenyl degrader Rhodococcus sp. strain RHA1. Appl. Environ. Microbiol. 61:2079-2085.
34. Mason, J. R., and R. Cammack. 1992. The electron transport proteins of hydroxylating bacterial dioxygenases. Annu. Rev. Microbiol. 46:277-305.
35. Matsudaira, P. 1987. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J. Biol. Chem. 21:10035-10038.
36. McDonald, I. R., E. M. Kenna, and J. C. Murrell. 1995. Detection of methanotrophic bacteria in environmental samples with the PCR. Appl. Environ. Microbiol. 61:116-121.
37. Mihalopoulos, N., B. C. Nguyen, C. Boissard, J. M. Campin, J. P. Putaud, S. Belviso, I. Barnes, and K. H. Becker. 1992. Field studies of dimethylsulfide oxidation in the boundary layer: variations of dimethylsulfide, methanesulfonic acid, sulfur dioxide, non-sea-salt sulfate and Aitken nuclei at a coastal site. J. Atm. Chem. 14:459-477.
38. Murrell, J. C., V. McGowan, and D. L. N. Cardy. 1993. Detection of methylotrophic bacteria in natural samples by molecular probing techniques. Chemosphere 26:1-11.
39. Murrell, J. C. 1992. Genetics and molecular biology of methanotrophs. FEMS Microbiol. Rev. 88:233-248.
40. National Center for Biotechnology Information Website. September 1998, copyright date. [Online.] http://www.ncbi.nlm.nih.gov. [1 October 1998, last date accessed.]
41. Neidle, E. L., C. Hartnett, L. N. Ornston, A. Bairoch, M. Rekik, and S. Harayama, 1991. Nucleotide sequences of the Acinetobacter calcoaceticus benABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases. J. Bacteriol. 173:5385-5395.
42. Nomura, Y., M. Nakagawa, N. Ogawa, S. Harashima, and Y. Oshima. 1992. Genes in PHT plasmid encoding the initial degradation pathway of phthalate in Pseudomonas putida. J. Ferment. Bioeng. 74:333-344.
43. Nordlund, I., J. Powlowski, and V. Shingler. 1990. Complete nucleotide sequence and polypeptide analysis of multicomponent phenol hydroxylase from Pseudomonas sp. strain CF600. J. Bacteriol. 172:6826-6833.
44. Oakley, C. J., and J. C. Murrell. 1988. nifH genes in the obligate methane oxidising bacteria. FEMS Microbiol. Lett. 49:53-57.
45. Omori, T. Unpublished data.
46. Parales, R. E., M. D. Emig, N. A. Lynch, and D. T. Gibson. 1998. Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems. J. Bacteriol. 180:2337-2344.
47. Reichenbecher, W., and J. C. Murrell. Unpublished data.
48. Saeki, H., and K. Furuhashi. 1994. Cloning and characterization of a Nocardia corallina B-276 gene cluster encoding alkene monooxygenase. J. Ferment. Bioeng. 78:339-406.
49. Saigne, C., and M. Legrand. 1987. Measurements of methanesuphonic acid in Antarctic ice. Nature 330:240-242.
50. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press. Cold Spring Harbor, N. Y.
51. Sato, S. I., N. Ouchiyama, T. Kimura, H. Nojiri, H. Yamane, and T. Omori. 1997. Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequences of genes and characterization of metacleavage enzymes and hydrolase. J. Bacteriol. 179:4841-4849.
52. Saunders, S. E., and J. F. Burke. 1990. Rapid isolation of miniprep DNA for double strand sequencing. Nucleic Acids Res. 18:4948.
53. Scanlan, J., N. Baxter, and J. C. Murrell. Unpublished data.
54. Shine, J., and L. Dalgarno. 1975. Determination of cistron specificity in bacterial ribosomes. Nature 254:34-38.
55. Simon, M. J., T. D. Osslund, R. Saunders, B. D. Ensley, S. Suggs, A. Harcourt, W. C. Suen, D. L. Cruden, D. T. Gibson, and G. J. Zylstra. 1993. Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene 127:31-37.
56. Stainthorpe, A. C., V. Lees, G. P. C. Salmond, H. Dalton, and J. C. Murrell. 1990. The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 91:27-34.
57. Swiss Institute of Bioinformatics, ExPaSy Molecular Biology Server. September 1998, posting date. [Online.] http://expasy.hcuge.ch. [1 October 1998, last date accessed.]
58. Taira, K., J. Hirose, S. Hayashida, and K. Furukawa. 1992. Analysis of bph operon from the polychlorinated biphenyl-degrading strain of Pseudomonas pseudoalcaligenes KF707. J. Biol. Chem. 267:4844-4853.
59. Tan, H. M., H. Y. Tang, C. L. Joannou, N. H. Abdel-Wahab, and J. R. Mason. 1993. The Pseudomonas putida ML2 plasmid-encoded genes for benzene dioxygenase are unusual in codon usage and low in G+C content. Gene 130: 33-39.
60. Thompson, A. S., N. J. P. Owens, and J. C. Murrell. 1995. Isolation and characterization of methanesulfonic acid-degrading bacteria from the marine environment. Appl. Environ. Microbiol. 61:2388-2393.
61. Wackett, L. P., L. D. Kwart, and D. T. Gibson. 1988. Benzylic monooxygenation catalysed by toluene dioxygenase from Pseudomonas putida. Biochemistry 27:1360-1367.
62. Wende, P., F.-H. Bernhardt, and K. Pfleger. 1989. Substrate-modulated reactions of putidamonooxin. The nature of the active oxygen species formed and its reaction mechanism. Eur. J. Biochem. 181:189-197.
63. Whung, P.-Y., E. S. Saltzman, M. J. Spencer, P. A. Mayewski, and N. Gundestrup. 1994. Two-hundred-year record of biogenic sulfur in a south Greenland ice core (20D). J. Geophys. Res. 99:1147-1156.
64. Yen, K. M., and M. R. Karl. 1992. Identification of a new gene, tmoF, in the Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase. J. Bacteriol. 174:7253-7261.
65. Zehr, J. P., M. Mellon, S. Braun, W. Litaker, T. Steppe, and H. W. Paerl, 1995. Diversity of heterotrophic nitrogen fixation genes in a marine cyanobacterial mat. Appl. Environ. Microbiol. 61:2527-2532.
66. Zylstra, G. J., and D. T. Gibson. 1989. Toluene degradation by Pseudomonas putida F1. J. Biol. Chem. 264:14940-14946.