Sequencing and analysis of the Methylococcus capsulatus (Bath) soluble methane monooxygenase genes

European Journal of Biochemistry

Volumn 267, Issue 8, 2000, Pages 2174-2185

  Coufal, David E ^a   Blazyk, Jessica L ^a   Whittington, Douglas A ^a   Wu, Wayne W ^a   Rosenzweig, Amy C ^a   Lippard, Stephen J ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

Author keywords

Diiron; DNA sequence; Hydroxylase; Methane oxidation; Sequence alignment

Indexed keywords

BACTERIAL DNA; DNA; METHANE; METHANE MONOOXYGENASE; OXYGENASE; IRON; METALLOPROTEIN; MULTIENZYME COMPLEX; RECOMBINANT PROTEIN;

AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; DNA SEQUENCE; ENZYME ACTIVE SITE; ENZYME ANALYSIS; ENZYME STRUCTURE; FAST PROTEIN LIQUID CHROMATOGRAPHY; METHANOTROPHIC BACTERIUM; NONHUMAN; OXIDATION; PRIORITY JOURNAL; PROTEIN EXPRESSION; AMINO ACID SEQUENCE; BACTERIAL GENE; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; ELECTRON TRANSPORT; ENZYMOLOGY; GENETICS; HYDROGEN BOND; METHYLOCOCCUS CAPSULATUS; MOLECULAR CLONING; MOLECULAR GENETICS; NUCLEOTIDE SEQUENCE; PROTEIN SECONDARY STRUCTURE; SEQUENCE ALIGNMENT;

METHYLOCOCCUS CAPSULATUS;

AMINO ACID SEQUENCE; BINDING SITES; CLONING, MOLECULAR; CONSERVED SEQUENCE; ELECTRON TRANSPORT; GENES, BACTERIAL; HYDROGEN BONDING; IRON; METALLOPROTEINS; METHYLOCOCCUS CAPSULATUS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; MULTIENZYME COMPLEXES; OXYGENASES; PROTEIN STRUCTURE, SECONDARY; RECOMBINANT PROTEINS; SEQUENCE ALIGNMENT;

EID: 0033624799     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1432-1327.2000.01210.x     Document Type: Article

References (74)

1. 1. Lippard, S.J. & Berg, J.M. (1994). Principles of Bioinorganic Chemistry. University Science Books, Mill Valley, CA, USA.
2. 2. Feig, A.L. & Lippard, S.J. (1994) Reactions of non-heme iron(II) centers with dioxygen in biology and chemistry. Chem. Rev. 94, 759-805.
3. 3. Wallar, B.J. & Lipscomb, J.D. (1996) Dioxygen activation by enzymes containing binuclear non-heme iron clusters. Chem. Rev. 96, 2625-2657.
4. 4. Kurtz, D.M. Jr (1990) Oxo- and hydroxo-bridged diiron complexes: a chemical perspective on a biological unit. Chem. Rev. 90, 585-606.
5. 5. Vincent, J.B., Olivier-Lilley, G.L. & Averill, B.A. (1990) Proteins containing oxo-bridged dinuclear iron centers: a bioinorganic perspective. Chem. Rev. 90, 1447-1467.
6. 6. Valentine, A.M. & Lippard, S.J. (1997) Principles of small molecule activation by metalloenzymes as exemplified by the soluble methane monooxygenase from Methylococcus capsulatus (Bath). Dalton Trans. 21, 3925-3931.
7. 7. Liu, K.E. & Lippard, S.J. (1995) Studies of the soluble methane monooxygenase protein system: structure, component interactions, and hydroxylation mechanism. In Advanced Inorganic Chemistry (Sykes, A.G., ed.), Vol. 42, pp. 263-289. Academic Press, San Diego, CA, USA.
8. 8. Lipscomb, J.D. (1994) Biochemistry of the soluble methane monooxygenase. Annu. Rev. Microbiol. 48, 371-399.
9. 9. Colby, J. & Dalton, H. (1978) Resolution of the methane monooxygenase of Methylococcus capsulatus (Bath) into three components. Biochem. J. 171, 461-468.
10. 10. Woodland, M.P. & Dalton, H. (1984) Purification and characterization of component A of the methane monooxygenase from Methylococcus capsulatus (Bath). J. Biol. Chem. 259, 53-59.
11. 2 redox centres of component C, the NADH: acceptor reductase of the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur. J. Biochem. 147, 291-296.
12. 12. Lund, J., Woodland, M.P. & Dalton, H. (1985) Electron transfer reactions in the soluble methane monooxygenase of Methylococcus capsulatus (Bath). Eur. J. Biochem. 147, 297-305.
13. 13. Stainthorpe, A.C., Murrell, J.C., Salmond, G.P.C., Dalton, H. & Lees, V. (1989) Molecular analysis of methane monooxygenase from Methylococcus capsulatus (Bath). Arch. Microbiol. 152, 154-159.
14. 14. Stainthorpe, A.C., Lees, V., Salmond, G.P.C., Dalton, H. & Murrell, J.C. (1990) The methane monooxygenase gene cluster of Methylococcus capsulatus (Bath). Gene 91, 27-34.
15. 15. Cardy, D.L.N., Laidler, V., Salmond, G.P.C. & Murrell, J.C. (1991) Molecular analysis of the methane monooxygenase (MMO) gene cluster of Methylosinus trichosporium OB3b. Mol. Microbiol. 5, 335-342.
16. 16. Cardy, D.L.N., Laidler, V., Salmond, G.P.C. & Murrell, J.C. (1991) The methane monooxygenase gene cluster of Methylosinus trichosporium: cloning and sequencing of the mmoC gene. Arch. Microbiol. 156, 477-483.
17. 17. McDonald, I.R., Uchiyama, H., Kambe, S., Yagi, O. & Murrell, J.C. (1997) The soluble methane monooxygenase gene cluster of the trichloroethylene-degrading methanotroph Methylocystis sp. strain M. Appl. Environ. Microbiol. 63, 1898-1904.
18. 18. Rosenzweig, A.C., Frederick, C.A., Lippard, S.J. & Nordlund, P. (1993) Crystal structure of a bacterial non-haem iron hydroxylase that catalyses the biological oxidation of methane. Nature (London) 366, 537-543.
19. 19. Buzy, A., Millar, A.L., Legros, V., Wilkins, P.C., Dalton, H. & Jennings, K.R. (1998) The hydroxylase component of soluble methane monooxygenase from Methylococcus capsulatus (Bath) exists in several forms as shown by electrospray-ionisation mass spectrometry. Eur. J. Biochem. 254, 602-609.
20. 20. Elango, N., Radhakrishnan, R., Froland, W.A., Wallar, B.J., Earhart, C.A., Lipscomb, J.D. & Ohlendorf, D.H. (1997) Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci. 6, 556-568.
21. 21. Johnson, G.R. & Olsen, R.H. (1995) Nucleotide sequence analysis of genes encoding a toluene/benzene-2-monooxygenase from Pseudomonas sp. strain JS150. Appl. Environ. Microbiol. 61, 3336-3346.
22. 22. Byrne, A.M., Kukor, J.J. & Olsen, R.H. (1995) Sequence analysis of the gene cluster encoding toluene-3-monooxygenase from Pseudomonas pickettii PKO1. Gene 154, 65-70.
23. 23. Olsen, R.H., Kukor, J.J. & Kaphammer, B. (1994) A novel toluene-3-monooxygenase pathway cloned from Pseudomonas pickettii PKO1. J. Bacteriol. 176, 3749-3756.
24. 24. Yen, K.-M., Karl, M.R., Blatt, L.M., Simon, M.J., Winter, R.B., Fausset, P.R., Lu, H.S., Harcourt, A.A. & Chen, K.K. (1991) Cloning and characterization of a Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase. J. Bacteriol. 173, 5315-5327.
25. 25. Yen, K.-M. & Karl, M.R. (1992) Identification of a new gene, tmoF, in the Pseudomonas mendocina KR1 gene cluster encoding toluene-4-monooxygenase. J. Bacteriol. 174, 7253-7261.
26. 26. Pikus, J.D., Studts, J.M., Achim, C., Kauffmann, K.E., Münck, E., Steffan, R.J., McClay, K. & Fox, B.G. (1996) Recombinant toluene-4-monooxygenase: catalytic and Mössbauer studies of the purified diiron and Rieske components of a four-protein complex. Biochemistry 35, 9106-9119.
27. 27. Whited, G.M. & Gibson, D.T. (1991) Toluene-4-monooxygenase, a three-component enzyme system that catalyzes the oxidation of toluene to p-cresol in Pseudomonas mendocina KR1. J. Bacteriol. 173, 3010-3016.
28. 28. Nordlund, I., Powlowski, J. & Shingler, V. (1990) Complete nucleotide sequence and polypeptide analysis of multicomponent phenol hydroxylase from Pseudomonas sp. strain CF600. J. Bacteriol. 172, 6826-6833.
29. 29. Nordlund, I., Powlowski, J., Hagström, Å & Shingler, V. (1993) Conservation of regulatory and structural genes for a multicomponent phenol hydroxylase within phenol-catabolizing bacteria that utilize a meta-cleavage pathway. J. Gen. Microbiol. 139, 2695-2703.
30. 30. Shingler, V., Franklin, F.C.H., Tsuda, M., Holroyd, D. & Bagdasarian, M. (1989) Molecular analysis of a plasmid-encoded phenol hydroxylase from Pseudomonas CF600. J. Gen. Microbiol. 135, 1083-1092.
31. 31. Powlowski, J. & Shingler, V. (1990) In vitro analysis of polypeptide requirements of multicomponent phenol hydroxylase from Pseudomonas sp. strain CF600. J. Bacteriol. 172, 6834-6840.
32. 32. Gallagher, S.C., Cammack, R. & Dalton, H. (1997) Alkene monooxygenase from Nocardia corallina B-276 is a member of the class of dinuclear iron proteins capable of stereospecific epoxygenation reactions. Eur. J. Biochem. 247, 635-641.
33. 33. Saeki, H. & Furuhashi, K. (1994) Cloning and characterization of a Nocardia corallina B-276 gene cluster encoding alkene monooxygenase. J. Ferment. Bioeng. 78, 399-406.
34. 34. Miura, A. & Dalton, H. (1995) Purification and characterization of the alkene monooxygenase from Nocardia corallina B-276. Biosci. Biotech. Biochem. 59, 853-859.
35. 35. Small, F.J. & Ensign, S.A. (1997) Alkene monooxygenase from Xanthobacter strain Py2. J. Biol. Chem. 272, 24913-24920.
36. 36. Zhou, N.-Y., Jenkins, A., Chan Kwo Chion, C.K.N. & Leak, D.J. (1998) The alkene monooxygenase from Xanthobacter Py2 is a binuclear non-haem iron protein closely related to toluene 4-monooxygenase. FEBS Lett. 430, 181-185.
37. 37. Zhou, N.-Y., Jenkins, A., Chan Kwo Chion, C.K.N. & Leak, D.J. (1999) The alkene monooxygenase from Xanthobacter strain Py2 is closely related to aromatic monooxygenases and catalyzes aromatic monohydroxylation of benzene, toluene, and phenol. Appl. Environ. Microbiol. 65, 1589-1595.
38. 38. Nordlund, P., Dalton, H. & Eklund, H. (1992) The active site structure of methane monooxygenase is closely related to the binuclear iron center of ribonucleotide reductase. FEBS Lett. 307, 257-262.
39. 39. Fox, B.G., Shanklin, J., Ai, J., Loehr, T.M. & Sanders-Loehr, J. (1994) Resonance Raman evidence for an Fe-O-Fe center in steroyl-ACP desaturase. Primary sequence identity with other diiron-oxo proteins. Biochemistry 33, 12776-12786.
40. 40. Gallagher, S.C., George, A. & Dalton, H. (1998) Sequence-alignment modelling and molecular docking studies of the epoxygenase component of alkene monooxygenase from Nocardia corallina B-276. Eur. J. Biochem. 254, 480-489.
41. + reductase: prototype for a structurally novel flavoenzyme family. Science 251, 60-66.
42. 42. Correll, C.C., Batie, C.J., Ballou, D.P. & Ludwig, M.L. (1992) Phthalate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe-2S]. Science 258, 1604-1610.
43. + reductases. FEBS Lett. 302, 247-252.
44. 44. Neidle, E.L., Hartnett, C., Ornston, L.N., Bairoch, A., Rekik, M. & Harayama, S. (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.
45. 45. De Marco, P., Moradas-Ferreira, P., Higgins, T.P., McDonald, I., Kenna, E.M. & Murrell, J.C. (1999) Molecular analysis of a novel methanesulfonic acid monooxygenase from the methylotroph Methylosulfonomonas methylovora. J. Bacteriol. 181, 2244-2251.
46. 46. Qian, H., Edlund, U., Powlowski, J., Shingler, V. & Sethson, I. (1997) Solution structure of phenol hydroxylase protein component P2 determined by NMR spectroscopy. Biochemistry 36, 495-504.
47. 47. Brandstetter, H., Whittington, D.A., Lippard, S.J. & Frederick, C.A. (1999) Mutational and structural analyses of the regulatory protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath). Chem. Biol. 6, 441-449.
48. 48. Walters, K.J., Gassner, G.T., Lippard, S.J. & Wagner, G. (1999) Structure of the soluble methane monooxygenase regulatory protein B. Proc. Natl Acad. Sci. USA 96, 7877-7882.
49. 49. DeWitt, J.G., Bentsen, J.G., Rosenzweig, A.C., Hedman, B., Green, J., Pilkington, S., Papaefthymiou, G.C., Dalton, H., Hodgson, K.O. & Lippard, S.J. (1991) X-ray absorption, Mössbauer, and EPR studies of the dinuclear iron center in the hydroxylase component of methane monooxygenase. J. Am. Chem. Soc. 113, 9219-9235.
50. 50. Fox, B.G., Froland, W.A., Dege, J.E. & Lipscomb, J.D. (1989) Methane monooxygenase from Methylosinus trichosporium OB3b: purification and properties of a three-component system with high specific activity from a type II methanotroph. J. Biol. Chem. 264, 10023-10033.
51. 51. Oakley, C.J. & Murrell, J.C. (1988) nifH genes in the obligate methane oxidizing bacteria. FEMS Microbiol. Lett. 49, 53-57.
52. 52. Sambrook, J., Fritsch, E.F. & Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York, USA.
53. 53. Valentine, A.M., Wilkinson, B., Liu, K.E., Komar-Panicucci, S., Priestley, N.D., Williams, P.G., Morimoto, H., Floss, H.G. & Lippard, S.J. (1997) Tritiated chiral alkanes as substrates for soluble methane monooxygenase from Methylococcus capsulatus (Bath): probes for the mechanism of hydroxylation. J. Am. Chem. Soc. 119, 1818-1827.
54. 54. Genetics Computer Group (1991) Wisconsin Package Manual, Version 7.3. Genetics Computer Group, Madison, WI, USA.
55. 55. Clark, S.P. (1992) MALIGNED: a multiple sequence alignment editor. Comput. Appl. Biosci. 8, 535-538.
56. 56. Rosenzweig, A.C., Nordlund, P., Takahara, P.M., Frederick, C.A. & Lippard, S.J. (1995) Geometry of the soluble methane monooxygenase catalytic diiron center in two oxidation states. Chem. Biol. 2, 409-418.
57. 57. Molecular Simulations, Inc. (1997) Quanta97, Version 97.0. Molecular Simulations, Inc., San Diego, CA, USA.
58. 58. Kraulis, P.J. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24, 946-950.
59. 59. Lloyd, J.S., Bhambra, A., Murrell, J.C. & Dalton, H. (1997) Inactivation of the regulatory protein B of soluble methane monooxygenase from Methylococcus capsulatus (Bath) by proteolysis can be overcome by a Gly to Gln modification. Eur. J. Biochem. 248, 72-79.
60. 60. Gassner, G.T. & Lippard, S.J. (1999) Component interactions in the soluble methane monooxygenase system from Methylococcus capsulatus (Bath). Biochemistry 38, 12768-12785.
61. 61. West, C.A., Salmond, G.P.C., Dalton, H. & Murrell, J.C. (1992) Functional expression in Escherichia colli of proteins B and C from soluble methane monooxygenase of Methylococcus capsulatus (Bath). J. Gen. Microbiol. 138, 1301-1307.
62. 62. Homer, M.J., Dean, D.R. & Roberts, G.P. (1995) Characterization of the γ protein and its involvement in the metallocluster assembly and maturation of dinitrogenase from Azotobacter vinelandii. J. Biol. Chem. 270, 24745-24752.
63. 63. Nordlund, P., Sjöberg, B.-M. & Eklund, H. (1990) Three-dimensional structure of the free radical protein of ribonucleotide reductase. Nature (London) 345, 593-598.
64. 64. Nordlund, P., Åberg, A., Uhlin, U. & Eklund, H. (1993) Crystallographic investigations of ribonucleotide reductase. Biochem. Soc. Trans. 21, 735-738.
65. 65. Nordlund, P. & Eklund, H. (1993) Structure and function of the Escherichia coli ribonucleotide reductase protein R2. J. Mol. Biol. 232, 123-164.
66. 66. Kauppi, B., Nielsen, B.B., Ramaswamy, S., Kjøller Larsen, I., Thelander, M., Thelander, L. & Eklund, H. (1996) The three-dimensional structure of mammalian ribonucleotide reductase protein R2 reveals a more-accessible iron-radical site than Escherichia coli R2. J. Mol. Biol. 262, 706-720.
67. 1 Compounds (Lidstrom, M.E. & Tabita, F.R., eds), pp. 141-149. Kluwer Academic Publishers, Dordrecht, the Netherlands.
68. 68. Regnström, K., Åberg, A., Ormö, M., Sahlin, M. & Sjøberg, B.-M. (1994) The conserved serine 211 is essential for reduction of the dinuclear iron center in protein R2 of Escherichia coli ribonucleotide reductase. J. Biol. Chem. 269, 6355-6361.
69. 69. Poulos, T.L., Finzel, B.C., Gunsalus, I.C., Wagner, G.C. & Kraut, J. (1985) The 2.6-Å crystal structure of Pseudomonas putida cytochrome P-450. J. Biol. Chem. 260, 16122-16130.
70. CAM active site mutant Thr252Ala. Biochemistry 30, 11420-11429.
71. 71. Pikus, J.D., Mitchell, K.H., Studts, J.M., McClay, K., Steffan, R.J. & Fox, B.G. (2000) Threonine 201 in the diiron enzyme toluene 4-monooxygenase is not required for catalysis. Biochemistry 39, 791-799.
72. 72. Rosenzweig, A.C., Brandstetter, H., Whittington, D.A., Nordlund, P., Lippard, S.J. & Frederick, C.A. (1997) Crystal structures of the methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath): implications for substrate gating and component interactions. Proteins 29, 141-152.
73. 73. Fox, B.G., Liu, Y., Dege, J.E. & Lipscomb, J.D. (1991) Complex formation between the protein components of methane monooxygenase from Methylosinus trichosporium OB3b. J. Biol. Chem. 266, 540-550.
74. 74. Gallagher, S.C., Callaghan, A.J., Zhao, J., Dalton, H. & Trewhella, J. (1999) Global conformational changes control the reactivity of methane monooxygenase. Biochemistry 38, 6752-6760.