Mutagenesis of the "leucine gate" to explore the basis of catalytic versatility in soluble methane monooxygenase

Applied and Environmental Microbiology

Volumn 73, Issue 20, 2007, Pages 6460-6467

  Borodina, Elena ^a   Nichol, Tim ^b   Dumont, Marc G ^a   Smith, Thomas J ^b   Murreil, J Colin ^a  

^a UNIVERSITY OF WARWICK   (United Kingdom)

^b SHEFFIELD HALLAM UNIVERSITY   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; CRYSTALLOGRAPHY; MUTAGENESIS; REGIOSELECTIVITY; SOLUBILITY; SUBSTRATES;

MONOAROMATIC SUBSTRATES; MUTANTS; TRIAROMATIC HYDROCARBONS;

ENZYME ACTIVITY;

ANTHRACENE; ARGININE; AROMATIC HYDROCARBON; BENZENE; BIPHENYL DERIVATIVE; CYSTEINE; GLYCINE; LEUCINE; METHANE; METHANE MONOOXYGENASE; METHANOL; NAPHTHALENE; PHENANTHRENE; TRYPTOPHAN; TYROSINE;

AMINO ACID; CATALYSIS; ENZYME ACTIVITY; METHANE; MUTATION;

ACCURACY; ALPHA CHAIN; ARTICLE; CRYSTALLOGRAPHY; ENZYME ACTIVE SITE; ENZYME CONFORMATION; ENZYME MECHANISM; ENZYME SUBSTRATE COMPLEX; ESCHERICHIA COLI; HYDROXYLATION; MUTAGENESIS; MUTATION; NONHUMAN; OXIDATION; SITE DIRECTED MUTAGENESIS; STEREOCHEMISTRY; WILD TYPE;

CATALYSIS; LEUCINE; METHYLOSINUS TRICHOSPORIUM; MUTAGENESIS, SITE-DIRECTED; NAPHTHALENES; OXYGENASES; RECOMBINANT PROTEINS; SOLUBILITY;

EID: 35449005838     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.00823-07     Document Type: Article

References (45)

1. Bodrossy, L., J. C. Murrell, H. Dalton, M. Kalman, L. G. Puskas, and K. L. Kovacs. 1995. Heat-tolerant methanotrophic bacteria from the hot-water effluent of a natural-gas field. Appl. Environ. Microbiol. 61:3549-3555.
2. Brusseau, G. A., H.-C. Tsien, R. S. Hanson, and L. P. Wackett. 1990. Optimization of trichloroethylene oxidation by methanotrophs and the use of a colorimetric assay to detect soluble methane mono-oxygenase activity. Biodegradation 1:19-29.
3. Burrows, K. J., A. Cornish, D. Scott, and I. J. Higgins. 1984. Substrate specificity of the soluble and particulate methane mono-oxygenase of Methylosinus trichosporium OB3b. J. Gen. Microbiol. 130:3327-3333.
4. Canada, K. A., S. Iwashita, H. Shim, and T. K. Wood. 2002. Directed evolution of toluene ortho-monooxygenase for enhanced naphthol synthesis and chlorinated ethene degradation. J. Bacteriol. 184:344-349.
5. 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.
6. Carredano, E., A. Karlsson, B. Kauppi, D. Choudhury, R. E. Parales, J. V. Parales, K. Lee, D. T. Gibson, H. Eklund, and S. Ramaswamy. 2000. Substrate binding site of naphthalene 1,2-dioxygenase: functional implications of indole binding. J. Mol. Biol. 296:701-712.
7. Dennis, J. J., and G. J. Zylstra. 1998. Plasposons: modular self-cloning minitransposon derivatives for rapid genetic analysis of gram-negative bacterial genomes. Appl. Environ. Microbiol. 64:2710-2715.
8. DeWitt, J. G., J. G. Bentsen, A. C. Rosenzweig, B. Hedman, J. Green, S. Pilkington, G. C. Papaefthymiou, H. Dalton, K. O. Hodgson, and S. J. Lippard. 1991. X-ray absorption, Mossbauer, and EPR studies of the dinuclear iron center in the hydroxylase component of methane monooxygenase. J. Am. Chem. Soc. 113:9219-9235.
9. Elango, N., R. Radmakrishnan, W. A. Froland, B. J. Wallar, C. A. Earhart, J. D. Lipscomb, and D. H. Ohlendorf. 1997. Crystal structure of the hydroxylase component of methane monooxygenase from Methylosinus trichosporium OB3b. Protein Sci. 6:556-568.
10. Feinberg, A. P., and B. Vogelstein. 1983. A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity. Anal. Biochem. 132:6-13.
11. Feinberg, A. P., and B. Vogelstein. 1984. "A technique for radiolabeling DNA restriction endonuclease fragments to high specific activity". Addendum. Anal. Biochem. 137:266-267.
12. George, A. R., P. C. Wilkins, and H. Dalton. 1996. A computational investigation of the possible substrate binding sites in the hydroxylase of soluble methane monooxygenase. J. Mol. Catal. B 2:103-113.
13. Halsey, K. H., L. A. Sayavedra-Soto, P. J. Bottomley, and D. J. Arp. 2006. Site-directed amino acid substitutions in the hydroxylase subunit of butane monooxygenase from Pseudomonas butanovora: implications for substrates knocking at the gate. J. Bacteriol. 188:4962-4969.
14. Higgins, I. J., D. J. Best, and R. C. Hammond. 1980. New findings in methane-utilizing bacteria highlight their importance in the biosphere and their commercial potential. Nature 286:561-564.
15. Ho, S. N., H. D. Hunt, R. M. Horton, J. K. Pullen, and R. L. Pease. 1989. Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77:51-59.
16. Jahng, D., K. S. Kim, R. S. Hanson, and T. K. Wood. 1996. Optimization of trichloroethylene degradation using soluble methane monooxygenase of Methylosinus trichosporium OB3b expressed in recombinant bacteria. Biotechnol. Bioeng. 51:349-359.
17. Jahng, D., and T. K. Wood. 1994. Trichloroetheylene and chloroform degradation by a recombinant pseudomonad expressing soluble methane monooxygenase from Methylosinus trichosporium OB3b. Appl. Environ. Microbiol. 60:2473-2482.
18. Kauppi, B., K. Lee, E. Carredano, R. E. Parales, D. T. Gibson, H. Eklund. and S. Ramaswamy. 1998. Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure 6:571-586.
19. Keenan, B. G., T. Leungsakul, B. F. Smets, and T. K. Wood. 2004. Saturation mutagenesis of Burkholderia cepacia R34 2,4-dinitrotoluene dioxygenase at DntAC valine 350 for synthesizing nitrohydroquinone, methylhydroquinone, and methoxyhydroquinone. Appl. Environ. Microbiol. 70:3222-3231.
20. Kovach, M. E., P. H. Elzera, D. S. Hill, G. T. Robertson, M. A. Farrisa, R. M. Roop, and K. M. Peterson. 1995. Four new derivatives of the broad-host-range cloning vector pBBR1MCS, carrying different antibiotic-resistance cassettes. Gene 166:175-176.
21. Leahy, J. G., P. J. Batchelor, and S. M. Morcomb. 2003. Evolution of the soluble diiron monooxygenases. FEMS Microbiol. Rev. 27:449-479.
22. Lee, S.-K., J. C. Nesheim, and J. D. Lipscomb. 1993. Transient intermediates in the methane monooxygenase catalytic cycle. J. Biol. Chem. 268:21569-21577.
23. Lindner, A. S., P. Adriaens, and J. D. Semrau. 2000. Transformation of ortho-substituted biphenyls by Methylosinus trichosporium OB3b: substituent effects on oxidation kinetics and product formation. Arch. Microbiol. 174: 35-41.
24. Lloyd, J. S., P. De Marco, H. Dalton, and J. C. Murrell. 1999. Heterologous expression of soluble methane monooxygenase genes in methanotrophs containing only particulate methane monooxygenase. Arch. Microbiol. 171:364-370.
25. Lloyd, J. S., R. Finch, H. Dalton, and J. C. Murrell. 1999. Homologous expression of soluble methane monooxygenase genes in Methylosinus trichosporium OB3b. Microbiology 145:461-470.
26. Martin, H., and J. C. Murrell. 1995. Methane monooxygenase mutants from Methylosinus trichosporium constructed by marker-exchange mutagenesis. FEMS Microbiol Lett. 127:243-248.
27. Merkx, M., and S. J. Lippard. 2002. Why OrfY? Characterization of MmoD, a long overlooked component of the soluble methane monooxygenase from Methylococcus capsulatus (Bath). J. Biol. Chem. 277:5858-5865.
28. Murrell, J. C., B. Gilbert, and I. R. McDonald. 2000. Molecular biology and regulation of methane monooxygenase. Arch. Microbiol. 173:325-332.
29. Parales, R. E., K. Lee, S. M. Resnick, H. Jiang, D. J. Lessner, and D. T. Gibson. 2000. Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J. Bacteriol. 182:1641-1649.
30. Rosenzweig, A. C., H. Brandstetter, D. A. Whittington, P. Nordlund, S. J. Lippard, and C. A. Frederick. 1997. Crystal structure of the methane monooxygenase hydroxylase from Methylococcus capsulatus (Bath): implications for substrate gating and component interactions. Proteins 29:141-152.
31. Rosenzweig, A. C., C. A. Frederick, S. J. Lippard, and P. Nordlund. 1993. Crystal structure of a bacterial nonheme iron hydroxylase that catalyzes the biological oxidation of methane. Nature 366:537-543.
32. Sambrook, J., E. F. Friteh, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
33. Sazinsky, M. H., J. Bard, A. Di Donato, and S. J. Lippard. 2004. Crystal structure of the toluene/o-xylene monooxygenase hydroxylase from Pseudomonas stutzen OX1. J. Biol. Chem. 279:30600-30610.
34. Schäfer, A., A. Tauch, W. Jäger, J. Kalinowski, G. Thierbach, and A. Pühler. 1994. Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69-73.
35. 2 diamond core structure for the key intermediate Q of methane monooxygenase. Science 275:515-517.
36. Simon, R., U. Priefer, and A. Pühler. 1983. A broad host range mobilization system for in vivo genetic engineering - transposon mutagenesis in Gram-negative bacteria. Biotechnology 1:784-791.
37. Smith, T. J., and H. Dalton. 2004. Biocatalysis by methane monooxygenase and its implications for the petroleum industry, p. 177-192. In R. Vazquez-Duhalt and R. Quintero-Ramirez (ed.), Petroleum biotechnology, developments and perspectives. Elsevier, Amsterdam, The Netherlands.
38. Smith, T. J., S. E. Slade, N. P. Burton, J. C. Murrell, and H. Dalton. 2002. Improved system for protein engineering of the hydroxylase component of soluble methane monooxygenase. Appl. Environ. Microbiol. 68:5265-5273.
39. Stafford, G. P., J. Scanlan, I. R. McDonald, and J. C. Murrell. 2003. rpoN, mmoR and mmoG, genes involved in regulating the expression of soluble methane monooxygenase in Methylosinus trichosporium OB3b. Microbiology 149:1771-1784.
40. Steffan, R. J., and K. R. McClay. December 2000. Preparation of enantiospecific epoxides. International patent no. WO 00/73425.
41. Tao, Y., A. Fishman, W. E. Bentley, and T. K. Wood. 2004. Altering toluene 4-monooxygenase by active-site engineering for the synthesis of 3-methoxy-catechol, methoxyhydroquinone, and methylhydroquinone. J. Bacteriol. 186: 4705-4713.
42. Vardar, G., and T. K. Wood. 2004. Protein engineering of toluene-o-xylene monooxygenase from Pseudomonas stutzeri OX1 for synthesizing 4-methylresorcinol, methylhydroquinone, and pyrogallol Appl. Environ. Microbiol. 70:3253-3262.
43. Vieira, J., and J. Messing. 1982. The pUC plasmids, an M13mp7-derived system for insertion mutagenesis and sequencing with synthetic universal primers. Gene 19:259-268.
44. West, C. A., G. P. C. Salmond, H. Dalton, and J. C. Murrell. 1992. Functional expression in Escherichia coli of protein B and protein C from soluble methane monooxygenase of Methylococcus capsulatus (Bath). J. Gen. Microbiol. 138:1301-1307.
45. Woodland, M. P., D. S. Patil, R. Cammack, and H. Dalton. 1986. Electron-spin-resonance studies of protein A of the soluble methane monooxygenase from Methylococcus capsulatus (Bath). Biochim. Biophys. Acta 873:237-242.