Molecular determinants of the regioselectivity of toluene/o-xylene monooxygenase from pseudomonas sp. strain OX1

Applied and Environmental Microbiology

Volumn 75, Issue 3, 2009, Pages 823-836

  Notomista, Eugenio ^a,b   Cafaro, Valeria ^a   Bozza, Giuseppe ^a   Donato, Alberto Di ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

A-PRIORI; ACTIVE SITE POCKETS; ACTIVE SITES; ENERGY ANALYSIS; ENERGY VALUES; MOLECULAR DETERMINANTS; MONOOXYGENASE; MONOOXYGENASES; MONTE CARLO APPROACHES; MULTI COMPONENTS; P CRESOLS; PSEUDOMONAS SP; REACTION INTERMEDIATES; SUBSTRATE SPECIFICITIES; WILD TYPES;

BINDING ENERGY; HYDROCARBONS; HYDROXYLATION; ISOMERS; PROTEINS; REGIOSELECTIVITY; TOLUENE; XYLENE;

AROMATIC HYDROCARBONS;

BACTERIUM; ENZYME ACTIVITY; HETEROGENEITY; MOLECULAR ANALYSIS; TOLUENE; XYLENE;

CATALYTIC DOMAIN; CRESOLS; DNA MUTATIONAL ANALYSIS; KINETICS; MODELS, MOLECULAR; MODELS, THEORETICAL; MUTATION, MISSENSE; OXYGENASES; PSEUDOMONAS; STEREOISOMERISM; SUBSTRATE SPECIFICITY; TOLUENE;

BACTERIA (MICROORGANISMS); PSEUDOMONAS SP.;

EID: 59649089569     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.01951-08     Document Type: Article

References (40)

1. Bertoni, G., F. Bolognesi, E. Galli, and P. Barbieri. 1996. Cloning of the genes for and characterization of the early stages of toluene catabolism in Pseudomonas stutzeri OX1. Appl. Environ. Microbiol. 62:3704-3711.
2. Borodina, E., T. Nichol, M. G. Dumont, T. J. Smith, and J. C. Murrell. 2007. Mutagenesis of the "leucine gate" to explore the basis of catalytic versatility in soluble methane monooxygenase. Appl. Environ. Microbiol. 73:6460-6467.
3. Cafaro, V., V. Izzo, R. Scognamiglio, E. Notomista, P. Capasso, A. Casbarra, P. Pucci, and A. Di Donato. 2004. Phenol hydroxylase and toluene/o-xylene monooxygenase from Pseudomonas stutzeri OX1: interplay between two enzymes. Appl. Environ. Microbiol. 70:2211-2219.
4. Cafaro, V., E. Notomista, P. Capasso, and A. Di Donato. 2005. Mutation of glutamic acid 103 of toluene o-xylene monooxygenase as a means to control the catabolic efficiency of a recombinant upper pathway for degradation of methylated aromatic compounds. Appl. Environ. Microbiol. 71:4744-4750.
5. Cafaro, V., E. Notomista, P. Capasso, and A. Di Donato. 2005. Regiospecificity of two multicomponent monooxygenases from Pseudomonas stutzeri OX1: molecular basis for catabolic adaptation of this microorganism to methylated aromatic compounds. Appl. Environ. Microbiol. 71:4736-4743.
6. Cafaro, V., R. Scognamiglio, A. Viggiani, V. Izzo, I. Passaro, E. Notomista, F. Dal Piaz, A. Amoresano, A. Casbarra, P. Pucci, and A. Di Donato. 2002. Expression and purification of the recombinant subunits of toluene/o-xylene monooxygenase and reconstitution of the active complex. Eur. J. Biochem. 269:5689-5699.
7. Fishman, A., Y. Tao, L. Rui, and T. K. Wood. 21 October 2004. Controlling the regiospecific oxidation of aromatics via active site engineering of toluene para-monooxygenase of Ralstonia pickettii PKO1. J. Biol. Chem. 280:506-514. [Epub ahead of print.]
8. Gallagher, S. C., R. Cammark, and H. Dalton. 1997. Alkene monooxygenase from Nocardia corattina B-276 is a member of the class of dinuclear iron proteins capable of stereospecific epoxygenation reactions. Eur. J. Biochem. 247:635-641.
9. Hemmi, H., J. M. Studts, Y. K. Chae, J. Song, J. L. Markley, and B. G. Fox. 2001. Solution structure of the toluene 4-monooxygenase effector protein (T4moD). Biochemistry 40:3512-3524.
10. 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.
11. Kraut, D. A., P. A. Sigala, B. Pybus, C. W. Liu, D. Ringe, G. A. Petsko, and D. Herschlag. 28 March 2006. Testing electrostatic complementarity in enzyme catalysis: hydrogen bonding in the ketosteroid isomerase oxyanion hole. PLoS Biol. 4:e99. [Epub ahead of print.]
12. Lahiri, S. D., G. Zhang, D. Dunaway-Mariano, and K. N. Allen. 13 March 2003. The pentacovalent phosphorus intermediate of a phosphoryl transfer reaction. Science 299:2067-2071. [Epub ahead of print.]
13. Leahy, J. G., P. J. Batchelor, and S. M. Morcomb. 2003. Evolution of the soluble diiron monooxygenases. FEMS Microbiol. Rev. 27:449-479.
14. Lippard, S. J. 2005. Hydroxylation of C-H bonds at carboxylate-bridged diiron centres. Philos. Trans. A 363:861-877, 1035-1040.
15. Lipscomb, J. D. 1994. Biochemistry of the soluble methane monooxygenase. Annu. Rev. Microbiol. 48:371-399.
16. Mitchell, K. H., C. E. Rogge, T. Gierahn, and B. G. Fox. 14 March 2003. Insight into the mechanism of aromatic hydroxylation by toluene 4-monooxygenase by use of specifically deuterated toluene and p-xylene. Proc. Natl. Acad. Sci. USA 100:3784-3789. [Epub ahead of print.]
17. Mitchell, K. H., J. M. Studts, and B. G. Fox. 2002. Combined participation of hydroxylase active site residues and effector protein binding in a para to ortho modulation of toluene 4-monooxygenase regiospecificity. Biochemistry 41:3176-3188.
18. Murray, L. J., R. Garcia-Serres, M. S. McCormick, R. Davydov, S. G. Naik, S. H. Kim, B. M. Hoffman, B. H. Huynh, and S. J. Lippard. 29 November 2007. Dioxygen activation at non-heme diiron centers: oxidation of a proximal residue in the I100W variant of toluene/o-xylene monooxygenase hydroxylase. Biochemistry 46:14795-14809. [Epub ahead of print.]
19. Murray, L. J., and S. J. Lippard. 23 May 2007. Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygenases. Acc. Chem. Res. 40:466-474. [Epub ahead of print.]
20. Murray, L. J., S. G. Naik, D. O. Ortillo, R. Garcia-Serres, J. K. Lee, B. H. Huynh, and S. J. Lippard. 30 October 2007. Characterization of the arene-oxidizing intermediate in ToMOH as a diiron(III) species. J. Am. Chem. Soc. 129:14500-14510. [Epub ahead of print.]
21. Murrell, J. C., B. Gilbert, and I. R. McDonald. 2000. Molecular biology and regulation of methane monooxygenase. Arch. Microbiol. 173:325-332.
22. Newman, L. M., and L. P. Wackett. 1995. Purification and characterization of toluene 2-monooxygenase from Burkholderia cepacia G4. Biochemistry 34: 14066-14076.
23. Notomista, E., A. Lahm, A. Di Donato, and A. Tramontano. 2003. Evolution of bacterial and archaeal multicomponent monooxygenases. J. Mol. Evol. 56:435-445.
24. Otyepka, M., P. Banas, A. Magistrato, P. Carloni, and J. Damborsky. 2007. Second step of hydrolytic dehalogenation in haloalkane dehalogenase investigated by QM/MM methods. Proteins 70:707-717.
25. Pikus, J. D., J. M. Studts, C. Achim, K. E. Kauffmann, E. Munck, R. J. Steffan, K. McClay, and B. G. Fox. 1996. Recombinant toluene-4- monooxygenase: catalytic and Mossbauer studies of the purified diiron and rieske components of a four-protein complex. Biochemistry 35:9106-9119.
26. Pikus, J. D., J. M. Studts, K. McClay, R. J. Steffan, and B. G. Fox. 1997. Changes in the regiospecificity of aromatic hydroxylation produced by active site engineering in the diiron enzyme toluene 4-monooxygenase. Biochemistry 36:9283-9289.
27. Pompliano, D. L., A. Peyman, and J. R. Knowles. 1990. Stabilization of a reaction intermediate as a catalytic device: definition of the functional role of the flexible loop in triosephosphate isomerase. Biochemistry 29:3186-3194.
28. Reisner, E., T. C. Abikoff, and S. J. Lippard. 31 October 2007. Influence of steric hindrance on the core geometry and sulfoxidation chemistry of carboxylate-rich diiron(II) complexes. Inorg. Chem. 46:10229-10240. [Epub ahead of print.]
29. Rosenzweig, A. C., H. Brandstetter, D. A. Whittington, P. Nordlund, S. J. Lippard, and C. A. Frederick. 1997. Crystal structures of the methane mono-oxygenase hydroxylase from Methylococcus capsulatus (Bath): implications for substrate gating and component interactions. Proteins 29:141-152.
30. Rui, L., Y. M. Kwon, A. Fishman, K. F. Reardon, and T. K. Wood. 2004. Saturation mutagenesis of toluene ortho-monooxygenase of Burkholderia cepacia G4 for enhanced 1-naphthol synthesis and chloroform degradation. Appl. Environ. Microbiol. 70:3246-3252.
31. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual, 2nd ed. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
32. Sazinsky, M. H., J. Bard, A. Di Donato, and S. J. Lippard. 2004. Crystal structure of the toluene/o-xylene monooxygenase hydroxylase from Pseudomonas stutzeri OX1. Insight into the substrate specificity, substrate channeling, and active site tuning of multicomponent monooxygenases. J. Biol. Chem. 279:30600-30610.
33. St. Maurice, M., and S. L. Bearne. 2000. Reaction intermediate analogues for mandelate racemase: interaction between Asn 197 and the alpha-hydroxyl of the substrate promotes catalysis. Biochemistry 39:13324-13335.
34. 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.
35. Vardar, G., and T. K. Wood. 2004. Protein engineering of toluene-o-xylene monooxygenase from Pseudomonas stutzeri OX1 for synthesizing 4-methyl-resorcinol, methylhydroquinone, and pyrogallol. Appl. Environ. Microbiol. 70:3253-3262.
36. Viggiani, A., L. Siani, E. Notomista, L. Birolo, P. Pucci, and A. Di Donato. 2004. The role of conserved residues H246, H199 and Y255 in the catalysis of catechol 2,3-dioxygenase from Pseudomonas stutzeri OX1. J. Biol. Chem. 279:48630-48639.
37. Weiner, S. J., P. A. Kollman, D. A. Case, U. C. Singh, C. Ghio, G. Alagona, S. Profeta, and P. Weiner. 1984. A new force field for molecular mechanical simulation of nucleic acids and proteins. J. Am. Chem. Soc. 106:765-784.
38. Whited, G. M., and D. T. Gibson. 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.
39. Zhao, M., B. Helms, E. Slonkina, S. Friedle, D. Lee, J. Dubois, B. Hedman, K. O. Hodgson, J. M. Frechet, and S. J. Lippard. 2008. Iron complexes of dendrimer-appended carboxylates for activating dioxygen and oxidizing hydrocarbons. J. Am. Chem. Soc. 11:11.
40. Zhorov, B. S., and P. D. Bregestovski. 2000. Chloride channels of glycine and GABA receptors with blockers: Monte Carlo minimization and structure-activity relationships. Biophys. J. 78:1786-1803.