Tuning the specificity of the recombinant multicomponent toluene o-xylene monooxygenase from Pseudomonas sp. Strain OX1 for the biosynthesis of tyrosol from 2-phenylethanol

Applied and Environmental Microbiology

Volumn 77, Issue 15, 2011, Pages 5428-5437

  Notomista, Eugenio ^a,b   Scognamiglio, Roberta ^a,b   Troncone, Luca ^a,b   Donadio, Giuliana ^a,b   Pezzella, Alessandro ^a   Di Donato, Alberto ^a,b   Izzo, Viviana ^a,b  

^a UNIVERSITY OF NAPLES FEDERICO II   (Italy)

^b CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIA; BIOCATALYSTS; BIOCHEMISTRY; BIOSYNTHESIS; ENZYMES; ESCHERICHIA COLI; HYDROXYLATION; INDUSTRIAL CHEMICALS; OLIVE OIL; REACTION INTERMEDIATES; SUBSTRATES; TOLUENE; XYLENE;

ACTIVE SITE RESIDUES; BIOTRANSFORMATION PROCESS; COMPUTATIONAL MODEL; INDUSTRIAL PRODUCTION; MOLECULAR DETERMINANTS; PHENOLIC COMPOUNDS; STANDARD TECHNOLOGY; TOLUENE-O-XYLENE MONOOXYGENASE;

ANTIOXIDANTS;

ALCOHOL; ANTIOXIDANT; AROMATIC HYDROCARBON; BACTERIUM; BIOTRANSFORMATION; CATALYSIS; CATALYST; CELL ORGANELLE; COMPUTER SIMULATION; ENZYME ACTIVITY; INDUSTRIAL PRODUCTION; MOLECULAR ANALYSIS; MUTATION; OXIDATION; PHENOLIC COMPOUND; RECOMBINATION; SUBSTRATE; TOLUENE;

BACTERIA (MICROORGANISMS); ESCHERICHIA COLI; PSEUDOMONAS; PSEUDOMONAS SP.;

EID: 79961074468     PISSN: 00992240     EISSN: 10985336     Source Type: Journal    
DOI: 10.1128/AEM.00461-11     Document Type: Article

References (56)

1. Allouche, N., M. Damak, R. Ellouz, and S. Sayadi. 2004. Use of whole cells of Pseudomonas aeruginosa for synthesis of the antioxidant hydroxytyrosol via conversion of tyrosol. Appl. Environ. Microbiol. 70:2105-2109.
2. Allouche, N., and S. Sayadi. 2005. Synthesis of hydroxytyrosol, 2-hydroxyphenylacetic acid, and 3-hydroxyphenylacetic acid by differential conversion of tyrosol isomers using Serratia marcescens strain. J. Agric. Food Chem. 53:6525-6530.
3. Bailey, L. J., J. G. McCoy, G. N. Phillips, Jr., and B. G. Fox. 2008. Structural consequences of effector protein complex formation in a diiron hydroxylase. Proc. Natl. Acad. Sci. U. S. A. 105:19194-19198.
4. Bertoni, G., F. Bolognese, E. Galli, and P. Barbieri. 1996. Cloning of the genes for and characterization of the early stages of toluene and o-xylene catabolism in Pseudomonas stutzeri OX1. Appl. Environ. Microbiol. 62:3704-3711.
5. Bertoni, G., M. Martino, E. Galli, and P. Barbieri. 1998. Analysis of the gene cluster encoding toluene/o-xylene monooxygenase from Pseudomonas stutzeri OX1. Appl. Environ. Microbiol. 64:3626-3632.
6. Bouallagui, Z., and S. Sayadi. 2006. Production of high hydroxytyrosol yields via tyrosol conversion by Pseudomonas aeruginosa immobilized resting cells. J. Agric. Food Chem. 54:9906-9911.
7. Boyd, D. R., and T. D. Bugg. 2006. Arene cis-dihydrodiol formation: from biology to application. Org. Biomol. Chem. 4:181-192.
8. Boyd, D. R., N. D. Sharma, and C. C. Allen. 2001. Aromatic dioxygenases: molecular biocatalysis and applications. Curr. Opin. Biotechnol. 12:564-573.
9. Bradford, M. M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 72:248-254.
10. Brouk, M., and A. Fishman. 2009. Protein engineering of toluene monooxygenases for synthesis of hydroxytyrosol. Food Chem. 116:114-121.
11. Brouk, M., Y. Nov, and A. Fishman. 2010. Improving biocatalyst performance by integrating statistical methods into protein engineering. Appl. Environ. Microbiol. 76:6397-6403.
12. Cafaro, V., et al. 2004. Phenol hydroxylase and toluene/o-xylene monooxygenase from Pseudomonas stutzeri OX1: interplay between two enzymes. Appl. Environ. Microbiol. 70:2211-2219.
13. 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.
14. 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.
15. Cafaro, V., et al. 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.
16. Capasso, R., et al. 1995. Antibacterial polyphenols from olive oil mill waste waters. J. Appl. Bacteriol. 79:393-398.
17. Covas, M. I., et al. 2003. Bioavailability of tyrosol, an antioxidant phenolic compound present in wine and olive oil, in humans. Drugs Exp. Clin. Res. 29:203-206.
18. Deiana, M., et al. 1999. Inhibition of peroxynitrite dependent DNA base modification and tyrosine nitration by the extra virgin olive oil-derived antioxidant hydroxytyrosol. Free Radic. Biol. Med. 26:762-769.
19. de la Puerta, R., V. Ruiz Gutierrez, and J. R. Hoult. 1999. Inhibition of leukocyte 5-lipoxygenase by phenolics from virgin olive oil. Biochem. Pharmacol. 57:445-449.
20. Dordick, J. S., Y. L. Khmelnitsky, and M. V. Sergeeva. 1998. The evolution of biotransformation technologies. Curr. Opin. Microbiol. 1:311-318.
21. Espin, J. C., C. Soler-Rivas, E. Cantos, F. A. Tomas-Barberan, and H. J. Wichers. 2001. Synthesis of the antioxidant hydroxytyrosol using tyrosinase as biocatalyst. J. Agric. Food Chem. 49:1187-1193.
22. Etschmann, M. M., W. Bluemke, D. Sell, and J. Schrader. 2002. Biotechnological production of 2-phenylethanol. Appl. Microbiol. Biotechnol. 59:1-8.
23. Feingersch, R., J. Shainsky, T. K. Wood, and A. Fishman. 2008. Protein engineering of toluene monooxygenases for synthesis of chiral sulfoxides. Appl. Environ. Microbiol. 74:1555-1566.
24. Fishman, A., Y. Tao, L. Rui, and T. K. Wood. 2005. Controlling the regio-specific oxidation of aromatics via active site engineering of toluene paramonooxygenase of Ralstonia pickettii PKO1. J. Biol. Chem. 280:506-514.
25. Gao, F., and A. J. Daugulis. 2009. Bioproduction of the aroma compound 2-phenylethanol in a solid-liquid two-phase partitioning bioreactor system by Kluyveromyces marxianus. Biotechnol. Bioeng. 104:332-339.
26. Ishige, T., K. Honda, and S. Shimizu. 2005. Whole organism biocatalysis. Curr. Opin. Chem. Biol. 9:174-180.
27. Kelsey, N. A., H. M. Wilkins, and D. A. Linseman. 2010. Nutraceutical antioxidants as novel neuroprotective agents. Molecules 15:7792-7814.
28. Laemmli, U. K. 1970. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680-685.
29. Lazaridis, T., and M. Karplus. 1999. Discrimination of the native from misfolded protein models with an energy function including implicit solvation. J. Mol. Biol. 288:477-487.
30. Lazaridis, T., and M. Karplus. 1999. Effective energy function for proteins in solution. Proteins 35:133-152.
31. Leahy, J. G., P. J. Batchelor, and S. M. Morcomb. 2003. Evolution of the soluble diiron monooxygenases. FEMS Microbiol. Rev. 27:449-479.
32. Lippard, S. J. 2005. Hydroxylation of C-H bonds at carboxylate-bridged diiron centres. Philos. Trans. A Math. Phys. Eng. Sci. 363:861-877.
33. Loughlin, W. A. 2000. Biotransformations in organic synthesis. Biores. Technol. 74:49-62.
34. Manna, C., V. Migliardi, F. Sannino, A. De Martino, and R. Capasso. 2005. Protective effects of synthetic hydroxytyrosol acetyl derivatives against oxidative stress in human cells. J. Agric. Food Chem. 53:9602-9607.
35. Merkx, M., et al. 2001. Dioxygen activation and methane hydroxylation by soluble methane monooxygenase: a tale of two irons and three proteins. Angew. Chem. Int. ed. Engl. 40:2782-2807.
36. Murray, L. J., and S. J. Lippard. 2007. Substrate trafficking and dioxygen activation in bacterial multicomponent monooxygenases. Acc. Chem. Res. 40:466-474.
37. Notomista, E., V. Cafaro, G. Bozza, and A. Di Donato. 2009. Molecular determinants of the regioselectivity of toluene/o-xylene monooxygenase from Pseudomonas sp. strain OX1. Appl. Environ. Microbiol. 75:823-836.
38. Notomista, E., A. Lahm, A. Di Donato, and A. Tramontano. 2003. Evolution of bacterial and archaeal multicomponent monooxygenases. J. Mol. Evol. 56:435-445.
39. Owen, R. W., et al. 2000. Olive-oil consumption and health: the possible role of antioxidants. Lancet Oncol. 1:107-112.
40. Parales, R. E., N. C. Bruce, A. Schmid, and L. P. Wackett. 2002. Biodegradation, biotransformation, and biocatalysis (b3). Appl. Environ. Microbiol. 68:4699-4709.
41. Park, J., et al. 2007. The analysis and application of a recombinant monooxygenase library as a biocatalyst for the Baeyer-Villiger reaction. J. Microbiol. Biotechnol. 17:1083-1089.
42. Petroni, A., et al. 1995. Inhibition of platelet aggregation and eicosanoid production by phenolic components of olive oil. Thromb. Res. 78:151-160.
43. Rietjens, S. J., A. Bast, and G. R. Haenen. 2007. New insights into controversies on the antioxidant potential of the olive oil antioxidant hydroxytyrosol. J. Agric. Food Chem. 55:7609-7614.
44. 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.
45. 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.
46. Sazinsky, M. H., and S. J. Lippard. 2006. Correlating structure with function in bacterial multicomponent monooxygenases and related diiron proteins. Acc. Chem. Res. 39:558-566.
47. Singleton, V. L., R. Orthofer, and R. M. Lamuela-Raventoś. 1999. Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin-Ciocalteu reagent. Methods Enzymol. 299:152-178.
48. Straathof, A. J., S. Panke, and A. Schmid. 2002. The production of fine chemicals by biotransformations. Curr. Opin. Biotechnol. 13:548-556.
49. 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-methoxycatechol, methoxyhydroquinone, and methylhydroquinone. J. Bacteriol. 186: 4705-4713.
50. Torres Pazmino, D. E., M. Winkler, A. Glieder, and M. W. Fraaije. 2010. Monooxygenases as biocatalysts: classification, mechanistic aspects and biotechnological applications. J. Biotechnol. 146:9-24.
51. Vardar, G., Y. Tao, J. Lee, and T. K. Wood. 2005. Alanine 101 and alanine 110 of the alpha subunit of Pseudomonas stutzeri OX1 toluene-o-xylene monooxygenase influence the regiospecific oxidation of aromatics. Biotechnol. Bioeng. 92:652-658.
52. Vardar, G., and T. K. Wood. 2005. Protein engineering of toluene-o-xylene monooxygenase from Pseudomonas stutzeri OX1 for enhanced chlorinated ethene degradation and o-xylene oxidation. Appl. Microbiol. Biotechnol. 68:510-517.
53. Viggiani, A., et al. 2004. The role of the conserved residues His-246, His-199, and Tyr-255 in the catalysis of catechol 2,3-dioxygenase from Pseudomonas stutzeri OX1. J. Biol. Chem. 279:48630-48639.
54. Visioli, F., A. Poli, and C. Gall. 2002. Antioxidant and other biological activities of phenols from olives and olive oil. Med. Res. Rev. 22:65-75.
55. Watanabe, K., H. Futamata, and S. Harayama. 2002. Understanding the diversity in catabolic potential of microorganisms for the development of bioremediation strategies. Antonie Van Leeuwenhoek 81:655-663.
56. Waterman, E., and B. Lockwood. 2007. Active components and clinical applications of olive oil. Altern. Med. Rev. 12:331-342.