Characterization of a C-C bond hydrolase from Sphingomonas wittichii RW1 with novel specificities towards polychlorinated biphenyl metabolites

Journal of Bacteriology

Volumn 189, Issue 11, 2007, Pages 4038-4045

  Seah, Stephen Y K ^a,b,c   Ke, Jiyuan ^d   Denis, Geoffroy ^a   Horsman, Geoff P ^b   Fortin, Pascal D ^b,e   Whiting, Cheryl J ^b   Eltis, Lindsay D ^a,b  

^a UNIVERSITÉ LAVAL   (Canada)

^b UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^c UNIVERSITY OF GUELPH   (Canada)

^d UNIVERSITY OF KENTUCKY   (United States)

^e HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

2 HYDROXY 6 OXO 6 PHENYLHEXA 2,4 DIENOATE; ALKADIENE; CARBON; HYDROLASE; HYDROXYL GROUP; PHENYLALANINE; POLYCHLORINATED BIPHENYL; POLYCHLORINATED DIBENZODIOXIN; POLYCHLORINATED DIBENZOFURAN; TRYPTOPHAN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL GENE; BURKHOLDERIA; BURKHOLDERIA XENOVORANS; CATALYSIS; CHEMICAL BOND; DXNB2 GENE; ENZYME ANALYSIS; ENZYME SPECIFICITY; GENE AMPLIFICATION; HYDROLYSIS; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; RHODOCOCCUS; RHODOCOCCUS GLOBERULUS; SEQUENCE ALIGNMENT; SEQUENCE ANALYSIS; SPHINGOMONAS; SPHINGOMONAS WITTICHII RW1;

AMINO ACID SEQUENCE; BACTERIAL PROTEINS; BENZOFURANS; CLONING, MOLECULAR; DIOXINS; DNA, BACTERIAL; FATTY ACIDS, UNSATURATED; HYDROLASES; KINETICS; MOLECULAR SEQUENCE DATA; PHYLOGENY; POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, DNA; SEQUENCE HOMOLOGY, AMINO ACID; SPHINGOMONAS; SUBSTRATE SPECIFICITY;

BURKHOLDERIA XENOVORANS; RHODOCOCCUS GLOBERULUS; SPHINGOMONAS WITTICHII;

EID: 34249790861     PISSN: 00219193     EISSN: None     Source Type: Journal    
DOI: 10.1128/JB.01950-06     Document Type: Article

References (38)

1. Arfmann, H. A., K. N. Timmis, and R. M. Wittich. 1997. Mineralization of 4-chlorodibenzofuran by a consortium consisting of Sphingomonas sp. strain RW1 and Burkholderia sp. strain JWS. Appl. Environ. Microbiol. 63:3458-3462.
2. Armengaud, J., B. Happe, and K. N. Timmis. 1998. Genetic analysis of dioxin dioxygenase of Sphingomonas sp. strain RW1: catabolic genes dispersed on the genome. J. Bacteriol. 180:3954-3966.
3. Armengaud, J., K. N. Timmis, and R.-M. Wittich. 1999. A functional 4-hydroxysalicylate/hydroxyquinol degradative pathway gene cluster is linked to the initial dibenzo-p-dioxin pathway genes in Sphingomonas sp. strain RW1. J. Bacteriol. 181:3452-3461.
4. 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.
5. Bünz, P. V., R. Falchetto, and A. M. Cook. 1993. Purification of two isofunctional hydrolases (EC 3.7.1.8) in the degradative pathway for dibenzofuran in Sphingomonas sp. strain RW1. Biodegradation 4:171-178.
6. Cornish-Bowden, A. 1995. Analysis of enzyme kinetic data. Oxford University Press, New York, NY.
7. Dente, L., and R. Cortese. 1987. pEMBL: a new family of single-stranded plasmids for sequencing DNA. Methods Enzymol. 155:111-119.
8. Dunn, G., M. G. Montgomery, F. Mohammed, A. Coker, J. B. Cooper, T. Robertson, J. L. Garcia, T. D. H. Bugg, and S. P. Wood. 2005. The structure of the C-C bond hydrolase MhpC provides insights into its catalytic mechanism. J. Mol. Biol. 346:253-265.
9. Felsenstein, J. 2006. PHYLIP (Phylogeny Inference Package), version 3.66. Department of Genome Sciences, University of Washington, Seattle.
10. Fleming, S. M., T. A. Robertson, G. J. Langley, and T. D. H. Bugg. 2000. Catalytic mechanism of a C-C hydrolase enzyme: evidence for a gem-diol intermediate, not an acyl enzyme. Biochemistry 39:1522-1531.
11. Focht, D. D. 1995. Strategies for the improvement of aerobic metabolism of polychlorinated-biphenyls. Curr. Opin. Biotechnol. 6:341-346.
12. Furukawa, K., J. Hirose, A. Suyama, T. Zaiki, and S. Hayashida. 1993. Gene components responsible for discrete substrate specificity in the metabolism of biphenyl (bph operon) and toluene (tod operon). J. Bacteriol. 175:5224-5232.
13. Furukawa, K., N. Tomizuka, and A. Kamibayashi. 1979. Effect of chlorine substitution on the bacterial metabolism of various polychlorinated biphenyls. Appl. Environ. Microbiol. 38:301-310.
14. Fushinobu, S., T. Saku, M. Hidaka, S. Y. Jun, H. Nojiri, H. Yamane, H. Shoun, T. Omori, and T. Wakagi. 2002. Crystal structures of a meta-cleavage product hydrolase from Pseudomonas fluorescens IP01 (CumD) complexed with cleavage products. Protein Sci. 11:2184-2195.
15. Habe, H., K. Morii, S. Fushinobu, J. W. Nam, Y. Ayabe, T. Yoshida, T. Wakagi, H. Yamane, H. Nojiri, and T. Omori. 2003. Crystal structure of a histidine-tagged serine hydrolase involved in the carbazole degradation (CarC enzyme). Biochem. Biophys. Res. Commun. 303:631-639.
16. Hernáez, M. J., E. Andujar, J. L. Rios, S. R. Kaschabek, W. Reineke, and E. Santero. 2000. Identification of a serine hydrolase which cleaves the alicyclic ring of tetralin. J. Bacteriol. 182:5448-5453.
17. Hickey, W. J., G. Sabat, A. S. Yuroff, A. R. Arment, and J. Perez-Lesher. 2001. Cloning, nucleotide sequencing, and functional analysis of a novel, mobile cluster of biodegradation genes from Pseudomonas aeruginosa strain JB2. Appl. Environ. Microbiol. 67:4603-4609.
18. Hong, H. B., Y. S. Chang, I. H. Nam, P. Fortnagel, and S. Schmidt. 2002. Biotransformation of 2,7-dichloro- and 1,2,3,4-tetrachlorodibenzo- p-dioxin by Sphingomonas wittichii RW1. Appl. Environ. Microbiol. 68:2584-2588.
19. Horsman, G. P., J. Ke, S. Dai, S. Y. K. Seah, J. T. Bolin, and L. D. Eltis. 2006. Kinetic and structural insight into the mechanism of BphD, a C-C bond hydrolase from the biphenyl degradation pathway. Biochemistry 45:11071-11086.
20. Jones, T. A., J. Y. Zou, S. W. Cowan, and M. Kjeldgaard. 1991. Improved methods for building protein models in electron density maps and the location of errors in these models. Acta Crystallogr. A 47:110-119.
21. Kleywegt, G. J., and T. A. Jones. 1997. Detecting folding motifs and similarities in protein structures. Methods Enzymol. 277:525-545.
22. Kohler, H. P. E., A. Schmid, and M. Vandermaarel. 1993. Metabolism of 2,2′-dihydroxybiphenyl by Pseudomonas sp. strain Hbp1: production and consumption of 2,2′,3-trihydroxybiphenyl. J. Bacteriol. 175:1621-1628.
23. Lam, W. W. Y., and T. D. H. Bugg. 1997. Purification, characterization, and stereochemical analysis of a C-C hydrolase: 2-hydroxy-6-keto-nona-2,4-diene-1,9-dioic acid 5,6-hydrolase. Biochemistry 36:12242-12251.
24. Li, C., M. G. Montgomery, F. Mohammed, J. J. Li, S. P. Wood, and T. D. H. Bugg. 2005. Catalytic mechanism of C-C hydrolase MhpC from Escherichia coli: kinetic analysis of His263 and Ser110 site-directed mutants. J. Mol. Biol. 346:241-251.
25. Li, J. J., C. Li, C. A. Blindauer, and T. D. H. Bugg. 2006. Evidence for a gem-diol reaction intermediate in bacterial C-C hydrolase enzymes BphD and MhpC from C-13 NMR spectroscopy. Biochemistry 45:12461-12469.
26. Mukerjee-Dhar, G., M. Shimura, D. Miyazawa, K. Kimbara, and T. Hatta. 2005. bph genes of the thermophilic PCB degrader, Bacillus sp. JF8: characterization of the divergent ring-hydroxylating dioxygenase and hydrolase genes upstream of the Mn-dependent BphC. Microbiology 151:4139-4151.
27. Nandhagopal, N., A. Yamada, T. Hatta, E. Masai, M. Fukuda, Y. Mitsui, and T. Senda. 2001. Crystal structure of 2-hydroxyl-6-oxo-6-phenylhexa-2,4- dienoic acid (HPDA) hydrolase (BphD enzyme) from the Rhodococcus sp. strain RHA1 of the PCB degradation pathway. J. Mol. Biol. 309:1139-1151.
28. Nerdinger, S., C. Kendall, R. Marchhart, P. Riebel, M. R. Johnson, C. F. Yin, L. D. Eltis, and V. Snieckus. 1999. Directed ortho metalation and Suzuki-Miyaura cross-coupling connections: regiospecific synthesis of all isomeric chlorodihydroxybiphenyls for microbial degradation studies of PCBs. Chem. Commun. 22:2259-2260.
29. Ollis, D. L., E. Cheah, M. Cygler, B. Dijkstra, F. Frolow, S. M. Franken, M. Harel, S. J. Remington, I. Silman, J. Schrag, J. L. Sussman, K. H. G. Verscheuren, and A. Goldman. 1992. The alpha/beta hydrolase fold. Protein Eng. 5:197-211.
30. Sambrook, J., E. F. Fritsch, and T. Maniatis. 1989. Molecular cloning: a laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, NY.
31. Seah, S. Y. K., G. Labbé, S. R. Kaschabek, F. Reifenrath, W. Reineke, and L. D. Eltis. 2001. Comparative specificities of two evolutionarily divergent hydrolases involved in microbial degradation of polychlorinated biphenyls. J. Bacteriol. 183:1511-1516.
32. Seah, S. Y. K., G. Labbé, S. Nerdinger, M. R. Johnson, V. Snieckus, and L. D. Eltis. 2000. Identification of a serine hydrolase as a key determinant in the microbial degradation of polychlorinated biphenyls. J. Biol. Chem. 275:15701-15708.
33. Seah, S. Y. K., G. Terracina, J. T. Bolin, P. Riebel, V. Snieckus, and L. D. Eltis. 1998. Purification and preliminary characterization of a serine hydrolase involved in the microbial degradation of polychlorinated biphenyls. J. Biol. Chem. 273:22943-22949.
34. Tabor, S., and C. C. Richardson. 1985. A bacteriophage T7 RNA polymerase/promoter system for controlled exclusive expression of specific genes. Proc. Natl. Acad. Sci. USA 82:1074-1078.
35. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins. 1997. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25:4876-4882.
36. Van der Geize, R., K. Yam, T. Heuser, M. H. Wilbrink, H. Hara, M. C. Anderton, E. Sim, L. Dijkhuizen, J. E. Davies, W. W. Mohn, and L. D. Eltis. 2007. A gene cluster encoding cholesterol catabolism in a soil actinomycete provides insight into Mycobacterium tuberculosis survival in macrophages. Proc. Natl. Acad. Sci. USA 104:1947-1952.
37. Wilkes, H., R. M. Wittich, K. N. Timmis, P. Fortnagel, and W. Francke. 1996. Degradation of chlorinated dibenzofurans and dibenzo-p-dioxins by Sphingomonas sp. strain RW1. Appl. Environ. Microbiol. 62:367-371.
38. Wittich, R. M., H. Wilkes, V. Sinnwell, W. Francke, and P. Fortnagel. 1992. Metabolism of dibenzo-p-dioxin by Sphingomonas sp. strain RW1. Appl. Environ. Microbiol. 58:1005-1010.