Aerobic metabolism of 4-hydroxybenzoic acid in Archaea via an unusual pathway involving an intramolecular migration (NIH shift)

Applied and Environmental Microbiology

Volumn 68, Issue 12, 2002, Pages 6246-6255

  Fairley, D J ^a   Boyd, D R ^a   Sharma, N D ^a   Allen, C C R ^a   Morgan, P ^b,c   Larkin, M J ^a  

^a QUEEN'S UNIVERSITY BELFAST   (United Kingdom)

^b AKZO NOBEL CENTRAL RESEARCH   (Netherlands)

^c ESI   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

CARBOXYLIC ACIDS; ENZYMES; GAS CHROMATOGRAPHY; GENES; GROWTH KINETICS; HYDROXYLATION; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY;

INTRAMOLECULAR MIGRATION;

METABOLISM;

4 HYDROXYBENZOIC ACID; CATECHOL; GENTISIC ACID; HYDROQUINONE; PROTOCATECHUIC ACID;

BACTERIUM;

AEROBIC METABOLISM; ARCHAEBACTERIUM; ARTICLE; GAS CHROMATOGRAPHY; HALOARCULA; HYDROXYLATION; MASS SPECTROMETRY; NONHUMAN; PROTON NUCLEAR MAGNETIC RESONANCE; STOICHIOMETRY;

ACTINOBACTERIA (CLASS); ARCHAEA; BACTERIA (MICROORGANISMS); HALOARCULA; HALOARCULA SP.; UNCULTURED ACTINOMYCETE;

EID: 0242585459     PISSN: 00992240     EISSN: None     Source Type: Journal    
DOI: 10.1128/AEM.68.12.6246-6255.2002     Document Type: Article

References (73)

1. Agarwal, S. K., D. R. Boyd, H. P. Porter, W. B. Jennings, S. J. Grossman, and D. M. Jerina. 1986. Arene oxides and trans-dihydrodiols of quinoline. Tetrahedron Lett. 27:4253-4256.
2. Altenschmidt, U., B. Oswald, and G. Fuchs. 1991. Purification and characterization of benzoate-coenzyme A ligase and 2-aminobenzoate-coenzyme A ligases from a denitrifying Pseudomonas sp. J. Bacteriol. 173:5494-5501.
3. Altenschmidt, U., B. Oswald, E. Steiner, H. Herrmann, and G. Fuchs. 1993. New aerobic benzoate oxidation pathway via benzoyl-coenzyme A and 3-hydroxybenzoyl-coenzyme A in a denitrifying Pseudomonas sp. J. Bacteriol. 175:4851-4858.
4. Anderson, J. J., and S. Dagley. 1980. Catabolism of aromatic acids in Trichosporon cutaneum. J. Bacteriol. 141:534-543.
5. Barns, S. M., C. F. Delwiche, J. D. Palmer, and N. R. Pace. 1996. Perspectives on Archaeal diversity, thermophily and monophyly from environmental rRNA sequences. Proc. Natl. Acad. Sci. USA 93:9188-9193.
6. Barr, S. A., N. Bowers, D. R. Boyd, N. D. Sharma, L. Hamilton, R. Austin, S. McMordie, and H. Dalton. 1998. The potential role of cis-dihydrodiol intermediates in bacterial aromatic hydroxylation and the NIH shift. J. Chem. Soc. Perkin 1 20:3443-3451.
7. Benitez, F. J., J. Beltran-Heredia, J. A. Peres, and J. R. Dominguez. 2000. Kinetics of p-hydroxybenzoic acid photodecomposition and ozonation in a batch reactor. J. Hazard. Mater. 73:161-178.
8. Bintrim, S. B., T. J. Donohue, J. Haldelsman, G. P. Roberts, and R. M. Goodman. 1997. Molecular phylogeny of Archaea from soil. Proc. Natl. Acad. Sci. USA 94:277-282,
9. Boyd, D. R., and G. A. Berchtold. 1979. Aromatization of arene 1,2-oxides. 1-carboxy- and 1-carboalkoxybenzene oxides. J. Am. Chem. Soc. 101:2470-2474.
10. Boyd, D. R., and N. D. Sharma. 1996. The changing face of arene oxide-oxepine chemistry. Chem. Soc. Rev. 25:289-296.
11. Boyd, D. R., J. T. G. Hamilton, N. D. Sharma, J. S. Harrison, W. C. McRoberts, and D. B. Harper. 2000. Isolation of stable benzene oxide from a fungal biotransformation and evidence for an 'NIH shift' of the carbomethoxy group during hydroxylation of methyl benzoates. Chem. Commun. 16:1481-1482.
12. Busch, F. R., and G. A. Berchold. 1985. Aromatization of benzamide 1,2-oxide and N,N-dimethylbenzamide 1,2-oxide. J. Org. Chem. 50:1590-1592.
13. Buswell, J. A., and J. S. Clark. 1976. Oxidation of aromatic acids by a facultative thermophilic Bacillus sp. J. Gen. Microbiol. 96:209-213.
14. Cain, R. B., R. F. Bilton, and J. A. Darrah. 1968. The metabolism of aromatic acids by microorganisms. Metabolic pathways in the fungi. Biochem. J. 108:797-828.
15. Cerniglia, C. E. 1992. Biodegradation of polycyclic aromatic hydrocarbons. Biodegradation 3:351-368.
16. Crawford, R. L. 1976. Pathways of 4-hydroxybenzoate degradation among species of Bacillus. J. Bacteriol. 127:204-210.
17. Dagli, D. J., R. A. Gorski, and J. Wemple. 1975. Synthesis and rearrangement of glycidic thiol esters; migratory aptitudes. J. Org. Chem. 40:1741-1745.
18. Daly, J., D. Jerina, and B. Witkop. 1968. Migration of deuterium during hydroxylation of aromatic substrates by liver microsomes. Arch. Biochem. Biophys. 128:517-527.
19. Daly, J. W., D. M. Jerina, and B. Witkop. 1972. Arene oxides and the NIH shift: the metabolism, toxicity and carcinogenicity of aromatic compounds. Experientia 28:1129-1264.
20. Danson, M. J., and D. W. Hough. 1997. The structural basis of protein halophilicity. Comp. Biochem. Physiol. A 117:307-312.
21. DeLong, E. F., K. Y. Wu, B. B. Prezelin, and R. V. M. Jovine. 1994. High abundance of Archaea in Antarctic marine picoplankton. Nature 371:695-697.
22. Di Gioia, D., L. Bertin, F. Fava, and L. Marchetti. 2001. Biodegradation of hydroxylated and methoxylated benzoic, phenylacetic and phenylpropionic acids present in olive mill wastewaters by two bacterial strains. Res. Microbiol. 152:83-93.
23. El-Said Mohamed, M., A. Zaar, C. Ebenau-Jehle, and G. Fuchs. 2001. Reinvestigation of a new type of aerobic benzoate metabolism in the proteobacterium Azoarcus evansii. J. Bacteriol. 183:1899-1908.
24. Emerson, D., S. Chauhan, P. Oriel, and J. A. Breznak. 1994. Haloferax sp. D1227, a halophilic archaeon capable of growth on aromatic compounds. Arch. Microbiol. 161:445-452.
25. Engelhardt, G., H. G. Rast, and P. R. Wallnöfer. 1979. Degradation of aromatic carboxylic acids by Nocardia spec. DSM 43251. FEMS Microbiol. Lett. 5:245-251.
26. Eppink, M. H. M., S. A. Boeren, J. Vervoort, and W. J. H. Vanberkel. 1997. Purification and properties of 4-hydroxybenzoate 1-hydroxylase (decarboxylating), a novel flavin adenine dinucleotide-dependent monooxygenase from Candida parapsilosis CBS604. J. Bacteriol. 179:6680-6687.
27. Feng, Y., H. E. Khoo, and C. L. Poh. 1999. Purification and characterization of gentisate 1,2-dioxygenases from Pseudomonas alcaligenes NCIB 9867 and Pseudomonas putida NCIB 9869. Appl. Environ. Microbiol. 65:946-950.
28. Fernandez, J., A. A. Dimarco, L. N. Ornston, and S. Harayama. 1995. Purification and characterization of Acinetobacter calcoaceticus 4-hydroxybenzoate 3-hydroxylase after its overexpression in Escherichia coli. J. Biochem. 117:1261-1266.
29. Fu, W. J., and P. Oriel. 1998. Gentisate 1,2-dioxygenase from Haloferax sp. D1227. Extremophiles 2:439-446.
30. Fu, W. J., and P. Oriel. 1999. Degradation of 3-phenylpropionic acid by Haloferax sp. D1227. Extremophiles 3:45-53.
31. Galinski, E. A. 1995. Osmoadaptation in bacteria. Adv. Microb. Physiol. 37:272-328.
32. Gevantman, L. H. 2000. Solubility of selected gases in water, p. 8-86. In D. R. Lide (ed.), CRC handbook of chemistry and physics, 80th ed. CRC Press, London, United Kingdom.
33. Glöckler, R., A. Tschech, and G. Fuchs. 1989. Reductive dehydroxylation of 4-hydroxybenzoyl-CoA to benzoyl-CoA in a denitrifying Pseudomonas species. FEBS. Lett. 251:237-240.
34. Grund, E., C. Knorr, and R. Eichenlaub. 1990. Catabolism of benzoate and monohydroxylated benzoates by Amycolatopsis and Streptomyces spp. Appl. Environ. Microbiol. 56:1459-1464.
35. Grund, E., and H. J. Kutzner. 1998. Utilisation of quinate and p-hydroxybenzoate by actinomycetes: key enzymes and taxonomic relevance. J. Basic Microbiol. 38:241-255.
36. Guroff, G., J. W. Daly, D. M. Jerina, J. Renson, B. Witkop, and S. Udenfriend. 1967. Hydroxylation-induced migration: the NIH shift. Science 157:1524-1530.
37. Hamilton, G. A. 1974. Chemical models and mechanisms for oxygenases, p. 405-452. In O. Hayaishi (ed.), Molecular mechanisms of oxygen activation. Academic Press, New York, N.Y.
38. Hammann, R., and H. J. Kutzner. 1998. Key enzymes for the degradation of benzoate, m- and p-hydroxybenzoate by some members of the order Actinomycetales. J. Basic Microbiol. 38:207-220.
39. Haribabu, B., A, V. Kamath, and C. S. Vaidyanathan. 1984. Degradation of substituted benzoic acids by a Micrococcus species. FEMS Microbiol. Lett. 21:197-200.
40. 2+ and mechanism of turnover. J. Biol. Chem. 265:22187-22196.
41. Harpel, M. R., and J. D. Lipscomb. 1990. Gentisate 1,2-dioxygenase from Pseudomonas acidovorans. Methods Enzymol. 188:101-107.
42. Harrison, J. 1999. Fungal oxidation of arene compounds. Ph.D. thesis. The Queen's University of Belfast, Belfast, Northern Ireland.
43. Hinrichs, K. U., J. M. Hayes, S. P. Sylva, P. G. Brewer, and E. F. DeLong. 1999. Methane-consuming archaebacteria in marine sediments. Nature 398:802-805.
44. Hough, D. W., and M. J. Danson. 1999. Extremozymes. Curr. Opin. Chem. Biol. 3:39-46.
45. Jerina, D. M., J. W. Daly, B. Witkop, P. Zaltzman-Nirenberg, and S. Udenfriend. 1968. The role of arene oxide-oxepin systems in the metabolism of aromatic substrates. III. Formation of 1,2-naphthalene oxide from naphthalene by liver microsomes. J. Am. Chem. Soc. 90:6525-6527.
46. Jerina, D. M., J. W. Daly, B. Witkop, P. Zaltzman-Nirenberg, and S. Udenfriend. 1970. 1,2-Naphthalene oxide as an intermediate in the microsomal hydroxylation of naphthalene. Biochemistry 9:147-155.
47. Jurgens, G., K. Lindström, and A. Saano. 1997. Novel group within the kingdom Crenarchaeota from boreal forest soil. Appl. Environ. Microbiol. 63:803-805.
48. Kasmi, A. E., R. Brachmann, G. Fuchs, and S. W. Ragsdale. 1995. Hydroxybenzoyl-CoA reductase: coupling kinetics and electrochemistry to derive enzyme mechanisms. Biochemistry 34:11668-11677.
49. Keenan, S. L., and P. J. Chapman. 1978. Carboxy-migration facilitated by bacterial hydroxylation of 4-hydroxybenzoate. J. Chem. Soc. Chem. Commun. 17:731-732.
50. Kiemer, P., B. Tshisuaka, S. Fetzner, and F. Lingens. 1996. Degradation of benzoate via benzoyl-coenzyme A and gentisate by Bacillus stearothermophilus PK1, and purification of gentisate 1,2-dioxygenase. Biol. Fertil. Soils 23:307-313.
51. Kushner, D. J. 1986. Molecular adaptation of enzymes, metabolic systems and transport systems in halophilic bacteria. FEMS Microbiol. Rev. 39:121-127.
52. Lipscomb, J. D., and A. M. Orville. 1992. Mechanistic aspects of dihydroxybenzoate dioxygenases, Met. Ions Biol. Syst. 28:243-298.
53. Madern, D., C. Ebel, and G. Zaccai. 2000. Halophilic adaptation of enzymes. Extremophiles 4:91-98.
54. Margesin, R., and F. Schinner. 2001. Potential of halotolerant and halophilic microorganisms for biotechnology. Extremophiles 5:73-83.
55. Middlehoven, W. J., A. Coenen, B. Kraakman, and M. D. Sollewijn Gelpke. 1992. Degradation of some phenols and hydroxybenzoates by the imperfect ascomycetous yeasts Candida parapsolisis and Arxula adeninivorans: evidence for an operative gentisate pathway. Antonie Leeuwenhoek 62:181-187.
56. Middlehoven, W. J. 1993, Catabolism of benzene compounds by ascomycetous and basidiomycetous yeasts and yeastlike fungi. Antonie Leeuwenhoek 63:125-144.
57. Nasir, M. S., B. I. Cohen, and K. D. Karlin. 1992. Mechanism of aromatic hydroxylation in a copper monooxygenase model system-1,2-methyl migrations and the NIH shift in copper chemistry. J. Am. Chem. Soc. 114:2482-2494.
58. Neidle, E. L., C. Hartnett, L. N. Ornston, A. Bairoch, M. Rekik, and S. Harayama. 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.
59. Niemetz, R., U. Altenschmidt, S. Brucker, and G. Fuchs. 1995. Benzoyl-CoA 3-monooxygenase, a flavin-dependent hydroxylase: purification, some properties and its role in aerobic benzoate metabolism via gentisate in a denitrifying bacterium. Eur. J. Biochem. 227:161-168.
60. Seibold, B., M. Matthes, M. H. Eppink, F. Lingens, W. J. H. Vanberkel, and R. Müller. 1996. 4-hydroxybenzoate hydroxylase from Pseudomonas sp. CBS3 - purification, characterization, gene cloning, sequence analysis and assignment of structural features determining the coenzyme specificity. Eur. J. Biochem. 239:469-478.
61. Sprecher, M., M. J. Clark, and D. B. Sprinson. 1966. The absolute configuration of methylmalonyl coenzyme A and stereochemistry of the methylmalonyl coenzyme A mutase reaction. J. Biol. Chem. 241:872-877.
62. Sterjiades, R. 1993. Properties of NADH/NADPH-dependent p-hydroxybenzoate hydroxylase from Moraxella sp. Biotechnol. Appl. Biochem. 17:77-90.
63. Suemori, A., R. Kurane, and N. Tomizuka. 1993. Purification and properties of gentisate 1,2-dioxygenase from Rhodococcus erythropolis S-1. Biosci. Biotechnol. Biochem. 57:1781-1783.
64. Suemori, A., K. Nakajima, R. Kurane, and Y. Nakamura. 1995. o-, m- and p-hydroxybenzoate degradative pathways in Rhodococcus erythropolis. FEMS Microbiol. Lett. 125:31-36.
65. Sutherland, J. B., F. Rafii, A. A. Khan, and C. E. Cerniglia. 1995, Mechanisms of polycyclic aromatic hydrocarbon degradation, p. 269-306. In L. Y. Young and C. E. Cerniglia (ed.), Microbial transformation and degradation of toxic organic chemicals. Wiley-Liss, New York, N.Y.
66. Sze, I. S., and S. Dagley, 1984. Properties of salicylate hydroxylase and hydroxyquinol 1,2-dioxygenase purified from Trichosporon cutaneum. J. Bacteriol. 159:353-359.
67. Tindall, B. J. 1992. The family Halobacteriaceae, p. 768-808. In A. Balows, H. G. Trüper, M. Dworkin, W. Harder, and K. H. Schleifer (ed.), The prokaryotes, 2nd ed., volume 1. Springer Verlag, New York, N.Y.
68. Vanberkel, W. J. H., H. M. Eppink, W. J. Middelhoven, J. Vervoort, and I. M. C. M. Rietjens. 1994, Catabolism of 4-hydroxybenzoate in Candida parapsilosis proceeds through initial oxidative decarboxylation by a FAD-dependent 4-hydroxybenzoate 1-hydroxylase. FEMS Microbiol. Lett. 121:207-215.
69. Vannelli, T., and A. B. Hooper. 1995. NIH shift in the hydroxylation of aromatic-compounds by the ammonia-oxidizing bacterium Nitrosomonas europaea - evidence against an arene oxide intermediate. Biochemistry 34:11743-11749.
70. Ventosa, A., and J. J. Nieto. 1995. Biotechnological applications and potentialities of halophilic microorganisms. World J. Microbiol. Biotechnol, 11:85-94.
71. Yamaguchi, M., and H. Fujisawa. 1980. Purification and characterization of an oxygenase component in benzoate 1,2-dioxygenase system from Pseudomonas arvilla C-1. J. Biol. Chem. 255:5058-5063.
72. Yamaguchi, M., and H. Fujisawa. 1981. Reconstitution of iron-sulfur cluster of NADH-cytochrome C reductase, a component of benzoate 1,2-dioxygenase system from Pseudomonas arvilla C-1. J. Biol, Chem. 256:6783-6787.
73. Yamaguchi, M., and H. Fujisawa. 1982. Subunit structure of oxygenase component in benzoate-1,2-dioxygenase system from Pseudomonas arvilla C-1. J. Biol. Chem. 257:12497-12502.