4-Hydroxybenzoate hydroxylase from Pseudomonas sp. CBS3 - Purification, characterization, gene cloning, sequence analysis and assignment of structural features determining the coenzyme specificity

European Journal of Biochemistry

Volumn 239, Issue 2, 1996, Pages 469-478

  Seibold, Birgit ^a   Matthes, Martina ^b   Eppink, Michel H M ^c   Lingens, Franz ^a   Van Berkel, Willem J H ^c   Müller, Rudolf ^b  

^a UNIVERSITY OF HOHENHEIM   (Germany)

^b HAMBURG UNIVERSITY OF TECHNOLOGY   (Germany)

^c WAGENINGEN UNIVERSITY   (Netherlands)

Author keywords

Cloning; Coenzyme specificity; Flavoprotein hydroxylase; Haloaromatic biodegradation; Sequence alignment

Indexed keywords

4 HYDROXYBENZOIC ACID; OXYGENASE; UNSPECIFIC MONOOXYGENASE;

ARTICLE; COENZYME; ENZYME ANALYSIS; ENZYME ISOLATION; ENZYME PURIFICATION; ENZYME SPECIFICITY; ENZYME STRUCTURE; MOLECULAR CLONING; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PSEUDOMONAS; SEQUENCE ANALYSIS;

ESCHERICHIA COLI; PSEUDOMONAS; PSEUDOMONAS FLUORESCENS; PSEUDOMONAS SP.;

EID: 0030039134     PISSN: 00142956     EISSN: None     Source Type: Journal    
DOI: 10.1111/j.1432-1033.1996.0469u.x     Document Type: Article

References (64)

1. Arnow, L. E. (1937) Colorimetric determination of the components of 3,4-dihydroxyphenylalanine-tyrosine mixtures, J. Biol. Chem. 118, 531-537.
2. Babbitt, P. C., Kenyon, G. L., Martin, B. M., Charest, H., Sylvestre, M., Scholten, J. D., Chang, K.-H., Liang, P.-H. & Dunaway-Mariano, D. (1992) Ancestry of 4-chlorobenzoate dehalogenase: analysis of the amino acid sequence identities among families of acyl:adenyl ligases, enoyl-CoA hydratases/isomerases, and acyl-CoA thioesterases, Biochemistry 31, 5594-5604.
3. Birnboim, H. C. & Doly, J. (1979) A rapid alkaline extraction procedure for screening recombinant plasmid DNA, Nucleic Acids Res. 7, 1513-1523.
4. Chang, K. H., Liang, P.-H., Beck, W., Scholten, J. D. & Dunaway-Mariano, D. (1992) Isolation and characterization of the three polypeptide components of 4-chlorobenzoate dehalogenase from Pseudomonas sp. strain CBS-3, Biochemistry 31, 5605-5610.
5. Clewell, D. B. & Helinski, D. R. (1969) Supercoiled circular DNA-protein complex in E. coli: purification and induced conversion to an open circular form, Proc. Natl Acad. Sci. USA 62, 1159-1166.
6. DiMarco, A. A., Averhoff, B. A., Kim, E. E. & Ornston, L. N. (1993) Evolutionary divergence of pobA, the structural gene encoding p-hydroxybenzoate hydroxylase in an Acinetobacter calcoaceticus strain well suited for genetic analysis, Gene (Amst.) 125, 25-33.
7. Eggink, G., Engel, H., Vriend, G., Terpstra, P. & Witholt, B. (1990) Rubredoxin reductase of Pseudomonas oleovorans. Structural relationship to other flavoprotein oxidoreductases based on one NAD and two FAD fingerprints, J. Mol. Biol. 212, 135-142.
8. Elsner, A., Löffler, F., Miyashita, K., Müller, R. & Lingens, F. (1991a) Resolution of 4-chlorobenzoate dehalogenase from Pseudomonas sp. CBS3 into three components, Appl. Environ. Microbiol. 57, 324-326.
9. Elsner, A., Müller, R. & Lingens, F. (1991b) Separate cloning and expression analysis of two components of 4-chlorobenzoate dehalogenase from Pseudomonas sp. CBS3, J. Gen. Micobiol. 137, 477-481.
10. Entsch, B., Nan, Y., Weaich, K. & Scott, K. F. (1988) Sequence and organization of pobA, the gene coding for p-hydroxybenzoate hydroxylase, an inducible enzyme from Pseudomonas aeruginosa, Gene (Amst.) 71, 279-291.
11. Entsch, B., Palfey, B. A., Ballou, D. P. & Massey, V. (1991) Catalytic function of tyrosine residues in para-hydroxybenzoate hydroxylase as determined by the study of site-directed mutants, J. Biol. Chem. 260, 17341-17349.
12. Entsch, B. & van Berkel, W. J. H. (1995) Structure and mechanism of p-hydroxybenzoate hydroxylase, FASEB J. 9, 476-483.
13. Eppink, M. H. M., Schreuder, H. A. & van Berkel, W. J. H. (1995) Structure and function of mutant Arg44Lys of p-hydroxybenzoate hydroxylase, Eur. J. Biochem. 231, 157-165.
14. Eschrich, K., van der Bolt, F. J. T., de Kok, A. & van Berkel, W. J. H. (1993) Role of Tyr201 and Tyr385 in substrate activation by p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens, Eur. J. Biochem. 216, 137-146.
15. Eujii, T. & Kaneda, T. (1985) Purification and properties of NADH/ NADPH-dependent p-hydroxybenzoate hydroxylase from Cyclobacterium cyclohexanicum, Eur. J. Biochem. 147, 97-104.
16. Friedman, A. M., Long, S. R., Brown, S. E., Buikema, W. J. & Ausubel, F. M. (1982) Construction of a broad host range cosmid cloning vector and its use in the genetic analysis of Rhizobium mutants, Gene (Amst.) 18, 289-296.
17. Gatti, D. L., Palfey, B. A., Lah, M. S., Entsch, B., Massey, V., Ballou, D. P. & Ludwig, M. L. (1994) The mobile flavin of 4-OH benzoate hydroxylase, Science 266, 110-114.
18. Gatti, D. L., Entsch, B., Ballou, D. P. & Ludwig, M. L. (1996) pH-dependent structural changes in the active-site of p-hydroxybenzoate hydroxylase point to the importance of proton and water movements during catalysis, Biochemistry 35, 567-578.
19. Harayama, S., Kok, M. & Neidle, E. L. (1992) Functional and evolutionary relationships among diverse oxygenases, Annu. Rev. Microbiol. 46, 565-601.
20. Hartnett, C., Neidle, E. L., Ngai, K.-L., & Ornston, L. N. (1990) DNA sequences of genes encoding Acinetobacter calcoaceticus protocatechuate 3,4-dioxygenase: evidence indicating shuffling of genes and of DNA sequences within genes during their evolutionary divergence, J. Bacteriol. 172, 956-966.
21. Klages, U. & Lingens, F. (1980) Degradation of 4-chlorobenzoic acid by a Pseudomonas species, Zentralbl. Bakteriologie, Parasitenk., Deinfektionskr. Hyg. Abt. Orig. Reihe C 1, 215-223.
22. Kraulis, P. (1991) MOLSCRIPT: a program to produce both detailed and schematic plots of protein structure, J. Appl. Crystallogr. 24, 946-950.
23. Löffler, F., Lingens, F. & Müller, R. (1995) Dehalogenation of 4-chlorobenzoate: characterisation of 4-chlorobenzoyl-coenzyme A dehalogenase from Pseudomonas sp. CBS3. Biodegradation 6, 203-212.
24. Lowry, O. H., Rosebrough, N. J., Farr, A. L. & Randall, R. J. (1951) Protein measurement with the folin phenol reagent, J. Biol. Chem. 193, 265-275.
25. Lüthy, R., Bowie, J. U. & Eisenberg, D. (1992) Assessment of protein models with three-dimensional profiles, Nature 356, 83-85.
26. Mandel, M. & Higa, A. (1970) Calcium dependent bacteriophage DNA infection, J. Mol. Biol. 53, 159-162.
27. Manstein, D. J., Pai, E. F., Schopfer, L. M. & Massey, V. (1986) Absolute stereochemistry of flavins in enzyme-catalyzed reactions, Biochemistry 25, 6807-6816.
28. Marmur, J. (1961) A procedure for the isolation of deoxyribonucleic acid from microorganisms, J. Mol. Biol. 3, 208-218.
29. Müller, F., Voordouw, G., van Berkel, W. J. H., Steennis, P. J., Visser, S. & van Rooijen, P. (1979) A study of p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens: improved purification, relative molecular mass and amino acid composition, Eur. J. Biochem. 101, 235-244.
30. 18O] water into 4-hydroxybenzoic acid in the reaction of 4-chlorobenzoate dehalogenase from Pseudomonas sp. CBS3, Biochem. Biophys. Res. Commun. 124, 178-182.
31. Nakai, C., Kagamiyama, H. & Nozaki, M. (1983) Complete nucleotide sequence of the metapyrocatechase gene on the TOL plasmid of Pseudomonas putida mt-2, J. Biol. Chem. 258, 2923-2928.
32. Neidle, E. L., Hartnett, C., Ornston, L. N., Bairoch, A., Rekik, M. & Harayama, S. (1991) Nucleotide sequences of the Acinetobacter calcoaceticus ben ABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases, J. Bacteriol. 173, 5385-5395.
33. Peitsch, M. C. (1995) Protein modelling by E-mail, Biotechnology 13, 658-660.
34. Rosenberg, M. & Court, D. (1979) Regulatory sequences involved in the promotion and termination of RNA transcription, Annu. Rev. Genet. 13, 319-353.
35. Sambrook, J., Fritsch E. F. & Maniatis, T. (1989) Molecular cloning: a laboratory manual, 2nd edn, Cold Spring Harbor Laboratory, Cold Spring Harbor NY.
36. Sanger, F., Nicklen, S. & Coulsen, A. R. (1977) DNA sequencing with chain-terminating inhibitors, Proc. Natl Acad. Sci. USA 74, 5463-5467.
37. Savard, P., Peloquin, L. & Sylvestre, M. (1986) Cloning of Pseudomonas sp. strain CBS3 genes specifying dehalogenation of 4-chlorobenzoate, J. Bacteriol. 168, 81-85.
38. Schreuder, H. A., Prick, P., Wierenga, R. K., Vriend, G., Wilson, K. S., Hol, W. G. J. & Drenth, J. (1989) Crystal structure of the p-hydroxybenzoate hydroxylase-substrate complex refined at 1.9 Å resolution, J. Mol. Biol. 208, 679-696.
39. Schreuder, H. A., van der Laan, J. M., Hol, W. G. J. & Drenth, J. (1991) The structure of p-hydroxybenzoate hydroxylase, in Chemistry and biochemistry of flavoenzymes (Müller, F., ed.) vol. 2, pp. 31-64, CRC Press, Boca Raton FL.
40. Schreuder, H. A., Mattevi, A., Obmolova, G., Kalk, K. H., Hol, W. G. J., van der Bolt, F. J. T. & van Berkel, W. J. H. (1994) Crystal structures of wild-type p-hydroxybenzoate hydroxylase complexed with 4-aminobenzoate, 2,4-dihydroxybenzoate and 2-hydroxy-4-aminohenzoate and mutant Tyr222Ala. complexed with 2-hydroxy-4-aminobenzoate. Evidence for a proton channel and a new binding mode of the flavin ring, Biochemistry 33, 10161-10170.
41. Shine, J. & Dalgarno, L. (1974) The 3′-terminal sequence of Escherichia coli 16S ribosomal RNA: complementarity to nonsense triplets and ribosome binding sites, Proc. Natl Acad. Sci. USA 71, 1342-1346.
42. Shuman, B. & Dix, T. A. (1993) Cloning, nucleotide sequence, and expression of a p-hydroxybenzoate hydroxylase isozyme gene from Pseudomonas fluorescens, J. Biol. Chem. 268, 17057-17062.
43. Slater, J. H., Weightman, A. J. & Hall, B. G. (1985) Dehalogenase genes of Pseudomonas putida PP3 on chromosomally located transposable elements, Mol. Biol. Evol. 2, 557-567.
44. Steennis, P. J., Cordes, M. M., Hilkens, J. G. H. & Müller, F. (1973) On the interaction of p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens with halogen ions, FEBS Lett. 36, 177-179.
45. Sterjiades, R. (1993) Properties of NADH/NADPH-dependent p-hydroxybenzoate hydroxylase from Moraxella sp., Biotechnol. Appl. Biochem. 17, 77-90.
46. Suemori, A., Kurane, R. & Tomizuka, N. (1993) Purification and properties of 3 types of monohydroxybenzoate oxygenase from Rhodococcus erythropolis, Biosci. Biotech. Biochem. 57, 1487-1491.
47. van Berkel, W. J. H. & Müller, F. (1987) The elucidation of the microheterogeneity of highly purified p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens by various biochemical techniques, Eur. J. Biochem. 167, 35-46.
48. van Berkel, W. J. H., Müller, F., Jekel, P. A., Weijer, W. J., Schreuder, H. A. & Wierenga, R. K. (1988) Chemical modification of tyrosine-38 in p-hydroxybenzoate hydroxylase from Pseudomonas fluorescent by 5′-P-fluorosulfonylbenzoyladenosine: a probe for the elucidation of the NADPH binding site? Eur. J. Biochem. 176, 449-459.
49. van Berkel, W. J. H. & Müller, F. (1989) The temperature and pH dependence of some properties of p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens, Eur. J. Biochem. 179, 307-314.
50. van Berkel, W. J. H. & Müller, F. (1991) Flavin-dependent monooxygenases with special reference to p-hydroxybenzoate hydroxylase, in Chemistry and biochemistry of flavoenzymes (Müller, F., ed.) vol. 2, pp. 1-29, CRC Press, Boca Raton FL.
51. van Berkel, W. J. H., Westphal, A. H., Eschrich, K., Eppink, M. & de Kok, A. (1992) Substitution of Arg214 at the substrate-binding site of p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens, Eur. J. Biochem. 210, 411-419.
52. van Berkel, W. J. H., Eppink, M. H. M., Middelhoven, W. J., Vervoort, J. & Rietjens, I. M. C. M. (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, 207-216.
53. van der Bolt, F. J. T. Drijfhout, M. C., Eppink, M. H. M., Hagen, W. R. & van Berkel, W. J. H. (1994) Selective cysteine-serine replacements in p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens allow the unambiguous assignment of Cys211 as the site of modification by spin-labeled p-chloromercuribenzoate, Protein Eng. 7, 801-804.
54. van der Laan, J. M., Schreuder, H. A., Swarte, M. B. A., Wierenga, R. K., Kalk, K. H., Hol, W. G. J. & Drenth, J. (1989) The coenzyme analogue adenosine 5-diphosphoribose displaces FAD in the active site of p-hydroxybenzoate hydroxylase. An X-ray crystallographic investigation, Biochemistry 28, 7199-7205.
55. Webb, E. C. (1992) Oxidoreductases, in Enzyme nomenclature (Webb, E. C., ed.) pp. 133-141, Academic Press, San Diego.
56. Weijer, W. J., Hofsteenge, J., Vereijken, J., Jekel, P. A. & Beintema, J. J. (1982) Primary structure of p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens, Biochim. Biophys. Acta 704, 385-388.
57. Wierenga, R. K., de Jong, R. J., Kalk, K. H., Hol, W. G. J. & Drenth, J. (1979) Crystal structure of p-hydroxybenzoate hydroxylase, J. Mol. Biol. 131, 55-73.
58. Wierenga, R. K., Drenth, J. & Schulz, G. E. (1983) Comparison of the three-dimensional protein and nucleotide structure of the FAD-binding domain of p-hydroxybenzoate hydroxylase with the FAD- as well as NADPH-binding domains of glutathione reductase, J. Mol. Biol. 167, 725-739.
59. Wierenga, R. K., Terpstra, P. & Hol, W. G. J. (1986) Prediction of the occurence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint, J. Mol. Biol. 187, 101-107.
60. Wijnands, R. A., van der Zee, J., van Leeuwen, J. W., van Berkel, W. J. H. & Müller, F. (1984) The importance of monopole-monopole and monopole-dipole interactions on the binding of NADPH and NADPH analogues to p-hydroxybenzoate hydroxylase from Pseudomonas fluorescens, Eur. J. Biochem. 139, 637-644.
61. Woese, C. R. (1987) Bacterial evolution, Microbiol. Rev. 51, 221-271.
62. Wong, C. M., Dilworth, M. J. & Glenn, A. R. (1994) Cloning and sequencing show that 4-hydroxybenzoate hydroxylase (pobA) is required for uptake of 4-hydroxybenzoate in Rhizobium leguminosarum. Microbiology 140, 2775-2786.
63. Yanisch-Perron, C., Vieira, J. & Messing, J. (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors, Gene (Amst.) 33, 103-109.
64. You, I.-S., Ghosal, D. & Gunsalus, I. C. (1990) Nucleotide sequence analysis of the Pseudomonos putidu PpG7 salicylate hydroxylase gene (nahG) and its flanking region, Biochemistry 30, 1635-1641.