1887

Abstract

SUMMARY:

The nucleotide sequence of the 3-chlorobenzoate 3,4-dioxygenase genes, designated ,from the transposon Tn5271 was determined. The function of the two sequenced open reading frames was evaluated by mutagenesis and expression to show that the and genes code for dioxygenase and reductase proteins, respectively. Comparison of the deduced amino acid sequences of the genes with sequences for other oxygenases revealed a clearly defined lineage among the class IA oxygenases that shows several unique features. This lineage includes phthalate 4,5-dioxygenase (), and based on the available NH-terminal sequence of component A, also includes 4-sulphobenzoate 3,4-dioxygenase. Vanillate demethylase, encoded by the genes and formally a monooxygenase enzyme catalysing an oxidative demethylation, is also included in this lineage. The terminal chlorobenzoate dioxygenase (CbaA) component is characterized by a conserved Rieske-type [2Fe-2S] ligand centre. The reductase component (CbaB) contains a plant-type ferredoxin [2Fe-2S],� FMN-isoalloxazine and NAD-ribose-binding domains and the orientation of these domains is conserved in all known class IA reductases. These results support the hypothesis that alternative fusions of the electron transfer modules of the reductases arose early in the divergence of oxygenase systems. The over-riding evolutionary constraint acting on the divergence of the class IA oxygenases would appear to be the requirement for a carboxyl group to the site of oxygen insertion into the aromatic ring.

Loading

Article metrics loading...

/content/journal/micro/10.1099/13500872-141-2-485
1995-02-01
2021-07-30
Loading full text...

Full text loading...

/deliver/fulltext/micro/141/2/mic-141-2-485.html?itemId=/content/journal/micro/10.1099/13500872-141-2-485&mimeType=html&fmt=ahah

References

  1. Altschul S. F., Gish W., Miller M., Myers E. W., Lipman D. J. 1990; Basic local alignment search tool. J Mol Biol 215:403–410
    [Google Scholar]
  2. Batie C. J., Ballou D. P., Correll C. J. 1991 Phthallate dioxygenase reductase and related flavin-iron-sulphur containing electron transferases. In: Chemistry and Biochemistry of Flavoenzymes pp 544–554 Edited by Müller F. Boca Raton: CRC Press;
    [Google Scholar]
  3. Brunel F., Davison J. 1988; Cloning and sequencing of Pseudomonas genes encoding vanillate demethylase. J Bacteriol 170:4924–4930
    [Google Scholar]
  4. Bünz P. V., Cook A. M. 1993; Dibenzofuran-4,4a-dioxygenase from Sphingomonas sp. strain RW1: angular dioxygenation by a three-component enzyme system. J Bacterial 175:6467–6475
    [Google Scholar]
  5. Chan T.-M., Hermodson M. A., Ulrich E. L., Markley J. L. 1983; Nuclear magnetic resonance studies of two-iron-two- sulphur ferredoxins. 2. Determination of the sequence of Anabaena variabilis ferredoxin II, assignment of aromatic resonances in proton spectra, and effects of chemical modifications. Biochemistry 22:5988–5995
    [Google Scholar]
  6. Correll C. C., Batie C. J., Ballou D. P., Ludwig M. L. 1992; Phthallate dioxygenase reductase: a modular structure for electron transfer from pyridine nucleotides to [2Fe–2S]. Science 258:1604–1610
    [Google Scholar]
  7. Devereux J., Haeberli P., Smithies O. 1984; A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res 12:387–395
    [Google Scholar]
  8. Erickson B. D., Mondello F. J. 1992; Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400. J Bacteriol 174:2903–2912
    [Google Scholar]
  9. Fetzner S., Müller R., Lingens F. 1992; Purification and some properties of 2-halobenzoate 1,2-dioxygenase, a two component enzyme system from Pseudomonas cepacia 2CBS. J Bacterial 174:279–290
    [Google Scholar]
  10. Frantz B., Chakrabarty A. M. 1986 Degradative plasmids in Pseudomonas . In: The Bacteria vol. 10 pp 295–323 Edited by Sokatch J. R. New York: Academic Press;
    [Google Scholar]
  11. Frantz B., Chakrabarty A. M. 1987; Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. Proc Natl Acad Sci USA 84:4460–4464
    [Google Scholar]
  12. Furukawa K., Hayase N., Kazunari T., Tomizuka N. 1989; Molecular relationship of chromosomal genes encoding biphenyl/ polychlorinated biphenyl catabolism: some soil bacteria possess a highly conserved bph operon. J Bacteriol 171:5467–5472
    [Google Scholar]
  13. Gibson D. T., Subramanian V. 1984 Microbial degradation of aromatic hydrocarbons. In: Microbial Degradation of Organic Compounds pp 181–252 Edited by Gibson D. T. New York: Marcel Dekker;
    [Google Scholar]
  14. Harayama S., Rekik M., Bairoch A., Neidle E. L., Ornston L. N. 1991; Potential DNA slippage structures acquired during evolutionary divergence of Acinetobacter calcoaceticus chromosomal benABC and Pseudomonas putida TOL pWW0 plasmid xylXYZ, genes encoding benzoate dioxygenases. J Bacteriol 173:7540–7548
    [Google Scholar]
  15. Harayama S., Kok M., Neidle E. L. 1992; Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601
    [Google Scholar]
  16. Hickey W. J., Focht D. D. 1990; Degradation of mono-, di- and trihalogenated benzoic acids by Pseudomonas aeruginosa JB2. Appl Environ Microbiol 56:3842–3850
    [Google Scholar]
  17. Irie S., Doi S., Yorifugi T., Takagi M., Yano K. 1987; Nucleotide sequencing and characterization of the genes encoding benzene oxidation enzymes of Pseudomonas putida . J Bacterial 169:5174–5179
    [Google Scholar]
  18. Johnston H. W., Briggs G. G., Alexander M. 1972; Metabolism of 3-chlorobenzoic acid by a pseudomonad. Soil Biol Biochem 4:187–190
    [Google Scholar]
  19. Kurkela S., Lehvaeslaiho H., Palva E. T., Teeri T. H. 1988; Cloning, nucleotide sequence and characterization of genes encoding naphthalene dioxygenase of Pseudomonas putida strain NCIB9816. Gene 73:355–362
    [Google Scholar]
  20. Lange C. C., Edwards A. R., Orser C. S. 1994; Identification of two new genetic loci, pcpD and pcpR, involved in pentachlorophenol degradation by Flavobacterium sp. strain ATCC 39723. Abstracts of the American Society for Microbiology Annual Meeting Las Vegas, NV, USA: Q-414: p 461
    [Google Scholar]
  21. Locher H. H., Leisinger T., Cook A. M. 1991; 4-Sulpho-benzoate-3,4-dioxygenase. Purification and properties of a desul-phonative two-component enzyme system from Comamonas testosteroni T-2. Biochem J 274:833–842
    [Google Scholar]
  22. Markus A., Krekel D., Lingens F. 1986; Purification and some properties of component A of the 4-chlorophenylacetate-3,4-dioxygenase from Pseudomonas species strain CBS. J Biol Chem 261:12883–12888
    [Google Scholar]
  23. Mason J. R., Cammack R. 1992; The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu Rev Microbiol 46:277–305
    [Google Scholar]
  24. van der Meer J. R., Eggen R. I. L., Zehnder A. J. B., de Vos W. M. 1991; Sequence analysis of the Pseudomonas sp. strain P51 tcb gene cluster, which encodes metabolism of chlorinated catechols: evidence for specialization of catechol-1,2-dioxygenases for chlorinated substrates. J Bacterial 173:2425–2434
    [Google Scholar]
  25. van der Meer J. R., de Vos W. M., Harayama S., Zehnder A. J. B. 1992; Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol Rev 56:677–694
    [Google Scholar]
  26. Morrice N., Geary P., Cammack R., Harris A., Beg F., Aitken A. 1988; Primary structure of protein B from Pseudomonas putida, member of a new class of 2Fe–2S ferredoxins. FEBS Lett 231:336–340
    [Google Scholar]
  27. Nakatsu C. H., Wyndham R. C. 1993; Cloning and expression of the transposable chlorobenzoate-3,4-dioxygenase genes of Alcaligenes sp. BR60. Appl Environ Microbiol 59:3625–3633
    [Google Scholar]
  28. Nakatsu C., Ng J., Singh R., Straus N., Wyndham C. 1991; Chlorobenzoate catabolic transposon Tn5271 is a composite class I element with flanking class II insertion sequences. Proc Natl Acad Sci USA 88:8312–8316
    [Google Scholar]
  29. Neidle E. L., Hartnett C., Bonitz S., Ornston L. N. 1988; DNA sequence of the Acinetobacter calcoaceticus catechol 1,2-dioxygenase I structural gene catA: evidence for evolutionary divergence of intradiol dioxygenases by acquisition of DNA sequence repetitions. J Bacterial 170:4874–4880
    [Google Scholar]
  30. Neidle E. L., Hartnett C., Ornston L. N., Bairoch A., Rekik M., Harayama S. 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
    [Google Scholar]
  31. Nomura Y., Nakagawa M., Ogawa N., Harashima S., Oshima Y. 1992; Genes in PHT plasmid encoding the initial degradation pathway of phthalate in Pseudomonas putida . J Ferment Bioeng 74:333–344
    [Google Scholar]
  32. Orser C. S., Lange C. C., Xun L., Zahrt T. C., Schneider B. J. 1993; Cloning, sequence analysis, and expression of the Flavo- bacterium pentachlorophenol-4-monooxygenase gene in Escherichia coli . J Bacterial 175:411–416
    [Google Scholar]
  33. Otaka E., Ooi T. 1989; Examination of protein sequence homologies. V. New perspectives on evolution between bacterial and chloroplast-type ferredoxins inferred from sequence evidence. J Mol Evol 29:246–254
    [Google Scholar]
  34. Reineke W., Knackmuss H.-J. 1988; Microbial degradation of haloaromatics. Annu Rev Microbiol 42:263–287
    [Google Scholar]
  35. Romanov V., Hausinger R. P. 1994; Pseudomonas aeruginosa 142 uses a three-component ortbo-halobenzoate- 1,2-dioxygenase for metabolism of 2,4-dichloro- and 2-chlorobenzoate. J Bacteriol 176:3368–3374
    [Google Scholar]
  36. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
    [Google Scholar]
  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
    [Google Scholar]
  38. Sayler G. S., Hooper S. W., Layton A. C., Henry King J. M. 1990; Catabolic plasmids of environmental and ecological significance. Microb Ecol 19:1–20
    [Google Scholar]
  39. Scholten J. D., Chang K. H., Babbitt P. C., Charest H., Sylvestre M., Dunaway-Mariano D. 1991; Novel enzymic hydrolytic dehalogenation of a chlorinated aromatic. Science 253:182–185
    [Google Scholar]
  40. Schweizer D., Markus A., Seez M., Ruf H. H., Lingens F. 1987; Purification and some properties of component B of the 4-chlorophenylacetate-3,4-dioxygenase from Pseudomonas species strain CBS3. J Biol Chem 262:9340–9346
    [Google Scholar]
  41. Suzuki M., Hayakawa T., Shaw J. P., Rekik M., Harayama S. 1991; Primary structure of xylene monooxygenase: similarities to and differences from the alkane hydroxylation system. J Bacteriol TVS1690–1695
    [Google Scholar]
  42. Wackett L. P., Kwart L. D., Gibson D. T. 1988; Benzylic monooxygenation catalyzed by toluene dioxygenase from Pseudomonas putida . Biochemistry 27:1360–1367
    [Google Scholar]
  43. Wende P., Bernhardt F.-H., Pfleger K. 1989; Substrate-modulated reactions of putidamonooxin: the nature of the active oxygen species formed, and its reaction mechanism. Eur J Biochem 181:189–197
    [Google Scholar]
  44. West S. E. H., Iglewski B. H. 1988; Codon usage in Pseudomonas aeruginosa . Nucleic Acids Res 16:9323–9335
    [Google Scholar]
  45. Willems A., DeLey J., Gillis M., Kersters K. 1991; Comamon- adaceae, a new family encompassing the Acidovorans rRNA complex, including Variovorax paradoxus gen. nov., comb. nov., for Alcaligenes paradoxus (Davis 1969). Int J Syst Bacteriol 41:445–450
    [Google Scholar]
  46. Wyndham R. C., Straus N. A. 1988; Chlorobenzoate catabolism and interaction between Alcaligenes and Pseudomonas species from Bloody Run Creek. Arch Microbiol 150:230–236
    [Google Scholar]
  47. Wyndham R. C., Singh R. K., Straus N. A. 1988; Catabolic instability, plasmid gene deletion and recombination in Alcaligenes sp. BR60. Arch Microbiol 150:237–243
    [Google Scholar]
  48. Wyndham R. C., Cashore A., Nakatsu C., Peel M. 1994; Catabolic transposons. Biodegradation 5:323–342
    [Google Scholar]
  49. Yamaguchi M., Fujisawa H. 1982; Subunit structure of oxygenase component in benzoate-1,2-dioxygenase system from Pseudomonas arvilla C-l. J Biol Chem 257:12497–12502
    [Google Scholar]
  50. Yanisch-Perron C., Vieira J., Messing J. 1985; Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mpl8 and pU19 vectors. Gene 33:103–119
    [Google Scholar]
  51. Zylstra G. J., Gibson D. T. 1989; Toluene degradation by Pseudomonas putida Fl: nucleotide sequence of the todC1C2BADE genes and their expression in E. coli . J Biol Chem 264:14940–14946
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/13500872-141-2-485
Loading
/content/journal/micro/10.1099/13500872-141-2-485
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error