1887

Abstract

GJ31 has been reported to grow on chlorobenzene using a -cleavage pathway with chlorocatechol 2,3-dioxygenase (CbzE) as a key enzyme. The CbzE-encoding gene was found to be localized on the 180 kb plasmid pKW1 in a cluster, which is flanked by transposases and encodes only a partial (chloro)catechol -cleavage pathway comprising ferredoxin reductase, chlorocatechol 2,3-dioxygenase, an unknown protein, 2-hydroxymuconic semialdehyde dehydrogenase and glutathione -transferase. Downstream of are located , encoding a novel type of 2-hydroxypent-2,4-dienoate hydratase, and a transposon region highly similar to Tn. Upstream of , transfer genes were found. The search for gene clusters possibly completing the (chloro)catechol metabolic pathway of GJ31 revealed the presence of two additional catabolic gene clusters on pKW1. The cluster encodes enzymes for the dissimilation of 2,3-dihydroxyphenylpropionate in a novel arrangement characterized by the absence of a gene encoding 3-(3-hydroxyphenyl)propionate monooxygenase and the presence of a GntR-type regulator, whereas the cluster encodes part of the naphthalene metabolic pathway. Transcription studies supported their possible involvement in chlorobenzene degradation. The upper pathway cluster, comprising genes encoding a chlorobenzene dioxygenase and a chlorobenzene dihydrodiol dehydrogenase, was localized on the chromosome. A high level of transcription in response to chlorobenzene revealed it to be crucial for chlorobenzene degradation. The chlorobenzene degradation pathway in strain GJ31 is thus a mosaic encoded by four gene clusters.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032110-0
2009-12-01
2019-10-22
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/12/4069.html?itemId=/content/journal/micro/10.1099/mic.0.032110-0&mimeType=html&fmt=ahah

References

  1. Barnes, M. R., Duetz, W. A. & Williams, P. A. ( 1997; ). A 3-(3-hydroxyphenyl)propionic acid catabolic pathway in Rhodococcus globerulus PWD1: cloning and characterization of the hpp operon. J Bacteriol 179, 6145–6153.
    [Google Scholar]
  2. Bartels, F., Backhaus, S., Moore, E. R. B., Timmis, K. N. & Hofer, B. ( 1999; ). Occurrence and expression of glutathione-S-transferase-encoding bphK genes in Burkholderia sp. strain LB400 and other biphenyl-utilizing bacteria. Microbiology 145, 2821–2834.
    [Google Scholar]
  3. Beil, S., Happe, B., Timmis, K. N. & Pieper, D. H. ( 1997; ). Genetic and biochemical characterization of the broad-spectrum chlorobenzene dioxygenase from Burkholderia sp. strain PS12: dechlorination of 1,2,4,5-tetrachlorobenzene. Eur J Biochem 247, 190–199.[CrossRef]
    [Google Scholar]
  4. Beil, S., Mason, J. R., Timmis, K. N. & Pieper, D. H. ( 1998; ). Identification of chlorobenzene dioxygenase sequence elements involved in dechlorination of 1,2,4,5-tetrachlorobenzene. J Bacteriol 180, 5520–5528.
    [Google Scholar]
  5. Beil, S., Timmis, K. N. & Pieper, D. H. ( 1999; ). Genetic and biochemical analyses of the tec operon suggest a route for evolution of chlorobenzene degradation genes. J Bacteriol 181, 341–346.
    [Google Scholar]
  6. Bosch, R., Garcia-Valdes, E. & Moore, E. R. B. ( 2000; ). Complete nucleotide sequence and evolutionary significance of a chromosomally encoded naphthalene-degradation lower pathway from Pseudomonas stutzeri AN10. Gene 245, 65–74.[CrossRef]
    [Google Scholar]
  7. Bradford, M. M. ( 1976; ). A rapid and sensitive method for the quantitation of protein utilizing the principle of protein–dye binding. Anal Biochem 72, 248–254.[CrossRef]
    [Google Scholar]
  8. Bramucci, M., Chen, M. & Nagarajan, V. ( 2006; ). Genetic organization of a plasmid from an industrial wastewater bioreactor. Appl Microbiol Biotechnol 71, 67–74.[CrossRef]
    [Google Scholar]
  9. Bugg, T. D. H. ( 1993; ). Overproduction, purification and properties of 2,3-dihydroxyphenylpropionate 1,2-dioxygenase from Escherichia coli. Biochim Biophys Acta 1202, 258–264.[CrossRef]
    [Google Scholar]
  10. Collinsworth, W. L., Chapman, P. J. & Dagley, S. ( 1973; ). Stereospecific enzymes in the degradation of aromatic compounds by Pseudomonas putida. J Bacteriol 113, 922–931.
    [Google Scholar]
  11. Diaz, E., Ferrandez, A., Prieto, M. A. & Garcia, J. L. ( 2001; ). Biodegradation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev 65, 523–569.[CrossRef]
    [Google Scholar]
  12. Dorn, E. & Knackmuss, H.-J. ( 1978a; ). Chemical structure and biodegradability of halogenated aromatic compounds. Two catechol 1,2-dioxygenases from a 3-chlorobenzoate-grown pseudomonad. Biochem J 174, 73–84.
    [Google Scholar]
  13. Dorn, E. & Knackmuss, H.-J. ( 1978b; ). Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2-dioxygenation of catechol. Biochem J 174, 85–94.
    [Google Scholar]
  14. Eltis, L. D. & Bolin, J. T. ( 1996; ). Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178, 5930–5937.
    [Google Scholar]
  15. Ferrandez, A., Garcia, J. L. & Diaz, E. ( 1997; ). Genetic characterization and expression in heterologous hosts of the 3-(3-hydroxyphenyl)propionate catabolic pathway of Escherichia coli K-12. J Bacteriol 179, 2573–2581.
    [Google Scholar]
  16. Friemann, R., Lee, K., Brown, E. N., Gibson, D. T., Eklund, H. & Ramaswamy, S. ( 2009; ). Structures of the multicomponent Rieske non-heme iron toluene 2,3-dioxygenase enzyme system. Acta Crystallogr D Biol Crystallogr 65, 24–33.[CrossRef]
    [Google Scholar]
  17. Fukumori, F. & Saint, C. P. ( 2001; ). Complete nucleotide sequence of the catechol metabolic region of plasmid pTDN1. J Gen Appl Microbiol 47, 329–333.[CrossRef]
    [Google Scholar]
  18. Gibson, D. T. & Parales, R. E. ( 2000; ). Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11, 236–243.[CrossRef]
    [Google Scholar]
  19. Gibson, D. T., Koch, J. R., Schuld, C. L. & Kallio, R. E. ( 1968; ). Oxidative degradation of aromatic hydrocarbons by microorganisms. II. Metabolism of halogenated aromatic hydrocarbons. Biochemistry 7, 3795–3802.[CrossRef]
    [Google Scholar]
  20. Göbel, M., Kranz, O. H., Kaschabek, S. R., Schmidt, E., Pieper, D. H. & Reineke, W. ( 2004; ). Microorganisms degrading chlorobenzene via a meta-cleavage pathway harbor highly similar chlorocatechol 2,3-dioxygenase-encoding gene clusters. Arch Microbiol 182, 147–156.
    [Google Scholar]
  21. Gross, R., Guzman, C. A., Sebaihia, M., dos Santos, V. A., Pieper, D. H., Koebnik, R., Lechner, M., Bartels, D., Buhrmester, J. & other authors ( 2008; ). The missing link: Bordetella petrii is endowed with both the metabolic versatility of environmental bacteria and virulence traits of pathogenic Bordetellae. BMC Genomics 9, 449 [CrossRef]
    [Google Scholar]
  22. Hanahan, D. ( 1983; ). Studies on transformation of Escherichia coli with plasmids. J Mol Biol 166, 557–580.[CrossRef]
    [Google Scholar]
  23. Herrmann, H., Lauf, U. & Müller, C. ( 1998; ). The transposable elements resident on the plasmids of Pseudomonas putida strain H, Tn5501 and Tn5502, are cryptic transposons of the Tn3 family. Mol Gen Genet 259, 674–678.[CrossRef]
    [Google Scholar]
  24. Hülsmeyer, M., Hecht, H. J., Niefind, K., Hofer, B., Eltis, L. D., Timmis, K. N. & Schomburg, D. ( 1998; ). Crystal structure of cis-biphenyl-2,3-dihydrodiol-2,3-dehydrogenase from a PCB degrader at 2.0 Å resolution. Protein Sci 7, 1286–1293.[CrossRef]
    [Google Scholar]
  25. Junca, H. & Pieper, D. H. ( 2004; ). Functional gene diversity analysis in BTEX contaminated soils by means of PCR-SSCP DNA fingerprinting: comparative diversity assessment against bacterial isolates and PCR-DNA clone libraries. Environ Microbiol 6, 95–110.
    [Google Scholar]
  26. Kaschabek, S. R. & Reineke, W. ( 1992; ). Maleylacetate reductase of Pseudomonas sp. strain B13: dechlorination of chloromaleylacetates, metabolites in the degradation of chloroaromatic compounds. Arch Microbiol 158, 412–417.
    [Google Scholar]
  27. Kaschabek, S. R., Kasberg, T., Müller, D., Mars, A. E., Janssen, D. B. & Reineke, W. ( 1998; ). Degradation of chloroaromatics: purification and characterization of a novel type of chlorocatechol 2,3-dioxygenase of Pseudomonas putida GJ31. J Bacteriol 180, 296–302.
    [Google Scholar]
  28. Lau, P. C. K., Bergeron, H., Labbe, D., Wang, Y., Brousseau, R. & Gibson, D. T. ( 1994; ). Sequence and expression of the todGIH genes involved in the last three steps of toluene degradation by Pseudomonas putida F1. Gene 146, 7–13.[CrossRef]
    [Google Scholar]
  29. Lauf, U., Müller, C. & Herrmann, H. ( 1998; ). The transposable elements resident on the plasmids of Pseudomonas putida strain H, Tn5501 and Tn5502, are cryptic transposons of the Tn3 family. Mol Gen Genet 259, 674–678.[CrossRef]
    [Google Scholar]
  30. Mars, A. E., Kasberg, T., Kaschabek, S. R., van Agteren, M. H., Janssen, D. B. & Reineke, W. ( 1997; ). Microbial degradation of chloroaromatics: use of the meta-cleavage pathway for mineralization of chlorobenzene. J Bacteriol 179, 4530–4537.
    [Google Scholar]
  31. Mars, A. E., Kingma, J., Kaschabek, S. R., Reineke, W. & Janssen, D. B. ( 1999; ). Conversion of 3-chlorocatechol by various catechol 2,3-dioxygenases and sequence analysis of the chlorocatechol dioxygenase region of Pseudomonas putida GJ31. J Bacteriol 181, 1309–1318.
    [Google Scholar]
  32. Menn, F.-M., Zylstra, G. J. & Gibson, D. T. ( 1991; ). Location and sequence of the todF gene encoding 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase in Pseudomonas putida. Gene 104, 91–94.[CrossRef]
    [Google Scholar]
  33. Mosqueda, G., Ramos-Gonzalez, M. I. & Ramos, J. L. ( 1999; ). Toluene metabolism by the solvent-tolerant Pseudomonas putida DOT-T1 strain, and its role in solvent impermeabilization. Gene 232, 69–76.[CrossRef]
    [Google Scholar]
  34. Müller, T. A., Werlen, C., Spain, J. & van der Meer, J. R. ( 2003; ). Evolution of a chlorobenzene degradative pathway among bacteria in a contaminated groundwater mediated by a genomic island in Ralstonia. Environ Microbiol 5, 163–173.[CrossRef]
    [Google Scholar]
  35. Nozaki, M. ( 1970; ). Metapyrocatechase (Pseudomonas). Methods Enzymol 17A, 522–525.
    [Google Scholar]
  36. Oldenhuis, R., Kuijk, L., Lammers, A., Janssen, D. B. & Witholt, B. ( 1989; ). Degradation of chlorinated and non-chlorinated aromatic solvents in soil suspension by pure bacterial cultures. Appl Microbiol Biotechnol 30, 211–217.
    [Google Scholar]
  37. Olivera, E. R., Minambres, B., Garcia, B., Muniz, C., Moreno, M. A., Ferrandez, A., Diaz, E., Garcia, J. L. & Luengo, J. M. ( 1998; ). Molecular characterization of the phenylacetic acid catabolic pathway in Pseudomonas putida U: the phenylacetyl-CoA catabolon. Proc Natl Acad Sci U S A 95, 6419–6424.[CrossRef]
    [Google Scholar]
  38. Peters, M., Heinaru, E., Talpsep, E., Wand, H., Stottmeister, U., Heinaru, A. & Nurk, A. ( 1997; ). Acquisition of a deliberately introduced phenol degradation operon, pheBA, by different indigenous Pseudomonas species. Appl Environ Microbiol 63, 4899–4906.
    [Google Scholar]
  39. Poelarends, G. J., Veetil, V. P. & Whitman, C. P. ( 2008; ). The chemical versatility of the β-α-β fold: catalytic promiscuity and divergent evolution in the tautomerase superfamily. Cell Mol Life Sci 65, 3606–3618.[CrossRef]
    [Google Scholar]
  40. Pohlman, R. F., Genetti, H. D. & Winans, S. C. ( 1994; ). Entry exclusion of the IncN plasmid pKM101 is mediated by a single hydrophilic protein containing a lipid attachment motif. Plasmid 31, 158–165.[CrossRef]
    [Google Scholar]
  41. Powell, J. A. C. & Archer, J. A. C. ( 1998; ). Molecular characterisation of a Rhodococcus ohp operon. Antonie Van Leeuwenhoek 74, 175–188.[CrossRef]
    [Google Scholar]
  42. Providenti, M. A., Shaye, R. E., Lynes, K. D., McKenna, N. T., O'Brien, J. M., Rosolen, S., Wyndham, R. C. & Lambert, I. B. ( 2006; ). The locus coding for the 3-nitrobenzoate dioxygenase of Comamonas sp. strain JS46 is flanked by IS1071 elements and is subject to deletion and inversion events. Appl Environ Microbiol 72, 2651–2660.[CrossRef]
    [Google Scholar]
  43. Ravatn, R., Studer, S., Springael, D., Zehnder, A. J. B. & van der Meer, J. R. ( 1998; ). Chromosomal integration, tandem amplification, and deamplification in Pseudomonas putida F1 of a 105-kilobase genetic element containing the chlorocatechol degradative genes from Pseudomonas sp. strain B13. J Bacteriol 180, 4360–4369.
    [Google Scholar]
  44. Reineke, W. ( 1998; ). Development of hybrid strains for the mineralization of chloroaromatics by patchwork assembly. Annu Rev Microbiol 52, 287–331.[CrossRef]
    [Google Scholar]
  45. Reineke, W. ( 2001; ). Aerobic and anaerobic biodegradation potentials of microorganisms. In Biodegradation and Persistence (The Handbook of Environmental Chemistry, vol. 2K), pp. 1–161. Edited by B. Beek. Berlin/Heidelberg: Springer Verlag.
  46. Rojo, F., Pieper, D. H., Engesser, K.-H., Knackmuss, H.-J. & Timmis, K. N. ( 1987; ). Assemblage of ortho cleavage route for simultaneous degradation of chloro- and methylaromatics. Science 238, 1395–1398.[CrossRef]
    [Google Scholar]
  47. Saitou, N. & Nei, M. ( 1987; ). The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol Biol Evol 4, 406–425.
    [Google Scholar]
  48. Sambrook, J., Fritsch, E. F. & Maniatis, T. ( 1989; ). Molecular Cloning: a Laboratory Manual, 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
  49. Schmidt, E. & Knackmuss, H.-J. ( 1980; ). Chemical structure and biodegradability of halogenated aromatic compounds. Conversion of chlorinated muconic acids into maleoylacetic acid. Biochem J 192, 339–347.
    [Google Scholar]
  50. Schmidt, E., Remberg, G. & Knackmuss, H.-J. ( 1980; ). Chemical structure and biodegradability of halogenated aromatic compounds. Halogenated muconic acids as intermediates. Biochem J 192, 331–337.
    [Google Scholar]
  51. Schwarzenbach, R. P., Gschwend, P. M. & Imboden, D. M. ( 2003; ). Environmental Organic Chemistry, 2nd edn. Hoboken, NJ: Wiley-Interscience.
  52. Schweigert, N., Zehnder, A. J. B. & Eggen, R. I. L. ( 2001; ). Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3, 81–91.[CrossRef]
    [Google Scholar]
  53. Sherratt, D. ( 1989; ). Tn3 and related transposable elements: site-specific recombination and transposition. In Mobile DNA, pp. 1302–1308. Edited by D. E. Berg & M. M. Howe. Washington, DC: American Society for Microbiology.
  54. Shingler, V., Powlowski, J. & Marklund, U. ( 1992; ). Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600. J Bacteriol 174, 711–724.
    [Google Scholar]
  55. Sota, M., Yano, H., Nagata, Y., Ohtsubo, Y., Genka, H., Anbutsu, H., Kawasaki, H. & Tsuda, M. ( 2006; ). Functional analysis of unique class II insertion sequence IS1071. Appl Environ Microbiol 72, 291–297.[CrossRef]
    [Google Scholar]
  56. Stanley, T. M., Johnson, W. H., Burks, E. A., Whitman, C. P., Hwang, C. C. & Cook, P. F. ( 2000; ). Expression and stereochemical and isotope effect studies of active 4-oxalocrotonate decarboxylase. Biochemistry 39, 3514 [CrossRef]
    [Google Scholar]
  57. Tamura, K., Dudley, J., Nei, M. & Kumar, S. ( 2007; ). mega4: Molecular Evolutionary Genetics Analysis (mega) software version 4.0. Mol Biol Evol 24, 1596–1599.[CrossRef]
    [Google Scholar]
  58. Tropel, D., Meyer, C., Armengaud, J. & Jouanneau, Y. ( 2002; ). Ferredoxin-mediated reactivation of the chlorocatechol 2,3-dioxygenase from Pseudomonas putida GJ31. Arch Microbiol 177, 345–351.[CrossRef]
    [Google Scholar]
  59. Urata, M., Uchida, E., Nojiri, H., Omori, T., Obo, R., Miyaura, N. & Ouchiyama, N. ( 2004; ). Genes involved in aniline degradation by Delftia acidovorans strain 7N and its distribution in the natural environment. Biosci Biotechnol Biochem 68, 2457–2465.[CrossRef]
    [Google Scholar]
  60. van der Meer, J. R., Zehnder, A. J. B. & de Vos, W. M. ( 1991; ). Identification of a novel composite transposable element, Tn5280, carrying chlorobenzene dioxygenase genes of Pseudomonas sp. strain P51. J Bacteriol 173, 7077–7083.
    [Google Scholar]
  61. Volff, J. N., Eichenseer, C., Viell, P., Piendl, W. & Altenbuchner, J. ( 1996; ). Nucleotide sequence and role in DNA amplification of the direct repeats composing the amplificable element AUD1 of Streptomyces lividans 66. Mol Microbiol 21, 1037–1047.[CrossRef]
    [Google Scholar]
  62. Wackett, L. P. & Hershberger, C. D. ( 2001; ). Biocatalysis and biodegradation. Microbial Transformation of Organic Compounds. Washington, DC: American Society for Microbiology.
  63. Wehmhöner, D., Häussler, S., Tümmler, B., Jänsch, L., Bredenbruch, F., Wehland, J. & Steinmetz, I. ( 2003; ). Inter- and intraclonal diversity of the Pseudomonas aeruginosa proteome manifests within the secretome. J Bacteriol 185, 5807–5814.[CrossRef]
    [Google Scholar]
  64. Wheatcroft, R. & Williams, P. A. ( 1981; ). Rapid methods for the study of both stable and unstable plasmids in Pseudomonas. J Gen Microbiol 124, 433–437.
    [Google Scholar]
  65. Witzig, R., Junca, H., Hecht, H. J. & Pieper, D. H. ( 2006; ). Assessment of toluene/biphenyl dioxygenase gene diversity in benzene-polluted soils: links between benzene biodegradation and genes similar to those encoding isopropylbenzene dioxygenases. Appl Environ Microbiol 72, 3504–3514.[CrossRef]
    [Google Scholar]
  66. Witzig, R., Aly, H. A., Strömpl, C., Wray, V., Junca, H. & Pieper, D. H. ( 2007; ). Molecular detection and diversity of novel diterpenoid dioxygenase DitA1 genes from proteobacterial strains and soil samples. Environ Microbiol 9, 1202–1218.[CrossRef]
    [Google Scholar]
  67. Yano, H., Garruto, C. E., Sota, M., Ohtsubo, Y., Nagata, Y., Zylstra, G. J., Williams, P. A. & Tsuda, M. ( 2007; ). Complete sequence determination combined with analysis of transposition/site-specific recombination events to explain genetic organization of IncP-7 TOL plasmid pWW53 and related mobile genetic elements. J Mol Biol 369, 11–26.[CrossRef]
    [Google Scholar]
  68. Zhu, C., Zhang, L. & Zhao, L. ( 2008; ). Molecular cloning, genetic organization of gene cluster encoding phenol hydroxylase and catechol 2,3-dioxygenase in Alcaligenes faecalis IS-46. World J Microbiol Biotechnol 24, 1687–1695.[CrossRef]
    [Google Scholar]
  69. Zylstra, G. J. & Gibson, D. T. ( 1989; ). Toluene degradation by Pseudomonas putida F1. Nucleotide sequence of the todC1C2BADE genes and their expression in Escherichia coli. J Biol Chem 264, 14940–14946.
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032110-0
Loading
/content/journal/micro/10.1099/mic.0.032110-0
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