1887

Microbiology Society logo

Volume 155, Issue 11

Genuine genetic redundancy in maleylacetate-reductase-encoding genes involved in degradation of haloaromatic compounds by JMP134 Free

Abstract

Maleylacetate reductases (MAR) are required for biodegradation of several substituted aromatic compounds. To date, the functionality of two MAR-encoding genes ( and ) has been reported in JMP134(pJP4), a known degrader of aromatic compounds. These two genes are located in gene clusters involved in the turnover of 2,4-dichlorophenoxyacetate (2,4-D) and 3-chlorobenzoate (3-CB). The JMP134 genome comprises at least three other genes that putatively encode MAR (, and ), but confirmation of their functionality and their role in the catabolism of haloaromatic compounds has not been assessed. RT-PCR expression analyses of JMP134 cells exposed to 2,4-D, 3-CB, 2,4,6-trichlorophenol (2,4,6-TCP) or 4-fluorobenzoate (4-FB) showed that and are induced by haloaromatics channelled to halocatechols as intermediates. In contrast, 2,4,6-TCP only induces , and any haloaromatic compounds tested did not induce and . However, the , and gene products showed MAR activity in cell extracts and provided the MAR function for 2,4-D catabolism when heterologously expressed in MAR-lacking strains. Growth tests for mutants of the five MAR-encoding genes in strain JMP134 showed that none of these genes is essential for degradation of the tested compounds. However, the role of / and genes in the expression of MAR activity during catabolism of 2,4-D and 2,4,6-TCP, respectively, was confirmed by enzyme activity tests in mutants. These results reveal a striking example of genetic redundancy in the degradation of aromatic compounds.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): 2,4,6-TCP, 2,4,6-trichlorophenol , 2,4-D, 2,4-dichlorophenoxyacetate , 2-CMA, 2-chloromaleylacetate , 3-CB, 3-chlorobenzoate , 4-FB, 4-fluorobenzoate , MA, maleylacetate and MAR, maleylacetate reductase(s)
SGM
Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.032086-0
2009-11-01
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/micro/155/11/3641.html?itemId=/content/journal/micro/10.1099/mic.0.032086-0&mimeType=html&fmt=ahah

References

  1. Armengaud J., Timmis K. N., Wittich R. M. 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
     [Google Scholar]
  2. 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
     [Google Scholar]
  3. Bronstein P. A., Marrichi M., Cartinhour S., Schneider D. J., DeLisa M. P. 2005; Identification of a twin-arginine translocation system in Pseudomonas syringae pv. tomato DC3000 and its contribution to pathogenicity and fitness. J Bacteriol 187:8450–8461
     [Google Scholar]
  4. Clément P., Springael D., González B. 2000; Deletions of mob and tra pJP4 transfer functions after mating of Ralstonia eutropha JMP134 (pJP4) with Escherichia coli harboring F′ : :  Tn10. Can J Microbiol 46:485–489
     [Google Scholar]
  5. Datsenko K. A., Wanner B. L. 2000; One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640–6645
     [Google Scholar]
  6. Daubaras D. L., Saido K., Chakrabarty A. M. 1996; Purification of hydroxyquinol 1,2-dioxygenase and maleylacetate reductase: the lower pathway of 2,4,5-trichlorophenoxyacetic acid metabolism by Burkholderia cepacia AC1100. Appl Environ Microbiol 62:4276–4279
     [Google Scholar]
  7. Dorn E., Hellwig M., Reineke W., Knackmuss H.-J. 1974; Isolation and characterization of a 3-chlorobenzoate degrading pseudomonad. Arch Microbiol 99:61–70
     [Google Scholar]
  8. Endo R., Kamakura M., Miyauchi K., Fukuda M., Ohtsubo Y., Tsuda M., Nagata Y. 2005; Identification and characterization of genes involved in the downstream degradation pathway of γ-hexachlorocyclohexane in Sphingomonas paucimobilis UT26. J Bacteriol 187:847–853
     [Google Scholar]
  9. Filer K., Harker A. R. 1997; Identification of the inducing agent of the 2,4-dichlorophenoxyacetic acid pathway encoded by plasmid pJP4. Appl Environ Microbiol 63:317–320
     [Google Scholar]
  10. Gaal A. B., Neujahr H. Y. 1980; Maleylacetate reductase from Trichosporon cutaneum . Biochem J 185:783–786
     [Google Scholar]
  11. Gevers D., Vandepoele K., Simillon C., Van de Peer Y. 2004; Gene duplication and biased functional retention of paralogs in bacterial genomes. Trends Microbiol 12:148–154
     [Google Scholar]
  12. House B. L., Mortimer M. W., Kahn M. L. 2004; New recombination methods for Sinorhizobium meliloti genetics. Appl Environ Microbiol 70:2806–2815
     [Google Scholar]
  13. Huang Y., Zhao K. X., Shen X. H., Chaudhry M. T., Jiang C. Y., Liu S. J. 2006; Genetic characterization of the resorcinol catabolic pathway in Corynebacterium glutamicum . Appl Environ Microbiol 72:7238–7245
     [Google Scholar]
  14. Jones K. H., Trudgill P. W., Hopper D. J. 1995; Evidence of two pathways for the metabolism of phenol by Aspergillus fumigatus . Arch Microbiol 163:176–181
     [Google Scholar]
  15. Kasberg T., Daubaras D. L., Chakrabarty A. M., Kinzelt D., Reineke W. 1995; Evidence that operons tcb, tfd, and clc encode maleylacetate reductase, the fourth enzyme of the modified ortho pathway. J Bacteriol 177:3885–3889
     [Google Scholar]
  16. 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]
  17. Kaschabek S. R., Reineke W. 1995; Maleylacetate reductase of Pseudomonas sp. strain B13: specificity of substrate conversion and halide elimination. J Bacteriol 177:320–325
     [Google Scholar]
  18. Laemmli C. M., Leveau J. H., Zehnder A. J., van der Meer J. R. 2000; Characterization of a second tfd gene cluster for chlorophenol and chlorocatechol metabolism on plasmid pJP4 in Ralstonia eutropha JMP134(pJP4. J Bacteriol 182:4165–4172
     [Google Scholar]
  19. Laemmli C., Werlen C., van der Meer J. R. 2004; Mutation analysis of the different tfd genes for degradation of chloroaromatic compounds in Ralstonia eutropha JMP134. Arch Microbiol 181:112–121
     [Google Scholar]
  20. Ledger T., Pieper D. H., Pérez-Pantoja D., González B. 2002; Novel insights into the interplay between peripheral reactions encoded by xyl genes and the chlorocatechol pathway encoded by tfd genes for the degradation of chlorobenzoates by Ralstonia eutropha JMP134. Microbiology 148:3431–3440
     [Google Scholar]
  21. Leveau J. H., Konig F., Fuchslin H., Werlen C., van der Meer J. R. 1999; Dynamics of multigene expression during catabolic adaptation of Ralstonia eutropha JMP134 (pJP4) to the herbicide 2, 4-dichlorophenoxyacetate. Mol Microbiol 33:396–406
     [Google Scholar]
  22. Matus V., Sánchez M. A., Martínez M., González B. 2003; Efficient degradation of 2,4,6-trichlorophenol requires a set of catabolic genes related to tcp genes from Ralstonia eutropha JMP134(pJP4. Appl Environ Microbiol 69:7108–7115
     [Google Scholar]
  23. Moonen M. J., Kamerbeek N. M., Westphal A. H., Boeren S. A., Janssen D. B., Fraaije M. W., van Berkel W. J. 2008; Elucidation of the 4-hydroxyacetophenone catabolic pathway in Pseudomonas fluorescens ACB. J Bacteriol 190:5190–5198
     [Google Scholar]
  24. Muller D., Schlomann M., Reineke W. 1996; Maleylacetate reductases in chloroaromatic-degrading bacteria using the modified ortho pathway: comparison of catalytic properties. J Bacteriol 178:298–300
     [Google Scholar]
  25. Nikodem P., Hecht V., Schlomann M., Pieper D. H. 2003; New bacterial pathway for 4- and 5-chlorosalicylate degradation via 4-chlorocatechol and maleylacetate in Pseudomonas sp. strain MT1. J Bacteriol 185:6790–6800
     [Google Scholar]
  26. Padilla L., Matus V., Zenteno P., González B. 2000; Degradation of 2,4,6-trichlorophenol via chlorohydroxyquinol in Ralstonia eutropha JMP134 and JMP222. J Basic Microbiol 40:243–249
     [Google Scholar]
  27. Patel T. R., Hameed N., Armstrong S. 1992; Metabolism of gallate in Penicillium simplicissimum . J Basic Microbiol 32:233–240
     [Google Scholar]
  28. Pérez-Pantoja D., Guzmán L., Manzano M., Pieper D. H., González B. 2000; Role of tfdC(I)D(I) E(I) F(I) and tfdD(II) C(II) E(II) F(II) gene modules in catabolism of 3-chlorobenzoate by Ralstonia eutropha JMP134(pJP4). Appl Environ Microbiol 66:1602–1608
     [Google Scholar]
  29. Pérez-Pantoja D., Ledger T., Pieper D. H., González B. 2003; Efficient turnover of chlorocatechols is essential for growth of Ralstonia eutropha JMP134(pJP4) in 3-chlorobenzoic acid. J Bacteriol 185:1534–1542
     [Google Scholar]
  30. Pérez-Pantoja D., De la Iglesia R., Pieper D. H., González B. 2008; Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol Rev 32:736–794
     [Google Scholar]
  31. Perry L. L., Zylstra G. J. 2007; Cloning of a gene cluster involved in the catabolism of p-nitrophenol by Arthrobacter sp. strain JS443 and characterization of the p-nitrophenol monooxygenase. J Bacteriol 189:7563–7572
     [Google Scholar]
  32. Pieper D. H., Reineke W., Engesser K. H., Knackmuss H.-J. 1988; Metabolism of 2,4-dichlorophenoxyacetic acid, 4-chloro-2-methylphenoxyacetic acid and 2-methylphenoxyacetic acid by Alcaligenes eutrophus JMP 134. Arch Microbiol 150:95–102
     [Google Scholar]
  33. Plumeier I., Pérez-Pantoja D., Heim S., González B., Pieper D. H. 2002; Importance of different tfd genes for degradation of chloroaromatics by Ralstonia eutropha JMP134. J Bacteriol 184:4054–4064
     [Google Scholar]
  34. Sánchez M. A., González B. 2007; Genetic characterization of 2,4,6-trichlorophenol degradation in Cupriavidus necator JMP134. Appl Environ Microbiol 73:2769–2776
     [Google Scholar]
  35. Schlomann M., Fischer P., Schmidt E., Knackmuss H.-J. 1990a; Enzymatic formation, stability, and spontaneous reactions of 4-fluoromuconolactone, a metabolite of the bacterial degradation of 4-fluorobenzoate. J Bacteriol 172:5119–5129
     [Google Scholar]
  36. Schlomann M., Schmidt E., Knackmuss H.-J. 1990b; Different types of dienelactone hydrolase in 4-fluorobenzoate-utilizing bacteria. J Bacteriol 172:5112–5118
     [Google Scholar]
  37. Seibert V., Stadler-Fritzsche K., Schlomann M. 1993; Purification and characterization of maleylacetate reductase from Alcaligenes eutrophus JMP134(pJP4. J Bacteriol 175:6745–6754
     [Google Scholar]
  38. Seibert V., Kourbatova E. M., Golovleva L. A., Schlomann M. 1998; Characterization of the maleylacetate reductase MacA of Rhodococcus opacus 1CP and evidence for the presence of an isofunctional enzyme. J Bacteriol 180:3503–3508
     [Google Scholar]
  39. Seibert V., Thiel M., Hinner I. S., Schlomann M. 2004; Characterization of a gene cluster encoding the maleylacetate reductase from Ralstonia eutropha 335T, an enzyme recruited for growth with 4-fluorobenzoate. Microbiology 150:463–472
     [Google Scholar]
  40. Sessitsch A., Coenye T., Sturz A. V., Vandamme E., Barka P. A., Salles J. F., van Elsas J. D., Faure D., Reiter B. other authors 2005; Burkholderia phytofirmans sp. nov., a novel plant-associated bacterium with plant-beneficial properties. Int J Syst Evol Microbiol 55:1187–1192
     [Google Scholar]
  41. Sparnins V. L., Burbee D. G., Dagley S. 1979; Catabolism of l-tyrosine in Trichosporon cutaneum . J Bacteriol 138:425–430
     [Google Scholar]
  42. Travkin V. M., Linko E. V., Golovleva L. A. 1999; Purification and characterization of maleylacetate reductase from Nocardioides simplex 3E utilizing phenoxyalcanoic herbicides 2,4-D and 2,4,5-T. Biochemistry (Mosc 64:625–630
     [Google Scholar]
  43. Trefault N., De la Iglesia R., Molina A. M., Manzano M., Ledger T., Pérez-Pantoja D., Sánchez M. A., Stuardo M., González B. 2004; Genetic organization of the catabolic plasmid pJP4 from Ralstonia eutropha JMP134 (pJP4) reveals mechanisms of adaptation to chloroaromatic pollutants and evolution of specialized chloroaromatic degradation pathways. Environ Microbiol 6:655–668
     [Google Scholar]
  44. Vollmer M. D., Stadler-Fritzsche K., Schlomann M. 1993; Conversion of 2-chloromaleylacetate in Alcaligenes eutrophus JMP134. Arch Microbiol 159:182–188
     [Google Scholar]
  45. Yoshida M., Oikawa T., Obata H., Abe K., Mihara H., Esaki N. 2007; Biochemical and genetic analysis of the γ-resorcylate (2,6-dihydroxybenzoate) catabolic pathway in Rhizobium sp. strain MTP-10005: identification and functional analysis of its gene cluster. J Bacteriol 189:1573–1581
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.032086-0
Loading
Genuine genetic redundancy in maleylacetate-reductase-encoding genes involved in degradation of haloaromatic compounds by Cupriavidus necator JMP134
Microbiology 155, 3641 (2009); https://doi.org/10.1099/mic.0.032086-0
/content/journal/micro/10.1099/mic.0.032086-0
/content/journal/micro/10.1099/mic.0.032086-0
Loading

Data & Media loading...

Most cited Most Cited RSS feed

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