Table of Contents Author Guidelines Submit a Manuscript
Journal of Chemistry
Volume 2014, Article ID 157974, 10 pages
http://dx.doi.org/10.1155/2014/157974
Review Article

Role of Dehalogenases in Aerobic Bacterial Degradation of Chlorinated Aromatic Compounds

School of Biotechnology, Yeungnam University, Gyeongsan, Gyeongbuk 712-749, Republic of Korea

Received 29 July 2014; Revised 16 October 2014; Accepted 22 October 2014; Published 13 November 2014

Academic Editor: Davide Vione

Copyright © 2014 Pankaj Kumar Arora and Hanhong Bae. This is an open access article distributed under the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.

Linked References

  1. P. K. Arora and H. Bae, “Bacterial degradation of chlorophenols and their derivatives,” Microbial Cell Factories, vol. 13, no. 1, article 31, 2014. View at Publisher · View at Google Scholar · View at Scopus
  2. S. R. Sahasrabudhe and V. V. Modi, “Microbial degradation of chlorinated aromatic compounds,” Microbiological Sciences, vol. 4, no. 10, pp. 300–303, 1987. View at Google Scholar · View at Scopus
  3. S. D. Copley, “Diverse mechanistic approaches to difficult chemical transformations: microbial dehalogenation of chlorinated aromatic compounds,” Chemistry & Biology, vol. 4, no. 3, pp. 169–174, 1997. View at Publisher · View at Google Scholar · View at Scopus
  4. P. K. Arora, C. Sasikala, and C. V. Ramana, “Degradation of chlorinated nitroaromatic compounds,” Applied Microbiology and Biotechnology, vol. 93, no. 6, pp. 2265–2277, 2012. View at Publisher · View at Google Scholar · View at Scopus
  5. M. Kunze, K. F. Zerlin, A. Retzlaff et al., “Degradation of chloroaromatics by Pseudomonas putida GJ31: assembled route for chlorobenzene degradation encoded by clusters on plasmid pKW1 and the chromosome,” Microbiology, vol. 155, no. 12, pp. 4069–4083, 2009. View at Publisher · View at Google Scholar · View at Scopus
  6. P. K. Donnelly, J. A. Entry, and D. L. Crawford, “Degradation of atrazine and 2,4-dichlorophenoxyacetic acid by mycorrhizal fungi at three nitrogen concentrations in vitro,” Applied and Environmental Microbiology, vol. 59, no. 8, pp. 2642–2647, 1993. View at Google Scholar · View at Scopus
  7. P. K. Arora, A. Srivastava, and V. P. Singh, “Bacterial degradation of nitrophenols and their derivatives,” Journal of Hazardous Materials, vol. 266, pp. 42–59, 2014. View at Publisher · View at Google Scholar · View at Scopus
  8. S. Fetzner and F. Lingens, “Bacterial dehalogenases: biochemistry, genetics, and biotechnological applications,” Microbiological Reviews, vol. 58, no. 4, pp. 641–685, 1994. View at Google Scholar · View at Scopus
  9. P. K. Arora, A. Srivastava, and V. P. Singh, “Application of monooxygenases in dehalogenation, desulphurization, denitrification and hydroxylation of aromatic compounds,” Journal of Bioremediation and Biodegradation, vol. 1, p. 112, 2010. View at Google Scholar
  10. G. P. Crooks, “Purification and characterization of 4-chlorobenzoyl CoA dehalogenase from arthrobacter sp. strain 4-cb1,” Biochemistry, vol. 33, no. 38, pp. 11645–11649, 1994. View at Publisher · View at Google Scholar · View at Scopus
  11. L. A. Heppel and V. T. Porterfield, “Enzymatic dehalogenation of certain brominated and chlorinated compounds,” Journal of Biological Chemistry, vol. 176, pp. 763–769, 1948. View at Google Scholar
  12. G. Wang, R. Li, S. Li, and J. Jiang, “A novel hydrolytic dehalogenase for the chlorinated aromatic compound chlorothalonil,” Journal of Bacteriology, vol. 192, no. 11, pp. 2737–2745, 2010. View at Publisher · View at Google Scholar · View at Scopus
  13. M. L. de Souza, M. J. Sadowsky, and L. P. Wackett, “Atrazine chlorohydrolase from Pseudomonas sp. strain ADP: gene sequence, enzyme purification, and protein characterization,” Journal of Bacteriology, vol. 178, no. 16, pp. 4894–4900, 1996. View at Google Scholar · View at Scopus
  14. L. Xun, E. Topp, and C. S. Orser, “Purification and characterization of a tetrachloro-p-hydroquinone reductive dehalogenase from a Flavobacterium sp,” Journal of Bacteriology, vol. 174, no. 24, pp. 8003–8007, 1992. View at Google Scholar · View at Scopus
  15. K. Miyauchi, S.-K. Suh, Y. Nagata, and M. Takagi, “Cloning and sequencing of a 2,5-dichlorohydroquinone reductive dehalogenase gene whose product is involved in degradation of γ-hexachlorocyclohexane by Sphingomonas paucimobilis,” Journal of Bacteriology, vol. 180, no. 6, pp. 1354–1359, 1998. View at Google Scholar · View at Scopus
  16. P. K. Arora and R. K. Jain, “Metabolism of 2-chloro-4-nitrophenol in a gram negative bacterium, Burkholderia sp. RKJ 800,” PLoS ONE, vol. 7, no. 6, Article ID e38676, 2012. View at Publisher · View at Google Scholar · View at Scopus
  17. P. K. Arora, A. Srivastava, and V. Singh, “Novel degradation pathway of 2-chloro-4-aminophenol in Arthrobacter sp. SPG,” PeerJ PrePrints, vol. 2, p. e194v1, 2014. View at Publisher · View at Google Scholar
  18. P. K. Arora, A. Sharma, R. Mehta, B. D. Shenoy, A. Srivastava, and V. P. Singh, “Metabolism of 4-chloro-2-nitrophenol in a Gram-positive bacterium, Exiguobacterium sp. PMA,” Microbial Cell Factories, vol. 11, article 150, 2012. View at Publisher · View at Google Scholar · View at Scopus
  19. K. Miyauchi, Y. Adachi, Y. Nagata, and M. Takagi, “Cloning and sequencing of a novel meta-cleavage dioxygenase gene whose product is involved in degradation of γ-hexachlorocyclohexane in Sphingomonas paucimobilis,” Journal of Bacteriology, vol. 181, no. 21, pp. 6712–6719, 1999. View at Google Scholar · View at Scopus
  20. F. Löffler, F. Lingens, and R. Müller, “Dehalogenation of 4-chlorobenzoate. Characterisation of 4-chlorobenzoyl-coenzyme A dehalogenase from Pseudomonas sp. CBS3,” Biodegradation, vol. 6, no. 3, pp. 203–212, 1995. View at Google Scholar · View at Scopus
  21. L. Zhou, R. P. C. Poh, T. S. Marks, B. Z. Chowdhry, and A. R. W. Smith, “Structure and denaturation of 4-chlorobenzoyl coenzyme A dehalogenase from Arthrobacter sp. strain TM-1,” Biodegradation, vol. 19, no. 1, pp. 65–75, 2008. View at Publisher · View at Google Scholar · View at Scopus
  22. G. P. Crooks, L. Xu, R. M. Barkley, and S. D. Copley, “Exploration of possible mechanisms for 4-chlorobenzoyl CoA dehalogenase: evidence for an aryl-enzyme intermediate,” Journal of the American Chemical Society, vol. 117, no. 44, pp. 10791–10798, 1995. View at Publisher · View at Google Scholar · View at Scopus
  23. R. M. de Jong and B. W. Dijkstra, “Structure and mechanism of bacterial dehalogenases: different ways to cleave a carbon-halogen bond,” Current Opinion in Structural Biology, vol. 13, no. 6, pp. 722–730, 2003. View at Publisher · View at Google Scholar · View at Scopus
  24. E. Y. Lau and T. C. Bruice, “The active site dynamics of 4-chlorobenzoyl-CoA dehalogenase,” Proceedings of the National Academy of Sciences of the United States of America, vol. 98, no. 17, pp. 9527–9532, 2001. View at Publisher · View at Google Scholar · View at Scopus
  25. L. S. Luo, K. L. Taylor, H. Xiang, Y. Wei, W. Zhang, and D. Dunaway-Mariano, “Role of active site binding interactions in 4-chlorobenzoyl-coenzyme A dehalogenase catalysis,” Biochemistry, vol. 40, no. 51, pp. 15684–15692, 2001. View at Publisher · View at Google Scholar · View at Scopus
  26. M. M. Benning, K. L. Taylor, R.-Q. Liu et al., “Structure of 4-chlorobenzoyl coenzyme A dehalogenase determined to 1.8 Å resolution: an enzyme catalyst generated via adaptive mutation,” Biochemistry, vol. 35, no. 25, pp. 8103–8109, 1996. View at Publisher · View at Google Scholar · View at Scopus
  27. L. Zhou, T. S. Marks, R. P. C. Poh, R. J. Smith, B. Z. Chowdhry, and A. R. W. Smith, “The purification and characterisation of 4-chlorobenzoate:CoA ligase and 4-chlorobenzoyl CoA dehalogenase from Arthrobacter sp. strain TM-1,” Biodegradation, vol. 15, no. 2, pp. 97–109, 2004. View at Publisher · View at Google Scholar · View at Scopus
  28. B. Liang, G. Wang, Y. Zhao, K. Chen, S. Li, and J. Jiang, “Facilitation of bacterial adaptation to chlorothalonil-contaminated sites by horizontal transfer of the chlorothalonil hydrolytic dehalogenase gene,” Applied and Environmental Microbiology, vol. 77, no. 12, pp. 4268–4272, 2011. View at Publisher · View at Google Scholar · View at Scopus
  29. B. Liang, J. Jiang, J. Zhang, Y. Zhao, and S. Li, “Horizontal transfer of dehalogenase genes involved in the catalysis of chlorinated compounds: evidence and ecological role,” Critical Reviews in Microbiology, vol. 38, no. 2, pp. 95–102, 2012. View at Publisher · View at Google Scholar · View at Scopus
  30. X.-Z. Shi, R.-J. Guo, K. Takagi, Z.-Q. Miao, and S.-D. Li, “Chlorothalonil degradation by Ochrobactrum lupini strain TP-D1 and identification of its metabolites,” World Journal of Microbiology and Biotechnology, vol. 27, no. 8, pp. 1755–1764, 2011. View at Publisher · View at Google Scholar · View at Scopus
  31. G. Wang, B. Liang, F. Li, and S. Li, “Recent advances in the biodegradation of chlorothalonil,” Current Microbiology, vol. 63, no. 5, pp. 450–457, 2011. View at Publisher · View at Google Scholar · View at Scopus
  32. S. D. Copley, J. Rokicki, P. Turner, H. Daligault, M. Nolan, and M. Land, “The whole genome sequence of Sphingobium chlorophenolicum L-1: insights into the evolution of the pentachlorophenol degradation pathway,” Genome Biology and Evolution, vol. 4, no. 2, pp. 184–198, 2012. View at Publisher · View at Google Scholar · View at Scopus
  33. J. R. Warner, S. L. Lawson, and S. D. Copley, “A mechanistic investigation of the thiol-disulfide exchange step in the reductive dehalogenation catalyzed by tetrachlorohydroquinone dehalogenase,” Biochemistry, vol. 44, no. 30, pp. 10360–10368, 2005. View at Publisher · View at Google Scholar · View at Scopus
  34. J. R. Warner and S. D. Copley, “Pre-steady-state kinetic studies of the reductive dehalogenation catalyzed by tetrachlorohydroquinone dehalogenase,” Biochemistry, vol. 46, no. 45, pp. 13211–13222, 2007. View at Publisher · View at Google Scholar · View at Scopus
  35. G. Polekhina, P. G. Board, A. C. Blackburn, and M. W. Parker, “Crystal structure of maleylacetoacetate isomerase/glutathione transferase zeta reveals the molecular basis for its remarkable catalytic promiscuity,” Biochemistry, vol. 40, no. 6, pp. 1567–1576, 2001. View at Publisher · View at Google Scholar · View at Scopus
  36. M. Marsh, D. K. Shoemark, A. Jacob et al., “Structure of bacterial glutathione-S-transferase maleyl pyruvate isomerase and implications for mechanism of isomerisation,” Journal of Molecular Biology, vol. 384, no. 1, pp. 165–177, 2008. View at Publisher · View at Google Scholar · View at Scopus
  37. D. L. McCarthy, S. Navarrete, W. S. Willett, P. C. Babbitt, and S. D. Copley, “Exploration of the relationship between tetrachlorohydroquinone dehalogenase and the glutathione S-transferase superfamily,” Biochemistry, vol. 35, no. 46, pp. 14634–14642, 1996. View at Publisher · View at Google Scholar · View at Scopus
  38. D. L. McCarthy, D. F. Louie, and S. D. Copley, “Identification of a covalent intermediate between glutathione and cysteine13 formed during catalysis by tetrachlorohydroquinone dehalogenase,” Journal of the American Chemical Society, vol. 119, no. 46, pp. 11337–11338, 1997. View at Publisher · View at Google Scholar · View at Scopus
  39. M. Habash, B. C. H. Chu, J. T. Trevors, and H. Lee, “Mutational study of the role of N-terminal amino acid residues in tetrachlorohydroquinone reductive dehalogenase from Sphingomonas sp. UG30,” Research in Microbiology, vol. 160, no. 8, pp. 553–559, 2009. View at Publisher · View at Google Scholar · View at Scopus
  40. M. B. Habash, L. A. Beaudette, M. B. Cassidy et al., “Characterization of tetrachlorohydroquinone reductive dehalogenase from Sphingomonas sp. UG30,” Biochemical and Biophysical Research Communications, vol. 299, no. 4, pp. 634–640, 2002. View at Publisher · View at Google Scholar · View at Scopus
  41. E. Masai, Y. Katayama, and M. Fukuda, “Genetic and biochemical investigations on bacterial catabolic pathways for lignin-derived aromatic compounds,” Bioscience, Biotechnology and Biochemistry, vol. 71, no. 1, pp. 1–15, 2007. View at Publisher · View at Google Scholar · View at Scopus
  42. T. R. Miller, A. L. Delcher, S. L. Salzberg, E. Saunders, J. C. Detter, and R. U. Halden, “Genome sequence of the dioxin-mineralizing bacterium Sphingomonas wittichii RW1,” Journal of Bacteriology, vol. 192, no. 22, pp. 6101–6102, 2010. View at Publisher · View at Google Scholar · View at Scopus
  43. F. M. Lauro, D. McDougald, T. Thomas et al., “The genomic basis of trophic strategy in marine bacteria,” Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 37, pp. 15527–15533, 2009. View at Publisher · View at Google Scholar · View at Scopus
  44. Y. Nagata, S. Natsui, R. Endo et al., “Genomic organization and genomic structural rearrangements of Sphingobium japonicum UT26, an archetypal γ-hexachlorocyclohexane-degrading bacterium,” Enzyme and Microbial Technology, vol. 49, no. 6-7, pp. 499–508, 2011. View at Publisher · View at Google Scholar · View at Scopus
  45. C. S. Orser, C. C. Lange, L. Xun, T. C. Zahrt, and B. J. Schneider, “Cloning, sequence analysis, and expression of the Flavobacterium pentachlorophenol-4-monooxygenase gene in Escherichia coli,” Journal of Bacteriology, vol. 175, no. 2, pp. 411–416, 1993. View at Google Scholar · View at Scopus
  46. R. L. Crawford, C. M. Jung, and J. L. Strap, “The recent evolution of pentachlorophenol (PCP)-4-monooxygenase (PcpB) and associated pathways for bacterial degradation of PCP,” Biodegradation, vol. 18, no. 5, pp. 525–539, 2007. View at Publisher · View at Google Scholar · View at Scopus
  47. V. M. Saboo and M. A. Gealt, “Gene sequences of the pcpB gene of pentachlorophenol-degrading Sphingomonas chlorophenolica found in nondegrading bacteria,” Canadian Journal of Microbiology, vol. 44, no. 7, pp. 667–675, 1998. View at Publisher · View at Google Scholar · View at Scopus
  48. M. A. Tiirola, H. Wang, L. Paulin, and M. S. Kulomaa, “Evidence for natural horizontal transfer of the pcpB gene in the evolution of polychlorophenol-degrading sphingomonads,” Applied and Environmental Microbiology, vol. 68, no. 9, pp. 4495–4501, 2002. View at Publisher · View at Google Scholar · View at Scopus
  49. M. A. Tiirola, M. K. Männistö, J. A. Puhakka, and M. S. Kulomaa, “Isolation and characterization of Novosphingobium sp. strain MT1, a dominant polychlorophenol-degrading strain in a groundwater bioremediation system,” Applied and Environmental Microbiology, vol. 68, no. 1, pp. 173–180, 2002. View at Publisher · View at Google Scholar · View at Scopus
  50. M. B. Cassidy, H. Lee, J. T. Trevors, and R. B. Zablotowicz, “Chlorophenol and nitrophenol metabolism by Sphingomonas sp UG30,” Journal of Industrial Microbiology and Biotechnology, vol. 23, no. 4-5, pp. 232–241, 1999. View at Publisher · View at Google Scholar · View at Scopus
  51. M. Beaulieu, V. Bécaert, L. Deschênes, and R. Villemur, “Evolution of bacterial diversity during enrichment of PCP-degrading activated soils,” Microbial Ecology, vol. 40, no. 4, pp. 345–356, 2000. View at Google Scholar · View at Scopus
  52. G. Martin-Le Garrec, I. Artaud, and C. Capeillère-Blandin, “Purification and catalytic properties of the chlorophenol 4-monooxygenase from Burkholderia cepacia strain AC1100,” Biochimica et Biophysica Acta, vol. 1547, no. 2, pp. 288–301, 2001. View at Publisher · View at Google Scholar · View at Scopus
  53. B. N. Webb, J. W. Ballinger, E. Kim et al., “Characterization of chlorophenol 4-monooxygenase (TftD) and NADH:FAD oxidoreductase (TftC) of Burkholderia cepacia AC1100,” The Journal of Biological Chemistry, vol. 285, no. 3, pp. 2014–2027, 2010. View at Publisher · View at Google Scholar · View at Scopus
  54. M. R. Gisi and L. Y. Xun, “Characterization of chlorophenol 4-monooxygenase (TftD) and NADH:flavin adenine dinucleotide oxidoreductase (TftC) of Burkholderia cepacia AC1100,” Journal of Bacteriology, vol. 185, no. 9, pp. 2786–2792, 2003. View at Publisher · View at Google Scholar · View at Scopus
  55. L. Xun, “Purification and characterization of chlorophenol 4-monooxygenase from Burkholderia cepacia AC1100,” Journal of Bacteriology, vol. 178, no. 9, pp. 2645–2649, 1996. View at Google Scholar · View at Scopus
  56. L. Xun and C. M. Webster, “A monooxygenase catalyzes sequential dechlorinations of 2,4,6-trichlorophenol by oxidative and hydrolytic reactions,” The Journal of Biological Chemistry, vol. 279, no. 8, pp. 6696–6700, 2004. View at Publisher · View at Google Scholar · View at Scopus
  57. M. Wieser, B. Wagner, J. Eberspächer, and F. Lingens, “Purification and characterization of 2,4,6-trichlorophenol-4-monooxygenase, a dehalogenating enzyme from Azotobacter sp. strain GP1,” Journal of Bacteriology, vol. 179, no. 1, pp. 202–208, 1997. View at Google Scholar · View at Scopus
  58. R. P. Hayes, B. N. Webb, A. K. Subramanian et al., “Structural and catalytic differences between two FADH 2-dependent monooxygenases: 2,4,5- TCP 4-monooxygenase (TftD) from Burkholderia cepacia AC1100 and 2,4,6-TCP 4-monooxygenase (TcpA) from Cupriavidus necator JMP134,” International Journal of Molecular Sciences, vol. 13, no. 8, pp. 9769–9784, 2012. View at Publisher · View at Google Scholar · View at Scopus
  59. T. M. Louie, C. M. Webster, and L. Xun, “Genetic and biochemical characterization of a 2,4,6-trichlorophenol degradation pathway in Ralstonia eutropha JMP134,” Journal of Bacteriology, vol. 184, no. 13, pp. 3492–3500, 2002. View at Publisher · View at Google Scholar · View at Scopus
  60. A. Markus, D. Krekel, and F. Lingens, “Purification and some properties of component A of the 4-chlorophenylacetate 3,4-dioxygenase from Pseudomonas species strain CBS,” The Journal of Biological Chemistry, vol. 261, no. 27, pp. 12883–12888, 1986. View at Google Scholar · View at Scopus
  61. D. Schweizer, A. Markus, M. Seez, H. H. Ruf, and F. Lingens, “Purification and some properties of component B of the 4-chlorophenylacetate 3,4-dioxygenase from Pseudomonas species strain CBS 3,” The Journal of Biological Chemistry, vol. 262, no. 19, pp. 9340–9346, 1987. View at Google Scholar · View at Scopus
  62. S. Fetzner, R. Müller, and F. Lingens, “Purification and some properties of 2-halobenzoate 1,2-dioxygenase, a two-component enzyme system from Pseudomonas cepacia 2CBS,” Journal of Bacteriology, vol. 174, no. 1, pp. 279–290, 1992. View at Google Scholar · View at Scopus
  63. B. Haak, S. Fetzner, and F. Lingens, “Cloning, nucleotide sequence, and expression of the plasmid-encoded genes for the two-component 2-halobenzoate 1,2-dioxygenase from Pseudomonas cepacia 2CBS,” Journal of Bacteriology, vol. 177, no. 3, pp. 667–675, 1995. View at Google Scholar · View at Scopus
  64. K. Suzuki, N. Ogawa, and K. Miyashita, “Expression of 2-halobenzoate dioxygenase genes (cbdSABC) involved in the degradation of benzoate and 2-halobenzoate in Burkholderia sp. TH2,” Gene, vol. 262, no. 1-2, pp. 137–145, 2001. View at Publisher · View at Google Scholar · View at Scopus
  65. V. Romanov and R. P. Hausinger, “Pseudomonas aeruginosa 142 uses a three-component ortho-halobenzoate 1,2- dioxygenase for metabolism of 2,4-dichloro- and 2-chlorobenzoate,” Journal of Bacteriology, vol. 176, no. 11, pp. 3368–3374, 1994. View at Google Scholar · View at Scopus
  66. S. Beil, B. Happe, K. N. Timmis, and D. H. Pieper, “Genetic and biochemical characterization of the broad spectrum chlorobenzene dioxygenase from Burkholderia sp. strain PS12—dechlorination of 1,2,4,5-tetrachlorobenzene,” European Journal of Biochemistry, vol. 247, no. 1, pp. 190–199, 1997. View at Publisher · View at Google Scholar · View at Scopus
  67. S. Beil, K. N. Timmis, and D. H. Pieper, “Genetic and biochemical analyses of the tec operon suggest a route for evolution of chlorobenzene degradation genes,” Journal of Bacteriology, vol. 181, no. 1, pp. 341–346, 1999. View at Google Scholar · View at Scopus
  68. S. Beil, J. R. Mason, K. N. Timmis, and D. H. Pieper, “Identification of chlorobenzene dioxygenase sequence elements involved in dechlorination of 1,2,4,5-tetrachlorobenzene,” Journal of Bacteriology, vol. 180, no. 21, pp. 5520–5528, 1998. View at Google Scholar · View at Scopus