The recent evolution of pentachlorophenol (PCP)-4-monooxygenase (PcpB) and associated pathways for bacterial degradation of PCP

Biodegradation

Volumn 18, Issue 5, 2007, Pages 525-539

  Crawford, Ronald L ^a   Jung, Carina M ^a,b   Strap, Janice L ^a,c  

^a UNIVERSITY OF IDAHO   (United States)

^b NATIONAL CENTER FOR TOXICOLOGICAL RESEARCH   (United States)

^c UNIVERSITY OF ONTARIO INSTITUTE OF TECHNOLOGY   (Canada)

Author keywords

Gene recruitment; Lateral gene transfer; PCP; pcpB; Pentachlorophenol; Sphingomonas

Indexed keywords

CATABOLIC PATHWAYS; GENE RECRUITMENT; LATERAL GENE TRANSFER; PENTACHLOROPHENOL;

BACTERIA; DEGRADATION; FUNGI; GENES; IMPURITIES;

POLYCHLORINATED BIPHENYLS;

BACTERIAL PROTEIN; MIXED FUNCTION OXIDASE; PENTACHLOROPHENOL; PENTACHLOROPHENOL MONOOXYGENASE; UNCLASSIFIED DRUG; XENOBIOTIC AGENT;

BACTERIA; DEGRADATION; FUNGI; GENES; IMPURITIES; POLYCHLORINATED BIPHENYLS;

BACTERIUM; BIODEGRADATION; ENZYME; GENE; MICROBIAL ACTIVITY; PCP; XENOBIOTICS;

BIOLOGICAL MODEL; BIOREMEDIATION; CATALYSIS; CHEMICAL MODEL; CHEMISTRY; ENVIRONMENT; EVOLUTION; GENE TRANSFER; GENETICS; HYDROXYLATION; METABOLISM; MOLECULAR CLONING; PHYLOGENY; PHYSIOLOGY; REVIEW; SPHINGOMONAS;

BACTERIAL PROTEINS; BIODEGRADATION, ENVIRONMENTAL; CATALYSIS; CLONING, MOLECULAR; ENVIRONMENT; EVOLUTION; GENE TRANSFER TECHNIQUES; HYDROXYLATION; MIXED FUNCTION OXYGENASES; MODELS, CHEMICAL; MODELS, GENETIC; PENTACHLOROPHENOL; PHYLOGENY; SPHINGOMONAS; XENOBIOTICS;

BACTERIA (MICROORGANISMS); SPHINGOMONAS;

EID: 34548160442     PISSN: 09239820     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10532-006-9090-6     Document Type: Review

References (91)

1. Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402
2. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403-410
3. Anandarajah K, Kiefer Jr PM, Donohoe BS, Copley SD (2000) Recruitment of a double bond isomerase to serve as a reductive dehalogenase during biodegradation of pentachlorophenol. Biochemisty 39:5303-5311
4. Apajalahti JH, Karpanoja AP, Salkinoja-Salonen MS (1986) Rhodococcus chlorophenolicus sp. nov., a chlorophenol mineralizing actinomycete. Int J Syst Bacteriol 36:246-251
5. Apajalahti JH, Salkinoja-Salonen MS (1987a) Dechlorination and para-hydroxylation of polychlorinated phenols by Rhodococcus chlorophenolicus. J Bacteriol 169:675-681
6. Apajalahti JHA, Salkinoja-Salonen MS (1987b) Complete dechlorination of tetrachlorohydroquinone by cell extracts of pentachlorophenol-induced Rhodococcus chlorophenolicus. J Bacteriol 169:5125-5130
7. Beaulieu M, Becaert V, Deschenes L, Villemur R (2000) Evolution of bacterial diversity during enrichment of PCP-degrading activated soils. Microb Ecol 40:345-356
8. Berger RS (1983) Occurrence of 2,6-dichlorophenol in Dermacentor albipictus and Haemaphysalis leporispalustris (acari: Ixodidae). J Med Entomol 20:103
9. Bielefeldt AR, Cort T (2005) Dual substrate biodegradation of a nonionic surfactant and pentachlorophenol by Sphingomonas chlorophenolica RA2. Biotechnol Bioeng 89:680-689
10. Boon N, Depuydt S, Verstraete W (2006) Evolutionary algorithms and flow cytometry to examine the parameters influencing transconjugant formation. FEMS Microbiol Ecol 55:17-27
11. LM, Eiras AE, Ferri PH, Lobo AC (2002) The role of 2,6-dichlorophenol as sex pheromone of the tropical horse tick Anocentor nitens (Acari: Ixodidae). Exp Appl Acarol 27:223-230
12. Breitbart M, Miyake JH, Rohwer F (2004) Global distribution of nearly identical phage-encoded DNA sequences. FEMS Microbiol Lett 236:249-256
13. Briglia M, Eggen RI, Van Elsas DJ,De Vos WM (1994) Phylogenetic evidence for transfer of pentachlorophenol-mineralizing Rhodococcus chlorophenolicus PCP-I(T) to the genus Mycobacterium. Int J Syst Bacteriol 44:494-498
14. Cai M, Xun L (2002) Organization and regulation of pentachlorophenol- degrading genes in Sphingobium chlorophenolicum ATCC 39723. J Bacteriol 184:4672-4680
15. Camus JC, Pryor MJ, Medigue C,Cole ST (2002) Re-annotation of the genome sequence of Mycobacterium tuberculosis H37Rv. J Microbiol 148:2967-2973
16. Cassidy MB, Lee H, Trevors JT, Zablotowicz RB (1999) Chlorophenol and nitrophenol metabolism by Sphingomonas sp. UG30. J Ind Microbiol Biotechnol 23:232-241
17. Chai CT (2002) Characterization of PCP-degrading bacteria isolated from a PCP-contaminated site. Master thesis, National Sun Yat-Sen University, Kaohsiung, Taiwan
18. Coenye T, Henry D, Speert DP, Vandamme P (2004) Burkholderia phenoliruptrix sp. nov. to accommodate the 2,4,5-trichlorophenoxyacetic acid and halophenol-degrading strain AC1100. Syst Appl Microbiol 27:623-627
19. Colores GM, Radehaus PM, Schmidt SK (1995) Use of a pentachlorophenol degrading bacterium to bioremediate highly contaminated soil. Appl Biochem Biotechnol 54:271-275
20. Colosio C, Maroni M, Barcellini W, Meroni P, Alcini D, Colombi A, Cavallo D, Foa V (1993) Toxicological and immunological findings in workers exposed to pentachlorophenol (PCP). Arch Environ Health 48:81-88
21. Copley SD (2000) Evolution of a metabolic pathway for degradation of a toxic xenobiotic: the patchwork approach. Trends Biochem Sci 25:261-265
22. Crawford RL, Ederer MM (1999) Phylogeny of Sphingomonas species that degrade pentachlorophenol. J Ind Microbiol Biotechnol 23:320-325
23. Dai M, Copley SD (2004) Genome shuffling improves degradation of the anthropogenic pesticide pentachlorophenol by Sphingobium chlorophenolicum ATCC 39723. Appl Environ Microbiol 70:2391-2397
24. Dai M, Rogers JB, Warner JR, Copley SD (2003) A previously unrecognized step in pentachlorophenol degradation in Sphingobium chlorophenolicum is catalyzed by tetrachlorobenzoquinone reductase (PcpD). J Bacteriol 185:302-310
25. Danganan CE, Ye RW, Daubaras DL, Xun L, Chakrabarty AM (1994) Nucleotide sequence and functional analysis of the genes encoding 2,4,5- trichlorophenoxyacetic acid oxygenase in Pseudomonas cepacia AC1100. Appl Environ Microbiol 60:4100-4106
26. Ederer MM, Crawford RL, Herwig RP, Orser CS (1997) PCP degradation is mediated by closely related strains of the genus Sphingomonas. Mol Ecol 6:39-49
27. Edwards U, Rogall T, Blocker H, Emde M, Bottger E (1989) Isolation and direct complete nucleotide determination of entire genes. Characterization of a gene coding for 16S ribosomal RNA. Nucl Acids Res 17:7843-7853
28. Fenchel T (2003) Biogeography for bacteria. Science 301:925-926
29. Garnier T, Eiglmeier K, Camus JC, Medina N, Mansoor H, Pryor M, Duthoy S, Grondin S, Lacroix C, Monsempe C, Simon S, Harris B, Atkin R, Doggett J, Mayes R, Keating L, Wheeler PR, Parkhill J, Barrell BG, Cole ST, Gordon SV, Hewinson RG (2003) The complete genome sequence of Mycobacterium bovis. Proc Natl Acad Sci USA 100:7877-7882
30. Geng MM, Schuhmacher A, Muehldorfer I, Bensch KW, Schaefer KP, Schneider S, Pohl T, Essig A, Marre R, Melchers K (2003) The genome sequence of Chlamydia pneumoniae TW183 and comparison with other Chlamydia strains based on whole genome sequence analysis (GenBank accession number NC_005043)
31. Gisi MR, Xun L (2003) Characterization of chlorophenol 4-monooxygenase (TftD) and NADH:flavin adenine dinucleotide oxidoreductase (TftC) of Burkholderia cepacia AC1100. J Bacteriol 185:2786-279
32. Golovleva LA, Zaborina O, Pertsova R, Baskunov B, Schurukhin Y, Kuzmin S (1991-92) Degradation of polychlorinated phenols by Streptomyces rochei 303. Biodegradation 2:201-208
33. Gribble GW (1996) Naturally occurring organohalogen compounds-a comprehensive study. In: Herz GW, Kirby RE, Moore RE, Steglich W, Tamm CH (eds) Progress in the Chemistry of Organic Natural Products, Springer-Verlag, Vienna, Austria, pp 1-420
34. Habash MB, Beaudette LA, Cassidy MB, Leung KT, Hoang TA, Vogel HJ, Trevors JT, Lee H (2002) Characterization of tetrachlorohydroquinone reductive dehalogenase from Sphingomonas sp. UG30. Biochem Biophys Res Commun 299:634-640
35. Haggblom MM, Nohynek LJ, Palleroni NJ, Kronqvist K, Nurmiaho-Lassila EL, Salkinoja-Salonen MS, Klatte S, Kroppenstedt RM, Hagglblom MM (1994) Transfer of polychlorophenol-degrading Rhodococcus chlorophenolicus (Apajalahti et al. 1986) to the genus Mycobacterium as Mycobacterium chlorophenolicum comb. nov. Int J Syst Bacteriol 44:485-493. Erratum in: Int J Syst Bacteriol (1994) 44:854
36. Haggblom MM, Nohynek LJ, Salkinoja-Salonen MS (1988) Degradation and O-methylation of chlorinated phenolic compounds by Rhodococcus and Mycobacterium strains. Appl Environ Microbiol 54:3043-3052
37. Heylen K, Vanparys B, Wittebolle L, Verstraete W, Boon N, De Vos P (2006) Cultivation of denitrifying bacteria: optimization of isolation conditions and diversity study. Appl Environ Microbiol 72:2637-2643
38. Ikeda H, Ishikawa J, Hanamoto A, Shinose M, Kikuchi H, Shiba T, Sakaki Y, Hattori M, Omura S (2003) Complete genome sequence and comparative analysis of the industrial microorganism Streptomyces avermitilis. Nat Biotechnol 21:526-531
39. Kaneko T, Nakamura Y, Sato S, Asamizu E, Kato T, Sasamoto S, Watanabe A, Idesawa K, Ishikawa A, Kawashima K, Kimura T, Kishida Y, Kiyokawa C, Kohara M, Matsumoto M, Matsuno A, Mochizuki Y, Nakayama S, Nakazaki N, Shimpo S, Sugimoto M, Takeuchi C, Yamada M, Tabata S (2000) Complete genome structure of the nitrogen-fixing symbiotic bacterium Mesorhizobium loti. DNA Res 7:331-338
40. Kao CM, Chai CT, Liu JK, Yeh TY, Chen KF, Chen SC (2004) Evaluation of natural and enhanced PCP biodegradation at a former pesticide manufacturing plant. Water Res 38:663-672
41. Kao CM, Liu JK, Chen YL, Chai CT, Chen SC (2005) Factors affecting the biodegradation of PCP by Pseudomonas mendocina NSYSU. J Hazard Mater 124:68-73
42. Karlson U, Rojo F, van Elsas JD, Moore E (1996) Genetic and serological evidence for the recognition of four pentachlorophenol degrading bacterial strains as a species of the genus Sphingomonas. Syst Appl Microbiol 18:539-548
43. Lane DJ, Pace B, Olsen GJ, Stahl DA, Sogin ML, Pace NR (1985) Rapid determination of 16S ribosomal RNA sequences for phylogenetic analyses. Proc Nat Acad Sci USA 82:6955-6959
44. Lange CC, Schneider BJ, Orser CS (1996) Verification of the role of PCP 4-monooxygenase in chlorine elimination from pentachlorophenol by Flavobacterium sp. strain ATCC 39723. Biochem Biophys Res Commun 219:146-149
45. Leung KT, Campbell S, Gan Y, White DC, Lee H, Trevors JT (1999) The role of the Sphingomonas species UG30 pentachlorophenol-4-monooxygenase in p-nitrophenol degradation. FEMS Microbiol Lett 173:247-253
46. Leung KT, Cassidy MB, Shaw KW, Lee H, Trevors JT, Lohmeier-Vogel EM, Vogel HJ (1997) Pentachlorophenol biodegradation by Pseudomonas spp. UG25 and UG30. World J Microbiol Biotechnol 13:305-313
47. Li DY, Eberspacher J, Wagner B, Kuntzer J, Lingens F (1991) Degradation of 2,4,6-trichlorophenol by Azotobacter sp. strain GP1. Appl Environ Microbiol 57:1920-1928
48. Louie TM, Webster CM, Xun L (2002) Genetic and biochemical characterization of a 2,4,6-trichlorophenol degradation pathway in Ralstonia eutropha JMP134. J Bacteriol 184:3492-3500
49. Mahmood S, Paton GI, Prosser JI (2005) Cultivation-independent in situ molecular analysis of bacteria involved in degradation of pentachlorophenol in soil. Environ Microbiol 7:1349-1360
50. Mannisto MK, Tiirola MA, Salkinoja-Salonen MS, Kulomaa MS, Puhakka JA. (1999) Diversity of chlorophenol-degrading bacteria isolated from contaminated boreal groundwater. Arch Microbiol 171:189-197
51. Martin-Le Garrec G, Artaud I, Capeillere-Blandin C (2001) Purification and catalytic properties of the chlorophenol 4-monooxygenase from Burkholderia cepacia strain AC1100. Biochim Biophys Acta 1547:288-2301
52. Martins JM, Monrozier JL, Chalamet A, Bardin R (1997) Microbial response to repeated application of low concentrations of pentachlorophenol in an alfisol under pasture. Chemosphere 35:163-1650
53. McCarthy DL, Claude AA, Copley SD (1997) In vivo levels of chlorinated hydroquinones in a pentachlorophenol-degrading bacterium. Appl Environ Microbiol 63:1883-1888
54. Nam IH, Chang Y-S, Hong H-B, Lee H-E (2003) A novel catabolic activity of Pseudomonas veronii in biotransformation of pentachlorophenol. Appl Microbiol Biotechnol 62:284-290
55. Nierman WC, DeShazer D, Kim HS, Tettelin H, Nelson KE, Feldblyum T, Ulrich RL, Ronning CM, Brinkac LM, Daugherty SC, Davidson TD, Deboy RT, Dimitrov G, Dodson RJ, Durkin AS, Gwinn ML, Haft DH, Khouri H, Kolonay JF, Madupu R, Mohammoud Y, Nelson WC, Radune D, Romero CM, Sarria S, Selengut J, Shamblin C, Sullivan SA, White O, Yu Y, Zafar N, Zhou L, Fraser CM (2004) Structural flexibility in the Burkholderia mallei genome. Proc Natl Acad Sci USA 101:14247-14251
56. Nohynek LJ, Suhonen EL, Nurmiaho-Lassila EL, Hantula J, Salkinoja-Salonen M (1995) Description of four pentachlorophenol-degrading bacterial strains as Sphingomonas chlorophenolica sp. nov. Syst Appl Microbiol 18:527-538
57. Ohtsubo Y, Miyauchi K, Kanda K, Hatta T, Kiyohara H, Senda T, Nagata Y, Mitsui Y, Takagi M (1999) PcpA, which is involved in the degradation of pentachlorophenol in Sphingomonas chlorophenolica ATCC39723, is a novel type of ring-cleavage dioxygenase. FEBS Lett 459:395-398
58. Orser CS, Lange CC (1994) Molecular analysis of pentachlorophenol degradation. Biodegradation 5:277-288
59. Orser CS, Lange CC, Xun L, Zahrt TC, Schneider BJ (1993) Cloning, sequence analysis, and expression of the Flavobacterium pentachlorophenol-4- monooxygenase gene in Escherichia coli. J Bacteriol 175:411-416
60. Radehaus PM, Schmidt SK (1992) Characterization of a novel Pseudomonas sp. that mineralizes high concentrations of pentachlorophenol. Appl Environ Microbiol 58:2879-2885
61. Resnik SM, Chapman PJ (1994) Physiological properties and substrate specificity of a pentachlorophenoldegrading Pseudomonas species. Biodegradation 5:47-54
62. Saber D, Crawford RL (1985) Isolation and characterization of pentachlorophenol-degrading Flavobacterium strains. Appl Environ Microbiol 50:1512-1518
63. Saboo VM, Gealt MA (1998) Gene sequences of the pcpB gene of pentachlorophenol-degrading Sphingomonas chlorophenolica found in nondegrading bacteria. Can J Microbiol 44:667-675
64. Shah S, Thakur IS (2003) Enzymatic dehalogenation of pentachlorophenol by Pseudomonas fluorescens of the microbial community from tannery effluent. Curr Microbiol 47:65-70
65. Stanlake GJ, Finn RK (1982) Isolation and characterization of a pentachlorophenol-degrading bacterium. Appl Environ Microbiol 44:1421-1427
66. Steiert JG, Crawford RL (1986) Catabolism of pentachlorophenol by a Flavobacterium sp. Biochem Biophys Res Commun 141:825-830
67. Steiert JG, Pignatello JJ, Crawford RL (1987) Degradation of chlorinated phenols by a pentachlorophenol-degrading bacterium. Appl Environ Microbiol 53:907-910
68. Steinle P, Stucki G, Stettler R, Hanselmann KW (1998) Aerobic mineralization of 2,6-dichlorophenol by Ralstonia sp. strain RK1. Appl Environ Microbiol 64:2566-2571
69. Takami H, Takaki Y, Uchiyama I (2002) Genome sequence of Oceanobacillus iheyensis isolated from the Iheya Ridge and its unexpected adaptive capabilities to extreme environments. Nucl Acids Res 30:3927-3935
70. Takeuchi M, Hamana K, Hiraishi A (2001) Proposal of the genus Sphingomonas sensu stricto and three new genera, Sphingobium, Novosphingobium and Sphingopyxis, on the basis of phylogenetic and chemotaxonomic analyses. Int J Syst Evol Microbiol 51:1405-1417
71. Thakur IS, Verma P, Upadhayaya K. (2002) Molecular cloning and characterization of pentachlorophenol-degrading monooxygenase genes of Pseudomonas sp. from the chemostat. Biochem Biophys Res Comm 290:770-774
72. Tiirola MA, Mannisto MK, Puhakka JA, Kulomaa MS (2002a) Isolation and characterization of Novosphingobium sp. strain MT1, a dominant polychlorophenol-degrading strain in a groundwater bioremediation system. Appl Environ Microbiol 68:173-180
73. Tiirola MA, Wang H, Paulin L, Kulomaa MS (2002b) Evidence for natural horizontal transfer of the pcpB gene in the evolution of polychlorophenol- degrading sphingomonads. Appl Environ Microbiol 68:4495-4501
74. Tomasi I, Artaud I, Bertheau Y, Mansuy D (1995) Metabolism of polychlorinated phenols by Pseudomonas cepacia AC1100: determination of the first two steps and specific inhibitory effect of methimazole. J Bacteriol 177:307-311
75. Top EM, Springael D (2003) The role of mobile genetic elements in bacterial adaptation to xenobiotic organic compounds. Curr Opin Biotechnol 14:262-269
76. Topp E, Xun LY, Orser CS (1992) Biodegradation of the herbicide bromoxynil (3,5-dibromo-4-hydroxybenzonitrile) by purified pentachlorophenol hydroxylase and whole cells of Flavobacterium sp. strain ATCC 39723 is accompanied by cyanogenesis. Appl Environ Microbiol 58:502-506
77. Uotila JS, Kitunen VH, Coote T, Saastamoinen T, Salkinoja-Salonen M, Apajalahti JH (1995) Metabolism of halohydroquinones in Rhodococcus chlorophenolicus PCP-1. Biodegradation 6:119-126
78. Uotila JS, Salkinoja-Salonen MS, Apajalahti JH (1991) Dechlorination of pentachlorophenol by membrane bound enzymes of Rhodococcus chlorophenolicus PCP-I. Biodegradation 2:25-31
79. Vandecasteele FPJ, Hess TF, Crawford RL (2003) Constructing microbial consortia with optimal biomass production using a genetic algorithm. 2003 Genetic and Evolutionary Computation Conference (GECCO): Late-breaking papers, pp 299-302
80. Vandecasteele FPJ (2003) Constructing efficient microbial consortia using a genetic algorithm. Biological applications for genetic and evolutionary computation, Genetic and evolutionary computation conference workshop program, p 69
81. Vandecasteele FPJ, Crawford RL, Hess TF (2006) Demonstrating the suitability of genetic algorithms for driving microbial ecosystems in desirable directions. Antonie von Leeuwenhoek In press
82. Wieser M, Wagner B, Eberspacher J, Lingens F (1997) Purification and characterization of 2,4,6-trichlorophenol-4-monooxygenase, a dehalogenating enzyme from Azotobacter sp. strain GP1. J Bacteriol 179:202-208
83. Xun L (1996) Purification and characterization of chlorophenol 4-monooxygenase from Burkholderia cepacia AC1100. J Bacteriol 178:2645-2649
84. Xun L, Bohuslavek J, Cai M (1999) Characterization of 2,6-dichloro-p-hydroquinone 1,2-dioxygenase (PcpA) of Sphingomonas chlorophenolica ATCC 39723. Biochem Biophys Res Commun 266:322-325
85. Xun L, Orser CS (1991a) Biodegradation of triiodophenol by cell-free extracts of a pentachlorophenol-degrading Flavobacterium sp. Biochem Biophys Res Commun 174:43-48
86. Xun LY, Orser CS (1991b) Purification of a Flavobacterium pentachlorophenol-induced periplasmic protein (PcpA) and nucleotide sequence of the corresponding gene (pcpA). J Bacteriol 173:2920-2926
87. Xun L, Topp E, Orser CS (1992a) Diverse substrate range of a Flavobacterium pentachlorophenol hydroxylase and reaction stoichiometries. J Bacteriol 174:2898-2902
88. Xun L, Topp E, Orser CS (1992b) Purification and characterization of a tetrachloro-p-hydroquinone reductive dehalogenase from a Flavobacterium sp. J Bacteriol 174:8003-8007
89. Yan DZ, Liu H, Zhou NY (2006) Conversion of Sphingobium chlorophenolicum ATCC 39723 to a hexachlorobenzene degrader by metabolic engineering. Appl Environ Microbiol 72:2283-2286
90. Yang CF, Lee CM, Wang CC (2006) Isolation and physiological characterization of the pentachlorophenol degrading bacterium Sphingomonas chlorophenolica. Chemosphere 62:709-714
91. Zaborina O, Baskunov B, Baryshnikova L, Golovleva L (1997) Degradation of pentachlorophenol in soil by Streptomyces rochei 303. J Environ Sci Health B 32:55-70