Applied Microbiology and Biotechnology

, Volume 62, Issue 2–3, pp 110–123 | Cite as

Evolution of catabolic pathways for synthetic compounds: bacterial pathways for degradation of 2,4-dinitrotoluene and nitrobenzene

  • G. R. Johnson
  • J. C. SpainEmail author


The pathways for 2,4-dinitrotoluene (2,4-DNT) and nitrobenzene offer fine illustrations of how the ability to assimilate new carbon sources evolves in bacteria. Studies of the degradation pathways provide insight about two principal strategies for overcoming the metabolic block imposed by nitro- substituents on aromatic compounds. The 2,4-DNT pathway uses novel oxygenases for oxidative denitration and subsequent ring-fission. The nitrobenzene pathway links facile reduction of the nitro- substituent, a novel mutase enzyme, and a conserved operon encoding aminophenol degradation for mineralization of nitrobenzene. Molecular genetic analysis with comparative biochemistry reveals how the pathways were assembled in response to the recent appearance of the two synthetic chemicals in the biosphere.


Atrazine Nitrobenzene Catabolic Pathway Naphthalene Dioxygenase Strain JS45 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.



We thank Gerben Zylstra and Lloyd Nadeau for sharing unpublished data and Shirley Nishino for critical review of the manuscript. The work was supported in part by the Air Force Office of Scientific Research and the Strategic Environmental Research and Development Program.


  1. Ahmad F, Hughes JB (2002) Reactivity of partially reduced arylhydroxylamine and nitrosoarene metabolites of 2,4,6-trinitrotoluene (TNT) toward biomass and humic acids. Environ Sci Technol 36:4370–4381CrossRefPubMedGoogle Scholar
  2. Ahmed ZU, Vining LC (1983) Evidence for a chromosomal location of the genes coding for chloramphenicol production in Streptomyces venezuelae. J Bacteriol 154:239–244PubMedGoogle Scholar
  3. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410CrossRefPubMedGoogle Scholar
  4. Anandarajah K, Kiefer PM Jr, Donohoe BS, Copley SD (2000) Recruitment of a double bond isomerase to serve as a reductive dehalogenase during biodegradation of pentachlorophenol. Biochemistry 39:5303–5311CrossRefPubMedGoogle Scholar
  5. Armstrong RN (2000) Mechanistic diversity in a metalloenzyme superfamily. Biochemistry 39:13625–13632CrossRefPubMedGoogle Scholar
  6. Bang S-W, Zylstra GJ (1996) Cloning and characterization of the genes involved in p-nitrophenol degradation by Pseudomonas fluorescens ENV2030. Abstr Gen Meet Am Soc Microbiol 96:414Google Scholar
  7. Bang S-W, Zylstra GJ (1997) Cloning and sequencing of the hydroquinone 1,2-dioxygenase, 2-hydroxymuconic semialdehyde dehydrogenase, and maleylacetate reductase genes from Pseudomonas fluorescens ENV2030. Abstr Gen Meet Am Soc Microbiol 97:519Google Scholar
  8. Beil S, Timmis KN, Pieper DH (1999) Genetic and biochemical analyses of the tec operon suggest a route for evolution of chlorobenzene degradation genes. J Bacteriol 181:341–346PubMedGoogle Scholar
  9. Blotevogel K-H, Gorontzy T (2000) Microbial degradation of compounds with nitro functions. In: Rehm H-J, Reed G, Pühler A, Stadler P (eds) Biotechnology. Wiley–VCH, Weinheim, pp 274–294Google Scholar
  10. Bryant C, DeLuca M (1991) Purification and characterization of an oxygen-insensitive NAD(P)H nitroreductase from Enterobacter cloacae. J Biol Chem 266:4119–4125PubMedGoogle Scholar
  11. Cases I, de Lorenzo V (2001) The black cat/white cat principle of signal integration in bacterial promoters. EMBO J 20:1–11PubMedGoogle Scholar
  12. Cerniglia CE, Somerville CC (1995) Reductive metabolism of nitroaromatic and nitropolycyclic aromatic hydrocarbons. In: Spain JC (ed) Biodegradation of nitroaromatic compounds. Plenum, New York, pp 99–115Google Scholar
  13. Chapman PJ, Ribbons DW (1976a) Metabolism of resorcinylic compounds by bacteria: alternative pathways for resorcinol catabolism in Pseudomonas putida. J Bacteriol 125:985–998PubMedGoogle Scholar
  14. Chapman PJ, Ribbons DW (1976b) Metabolism of resorcinylic compounds by bacteria: orcinol pathway in Pseudomonas putida. J Bacteriol 125:975–984PubMedGoogle Scholar
  15. Crawford RL (1993) The microbiology and treatment of nitroaromatic compounds. Curr Opin Biotechnol 6:329–336CrossRefGoogle Scholar
  16. Dagley S (1986) Biochemistry of aromatic hydrocarbon degradation in pseudomonads. In: Sokatch JR (ed) The Bacteria. Academic Press, New York, pp 527–555Google Scholar
  17. Dai M, Rogers JB, Warner JR, Copley SD (2003) A previously unrecognized step in Sphingobium chlorophenolicum is catalyzed by tetrachlorobenzoquinone reductase (PcpD). J Bacteriol 195:302–310Google Scholar
  18. Davis JK, He Z, Somerville CC, Spain JC (1999) Genetic and biochemical comparison of 2-aminophenol-1,6-dioxygenase of Pseudomonas pseudoalcaligenes JS45 to meta-cleavage dioxygenases: divergent evolution of 2-aminophenol meta-cleavage pathway. Arch Microbiol 172:330–339CrossRefPubMedGoogle Scholar
  19. Davis JK, Paoli GC, He Z, Nadeau LJ, Somerville CC, Spain JC (2000) Sequence analysis and initial characterization of two isozymes of hydroxylaminobenzene mutase from Pseudomonas pseudoalcaligenes JS45. Appl Environ Microbiol 66:2965–2971CrossRefPubMedGoogle Scholar
  20. de Souza ML, Wackett LP, Sadowsky MJ (1998) The atzABC genes encoding atrazine catabolism are located on a self-transmissible plasmid in Pseudomonas sp. strain ADP. A van derppl Environ Microbiol 64:2323–2326PubMedGoogle Scholar
  21. Dua M, Singh A, Sethunathan N, Johri AK (2002) Biotechnology and bioremediation: successes and limitations. Appl Microbiol Biotechnol 59:143–152CrossRefPubMedGoogle Scholar
  22. Duque E, Haidour A, Godoy F, Ramos JL (1993) Construction of a Pseudomonas hybrid strain that mineralizes 2,4,6-trinitrotoluene. J Bacteriol 175:2278–2283PubMedGoogle Scholar
  23. Eaton RW, Karns JS (1991) Cloning and comparison of the DNA encoding ammelide aminohydrolase and cyanuric acid amidohydrolase from three s-triazine-degrading bacterial strains. J Bacteriol 173:1363–1366PubMedGoogle Scholar
  24. Ebert S, Rieger P-G, Knackmuss H-J (1999) Function of coenzyme F420 in aerobic catabolism of 2,4, 6-trinitrophenol and 2,4-dinitrophenol by Nocardioides simplex FJ2-1A. J Bacteriol 181:2669–2674PubMedGoogle Scholar
  25. Ebert S, Fischer P, Knackmuss HJ (2001) Converging catabolism of 2,4,6-trinitrophenol (picric acid) and 2,4-dinitrophenol by Nocardioides simplex FJ2-1A. Biodegradation 12:367–376CrossRefPubMedGoogle Scholar
  26. Eltis LD, Bolin JT (1996) Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178:5930–5937PubMedGoogle Scholar
  27. Erickson BD, Mondello FJ (1992) Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400. J Bacteriol 174:2903–2912PubMedGoogle Scholar
  28. Esteve-Nuñez A, Ramos JL (1998) Metabolism of 2,4,6-trinitrotoluene by Pseudomonas sp. JLR11. Environ Sci Technol 32:3802–3808CrossRefGoogle Scholar
  29. Esteve-Nuñez A, Lucchesi G, Philipp B, Schink B, Ramos JL (2000) Respiration of 2,4,6-trinitrotoluene by Pseudomonas sp. strain JLR11. J Bacteriol 182:1352–1355CrossRefPubMedGoogle Scholar
  30. Esteve-Nuñez A, Caballero A, Ramos JL (2001) Biological degradation of 2,4,6-trinitrotoluene. Microbiol Mol Biol Rev 65:335–352PubMedGoogle Scholar
  31. Fredrickson JK, Brockman FJ, Workman DJ, Li SW, Stevens TO (1991) Isolation and characterization of a subsurface bacterium capable of growth on toluene, naphthalene, and other aromatic compounds. Appl Environ Microbiol 57:796–803Google Scholar
  32. Fuenmayor SL, Wild M, Boyes AL, Williams PA (1998) A gene cluster encoding steps in conversion of naphthalene to gentisate in Pseudomonas sp. strain U2. J Bacteriol 180:2522–2530PubMedGoogle Scholar
  33. Gibson DT, Cruden DL, Haddock JD, Zylstra GJ, Brand JM (1993) Oxidation of polychlorinated biphenyls by Pseudomonas sp. strain LB400 and Pseudomonas psuedoalcaligenes KF707. J Bacteriol 175:4561–4564PubMedGoogle Scholar
  34. Goyal AK, Zylstra GJ (1997) Genetics of naphthalene and phenanthrene degradation by Comamonas testosteroni. Ind Microbiol Biotechnol 19:401–407CrossRefPubMedGoogle Scholar
  35. Gribble GW (1998) Naturally occurring organohalogen compounds. Acta Chem Res 31:141–152CrossRefGoogle Scholar
  36. Haigler BE, Suen W-C, Spain JC (1996) Purification and sequence analysis of 4-methyl-5-nitrocatechol oxygenase from Burkholderia sp. strain DNT. J Bacteriol 178:6019–6024PubMedGoogle Scholar
  37. Haigler BE, Johnson GR, Suen W-C, Spain JC (1999) Biochemical and genetic evidence for meta-ring cleavage of 2,4,5-trihydroxytoluene in Burkholderia sp. strain DNT. J Bacteriol 181:965–972PubMedGoogle Scholar
  38. Haigler BH, Nishino SF, Spain JC (1994) Biodegradation of 4-methyl-5-nitrocatechol by Pseudomonas sp. strain DNT. J Bacteriol 176:3433–3447PubMedGoogle Scholar
  39. Hanne LF, Kirk LL, Appel SM, Narayan AD, Bains KK (1993) Degradation and induction specificity in actinomycetes that degrade p-nitrophenol. Appl Environ Microbiol 59:3505–3508PubMedGoogle Scholar
  40. Harayama S, Kok M, Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601PubMedGoogle Scholar
  41. Harper DB (1994) Biosynthesis of halogenated methanes. Biochem Soc Trans 22:1007–1011PubMedGoogle Scholar
  42. Hasegawa Y, Muraki T, Tokuyama T, Iwaki H, Tatsuno M, Lau PCK (2000) A novel degradative pathway of 2-nitrobenzoate via 3-hydroxyanthranilate in Pseudomonas fluorescens strain KU-7. FEMS Micro Lett 190:185–190CrossRefGoogle Scholar
  43. He ZQ, Spain JC (1997) Studies of the catabolic pathway of degradation of nitrobenzene by Pseudomonas pseudoalcaligenes JS45: removal of the amino group from 2-aminomuconic semialdehyde. Appl Environ Microbiol 63:4839–4843PubMedGoogle Scholar
  44. He ZQ, Spain JC (1998) A novel 2-aminomuconate deaminase in the nitrobenzene degradation pathway of Pseudomonas pseudoalcaligenes JS45. J Bacteriol 180:2502–2506PubMedGoogle Scholar
  45. He ZQ, Spain JC (1999) Comparison of the downstream pathways for degradation of nitrobenzene by Pseudomonas pseudoalcaligenes JS45 (2-aminophenol pathway) and by Comamonas sp. JS765 (catechol pathway). Arch Microbiol 171:309–316CrossRefPubMedGoogle Scholar
  46. He ZQ, Davis JK, Spain JC (1998) Purification, characterization, and sequence analysis of 2-aminomuconic 6-semialdehyde dehydrogenase from Pseudomonas pseudoalcaligenes JS45. J Bacteriol 180:4591–4595PubMedGoogle Scholar
  47. Heiss G, Knackmuss H-J (2002) Bioelimination of trinitroaromatic compounds: immobilization versus mineralization. Curr Opin Microbiol 5:282–287CrossRefPubMedGoogle Scholar
  48. Heiss G, Hofmann KW, Tractmann N, Walters DM, Rouvière P, Knackmuss H-J (2002) npd gene functions of Rhodococcus (opacus) erythropolis HL PM-1 in the initial steps of 2,4,6-trinitrophenol degradation. Microbiol 148:799–806Google Scholar
  49. Hughes MA, Williams PA (2001) Cloning and characterization of the pnb genes, encoding enzymes for 4-nitrobenzoate catabolism in Pseudomonas putida TW3. J Bacteriol 183:1225–1232CrossRefPubMedGoogle Scholar
  50. James KD, Williams PA (1998) ntn genes determining the early steps in the divergent catabolism of 4-nitrotoluene and toluene in Pseudomonas sp. strain TW3. J Bacteriol 180:2043–2049PubMedGoogle Scholar
  51. James KD, Hughes MA, Williams PA (2000) Cloning and expression of ntnD, encoding a novel NAD(P)(+)-independent 4-nitrobenzyl alcohol dehydrogenase from Pseudomonas sp. strain TW3. J Bacteriol 182:3136–3141CrossRefPubMedGoogle Scholar
  52. Jiang HY, Parales RE, Lynch NA, Gibson DT (1996) Site directed mutagenesis of conserved amino acids in the alpha-subunit of toluene dioxygenase-potential mononuclear non-heme iron coordination sites. J Bacteriol 178:3133–3139PubMedGoogle Scholar
  53. Johnson GR, Jain RK, Spain JC (2000) Properties of the trihydroxytoluene oxygenase from Burkholderia cepacia R34; an extradiol dioxygenase from the 2,4-dinitrotoluene pathway. Arch Microbiol 173:86–90CrossRefPubMedGoogle Scholar
  54. Johnson GR, Jain RK, Spain JC (2002) Origins of the 2,4-dinitrotoluene pathway. J Bacteriol 184:4219–4232CrossRefPubMedGoogle Scholar
  55. Katsivela E, Wray V, Pieper DH, Wittich R-M (1999) Initial reactions in the biodegradation of 1-chloro-4-nitrobenzene by a newly isolated bacterium, strain LW1. Appl Environ Microbiol 65:1405–1412PubMedGoogle Scholar
  56. Kimura N, Nishi A, Goto M, Furukawa K (1997) Functional analyses of a variety of chimeric dioxygenases constructed from two biphenyl dioxygenases that are similar structurally but different functionally. J Bacteriol 179:3936–3943PubMedGoogle Scholar
  57. Kirner S, Hammer PE, Hill DS, Altmann A, Fischer I, Weislo LJ, Lanahan M, Pée K-H van, Ligon JM (1998) Functions encoded by pyrrolnitrin biosynthetic genes from Pseudomonas fluorescens. J Bacteriol 180:1939–1943PubMedGoogle Scholar
  58. Knackmuss H-J (1996) Basic knowledge and perspectives of bioelimination of xenobiotic compounds. J Biotechnol 51:287–295CrossRefGoogle Scholar
  59. Koder RL, Miller A-F (1998) Steady-state kinetic mechanism, stereospecificity, substrate and inhibitor specificity of Enterobacter cloacae nitroreductase. Biochim Biophys Acta 1387:395–405CrossRefPubMedGoogle Scholar
  60. Lee K, Gibson DT (1996) Toluene and ethylbenzene oxidation by purified naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816-4. Appl Environ Microbiol 62:3101–3106PubMedGoogle Scholar
  61. Lendenmann U, Spain JC (1996) 2-Aminophenol 1,6-dioxygenase: a novel aromatic ring cleavage enzyme purified from Pseudomonas pseudoalcaligenes JS45. J Bacteriol 178:6227–6232PubMedGoogle Scholar
  62. Lessner DJ, Johnson GR, Parales RE, Spain JC, Gibson DT (2002) Molecular characterization and substrate specificity of nitrobenzene dioxygenase from Comamonas sp. strain JS765. Appl Environ Microbiol 68:634–641CrossRefPubMedGoogle Scholar
  63. Leung KT, Tresse O, Errampalli D, Lee H, Trevors JT (1997) Mineralization of p-nitrophenol by pentachlorophenol-degrading Sphingomonas spp. FEMS Microbiol Lett 155:107–114CrossRefGoogle Scholar
  64. 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 173:247–253CrossRefPubMedGoogle Scholar
  65. Marchler-Bauer A, Anderson JB, DeWeese-Scott C, Fedorova ND, Geer LY, He S, Hurwitz DI, Jackson JD, Jacobs AR, Lanczycki CJ, Liebert CA, Liu C, Madej T, Marchler GH, Mazumder R, Nikolskaya AN, Panchenko AR, Rao BS, Shoemaker BA, Simonyan V, Song JS, Thiessen PA, Vasudevan S, Wang Y, Yamashita RA, Yin JJ, Bryant SH (2003) CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res 31:383–387CrossRefPubMedGoogle Scholar
  66. Michán C, Delgado A, Haïdour A, Lucchesi G, Ramos JL (1997) In vivo construction of a hybrid pathway for metabolism of 4-nitrotoluene in Pseudomonas fluorescens. J Bacteriol 63:3036–3038Google Scholar
  67. Mondello FJ, Turcich MP, Lobos JH, Erickson BD (1997) Identification and modification of biphenyl dioxygenase sequences that determine the specificity of polychlorinated biphenyl degradation. Appl Environ Microbiol 63:3096–3103PubMedGoogle Scholar
  68. Morrissey JP, Osbourn AE (1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 63:708–724PubMedGoogle Scholar
  69. Moser R, Stahl U (2001) Insights into the genetic diversity of initial dioxygenases from PAH-degrading bacteria. Appl Microbiol Biotechnol 55:609–618PubMedGoogle Scholar
  70. Müller T, Werlen C, Spain JC, van der Meer JR (2003) Evolution of a chlorobenzene degradative pathway among bacteria in a contaminated groundwater mediated by a genomic island in Ralstonia. Environ Microbiol 5 (in press)Google Scholar
  71. Nadeau LJ, He Z, Spain JC (2003) Bacterial conversion of hydroxylaminoaromatic compounds by both lyase and mutase enzymes involve intramolecular transfer of hydroxyl groups. Appl Environ Microbiol 69 (in press)Google Scholar
  72. Nam JW, Nojiri H, Yoshida T, Habe H, Yamane H, Omori T (2001) New classification system for oxygenase components involved in ring-hydroxylating oxygenations. Biosci Biotechnol Biochem 65:254–263CrossRefPubMedGoogle Scholar
  73. Nishino SF, Spain JC (1993) Degradation of nitrobenzene by a Pseudomonas pseudoalcaligenes. Appl Environ Microbiol 59:2520–2525PubMedGoogle Scholar
  74. Nishino SF, Paoli G, Spain JC (2000a) Aerobic degradation of dinitrotoluenes and pathway for bacterial degradation of 2,6-dinitrotoluene. Appl Environ Microbiol 66:2139–2147CrossRefPubMedGoogle Scholar
  75. Nishino SF, Spain JC, He Z (2000b) Strategies for aerobic degradation of nitroaromatic compounds by bacteria: process discovery to field application. In: Spain JC, Hughes JB, Knackmuss H-J (eds) Biodegradation of nitroaromatic compounds and explosives. Lewis, Boca Raton, Fla., pp 7–62Google Scholar
  76. Parales JV, Kumar A, Parales RE, Gibson DT (1996) Cloning and sequencing of the genes encoding 2-nitrotoluene dioxygenase from Pseudomonas sp. JS42. Gene 181:57–61CrossRefPubMedGoogle Scholar
  77. Parales JV, Parales RE, Resnick SM, Gibson DT (1998a) Enzyme specificity of 2-nitrotoluene 2,3-dioxygenase from Pseudomonas sp. strain JS42 is determined by the C-terminal region of the alpha subunit of the oxygenase component. J Bacteriol 180:1194–1199PubMedGoogle Scholar
  78. Parales RE (2000) Molecular biology of nitroarene degradation. In: Spain JC, Hughes EJ, Knackmuss H-J (eds) Biodegradation of nitroaromatic compounds and explosives. Lewis, Boca Raton, Fla., pp 63–90Google Scholar
  79. Parales RE, Emig MD, Lynch NA, Gibson DT (1998b) Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems. J Bacteriol 180: 2337–2344PubMedGoogle Scholar
  80. Parales RE, Lee K, Resnick SM, Jiang HY, Lessner DJ, Gibson DT (2000) Substrate specificity of naphthalene dioxygenase: effect of specific amino acids at the active site of the enzyme. J Bacteriol 182:1641–1649PubMedGoogle Scholar
  81. Park H-S, Kim H-S (2000) Identification and characterization of the nitrobenzene catabolic plasmids pNB1 and pNB2 in Pseudomonas putida HS12. J Bacteriol 182:573–580CrossRefPubMedGoogle Scholar
  82. Park H-S, Kim H-S (2001) Genetic and structural organization of the aminophenol catabolic operon and its implication for evolutionary process. J Bacteriol 183:5074–5081CrossRefPubMedGoogle Scholar
  83. Park H-S, Lim S-J, Chang YK, Livingston AG, Kim H-S (1999) Degradation of chloronitrobenzenes by a coculture of Pseudomonas putida and a Rhodococcus sp. Appl Environ Microbiol 65:1083–1091PubMedGoogle Scholar
  84. Peres CM, Agathos SN (2000) Biodegradation of nitroaromatic pollutants: from pathways to remediation. Biotechnol Annu Rev 6:197–220PubMedGoogle Scholar
  85. Perry L, Zylstra GJ (1999) Biochemical and molecular analysis of hydroxyquinol 1,2-dioxygenase involved in p-nitrophenol degradation by Arthrobacter sp. strain JS443. Abstr Gen Meet Am Soc Microbiol 99:581Google Scholar
  86. Poelarends GJ, Kulakov LA, Larkin MJ, Vlieg JETV, Janssen DB (2000) Roles of horizontal gene transfer and gene integration in evolution of 1,3-dichloropropene- and 1,2-dibromoethane-degradative pathways. J Bacteriol 182:2191–2199PubMedGoogle Scholar
  87. Reineke W (1998) Development of hybrid strains for the mineralization of chloroaromatics by patchwork assembly. Annu Rev Microbiol 52:287–331PubMedGoogle Scholar
  88. Riefler RG, Smets BF (2002) NAD(P)H:flavin mononucleotide oxidoreductase inactivation during 2,4,6-trinitrotoluene reduction. Appl Environ Microbiol 68:1690–1696CrossRefPubMedGoogle Scholar
  89. Rieger P-G, Meier HM, Gerle M, Vogt U, Groth T, Knackmuss H-J (2002) Xenobiotics in the environment: present and future strategies to obviate the problem of biological persistence. J Biotechnol 94:101–123CrossRefPubMedGoogle Scholar
  90. Rodgers JD, Bunce NJ (2001) Treatment methods for the remediation of nitroaromatic explosives. Water Res 35:2101–2111CrossRefPubMedGoogle Scholar
  91. Sakamoto T, Joern JM, Arisawa A, Arnold FH (2001) Laboratory evolution of toluene dioxygenase to accept 4-picoline as a substrate. Appl Environ Microbiol 67:3882–3887CrossRefPubMedGoogle Scholar
  92. Sander P, Wittaich R-M, Fortnagel P, Wilkes H, Francke W (1991) Degradation of 1,2,4-trichloro- and 1,2,4,5-tetrachlorobenzene by Pseudomonas strains. Appl Environ Microbiol 57:1430–1440Google Scholar
  93. Schenzle A, Lenke H, Spain JC, Knackmuss H-J (1999a) Chemoselective nitro group reduction and reductive dechlorination initiate degradation of 2-chloro-5-nitrophenol by Ralstonia eutropha JMP134. Appl Environ Microbiol 65:2317–2323PubMedGoogle Scholar
  94. Schenzle A, Lenke H, Spain JC, Knackmuss H-J (1999b) 3-Hydroxylaminophenol mutase from Ralstonia eutropha JMP134 catalyzes a Bamberger rearrangement. J Bacteriol 181:1444–1450PubMedGoogle Scholar
  95. Snellinx Z, Nepovim A, Taghavi S, Vangronsveld J, Vanek T, van der Lilie D (2002) Biological remediation of explosives and related nitroaromatic compounds. Environ Sci Pollut Res Int 9:48–61PubMedGoogle Scholar
  96. Somerville CC, Nishino SF, Spain JC (1995) Purification and characterization of nitrobenzene nitroreductase from Pseudomonas pseudoalcaligenes JS45. J Bacteriol 177:3837–3842PubMedGoogle Scholar
  97. Spain JC (1995) Biodegradation of nitroaromatic compounds. Annu Rev Microbiol 49:523–555CrossRefPubMedGoogle Scholar
  98. Spain JC, Gibson DT (1991) Pathway for biodegradation of p-nitrophenol in a Moraxella sp. Appl Environ Microbiol 57:812–819Google Scholar
  99. Spanggord RJ, Spain JC, Nishino SF, Mortelmans KE (1991) Biodegradation of 2,4-dinitrotoluene by a Pseudomonas sp. Appl Environ Microbiol 57:3200–3205PubMedGoogle Scholar
  100. Spiess T, Desiere F, Fischer P, Spain JC, Knackmuss H-J, Lenke H (1998) A new 4-nitrotoluene degradation pathway in a Mycobacterium strain. Appl Environ Microbiol 64:446–452PubMedGoogle Scholar
  101. Suen WC, Gibson DT (1993) Isolation and preliminary characterization of the subunits of the terminal component of naphthalene dioxygenase from Pseudomonas putida 9816-4. J Bacteriol 175:5877–5881PubMedGoogle Scholar
  102. Suen W-C, Spain JC (1993) Cloning and characterization of Pseudomonas sp. strain DNT genes for 2,4-dinitrotoluene degradation. J Bacteriol 175:1831–1837PubMedGoogle Scholar
  103. Suen W-C, Haigler BE, Spain JC (1996) 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase. J Bacteriol 178:4926–4934PubMedGoogle Scholar
  104. Takenaka S, Murakami S, Shinke R, Hatakeyama K, Yukawa H, Aoki K (1997) Novel genes encoding 2-aminophenol 1,6-dioxygenase from Pseudomonas species AP-3 growing on 2-aminophenol and catalytic properties of the purified enzyme. J Biol Chem 272:14727–14732CrossRefPubMedGoogle Scholar
  105. Takenaka S, Murakami S, Shinke R, Aoki K (1998) Metabolism of 2-aminophenol by Pseudomonas sp. AP-3: modified meta-cleavage pathway. Arch Microbiol 170:132–137CrossRefPubMedGoogle Scholar
  106. Takenaka S, Murakami S, Kim Y-J, Aoki K (2000) Complete nucleotide sequence and functional analysis of the genes for 2-aminophenol metabolism from Pseudomonas sp. AP-3. Arch MicrobiolGoogle Scholar
  107. van der Meer JR, Werlen C, Nishino SF, Spain JC (1998) Evolution of a pathway for chlorobenzene metabolism leads to natural attenuation in a contaminated groundwater. Appl Environ Microbiol 64:4185–4193PubMedGoogle Scholar
  108. Vorbeck C, Lenke H, Fischer P, Knackmuss H-J (1994) Identification of a hydride-Meisenheimer complex as a metabolite of 2,4,6-trinitrotoluene by a Mycobacterium strain. J Bacteriol 176:932–934PubMedGoogle Scholar
  109. Wackett LP, Hershberger CD (2001) Biocatalysis and Biodegradation. ASM Press, Washington, D.C.Google Scholar
  110. Walters DM, Russ R, Knackmuss H-J, Rouvière P (2001) High-density sampling of a bacterial operon using mRNA differential display. Gene 273:305–313CrossRefPubMedGoogle Scholar
  111. Werlen C, Kohler H-PE, van der Meer JR (1996) The broad substrate chlorobenzene dioxygenase and cis-chlorobenzene dihydrodiol dehydrogenase of Pseudomonas sp. strain P51 are linked evolutionarily to the enzymes for benzene and toluene degradation. J Biol Chem 271:4009–4016Google Scholar
  112. Xu L, Resing K, Lawson SL, Babbitt PC, Copley SD (1999) Evidence that pcpA encodes 2,6-dichlorohydroquinone dioxygenase, the ring cleavage enzyme required for pentachlorophenol degradation in Sphingomonas chlorophenolica strain ATCC 39723. Biochemistry 38:7659–7669CrossRefPubMedGoogle Scholar
  113. Yabannavar AV, Zylstra GJ (1995) Cloning and characterization of the genes for p-nitrobenzoate degradation from Pseudomonas pickettii YH105. Appl Environ Microbiol 61:4284–4290PubMedGoogle Scholar
  114. Yu C-L, Parales RE, Gibson DT (2001) Multiple mutations at the active site of naphthalene dioxygenase affect regioselectivity and enantioselectivity. Ind Microbiol Biotechnol 27:94–103CrossRefPubMedGoogle Scholar
  115. Zhou NY, Al-Dulayymi J, Baird MS, Williams PA (2002) Salicylate 5-hydroxylase from Ralstonia sp. strain U2: a monooxygenase with close relationships to and shared electron transport proteins with naphthalene dioxygenase. J Bacteriol 184:1547–1555CrossRefPubMedGoogle Scholar
  116. Zylstra GJ, Bang S-W, Newman LM, Perry L (2000) Microbial degradation of mononitrophenols and mononitrobenzoates. In: Spain JC, Hughes JB, Knackmuss H-J (eds) Biodegradation of nitroaromatic compounds and explosives. Lewis, Boca Raton, Fla., pp 145–160Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Air Force Research LaboratoryUnited States Air ForceTyndall Air Force BaseUSA

Personalised recommendations