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

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Abstract.

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.

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References

  • 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 36:4370–4381

    Article  CAS  PubMed  Google Scholar 

  • Ahmed ZU, Vining LC (1983) Evidence for a chromosomal location of the genes coding for chloramphenicol production in Streptomyces venezuelae. J Bacteriol 154:239–244

    CAS  PubMed  Google Scholar 

  • Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215:403–410

    Article  CAS  PubMed  Google Scholar 

  • 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 39:5303–5311

    Article  CAS  PubMed  Google Scholar 

  • Armstrong RN (2000) Mechanistic diversity in a metalloenzyme superfamily. Biochemistry 39:13625–13632

    Article  CAS  PubMed  Google Scholar 

  • 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 96:414

    Google Scholar 

  • 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 97:519

    Google Scholar 

  • 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 181:341–346

    CAS  PubMed  Google Scholar 

  • 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 274–294

  • Bryant C, DeLuca M (1991) Purification and characterization of an oxygen-insensitive NAD(P)H nitroreductase from Enterobacter cloacae. J Biol Chem 266:4119–4125

    CAS  PubMed  Google Scholar 

  • Cases I, de Lorenzo V (2001) The black cat/white cat principle of signal integration in bacterial promoters. EMBO J 20:1–11

    CAS  PubMed  Google Scholar 

  • 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 99–115

  • Chapman PJ, Ribbons DW (1976a) Metabolism of resorcinylic compounds by bacteria: alternative pathways for resorcinol catabolism in Pseudomonas putida. J Bacteriol 125:985–998

    CAS  PubMed  Google Scholar 

  • Chapman PJ, Ribbons DW (1976b) Metabolism of resorcinylic compounds by bacteria: orcinol pathway in Pseudomonas putida. J Bacteriol 125:975–984

    CAS  PubMed  Google Scholar 

  • Crawford RL (1993) The microbiology and treatment of nitroaromatic compounds. Curr Opin Biotechnol 6:329–336

    Article  Google Scholar 

  • Dagley S (1986) Biochemistry of aromatic hydrocarbon degradation in pseudomonads. In: Sokatch JR (ed) The Bacteria. Academic Press, New York, pp 527–555

  • Dai M, Rogers JB, Warner JR, Copley SD (2003) A previously unrecognized step in Sphingobium chlorophenolicum is catalyzed by tetrachlorobenzoquinone reductase (PcpD). J Bacteriol 195:302–310

    Google Scholar 

  • 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 172:330–339

    Article  CAS  PubMed  Google Scholar 

  • 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 66:2965–2971

    Article  CAS  PubMed  Google Scholar 

  • 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 64:2323–2326

    PubMed  Google Scholar 

  • Dua M, Singh A, Sethunathan N, Johri AK (2002) Biotechnology and bioremediation: successes and limitations. Appl Microbiol Biotechnol 59:143–152

    Article  CAS  PubMed  Google Scholar 

  • Duque E, Haidour A, Godoy F, Ramos JL (1993) Construction of a Pseudomonas hybrid strain that mineralizes 2,4,6-trinitrotoluene. J Bacteriol 175:2278–2283

    CAS  PubMed  Google Scholar 

  • 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 173:1363–1366

    CAS  PubMed  Google Scholar 

  • 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 181:2669–2674

    CAS  PubMed  Google Scholar 

  • 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 12:367–376

    Article  CAS  PubMed  Google Scholar 

  • Eltis LD, Bolin JT (1996) Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178:5930–5937

    CAS  PubMed  Google Scholar 

  • 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 174:2903–2912

    PubMed  Google Scholar 

  • Esteve-Nuñez A, Ramos JL (1998) Metabolism of 2,4,6-trinitrotoluene by Pseudomonas sp. JLR11. Environ Sci Technol 32:3802–3808

    Article  Google Scholar 

  • 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 182:1352–1355

    Article  PubMed  Google Scholar 

  • Esteve-Nuñez A, Caballero A, Ramos JL (2001) Biological degradation of 2,4,6-trinitrotoluene. Microbiol Mol Biol Rev 65:335–352

    PubMed  Google Scholar 

  • 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 57:796–803

    CAS  Google Scholar 

  • 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 180:2522–2530

    CAS  PubMed  Google Scholar 

  • 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 175:4561–4564

    CAS  PubMed  Google Scholar 

  • Goyal AK, Zylstra GJ (1997) Genetics of naphthalene and phenanthrene degradation by Comamonas testosteroni. Ind Microbiol Biotechnol 19:401–407

    Article  CAS  PubMed  Google Scholar 

  • Gribble GW (1998) Naturally occurring organohalogen compounds. Acta Chem Res 31:141–152

    Article  CAS  Google Scholar 

  • 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 178:6019–6024

    CAS  PubMed  Google Scholar 

  • 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 181:965–972

    CAS  PubMed  Google Scholar 

  • Haigler BH, Nishino SF, Spain JC (1994) Biodegradation of 4-methyl-5-nitrocatechol by Pseudomonas sp. strain DNT. J Bacteriol 176:3433–3447

    CAS  PubMed  Google Scholar 

  • Hanne LF, Kirk LL, Appel SM, Narayan AD, Bains KK (1993) Degradation and induction specificity in actinomycetes that degrade p-nitrophenol. Appl Environ Microbiol 59:3505–3508

    CAS  PubMed  Google Scholar 

  • Harayama S, Kok M, Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu Rev Microbiol 46:565–601

    CAS  PubMed  Google Scholar 

  • Harper DB (1994) Biosynthesis of halogenated methanes. Biochem Soc Trans 22:1007–1011

    CAS  PubMed  Google Scholar 

  • 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 190:185–190

    Article  CAS  Google Scholar 

  • 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 63:4839–4843

    CAS  PubMed  Google Scholar 

  • He ZQ, Spain JC (1998) A novel 2-aminomuconate deaminase in the nitrobenzene degradation pathway of Pseudomonas pseudoalcaligenes JS45. J Bacteriol 180:2502–2506

    CAS  PubMed  Google Scholar 

  • 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 171:309–316

    Article  CAS  PubMed  Google Scholar 

  • He ZQ, Davis JK, Spain JC (1998) Purification, characterization, and sequence analysis of 2-aminomuconic 6-semialdehyde dehydrogenase from Pseudomonas pseudoalcaligenes JS45. J Bacteriol 180:4591–4595

    CAS  PubMed  Google Scholar 

  • Heiss G, Knackmuss H-J (2002) Bioelimination of trinitroaromatic compounds: immobilization versus mineralization. Curr Opin Microbiol 5:282–287

    Article  CAS  PubMed  Google Scholar 

  • 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 148:799–806

    CAS  Google Scholar 

  • Hughes MA, Williams PA (2001) Cloning and characterization of the pnb genes, encoding enzymes for 4-nitrobenzoate catabolism in Pseudomonas putida TW3. J Bacteriol 183:1225–1232

    Article  CAS  PubMed  Google Scholar 

  • 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 180:2043–2049

    CAS  PubMed  Google Scholar 

  • 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 182:3136–3141

    Article  CAS  PubMed  Google Scholar 

  • 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 178:3133–3139

    CAS  PubMed  Google Scholar 

  • 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 173:86–90

    Article  CAS  PubMed  Google Scholar 

  • Johnson GR, Jain RK, Spain JC (2002) Origins of the 2,4-dinitrotoluene pathway. J Bacteriol 184:4219–4232

    Article  CAS  PubMed  Google Scholar 

  • 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 65:1405–1412

    CAS  PubMed  Google Scholar 

  • 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 179:3936–3943

    CAS  PubMed  Google Scholar 

  • 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 180:1939–1943

    CAS  PubMed  Google Scholar 

  • Knackmuss H-J (1996) Basic knowledge and perspectives of bioelimination of xenobiotic compounds. J Biotechnol 51:287–295

    Article  CAS  Google Scholar 

  • Koder RL, Miller A-F (1998) Steady-state kinetic mechanism, stereospecificity, substrate and inhibitor specificity of Enterobacter cloacae nitroreductase. Biochim Biophys Acta 1387:395–405

    Article  CAS  PubMed  Google Scholar 

  • Lee K, Gibson DT (1996) Toluene and ethylbenzene oxidation by purified naphthalene dioxygenase from Pseudomonas sp. strain NCIB 9816-4. Appl Environ Microbiol 62:3101–3106

    CAS  PubMed  Google Scholar 

  • Lendenmann U, Spain JC (1996) 2-Aminophenol 1,6-dioxygenase: a novel aromatic ring cleavage enzyme purified from Pseudomonas pseudoalcaligenes JS45. J Bacteriol 178:6227–6232

    CAS  PubMed  Google Scholar 

  • 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 68:634–641

    Article  CAS  PubMed  Google Scholar 

  • Leung KT, Tresse O, Errampalli D, Lee H, Trevors JT (1997) Mineralization of p-nitrophenol by pentachlorophenol-degrading Sphingomonas spp. FEMS Microbiol Lett 155:107–114

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  PubMed  Google Scholar 

  • 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 31:383–387

    Article  CAS  PubMed  Google Scholar 

  • 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 63:3036–3038

    Google Scholar 

  • 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 63:3096–3103

    CAS  PubMed  Google Scholar 

  • Morrissey JP, Osbourn AE (1999) Fungal resistance to plant antibiotics as a mechanism of pathogenesis. Microbiol Mol Biol Rev 63:708–724

    CAS  PubMed  Google Scholar 

  • Moser R, Stahl U (2001) Insights into the genetic diversity of initial dioxygenases from PAH-degrading bacteria. Appl Microbiol Biotechnol 55:609–618

    CAS  PubMed  Google Scholar 

  • 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)

  • 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)

  • 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 65:254–263

    Article  CAS  PubMed  Google Scholar 

  • Nishino SF, Spain JC (1993) Degradation of nitrobenzene by a Pseudomonas pseudoalcaligenes. Appl Environ Microbiol 59:2520–2525

    CAS  PubMed  Google Scholar 

  • Nishino SF, Paoli G, Spain JC (2000a) Aerobic degradation of dinitrotoluenes and pathway for bacterial degradation of 2,6-dinitrotoluene. Appl Environ Microbiol 66:2139–2147

    Article  CAS  PubMed  Google Scholar 

  • 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 7–62

  • Parales JV, Kumar A, Parales RE, Gibson DT (1996) Cloning and sequencing of the genes encoding 2-nitrotoluene dioxygenase from Pseudomonas sp. JS42. Gene 181:57–61

    Article  CAS  PubMed  Google Scholar 

  • 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 180:1194–1199

    CAS  PubMed  Google Scholar 

  • 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 63–90

  • Parales RE, Emig MD, Lynch NA, Gibson DT (1998b) Substrate specificities of hybrid naphthalene and 2,4-dinitrotoluene dioxygenase enzyme systems. J Bacteriol 180: 2337–2344

    CAS  PubMed  Google Scholar 

  • 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 182:1641–1649

    CAS  PubMed  Google Scholar 

  • Park H-S, Kim H-S (2000) Identification and characterization of the nitrobenzene catabolic plasmids pNB1 and pNB2 in Pseudomonas putida HS12. J Bacteriol 182:573–580

    Article  CAS  PubMed  Google Scholar 

  • Park H-S, Kim H-S (2001) Genetic and structural organization of the aminophenol catabolic operon and its implication for evolutionary process. J Bacteriol 183:5074–5081

    Article  CAS  PubMed  Google Scholar 

  • 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 65:1083–1091

    CAS  PubMed  Google Scholar 

  • Peres CM, Agathos SN (2000) Biodegradation of nitroaromatic pollutants: from pathways to remediation. Biotechnol Annu Rev 6:197–220

    CAS  PubMed  Google Scholar 

  • 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 99:581

    Google Scholar 

  • 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 182:2191–2199

    CAS  PubMed  Google Scholar 

  • Reineke W (1998) Development of hybrid strains for the mineralization of chloroaromatics by patchwork assembly. Annu Rev Microbiol 52:287–331

    CAS  PubMed  Google Scholar 

  • Riefler RG, Smets BF (2002) NAD(P)H:flavin mononucleotide oxidoreductase inactivation during 2,4,6-trinitrotoluene reduction. Appl Environ Microbiol 68:1690–1696

    Article  CAS  PubMed  Google Scholar 

  • 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 94:101–123

    Article  CAS  PubMed  Google Scholar 

  • Rodgers JD, Bunce NJ (2001) Treatment methods for the remediation of nitroaromatic explosives. Water Res 35:2101–2111

    Article  CAS  PubMed  Google Scholar 

  • Sakamoto T, Joern JM, Arisawa A, Arnold FH (2001) Laboratory evolution of toluene dioxygenase to accept 4-picoline as a substrate. Appl Environ Microbiol 67:3882–3887

    Article  CAS  PubMed  Google Scholar 

  • 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 57:1430–1440

    CAS  Google Scholar 

  • 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 65:2317–2323

    CAS  PubMed  Google Scholar 

  • Schenzle A, Lenke H, Spain JC, Knackmuss H-J (1999b) 3-Hydroxylaminophenol mutase from Ralstonia eutropha JMP134 catalyzes a Bamberger rearrangement. J Bacteriol 181:1444–1450

    CAS  PubMed  Google Scholar 

  • 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 9:48–61

    CAS  PubMed  Google Scholar 

  • Somerville CC, Nishino SF, Spain JC (1995) Purification and characterization of nitrobenzene nitroreductase from Pseudomonas pseudoalcaligenes JS45. J Bacteriol 177:3837–3842

    CAS  PubMed  Google Scholar 

  • Spain JC (1995) Biodegradation of nitroaromatic compounds. Annu Rev Microbiol 49:523–555

    Article  CAS  PubMed  Google Scholar 

  • Spain JC, Gibson DT (1991) Pathway for biodegradation of p-nitrophenol in a Moraxella sp. Appl Environ Microbiol 57:812–819

    CAS  Google Scholar 

  • Spanggord RJ, Spain JC, Nishino SF, Mortelmans KE (1991) Biodegradation of 2,4-dinitrotoluene by a Pseudomonas sp. Appl Environ Microbiol 57:3200–3205

    CAS  PubMed  Google Scholar 

  • 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 64:446–452

    CAS  PubMed  Google Scholar 

  • 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 175:5877–5881

    CAS  PubMed  Google Scholar 

  • Suen W-C, Spain JC (1993) Cloning and characterization of Pseudomonas sp. strain DNT genes for 2,4-dinitrotoluene degradation. J Bacteriol 175:1831–1837

    CAS  PubMed  Google Scholar 

  • Suen W-C, Haigler BE, Spain JC (1996) 2,4-Dinitrotoluene dioxygenase from Burkholderia sp. strain DNT: similarity to naphthalene dioxygenase. J Bacteriol 178:4926–4934

    CAS  PubMed  Google Scholar 

  • 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 272:14727–14732

    Article  CAS  PubMed  Google Scholar 

  • Takenaka S, Murakami S, Shinke R, Aoki K (1998) Metabolism of 2-aminophenol by Pseudomonas sp. AP-3: modified meta-cleavage pathway. Arch Microbiol 170:132–137

    Article  CAS  PubMed  Google Scholar 

  • 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 Microbiol

  • 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 64:4185–4193

    PubMed  Google Scholar 

  • 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 176:932–934

    CAS  PubMed  Google Scholar 

  • Wackett LP, Hershberger CD (2001) Biocatalysis and Biodegradation. ASM Press, Washington, D.C.

  • Walters DM, Russ R, Knackmuss H-J, Rouvière P (2001) High-density sampling of a bacterial operon using mRNA differential display. Gene 273:305–313

    Article  CAS  PubMed  Google Scholar 

  • 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 271:4009–4016

    CAS  Google Scholar 

  • 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 38:7659–7669

    Article  CAS  PubMed  Google Scholar 

  • Yabannavar AV, Zylstra GJ (1995) Cloning and characterization of the genes for p-nitrobenzoate degradation from Pseudomonas pickettii YH105. Appl Environ Microbiol 61:4284–4290

    CAS  PubMed  Google Scholar 

  • Yu C-L, Parales RE, Gibson DT (2001) Multiple mutations at the active site of naphthalene dioxygenase affect regioselectivity and enantioselectivity. Ind Microbiol Biotechnol 27:94–103

    Article  CAS  PubMed  Google Scholar 

  • 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 184:1547–1555

    Article  CAS  PubMed  Google Scholar 

  • 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 145–160

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Acknowledgements.

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.

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Correspondence to J. C. Spain.

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Johnson, G.R., Spain, J.C. Evolution of catabolic pathways for synthetic compounds: bacterial pathways for degradation of 2,4-dinitrotoluene and nitrobenzene. Appl Microbiol Biotechnol 62, 110–123 (2003). https://doi.org/10.1007/s00253-003-1341-4

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  • DOI: https://doi.org/10.1007/s00253-003-1341-4

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