Skip to main content

Aerobic degradation of polychlorinated biphenyls

Applied Microbiology and Biotechnology volume 67, pages 170–191 (2005)Cite this article

Abstract

The microbial degradation of polychlorinated biphenyls (PCBs) has been extensively studied in recent years. The genetic organization of biphenyl catabolic genes has been elucidated in various groups of microorganisms, their structures have been analyzed with respect to their evolutionary relationships, and new information on mobile elements has become available. Key enzymes, specifically biphenyl 2,3-dioxygenases, have been intensively characterized, structure/sequence relationships have been determined and enzymes optimized for PCB transformation. However, due to the complex metabolic network responsible for PCB degradation, optimizing degradation by single bacterial species is necessarily limited. As PCBs are usually not mineralized by biphenyl-degrading organisms, and cometabolism can result in the formation of toxic metabolites, the degradation of chlorobenzoates has received special attention. A broad set of bacterial strategies to degrade chlorobenzoates has recently been elucidated, including new pathways for the degradation of chlorocatechols as central intermediates of various chloroaromatic catabolic pathways. To optimize PCB degradation in the environment beyond these metabolic limitations, enhancing degradation in the rhizosphere has been suggested, in addition to the application of surfactants to overcome bioavailability barriers. However, further research is necessary to understand the complex interactions between soil/sediment, pollutant, surfactant and microorganisms in different environments.

This is a preview of subscription content, access via your institution.

Access options

Buy single article

Instant access to the full article PDF.

43,34 €

Price includes VAT (Finland)
Tax calculation will be finalised during checkout.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7a–d

References

  • Ahmed M, Focht DD (1973a) Degradation of polychlorinated biphenyls by two species of Achromobacter. Can J Microbiol 19:47–52

    CAS  PubMed  Google Scholar 

  • Ahmed M, Focht DD (1973b) Oxidation of polychlorinated biphenyls by Achromobacter pCB. Bull Environ Contam Toxicol 10:70–72

    CAS  PubMed  Google Scholar 

  • Ahn YB, Beaudette LA, Lee H, Trevors JT (2001) Survival of a GFP-labeled polychlorinated biphenyl degrading psychrotolerant Pseudomonas spp. in 4 and 22 degrees C soil microcosms. Microbial Ecol 42:614–623

    Article  CAS  Google Scholar 

  • Aoki Y (2001) Polychlorinated biphenyls, polychlorinated dibenzo-p-dioxins, and polychlorinated dibenzofurans as endocrine disrupters—what we have learned from Yusho disease. Environ Res 86:2–11

    Article  CAS  PubMed  Google Scholar 

  • Arai H, Kosono S, Taguchi K, Maeda M, Song E, Fuji F, Chung SY, Kudo T (1998) Two sets of biphenyl and PCB degradation genes on a linear plasmid in Rhodococcus erythropolis TA421. J Ferment Bioeng 86:595–599

    Article  CAS  Google Scholar 

  • Arensdorf JJ, Focht DD (1994) Formation of chlorocatechol meta cleavage products by a Pseudomonad during metabolism of monochlorobiphenyls. Appl Environ Microbiol 60:2884–2889

    Google Scholar 

  • Arensdorf JJ, Focht DD (1995) A meta cleavage pathway for 4-chlorobenzoate, an intermediate in the metabolism of 4-chlorobiphenyl by Pseudomonas cepacia P166. Appl Environ Microbiol 61:443–447

    Google Scholar 

  • Armengaud J, Happe B, Timmis KN (1998) Genetic analysis of dioxin dioxygenase of Sphingomonas sp. strain RW1: catabolic genes dispersed on the genome. J Bacteriol 180:3954–3966

    CAS  PubMed  Google Scholar 

  • Arnett CM, Parales JV, Haddock JD (2000) Influence of chlorine substituents on rates of oxidation of chlorinated biphenyls by the biphenyl dioxygenase of Burkholderia sp strain LB400. Appl Environ Microbiol 66:2928–2933

    Article  CAS  PubMed  Google Scholar 

  • Asturias JA, Timmis KN (1993) Three different 2,3-dihydroxybiphenyl-1,2-dioxygenase genes in the gram-positive polychlorobiphenyl-degrading bacterium Rhodococcus globerulus P6. J Bacteriol 175:4631–4640

    CAS  PubMed  Google Scholar 

  • ATSDR (2000) Toxicological profile for polychlorinated biphenyls (PCBs). Agency for Toxic Substances and Disease Registry, United States Department of Health and Human Services, Public Health Service, Atlanta, GA

    Google Scholar 

  • Babbitt PC, Kenyon GL, Martin BM, Charest H, Sylvestre M, Scholten JD, Chang K-H, Liang P-H, Dunaway-Mariano D (1992) Ancestry of the 4-chlorobenzoate dehalogenase: analysis of amino acid sequence identities among families of acyl: adenyl ligases, enoyl-CoA hydratases/isomerases, and acyl-CoA thioesterases. Biochemistry 31:5594–5604

    CAS  PubMed  Google Scholar 

  • Barriault D, Durand J, Maaroufi H, Eltis LD, Sylvestre M (1998) Degradation of polychlorinated biphenyl metabolites by naphthalene-catabolizing enzymes. Appl Environ Microbiol 64:4637–4642

    CAS  PubMed  Google Scholar 

  • Barriault D, Plante MM, Sylvestre M (2002) Family shuffling of a targeted bphA region to engineer biphenyl dioxygenase. J Bacteriol 184:3794–3800

    Article  CAS  PubMed  Google Scholar 

  • Barriault D, Sylvestre M (1999a) Catalytic activity of Pseudomonas putida strain G7 naphthalene 1,2-dioxygenase on biphenyl. Int Biodeterior Biodegrad 44:33–37

    Article  CAS  Google Scholar 

  • Barriault D, Sylvestre M (1999b) Functionality of biphenyl 2,3-dioxygenase components in naphthalene 1,2-dioxygenase. Appl Microbiol Biotechnol 51:592–597

    Article  CAS  PubMed  Google Scholar 

  • Barriault D, Vedadi M, Powlowski J, Sylvestre M (1999) cis-2,3-Dihydro-2,3-dihydroxybiphenyl dehydrogenase and cis-1,2-dihydro-1,2-dihydroxynaphathalene dehydrogenase catalyze dehydrogenation of the same range of substrates. Biochem Biophys Res Commun 260:181–187

    Article  CAS  PubMed  Google Scholar 

  • Bartels F, Backhaus S, Moore ERB, Timmis KN, Hofer B (1999) Occurrence and expression of glutathione-S-transferase-encoding bphK genes in Burkholderia sp. strain LB400 and other biphenyl-utilizing bacteria. Microbiology 145:2821–2834

    CAS  PubMed  Google Scholar 

  • Bartels I, Knackmuss H-J, Reineke W (1984) Suicide inactivation of catechol 2,3-dioxygenase from Pseudomonas putida mt-2 by 3-halocatechols. Appl Environ Microbiol 47:500–505

    CAS  Google Scholar 

  • Bayly RC, Dagley S, Gibson DT (1966) The metabolism of cresols by species of Pseudomonas. Biochem J 101:293–301

    CAS  PubMed  Google Scholar 

  • Bedard DL, Haberl ML (1990) Influence of chlorine substitution pattern on the degradation of polychlorinated biphenyls by eight bacterial strains. Microb Ecol 20:87–102

    CAS  Google Scholar 

  • Bedard DL, Haberl ML, May RJ, Brennan MJ (1987) Evidence for novel mechanisms of polychlorinated biphenyl metabolism in Alcaligenes eutrophus H850. Appl Environ Microbiol 53:1103–1112

    CAS  PubMed  Google Scholar 

  • Beltrametti F, Reniero D, Backhaus S, Hofer B (2001) Analysis of transcription of the bph locus of Burkholderia sp strain LB400 and evidence that the ORF0 gene product acts as a regulator of the promoter. Microbiology 147:2169–2182

    CAS  PubMed  Google Scholar 

  • Benning MM, Wesenberg G, Liu RQ, Taylor KL, Dunaway-Mariano D, Holden HM (1998) The three-dimensional structure of 4-hydroxybenzoyl-CoA thioesterase from Pseudomonas sp. strain CBS-3. J Biol Chem 273:33572–33579

    Article  CAS  PubMed  Google Scholar 

  • Billingsley KA, Backus SM, Ward OP (1999) Effect of surfactant solubilization on biodegradation of polychlorinated bipbenyl congeners by Pseudomonas LB400. Appl Microbiol Biotechnol 52:255–260

    Article  CAS  PubMed  Google Scholar 

  • Blasco R, Mallavarapu M, Wittich RM, Timmis KN, Pieper DH (1997) Evidence that formation of protoanemonin from metabolites of 4-chlorobiphenyl degradation negatively affects the survival of 4-chlorobiphenyl-cometabolizing microorganisms. Appl Environ Microbiol 63:427–434

    Google Scholar 

  • Blasco R, Wittich R-M, Mallavarapu M, Timmis KN, Pieper DH (1995) From xenobiotic to antibiotic. Formation of protoanemonin from 4-chlorocatechol by enzymes of the 3-oxoadipate pathway. J Biol Chem 270:29229–29235

    Article  CAS  PubMed  Google Scholar 

  • Blumenroth P, Wagner-Döbler I (1998) Survival of inoculants in polluted sediments: effect of strain origin and carbon source competition. Microb Ecol 35:279–288

    Article  CAS  PubMed  Google Scholar 

  • Brazil GM, Kenefick L, Callanan M, Haro A, Lorenzo V, Dowling DN, O’Gara F (1995) Construction of a rhizosphere pseudomonad with potential to degrade polychlorinated biphenyls and detection of bph gene expression in the rhizosphere. Appl Environ Microbiol 61:1946–1952

    CAS  PubMed  Google Scholar 

  • Broderick JB, O’Halloran TV (1991) Overproduction, purification, and characterization of chlorocatechol dioxygenase, a non-heme iron dioxygenase with broad substrate tolerance. Biochemistry 30:7349–7358

    CAS  PubMed  Google Scholar 

  • Brühlmann F, Chen W (1999a) Transformation of polychlorinated biphenyls by a novel BphA variant through the meta-cleavage pathway. FEMS Microbiol Lett 179:203–208

    Article  CAS  PubMed  Google Scholar 

  • Brühlmann F, Chen W (1999b) Tuning biphenyl dioxygenase for extended substrate specificity. Biotechnol Bioeng 63:544–551

    Article  CAS  PubMed  Google Scholar 

  • Burrus V, Pavlovic G, Decaris B, Guedon G (2002) Conjugative transposons: the tip of the iceberg. Mol Microbiol 46:601–610

    Article  CAS  PubMed  Google Scholar 

  • Cámara B, Herrera C, González M, Couve E, Hofer B, Seeger M (2004) From PCBs to highly toxic metabolites by the biphenyl pathway. Environ Microbiol 6:842–850

    Article  PubMed  Google Scholar 

  • Catelani D, Mosselmans G, Nienhaus J, Sorlini C, Treccani V (1970) Microbial degradation of aromatic hydrocarbons used as reactor coolants. Experientia 26:922–923

    CAS  Google Scholar 

  • Chang KH, Liang PH, Beck W, Scholten JD, Dunaway-Mariano D (1992) Isolation and characterization of the three polypeptide components of 4-chlorobenzoate dehalogenase from Pseudomonas sp. strain CBS-3. Biochemistry 31:5605–5610

    CAS  PubMed  Google Scholar 

  • Chatterjee DK, Chakrabarty AM (1983) Genetic homology between independently isolated chlorobenzoate-degradative plasmids. J Bacteriol 153:532–534

    CAS  PubMed  Google Scholar 

  • Chatterjee DK, Kellogg ST, Hamada S, Chakrabarty AM (1981a) Plasmid specifying total degradation of 3-chlorobenzoate by a modified ortho pathway. J Bacteriol 146:639–646

    CAS  PubMed  Google Scholar 

  • Chatterjee DK, Kellogg ST, Watkins DR, Chakrabarty AM (1981b) Plasmids in the biodegradation of chlorinated aromatic compounds. In: Levy SB, Clowes RC, Koenig EL (eds) Molecular biology, pathogenicity, and ecology of bacterial plasmids. Plenum, New York, pp 519–528

    Google Scholar 

  • Chun HK, Ohnishi Y, Shindo K, Misawa N, Furukawa K, Horinouchi S (2003) Biotransformation of flavone and flavanone by Streptomyces lividans cells carrying shuffled biphenyl dioxygenase genes. J Mol Catal B 21:113–121

    Article  CAS  Google Scholar 

  • Coco WM, Rothmel RK, Henikoff S, Chakrabarty AM (1993) Nucleotide sequence and initial functional characterization of the clcR gene encoding a LysR family activator of the clcABD chlorocatechol operon in Pseudomonas putida. J Bacteriol 175:417–427

    CAS  PubMed  Google Scholar 

  • Colores GM, Macur RE, Ward DM, Inskeep WP (2000) Molecular analysis of surfactant-driven microbial population shifts in hydrocarbon-contaminated soil. Appl Environ Microbiol 66:2959–2964

    Article  CAS  PubMed  Google Scholar 

  • Cowles CE, Nichols NN, Harwood CS (2000) BenR, a XylS homologue, regulates three different pathways of aromatic acid degradation in Pseudomonas putida. J Bacteriol 182:6339–6346

    Article  CAS  PubMed  Google Scholar 

  • Crooks GP, Xu L, Barkley RM, Copley SD (1995) Exploration of possible mechanisms for 4-chlorobenzoyl CoA dehalogenase: evidence for an aryl-enzyme intermediate. J Am Chem Soc 117:10791–10798

    CAS  Google Scholar 

  • Dai S, Vaillancourt F, Maaroufi H, Drouin N, Neau D, Snieckus V, Bolin J, Eltis L (2002) Identification and analysis of a bottleneck in PCB biodegradation. Nat Struct Biol 9:934–939

    Article  CAS  PubMed  Google Scholar 

  • Don RH, Pemberton JM (1981) Properties of six pesticide degradation plasmids isolated from Alcaligenes paradoxus and Alcaligenes eutrophus. J Bacteriol 145:681–686

    CAS  PubMed  Google Scholar 

  • Don RH, Pemberton JM (1985) Genetic and physical map of the 2,4-dichlorophenoxyacetic acid-degradative plasmid pJP4. J Bacteriol 161:466–468

    CAS  PubMed  Google Scholar 

  • Dong J, Carey PR, Wei YS, Luo LS, Lu XF, Liu RQ, Dunaway-Mariano D (2002) Raman evidence for Meisenheimer complex formation in the hydrolysis reactions of 4-fluorobenzoyl- and 4-nitrobenzoyl-coenzyme a catalyzed by 4-chlorobenzoyl-coenzyme A dehalogenase. Biochemistry 41:7453–7463

    Article  CAS  PubMed  Google Scholar 

  • Donnelly PK, Hedge RS, Fletcher JS (1994) Growth of PCB-degrading bacteria on compounds from photosynthetic plants. Chemosphere 28:981–988

    Article  Google Scholar 

  • Dorn E, Knackmuss H-J (1978a) Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2-dioxygenation of catechol. Biochem J 174:85–94

    CAS  PubMed  Google Scholar 

  • Dorn E, Knackmuss H-J (1978b) Chemical structure and biodegradability of halogenated aromatic compounds. Two catechol 1,2-dioxygenases from a 3-chlorobenzoate-grown pseudomonad. Biochem J 174:73–84

    CAS  PubMed  Google Scholar 

  • Drinker C, Warren M, Bennet G (1937) The problem of possible systemic effects from certain chlorinated hydrocarbons. J Ind Hyg Toxicol 19:283–311

    CAS  Google Scholar 

  • Elsner A, Löffler F, Miyashita K, Müller R, Lingens F (1991) Resolution of 4-chlorobenzoate dehalogenase from Pseudomonas sp. strain CBS3 into three components. Appl Environ Microbiol 57:324–326

    CAS  PubMed  Google Scholar 

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

    CAS  PubMed  Google Scholar 

  • Engesser KH, Schulte P (1989) Degradation of 2-bromo-, 2-chloro- and 2-fluorobenzoate by Pseudomonas putida CLB 250. FEMS Microbiol Lett 60:143–148

    Article  CAS  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

    CAS  PubMed  Google Scholar 

  • Erickson BD, Mondello FJ (1993) Enhanced biodegradation of polychlorinated biphenyls after site-directed mutagenesis of a biphenyl dioxygenase gene. Appl Environ Microbiol 59:3858–3862

    CAS  PubMed  Google Scholar 

  • Eulberg D, Kourbatova EM, Golovleva LA, Schlömann M (1998) Evolutionary relationship between chlorocatechol catabolic enzymes from Rhodococcus opacus 1CP and their counterparts in proteobacteria: sequence divergence and functional convergence. J Bacteriol 180:1082–1094

    CAS  PubMed  Google Scholar 

  • Faroon O, Jones D, de Rosa C (2001) Effects of polychlorinated biphenyls on the nervous system. Toxicol Ind Health 16:305–333

    CAS  PubMed  Google Scholar 

  • Faroon O, Keith L, Smith-Simon C, De Rosa C (2003) Polychlorinated biphenyls. Human health aspects. In: Concise international chemical assessment document 55. World Health Organization, Geneva

  • Fava F, Piccolo A (2002) Effects of humic substances on the bioavailability and aerobic biodegradation of polychlorinated biphenyls in a model soil. Biotechnol Bioeng 77:204–211

    Article  CAS  PubMed  Google Scholar 

  • Ferrer M, Golyshin P, Timmis KN (2003) Novel maltotriose esters enhance biodegradation of Aroclor 1242 by Burkholderia cepacia LB400. World J Microbiol Biotechnol 19:637–643

    Article  CAS  Google Scholar 

  • Fetzner S, Müller R, Lingens F (1989) Degradation of 2-chlorobenzoate by Pseudomonas cepacia 2CBS. Biol Chem Hoppe-Seyler 370:1173–1182

    CAS  PubMed  Google Scholar 

  • Fetzner S, Müller R, Lingens F (1992) Purification and some properties of 2-halobenzoate 1,2-dioxygenase, a two component enzyme system from Pseudomonas cepacia 2CBS. J Bacteriol 174:279–290

    CAS  PubMed  Google Scholar 

  • Focht D (1995) Strategies for the improvement of aerobic metabolism of polychlorinated biphenyls. Curr Opin Biotechnol 6:341–346

    Article  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 

  • Furukawa K, Hirose J, Suyama A, Zaiki T, Hayashida S (1993) Gene components responsible for discrete substrate specifity in the metabolism of biphenyl (bph operon) and toluene (tod operon). J Bacteriol 175:5224–5232

    CAS  PubMed  Google Scholar 

  • Furukawa K, Miyazaki T (1986) Cloning of a gene cluster encoding biphenyl and chlorobiphenyl degradation in Pseudomonas pseudoalcaligenes. J Bacteriol 166:392–398

    CAS  PubMed  Google Scholar 

  • Furukawa K, Simon JR, Chakrabarty AM (1983) Common induction and regulation of biphenyl, xylene/toluzene,m and salicylate catabolism catabolism in Pseudomonas paucimobilis. J Bacteriol 154:1356–1362

    CAS  PubMed  Google Scholar 

  • Furukawa K, Tomizuka N, Kamibayashi A (1979) Effect of chlorine substitution on the bacterial metabolism of various polychlorinated biphenyls. Appl Environ Microbiol 38:301–310

    CAS  PubMed  Google Scholar 

  • Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243

    Article  CAS  PubMed  Google Scholar 

  • Gibson DT, Roberts RL, Wells MC, Kobal VM (1973) Oxidation of biphenyl by a Beijerinckia species. Biochem Biophys Res Commun 50:211–215

    CAS  PubMed  Google Scholar 

  • Gilbert ES, Crowley DE (1997) Plant compounds that induce polychlorinated biphenyl biodegradation by Arthrobacter sp. strain B1B. Appl Environ Microbiol 63:1933–1938

    CAS  PubMed  Google Scholar 

  • Göbel M, Kranz OH, Kaschabek SR, Schmidt E, Pieper DH, Reineke W (2004) Microorganisms degrading chlorobenzene via a meta-cleavage pathway harbor highly similar chlorocatechol 2,3-dioxygenase-encoding gene clusters. Arch Microbiol 182:147–156

    PubMed  Google Scholar 

  • Golyshin PM, Fredrickson HL, Giuliano L, Rothmel R, Timmis KN, Yakimov MM (1999) Effect of novel biosurfactants on biodegradation of polychlorinated biphenyls by pure and mixed bacterial cultures. Microbiologica 22:257–267

    CAS  PubMed  Google Scholar 

  • Haak B, Fetzner S, Lingens F (1995) Cloning, nucleotide sequence, and expression of the plasmid-encoded genes for the two-component 2-halobenzoate 1,2-dioxygenase from Pseudomonas cepacia 2CBS. J Bacteriol 177:667–675

    CAS  PubMed  Google Scholar 

  • Haddock JD, Gibson DT (1995) Purification and characterization of the oxygenase component of biphenyl 2,3-dioxygenase from Pseudomonas sp. strain LB400. J Bacteriol 177:5834–5839

    CAS  PubMed  Google Scholar 

  • Haddock JD, Horton JR, Gibson DT (1995) Dihydroxylation and dechlorination of chlorinated biphenyls by purified biphenyl 2,3-dioxygenase from Pseudomonas sp. strain LB400. J Bacteriol 177:20–26

    CAS  PubMed  Google Scholar 

  • Harayama S, Rekik M, Bairoch A, Neidle EL, Ornston LN (1991) Potential DNA slippage structures acquired during evolutionary divergence of Acinetobacter calcoaceticus chromosomal benABC and Pseudomonas putida TOL pWW0 plasmid xylXYZ, genes encoding benzoate dioxygenases. J Bacteriol 173:7540–7548

    CAS  PubMed  Google Scholar 

  • Harwood CS, Parales RE (1996) The beta-ketoadipate pathway and the biology of self-identity. Annu Rev Microbiol 50:553–590

    Article  CAS  PubMed  Google Scholar 

  • Havel J, Reineke W (1991) Total degradation of various chlorobiphenyls by cocultures and in vivo constructed hybrid pseudomonads. FEMS Microbiol Lett 78:163–170

    Article  CAS  Google Scholar 

  • Havel J, Reineke W (1992) Degradation of Aroclor 1221 and survival of strains in soil microcosms. Appl Microbiol Biotechnol 38:129–134

    Article  CAS  Google Scholar 

  • Havel J, Reineke W (1993) Degradation of Aroclor 1221 in soil by a hybrid pseudomonad. FEMS Microbiol Lett 108:211–218

    Article  CAS  PubMed  Google Scholar 

  • Hayase N, Taira K, Furukawa K (1990) Pseudomonas putida KF715 bphABCD operon encoding biphenyl and polychlorinated biphenyl degradation: cloning analysis, and expression in soil bacteria. J Bacteriol 172:1160–1164

    CAS  PubMed  Google Scholar 

  • Hein P, Powlowski J, Barriault D, Hurtubise Y, Ahmad D, Sylvestre M (1998) Biphenyl-associated meta-cleavage dioxygenases from Comamonas testosteroni B-356. Can J Microbiol 44:42–49

    Article  CAS  PubMed  Google Scholar 

  • Heiss G, Stolz A, Kuhm AE, Müller C, Klein J, Altenbuchner J, Knackmuss H-J (1995) Characterization of a 2,3-dihydroxybiphenyl dioxygenase from the naphthalenesulfonate-degrading bacterium strain BN6. J Bacteriol 177:5865–5871

    CAS  PubMed  Google Scholar 

  • Hernandez BS, Higson FK, Kondrat R, Focht DD (1991) Metabolism of and inhibition by chlorobenzoates in Pseudomonas putida P111. Appl Environ Microbiol 57:3361–3366

    CAS  PubMed  Google Scholar 

  • Hernandez BS, Koh SC, Chial M, Focht DD (1997) Terpene-utilizing isolates and their relevance to enhanced biotransformation of polychlorinated biphenyls in soil. Biodegradation 8:153–158

    Article  Google Scholar 

  • Hickey WJ, Brenner V, Focht DD (1992) Mineralization of 2-chloro- and 2,5-dichlorobiphenyl by Pseudomonas sp. strain UCR2. FEMS Microbiol Lett 98:175–180

    Article  CAS  Google Scholar 

  • Hickey WJ, Focht DD (1990) Degradation of mono-, di-, and trihalogenated benzoic acids by Pseudomonas aeruginosa JB2. Appl Environ Microbiol 56:3842–3850

    CAS  PubMed  Google Scholar 

  • Hickey WJ, Sabat G (2001) Integration of matrix-assisted laser desorption ionization-time of flight mass spectrometry and molecular cloning for the identification and functional characterization of mobile ortho-halobenzoate oxygenase genes in Pseudomonas aeruginosa strain JB2. Appl Environ Microbiol 67:5648–5655

    Article  CAS  PubMed  Google Scholar 

  • Hickey WJ, Sabat G, Yuroff AS, Arment AR, Perez-Lesher J (2001) Cloning, nucleotide sequencing, and functional analysis of a novel, mobile cluster of biodegradation genes from Pseudomonas aeruginosa strain JB2. Appl Environ Microbiol 67:4603–4609

    Article  CAS  PubMed  Google Scholar 

  • Hickey WJ, Searles DB, Focht DD (1993) Enhanced mineralization of polychlorinated biphenyls in soil inoculated with chlorobenzoate-degrading bacteria. Appl Environ Microbiol 59:1194–1200

    CAS  PubMed  Google Scholar 

  • Higson FK, Focht DD (1990) Degradation of 2-bromobenzoic acid by a strain of Pseudomonas aeruginosa. Appl Environ Microbiol 56:1615–1619

    CAS  PubMed  Google Scholar 

  • Higson FK, Focht DD (1992) Utilization of 3-chloro-2-methylbenzoic acid by Pseudomonas cepacia MB2 through the meta fission pathway. Appl Environ Microbiol 58:2501–2504

    CAS  PubMed  Google Scholar 

  • Hofer B, Backhaus S, Timmis KN (1994) The biphenyl/polychlorinated biphenyl-degradation locus (bph) of Pseudomonas sp. LB400 encodes four additional metabolic enzymes. Gene 144:9–16

    Article  CAS  PubMed  Google Scholar 

  • Hoffmann D, Kleinsteuber S, Müller RH, Babel W (2003) A transposon encoding the complete 2,4-dichlorophenoxyacetic acid degradation pathway in the alkalitolerant strain Delftia acidovorans P4a. Microbiology 149:2545–2556

    Article  CAS  PubMed  Google Scholar 

  • Hollender J, Dott W, Hopp J (1994) Regulation of chloro- and ethylphenol degradation in Comamonas testosteroni JH5. Appl Environ Microbiol 60:2330–2338

    CAS  PubMed  Google Scholar 

  • Hollender J, Hopp J, Dott W (1997) Degradation of 4-chlorophenol via the meta cleavage pathway by Comamonas testosteroni JH5. Appl Environ Microbiol 63:4567–4572

    Google Scholar 

  • Hrywna Y, Tsoi TV, Maltseva OV, Quensen JF, Tiedje JM (1999) Construction and characterization of two recombinant bacteria that grow on ortho- and para-substituted chlorobiphenyls. Appl Environ Microbiol 65:2163–2169

    CAS  PubMed  Google Scholar 

  • Hülsmeyer M, Hecht H, Niefind K, Hofer B, Eltis L, Timmis K, Schomburg D (1998) Crystal structure of cis-biphenyl-2,3-dihydrodiol-2,3-dehydrogenase from a PCB degrader at 2.0 A resolution. Protein Sci 7:1286–1293

    PubMed  Google Scholar 

  • Janke D, Fritsche W (1979) Dechlorierung von 4-chlorphenol nach extradioler Ringspaltung durch Pseudomonas putida. Z Allg Mikrobiol 19:139–141

    CAS  PubMed  Google Scholar 

  • Kasai Y, Shindo K, Harayama S, Misawa N (2003) Molecular characterization and substrate preference of a polycyclic aromatic hydrocarbon dioxygenase from Cycloclasticus sp. strain A5. Appl Environ Microbiol 69:6688–6697

    Article  CAS  PubMed  Google Scholar 

  • Kaschabek SR, Kasberg T, Müller D, Mars AE, Janssen DB, Reineke W (1998) Degradation of chloroaromatics: purification and characterization of a novel type of chlorocatechol 2,3-dioxygenase of Pseudomonas putida GJ31. J Bacteriol 180:296–302

    CAS  PubMed  Google Scholar 

  • Kaschabek SR, Reineke W (1992) Maleylacetate reductase of Pseudomonas sp. strain B13: dechlorination of chloromaleylacetates, metabolites in the degradation of chloroaromatic compounds. Arch Microbiol 158:412–417

    Article  CAS  PubMed  Google Scholar 

  • Kaulmann U, Kaschabek SR, Schlömann M (2001) Mechanism of chloride elimination from 3-chloro- and 2,4-dichloro-cis,cis-muconate: new insight obtained from analysis of muconate cycloisomerase variant CatB-K169A. J Bacteriol 183:4551–4561

    Article  CAS  PubMed  Google Scholar 

  • Kauppi B, Lee K, Carredano E, Parales RE, Gibson DT, Eklund H, Ramaswamy S (1998) Structure of an aromatic-ring-hydroxylating dioxygenase-naphthalene 1,2-dioxygenase. Structure 6:571–586

    Article  CAS  PubMed  Google Scholar 

  • Kersten P, Chapman PJ, Dagley S (1985) Enzymatic release of halogens or methanol from some substituted protocatechuic acids. J Bacteriol 162:693–697

    CAS  PubMed  Google Scholar 

  • Kersten P, Dagley S, Whittaker J, Arciero D, Lipscomb J (1982) 2-Pyrone-4,6-dicarboxylic acid, a catabolite of gallic acids in Pseudomonas species. J Bacteriol 152:1154–1162

    CAS  PubMed  Google Scholar 

  • Kikuchi Y, Yasukochi Y, Nagata Y, Fukuda M, Takagi M (1994) Nucleotide sequence and functional analysis of the meta-cleavage pathway involved in biphenyl and polychlorinated biphenyl degradation in Pseudomonas sp. strain KKS102. J Bacteriol 176:4269–4276

    CAS  PubMed  Google Scholar 

  • Kim E, Zylstra GJ (1995) Molecular and biochemical characterization of two meta-cleavage dioxygenase involved in biphenyl and m-xylene degradation by Beijerinckia sp. strain B1. J Bacteriol 177:3095–3103

    CAS  PubMed  Google Scholar 

  • Kim E, Zylstra GJ (1999) Functional analysis of genes involved in biphenyl, naphthalene, phenanthrene, and m-xylene degradation by Sphingomonas yanoikuyae B1. J Ind Microbiol Biotechnol 23:294–302

    Article  PubMed  Google Scholar 

  • Kim SJ, Chun J, Bae KS, Kim YC (2000) Polyphasic assignment of an aromatic-degrading Pseudomonas sp., strain DJ77, in the genus Sphingomonas as Sphingomonas chungbukensis sp nov. Int J Syst Evol Microbiol 50:1641–1647

    CAS  PubMed  Google Scholar 

  • Kim SY, Jung JY, Lim YH, Ahn JH, Kim SI, Hur HG (2003) cis-2′,3′-Dihydrodiol production on flavone B-ring by biphenyl dioxygenase from Pseudomonas pseudoalcaligenes KF707 expressed in Escherichia coli. Antonie Van Leeuwenhoek 84:261–268

    Article  CAS  PubMed  Google Scholar 

  • Kimbara K, Hashimoto T, Fukuda M, Koana T, Takagi M, Oishi M, Yano K (1989) Cloning and sequencing of two tandem genes involved in degradation of 2,3-dihydroxybiphenyl to benzoic acid in the polychlorinated biphenyl-degrading soil bacterium Pseudomonas sp. strain KKS102. J Bacteriol 171:2740–2747

    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 

  • Kitagawa W, Miyauchi K, Masai E, Fukuda M (2001a) Cloning and characterization of benzoate catabolic genes in the gram-positive polychlorinated biphenyl degrader Rhodococcus sp strain RHA1. J Bacteriol 183:6598–6606

    Article  CAS  PubMed  Google Scholar 

  • Kitagawa W, Suzuki A, Hoaki T, Masai E, Fukuda M (2001b) Multiplicity of aromatic ring hydroxylation dioxygenase genes in a strong PCB degrader, Rhodococcus sp. strain RHA1 demonstrated by denaturing gradient gel electrophoresis. Biosci Biotechnol Biochem 65:1907–1911

    Article  CAS  PubMed  Google Scholar 

  • Kitayama A, Achioku T, Yanagawa T, Kanou K, Kikuchi M, Ueda H, Suzuki E, Nishimura H, Nagamune T, Kawakami Y (1996) Cloning and characterization of extradiol aromatic ring-cleavage dioxygenases from Pseudomonas aeruginosa JI104. J Ferment Bioeng 82:217–223

    Article  Google Scholar 

  • Klages U, Lingens F (1979) Degradation of 4-chlorobenzoic acid by a Nocardia species. FEMS Microbiol Lett 6:201–203

    Article  CAS  Google Scholar 

  • Klages U, Lingens F (1980) Degradation of 4-chlorobenzoic acid by a Pseudomonas sp. Zentralbl Bakteriol Parasitenkd Infektionskr Hyg Abt 1 C 1:215–223

    CAS  Google Scholar 

  • Klemba M, Jakobs B, Wittich R, Pieper D (2000) Chromosomal integration of the tcb chlorocatechol degradation pathway genes as a means of expanding the growth substrate range of bacteria to include haloaromatics. J Bacteriol 182:3255–3261

    Google Scholar 

  • Kosono S, Maeda M, Fuji F, Arai H, Kudo T (1997) Three of the seven bphC genes of Rhodococcus erythropolis TA421, isolated from a termite ecosystem, are located on an indigenous plasmid associated with biphenyl degradation. Appl Environ Microbiol 63:3282–3285

    CAS  PubMed  Google Scholar 

  • Kozlovsky SA, Zaitsev GM, Kunc F, Gabriel J, Boronin AM (1993) Degradation of 2-chlorobenzoic and 2,5-dichlorobenzoic acids in pure culture by Pseudomonas stutzeri. Folia Microbiol 38:371–375

    CAS  Google Scholar 

  • Krooneman J, Moore ERB, van Velzen JCL, Prins RA, Forney LJ, Gottschal JC (1998) Competition for oxygen and 3-chlorobenzoate between two aerobic bacteria using different degradation pathways. FEMS Microbiol Ecol 26:171–179

    Article  CAS  Google Scholar 

  • Krooneman J, Wieringa EBA, Moore ERB, Gerritse J, Prins RA, Gottschal JC (1996) Isolation of Alcaligenes sp. strain L6 at low oxygen concentrations and degradation of 3-chlorobenzoate via a pathway not involving (chloro)catechols. Appl Environ Microbiol 62:2427–2434

    CAS  PubMed  Google Scholar 

  • Kumamaru T, Suenaga H, Mitsuoka M, Watanabe T, Furukawa K (1998) Enhanced degradation of polychlorinated biphenyls by directed evolution of biphenyl dioxygenase. Nat Biotechnol 16:663–666

    CAS  PubMed  Google Scholar 

  • Labbe D, Garnon J, Lau PCK (1997) Characterization of the genes encoding a receptor-like histidine kinase and a cognate response regulator from a biphenyl/polychlorobiphenyl-degrading bacterium, Rhodococcus sp. strain M5. J Bacteriol 179:2772–2776

    CAS  PubMed  Google Scholar 

  • Lee J, Min KR, Kim Y-C, Kim C-K, Lim J-Y, Yoon H, Min K-H, Lee K-S, Kim Y (1995) Cloning of salicylate hydroxylase gene and catechol 2,3-dioxygenase gene and sequencing of an intergenic sequence between the two genes of Pseudomonas putida KF715. Biochem Biophys Res Commun 211:382–388

    Article  CAS  PubMed  Google Scholar 

  • Leesong M, Henderson B, Gillig J, Schwab J, Smith J (1996) Structure of a dehydratase-isomerase from the bacterial pathway for biosynthesis of unsaturated fatty acids: two catalytic activities in one active site. Structure 4:253–264

    Article  CAS  PubMed  Google Scholar 

  • Liang P-H, Yang G, Dunaway-Mariano D (1993) Specificity of 4-chlorobenzoyl coenzyme A dehalogenase catalyzed dehalogenation of halogenated aromatics. Biochemistry 32:12245–12250

    CAS  PubMed  Google Scholar 

  • Liu R-Q, Liang P-H, Scholten J, Dunaway-Mariano D (1995) Transient state kinetic analysis of the chemical intermediates formed in the enzymatic dehalogenation of 4-chlorobenzoyl coenzyme A. J Am Chem Soc 117:5003–5004

    CAS  Google Scholar 

  • Liu S, Ogawa N, Miyashita K (2001) The chlorocatechol degradative genes, tfdT-CDEF, of Burkholderia sp. strain NK8 are involved in chlorobenzoate degradation and induced by chlorobenzoates and chlorocatechols. Gene 268:207–214

    Article  CAS  PubMed  Google Scholar 

  • Lloyd-Jones G, Ogden RC, Williams PA (1995) Inactivation of 2,3-dihydroxybiphenyl 1,2-dioxygenase from Pseudomonas sp. strain CB406 by 3,4-dihydroxybiphenyl (4-phenylcatechol). Biodegradation 6:11–17

    CAS  Google Scholar 

  • Löffler F, Lingens F, Müller R (1995) Dehalogenation of 4-chlorobenzoate. Characterisation of 4-chlorobenzoyl-coenzyme A dehalogenase from Pseudomonas sp. CBS3. Biodegradation 6:203–212

    Article  PubMed  Google Scholar 

  • Löffler F, Müller R (1991) Identification of 4-chlorobenzoyl-coenzyme A as intermediate in the dehalogenation catalyzed by 4-chlorobenzoate dehalogenase from Pseudomonas sp CBS3. FEBS Lett 290:224–226

    Article  PubMed  Google Scholar 

  • Löffler F, Müller R, Lingens F (1992) Purification and properties of 4-halobenzoate-coenzyme A ligase from Pseudomonas sp. CBS3. Biol Chem Hoppe-Seyler 373:1001–1007

    PubMed  Google Scholar 

  • Lünsdorf H, Erb R, Abraham W, Timmis K (2000) ‘Clay hutches’: a novel interaction between bacteria and clay minerals. Environ Microbiol 2:161–168

    Article  PubMed  Google Scholar 

  • Lunt D, Evans WC (1970) The microbial metabolism of biphenyl. Biochem J 118:54–55

    Google Scholar 

  • Maeda M, Chung S-Y, Song E, Kudo T (1995) Multiple genes encoding 2,3-dihydroxybiphenyl 1,2-dioxygenase in the gram-positive polychlorinated biphenyl-degrading bacterium Rhodococcus erythropolis TA421, isolated from a termite ecosystem. Appl Environ Microbiol 61:549–555

    CAS  PubMed  Google Scholar 

  • Maeda T, Takahashi Y, Suenaga H, Suyama A, Goto M, Furukawa K (2001) Functional analyses of Bph-Tod hybrid dioxygenase, which exhibits high degradation activity toward trichloroethylene. J Biol Chem 276:29833–29838

    Article  CAS  PubMed  Google Scholar 

  • Maltseva OV, Solyanikova IP, Golovleva LA (1994a) Chlorocatechol 1,2-dioxygenase from Rhodococcus erythropolis 1 CP. Kinetic and immunochemical comparison with analogous enzymes from Gram-negative strains. Eur J Biochem 226:1053–1061

    CAS  PubMed  Google Scholar 

  • Maltseva OV, Solyanikova IP, Golovleva LA, Schlömann M, Knackmuss H-J (1994b) Dienelactone hydrolase from Rhodococcus erythropolis 1 CP: purification and properties. Arch Microbiol 162:386–374

    Google Scholar 

  • Mars AE, Kasberg T, Kaschabek SR, van Agteren MH, Janssen DB, Reineke W (1997) Microbial degradation of chloroaromatics: use of the meta-cleavage pathway for mineralization of chlorobenzene. J Bacteriol 179:4530–4537

    CAS  PubMed  Google Scholar 

  • Mars AE, Kingma J, Kaschabek SR, Reineke W, Janssen DB (1999) Conversion of 3-chlorocatechol by various catechol 2,3-dioxygenases and sequence analysis of the chlorocatechol dioxygenase region of Pseudomonas putida GJ31. J Bacteriol 181:1309–1318

    CAS  PubMed  Google Scholar 

  • Masai E, Sugiyama K, Iwashita N, Shimizu S, Hauschild JE, Hatta T, Kimbara K, Yano K, Fukuda M (1997) The bphDEF meta-cleavage pathway genes involved in biphenyl/polychlorinated biphenyl degradation are located on a linear plasmid and separated from the initial bphACB genes in Rhodococcus sp. strain RHA1. Gene 187:141–149

    Article  CAS  PubMed  Google Scholar 

  • Masai E, Yamada A, Healy JM, Hatta T, Kimbara K, Fukuda M, Yano K (1995) Characterization of biphenyls catabolic genes of gram-positive polychlorinated biphenyls degrader Rhodococcus sp. strain RHA1. Appl Environ Microbiol 61:2079–2085

    CAS  PubMed  Google Scholar 

  • Mayes B, McConnell E, Neal B, Brunner M, Hamilton S, Sullivan T, Peters A, Ryan M, Toft J, Singer A, Brown J, Menton R, Moore J (1998) Comparative carcinogenicity in Sprague-Dawley rats of the polychlorinated biphenyl mixtures aroclors 1016, 1242, 1254, and 1260. Toxicol Sci 41:62–76

    Article  CAS  PubMed  Google Scholar 

  • McCullar MV, Brenner V, Adams RH, Focht DD (1994) Construction of a novel polychlorinated biphenyl-degrading bacterium: utilization of 3,4-dichlorobiphenyl by Pseudomonas acidovorans M3GY. Appl Environ Microbiol 60:3833–3839

    CAS  Google Scholar 

  • McFall SM, Parsek MR, Chakrabarty AM (1997) 2-Chloromuconate and ClcR-mediated activation of the clcABD operon: in vitro transcriptional and DNase I footprint analyses. J Bacteriol 179:3655–3663

    CAS  PubMed  Google Scholar 

  • McKay DB, Prucha M, Reineke W, Timmis KN, Pieper DH (2003) Substrate specificity and expression of three 2,3-dihydroxybiphenyl 1,2-dioxygenases from Rhodococcus globerulus strain P6. J Bacteriol 185:2944–2951

    Article  CAS  PubMed  Google Scholar 

  • McKay DB, Seeger M, Zielinski M, Hofer B, Timmis KN (1997) Heterologous expression of biphenyl dioxygenase-encoding genes from a gram-positive broad-spectrum polychlorinated biphenyl degrader and characterization of chlorobiphenyl oxidation by the gene products. J Bacteriol 179:1924–1930

    CAS  PubMed  Google Scholar 

  • Meer JR van der, Ravatn R, Sentchilo V (2001) The clc element of Pseudomonas sp. strain B13 and other mobile degradative elements employing phage-like integrases. Arch Microbiol 175:79–85

    Article  PubMed  Google Scholar 

  • Meer JR van der, van Neerven ARW, de Vries EJ, de Vos WM, Zehnder AJB (1991) Cloning and characterization of plasmid-encoded genes for the degradation of 1,2-dichloro-, 1,4-dichloro-, and 1,2,4-trichlorobenzene of Pseudomonas sp. strain P51. J Bacteriol 173:6–15

    PubMed  Google Scholar 

  • Merlin C, Springael D, Mergeay M, Toussaint A (1997) Organisation of the bph gene cluster of transposon Tn4371, encoding enzymes for the degradation of biphenyl and 4-chlorobiphenyl compounds. Mol Gen Genet 253:499–506

    Article  CAS  PubMed  Google Scholar 

  • Merlin C, Springael D, Toussaint A (1999) Tn4371: a modular structure encoding a phage-like integrase, a Pseudomonas-like catabolic pathway, and RP4/Ti-like transfer functions. Plasmid 40:54

    Google Scholar 

  • Moiseeva OV, Belova OV, Solyanikova IP, Schlömann M, Golovleva LA (2001) Enzymes of a new modified ortho-pathway utilizing 2-chlorophenol in Rhodococcus opacus 1CP. Biochemistry (Moscow) 66:548–555

    Article  CAS  Google Scholar 

  • Moiseeva OV, Linko EV, Baskunov BP, Golovleva LA (1999) Degradation of 2-chlorophenol and 3-chlorobenzoate by Rhodococcus opacus 1CP. Microbiology (Moscow) 68:400–405

    CAS  Google Scholar 

  • Moiseeva OV, Solyanikova IP, Kaschabek SR, Groning J, Thiel M, Golovleva LA, Schlömann M (2002) A new modified ortho cleavage pathway of 3-chlorocatechol degradation by Rhodococcus opacus 1CP: genetic and biochemical evidence. J Bacteriol 184:5282–5292

    Article  CAS  PubMed  Google Scholar 

  • Mokross H, Schmidt E, Reineke W (1990) Degradation of 3-chlorobiphenyl by in vivo constructed hybrid pseudomonads. FEMS Microbiol Lett 71:179–186

    Article  CAS  Google Scholar 

  • Mondello FJ (1989) Cloning and expression in Escherichia coli of Pseudomonas strain LB400 genes encoding polychlorinated biphenyl degradation. J Bacteriol 171:1725–1732

    CAS  PubMed  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 

  • Mouz S, Merlin C, Springael D, Toussaint A (1999) A GntR-like negative regulator of the biphenyl degradation genes of the transposon Tn4371. Mol Gen Genet 262:790–799

    Article  CAS  PubMed  Google Scholar 

  • Murray K, Duggleby CJ, Sala-Trepat JM, Williams PA (1972) The metabolism of benzoate and methylbenzoates via the meta-cleavage by Pseudomonas arvilla mt-2. Eur J Biochem 28:301–310

    CAS  PubMed  Google Scholar 

  • Nakatsu C, Wyndham RC (1993) Cloning and expression of the transposable chlorobenzoate-3,4-dioxygenase genes of Alcaligenes sp. BR60. Appl Environ Microbiol 59:3625–3633

    CAS  PubMed  Google Scholar 

  • Nakatsu CH, Providenti M, Wyndham RC (1997) The cis-diol dehydrogenase cbaC gene of Tn5271 is required for growth on 3-chlorobenzoate but not 3,4-dichlorobenzoate. Gene 196:209–218

    Article  CAS  PubMed  Google Scholar 

  • Nakatsu CH, Straus NA, Wyndham RC (1995) The nucleotide sequence of the Tn5271 3-chlorobenzoate 3,4-dioxygenase genes (cbaAB) unites the class IA oxygenase in a single lineage. Microbiology 141:485–495

    CAS  PubMed  Google Scholar 

  • Narasimhan K, Basheer C, Bajic V, Swarup S (2003) Enhancement of plant-microbe interactions using a rhizosphere metabolomics-driven approach and its application in the removal of polychlorinated biphenyls. Plant Physiol 132:146–153

    Article  CAS  PubMed  Google Scholar 

  • Nikodem P, Hecht V, Schlömann M, Pieper DH (2003) New bacterial pathway for 4- and 5-chlorosalicylate degradation via 4-chlorocatechol and maleylacetate in Pseudomonas sp. strain MT1. J Bacteriol 185:6790–6800

    Article  CAS  PubMed  Google Scholar 

  • Nishi A, Tominaga K, Furukawa K (2000) A 90-kilobase conjugative chromosomal element coding for biphenyl and salicylate catabolism in Pseudomonas putida KF715. J Bacteriol 182:1949–1955

    Article  CAS  PubMed  Google Scholar 

  • Ogawa N, McFall SM, Klem TJ, Miyashita K, Chakrabarty AM (1999) Transcriptional activation of the chlorocatechol degradative genes of Ralstonia eutropha NH9. J Bacteriol 181:6697–6705

    CAS  PubMed  Google Scholar 

  • Ogawa N, Miyashita K (1999) The chlorocatechol-catabolic transposon Tn5707 of Alcaligenes eutrophus NH9, carrying a gene cluster highly homologous to that in the 1,2,4-trichlorobenzene-degrading bacterium Pseudomonas sp. strain P51, confers the ability to grow on 3-chlorobenzoate. Appl Environ Microbiol 65:724–731

    CAS  PubMed  Google Scholar 

  • Ohta Y, Maeda M, Kudo T (2001) Pseudomonas putida CE2010 can degrade biphenyl by a mosaic pathway encoded by the tod operon and cmtE, which are identical to those of P. putida F1 except for a single base difference in the operator-promoter region of the cmt operon. Microbiology 147:31–41

    CAS  PubMed  Google Scholar 

  • Ohtsubo Y, Delawary M, Kimbara K, Takagi M, Ohta A, Nagata Y (2001) BphS, a key transcriptional regulator of bph genes involved in polychlorinated biphenyl/biphenyl degradation in Pseudomonas sp. KKS102. J Biol Chem 276:36146–36154

    Article  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

    Article  CAS  PubMed  Google Scholar 

  • Patel TR, Gibson DT (1974) Purification and properties of (+)-cis-naphthalene dihydrodiol dehydrogenase of Pseudomonas putida. J Bacteriol 119:879–888

    CAS  PubMed  Google Scholar 

  • Pavlu L, Vosahlova J, Klierova H, Prouza M, Demnerova K, Brenner V (1999) Characterization of chlorobenzoate degraders isolated from polychlorinated biphenyl-contaminated soil and sediment in the Czech Republic. J Appl Microbiol 87:381–386

    Article  CAS  PubMed  Google Scholar 

  • Peloquin L, Greer CW (1993) Cloning and expression of the polychlorinated biphenyl-degradation gene cluster from Arthrobacter M5 and comparison to analogous genes from gram-negative bacteria. Gene 125:35–40

    Article  CAS  PubMed  Google Scholar 

  • Pelz O, Tesar M, Wittich RM, Moore ERB, Timmis KN, Abraham WR (1999) Towards elucidation of microbial community metabolic pathways: unravelling the network of carbon sharing in a pollutant-degrading bacterial consortium by immunocapture and isotopic ratio mass spectrometry. Environ Microbiol 1:167–174

    Article  CAS  PubMed  Google Scholar 

  • Perez-Pantoja D, Ledger T, Pieper DH, Gonzalez B (2003) Efficient turnover of chlorocatechols is essential for growth of Ralstonia eutropha JMP134(pJP4) in 3-chlorobenzoic acid. J Bacteriol 185:1534–1542

    Article  CAS  PubMed  Google Scholar 

  • Pieper DH, Knackmuss H-J, Timmis KN (1993) Accumulation of 2-chloromuconate during metabolism of 3-chlorobenzoate by Alcaligenes eutrophus JMP134. Appl Microbiol Biotechnol 39:563–567

    Article  CAS  Google Scholar 

  • Pinyakong O, Habe H, Omori T (2003) The unique aromatic catabolic genes in sphingomonads degrading polycyclic aromatic hydrocarbons (PAHs). J Gen Appl Microbiol 49:1–19

    Google Scholar 

  • Poh RPC, Smith ARW, Bruce IJ (2002) Complete characterisation of Tn5530 from Burkholderia cepacia strain 2a (pIJB1) and studies of 2,4-dichlorophenoxyacetate uptake by the organism. Plasmid 48:1–12

    Google Scholar 

  • Potrawfke T, Armengaud J, Wittich RM (2001) Chlorocatechols at positions 4 and 5 are substrates of the broad-spectrum chlorocatechol 1,2-dioxygenase Pseudomonas chlororaphis RW71. J Bacteriol 183:997–1011

    Article  CAS  PubMed  Google Scholar 

  • Providenti MA, Wyndham RC (2001) Identification and functional characterization of CbaR, a MarR-like modulator of the cbaABC-encoded chlorobenzoate catabolism pathway. Appl Environ Microbiol 67:3530–3541

    Article  CAS  PubMed  Google Scholar 

  • Prucha M, Peterseim A, Timmis KN, Pieper DH (1996a) Muconolactone isomerase of the 3-oxoadipate pathway catalyzes dechlorination of 5-chlorosubstituted muconolactones. Eur J Biochem 237:350–356

    Article  CAS  PubMed  Google Scholar 

  • Prucha M, Wray V, Pieper DH (1996b) Metabolism of 5-chlorosubstituted muconolactones. Eur J Biochem 237:357–366

    Article  CAS  PubMed  Google Scholar 

  • Raschke H, Fleischmann T, van der Meer JR, Kohler HPE (1999) cis-Chlorobenzene dihydrodiol dehydrogenase (TcbB) from Pseudomonas sp strain P51, expressed in Escherichia coli DH5 alpha(PTCB149), catalyzes enantioselective dehydrogenase reactions. Appl Environ Microbiol 65:5242–5246

    CAS  PubMed  Google Scholar 

  • Raschke H, Meier M, Burken JG, Hany R, Muller MD, Van der Meer JR, Kohler HPE (2001) Biotransformation of various substituted aromatic compounds to chiral dihydrodihydroxy derivatives. Appl Environ Microbiol 67:3333–3339

    Article  CAS  PubMed  Google Scholar 

  • Ravatn R, Studer S, Springael D, Zehnder AJB, van der Meer JR (1998a) Chromosomal integration, tandem amplification, and deamplification in Pseudomonas putida F1 of a 105-kilobase genetic element containing the chlorocatechol degradative genes from Pseudomonas sp. strain B13. J Bacteriol 180:4360–4369

    CAS  PubMed  Google Scholar 

  • Ravatn R, Studer S, Zehnder AJB, van der Meer JR (1998b) Int-B13, an unusual site-specific recombinase of the bacteriophage P4 integrase family, is responsible for chromosomal insertion of the 105-kilobase clc element of Pseudomonas sp. strain B13. J Bacteriol 180:5505–5514

    CAS  PubMed  Google Scholar 

  • Ravatn R, Zehnder AJB, van der Meer JR (1998c) Low-frequency horizontal transfer of an element containing the chlorocatechol degradation genes from Pseudomonas sp. strain B13 to Pseudomonas putida F1 and to indigenous bacteria in laboratory-scale activated-sludge microcosms. Appl Environ Microbiol 64:2126–2132

    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

    Article  CAS  PubMed  Google Scholar 

  • Reineke W, Knackmuss H-J (1978a) Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2-dioxygenation of benzoic acid. Biochim Biophy Acta 532:412–423

    Google Scholar 

  • Reineke W, Knackmuss H-J (1978b) Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on dehydrogenation of 3,5-cyclohexadiene-1,2-diol-1-carboxylic acid. Biochim Biophys Acta 542:424–429

    CAS  PubMed  Google Scholar 

  • Reineke W, Knackmuss H-J (1979) Construction of haloaromatics utilising bacteria. Nature 277:385–386

    CAS  PubMed  Google Scholar 

  • Rodrigues J, Maltseva O, Tsoi T, Helton R, Quensen J, Fukuda M, Tiedje J (2001) Development of a Rhodococcus recombinant strain for degradation of products from anaerobic dechlorination of PCBs. Environ Sci Technol 35:663–668

    Article  CAS  PubMed  Google Scholar 

  • Rogers JE, Gibson DT (1977) Purification and properties of cis-toluene dihydrodiol dehydrogenase from Pseudomonas putida. J Bacteriol 130:1117–1124

    CAS  PubMed  Google Scholar 

  • Romanov V, Hausinger RP (1994) Pseudomonas aeruginosa 142 uses a three-component ortho-halobenzoate 1,2-dioxygenase for the metabolism of 2,4-dichloro- and 2-chlorobenzoate. J Bacteriol 176:3368–3374

    CAS  PubMed  Google Scholar 

  • Romanov VP, Grechkina GM, Adanin VM, Starovoitov II (1993) Oxidative dehalogenation of 2-chloro- and 2,4-dichlorobenzoates by Pseudomonas aeruginosa. Microbiology 62:532–536

    Google Scholar 

  • Romine MF, Stillwell LC, Wong KK, Thurston SJ, Sisk EC, Sensen C, Gaasterland T, Fredrickson JK, Saffer JD (1999) Complete sequence of a 184-kilobase catabolic plasmid from Sphingomonas aromaticivorans F199. J Bacteriol 181:1585–1602

    CAS  PubMed  Google Scholar 

  • Ron EZ, Rosenberg E (2001) Natural roles of biosurfactants. Environ Microbiol 3:229–236

    Google Scholar 

  • Ruisinger S, Klages U, Lingens F (1976) Abbau der 4-Chlorbenzoesäure durch eine Arthrobacter-Species. Arch Microbiol 110:253–256

    Article  CAS  PubMed  Google Scholar 

  • Sakai M, Masai E, Asami H, Sugiyama K, Kimbara K, Fukuda M (2002) Diversity of 2,3-dihydroxybiphenyl dioxygenase genes in a strong PCB degrader, Rhodococcus sp. strain RHA1. J Biosci Bioeng 93:421–427

    CAS  Google Scholar 

  • Schell U, Helin S, Kajander T, Schlömann M, Goldman A (1999) Structural basis for the activity of two muconate cycloisomerase variants toward substituted muconates. Proteins 34:125–136

    CAS  PubMed  Google Scholar 

  • Schlömann M (1994) Evolution of chlorocatechol catabolic pathways. Biodegradation 5:301–321

    PubMed  Google Scholar 

  • Schlömann M, Schmidt E, Knackmuss H-J (1990) Different types of dienelactone hydrolase in 4-fluorobenzoate-utilizing bacteria. J Bacteriol 172:5112–5118

    PubMed  Google Scholar 

  • Schmidt E, Knackmuss H-J (1980) Chemical structure and biodegradability of halogenated aromatic compounds. Conversion of chlorinated muconic acids into maleoylacetic acid. Biochem J 192:339–347

    CAS  PubMed  Google Scholar 

  • Schmidt E, Remberg G, Knackmuss H-J (1980) Chemical structure and biodegradability of halogenated aromatic compounds. Halogenated muconic acids as intermediates. Biochem J 192:331–337

    CAS  PubMed  Google Scholar 

  • Schweigert N, Zehnder AJB, Eggen RIL (2001) Chemical properties of catechols and their molecular modes of toxic action in cells, from microorganisms to mammals. Environ Microbiol 3:81–91

    Article  CAS  PubMed  Google Scholar 

  • Seah SYK, Labbe G, Nerdinger S, Johnson MR, Snieckus V, Eltis LD (2000) Identification of a serine hydrolase as a key determinant in the microbial degradation of polychlorinated biphenyls. J Biol Chem 275:15701–15708

    Article  CAS  PubMed  Google Scholar 

  • Seegal B, Holden M (1945) The antibiotic activity of extracts of Ranunculaceae. Science 101:413–414

    Google Scholar 

  • Seeger M, Camara B, Hofer B (2001) Dehalogenation, denitration, dehydroxylation, and angular attack on substituted biphenyls and related compounds by a biphenyl dioxygenase. J Bacteriol 183:3548–3555

    Article  CAS  PubMed  Google Scholar 

  • Seeger M, Gonzalez M, Camara B, Munoz L, Ponce E, Mejias L, Mascayano C, Vasquez Y, Sepulveda-Boza S (2003) Biotransformation of natural and synthetic isoflavonoids by two recombinant microbial enzymes. Appl Environ Microbiol 69:5045–5050

    Article  CAS  PubMed  Google Scholar 

  • Seeger M, Timmis KN, Hofer B (1995) Degradation of chlorobiphenyls catalyzed by the bph-encoded biphenyl-2,3-dioxygenase and biphenyl-2,3-dihydrodiol-2,3-dehydrogenase of Pseudomonas sp. LB400. FEMS Microbiol Lett 133:259–264

    Article  CAS  PubMed  Google Scholar 

  • Seeger M, Timmis KN, Hofer B (1997) Bacterial pathways for the degradation of polychlorinated biphenyls. Marine Chem 58:327–333

    Article  Google Scholar 

  • Seeger M, Zielinski M, Timmis KN, Hofer B (1999) Regiospecificity of dioxygenation of di- to pentachlorobiphenyls and their degradation to chlorobenzoates by the bph-encoded catabolic pathway of Burkholderia sp. strain LB400. Appl Environ Microbiol 65:3614–3621

    CAS  PubMed  Google Scholar 

  • Sentchilo V, Ravatn R, Werlen C, Zehnder AJB, van der Meer JR (2003) Unusual integrase gene expression on the clc genomic island in Pseudomonas sp strain B13. J Bacteriol 185:4530–4538

    Article  CAS  PubMed  Google Scholar 

  • Shimizu S, Kobayashi H, Masai E, Fukuda M (2001) Characterization of the 450-kb linear plasmid in a polychlorinated biphenyl degrader, Rhodococcus sp. strain RHA1. Appl Environ Microbiol 67:2021–2028

    Article  CAS  PubMed  Google Scholar 

  • Shindo K, Ohnishi Y, Chun HK, Takahashi H, Hayashi M, Saito A, Iguchi K, Furukawa K, Harayama S, Horinouchi S, Misawa N (2001) Oxygenation reactions of various tricyclic fused aromatic compounds using Escherichia coli and Streptomyces lividans transformants carrying several arene dioxygenase genes. Biosci Biotechnol Biochem 65:2472–2481

    Google Scholar 

  • Shingler V, Powlowski J, Marklund U (1992) Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600. J Bacteriol 174:711–724

    CAS  PubMed  Google Scholar 

  • Skiba A, Hecht V, Pieper DH (2002) Formation of protoanemonin from 2-chloro-cis,cis-muconate by the combined action of muconate cycloisomerase and muconolactone isomerase. J Bacteriol 184:5402–5409

    Article  CAS  PubMed  Google Scholar 

  • Solyanikova IP, Malteva OV, Vollmer MD, Golovleva LA, Schlömann M (1995) Characterization of muconate and chloromuconate cycloisomerase from Rhodococcus erythropolis 1CP: indications for functionally convergent evolution among bacterial cycloisomerases. J Bacteriol 177:2821–2826

    CAS  PubMed  Google Scholar 

  • Sondossi M, Sylvestre M, Ahmad D (1992) Effects of chlorobenzoate transformation on the Pseudomonas testosteroni biphenyl and chlorobiphenyl degradation pathway. Appl Environ Microbiol 58:485–495

    CAS  PubMed  Google Scholar 

  • Springael D, Kreps S, Mergeay M (1993) Identification of a catabolic transposon, Tn4371, carrying biphenyl and 4-chlorobiphenyl degradation genes in Alcaligenes eutrophus A5. J Bacteriol 175:1674–1681

    CAS  PubMed  Google Scholar 

  • Springael D, Peys K, Ryngaert A, Van Roy S, Hooyberghs L, Ravatn R, Heyndrickx M, van der Meer JR, Vandecasteele C, Mergeay M, Diels L (2002) Community shifts in a seeded 3-chlorobenzoate degrading membrane biofilm reactor: indications for involvement of in situ horizontal transfer of the clc-element from inoculum to contaminant bacteria. Environ Microbiol 4:70–80

    Article  CAS  PubMed  Google Scholar 

  • Stanier RY, Ornston LN (1973) The β-ketoadipate pathway. In: Advances in microbial physiology. Academic, London, pp 89–151

  • Stecker C, Johann A, Herzberg C, Averhoff B, Gottschalk G (2003) Complete nucleotide sequence and genetic organization of the 210-kilobase linear plasmid of Rhodococcus erythropolis BD2. J Bacteriol 185:5269–5274

    Article  CAS  PubMed  Google Scholar 

  • Stelmack PL, Gray MR, Pickard MA (1999) Bacterial adhesion to soil contaminants in the presence of surfactants. Appl Environ Microbiol 65:163–168

    CAS  PubMed  Google Scholar 

  • Stratford J, Wright M, Reineke W, Mokross H, Havel J, Knowles C, Robinson G (1996) Influence of chlorobenzoates on the utilization of chlorobiphenyls and chlorobenzoate mixtures by chlorobiphenyl/chlorobenzoate-mineralising hybrid bacterial strains. Arch Microbiol 165:213–218

    Article  CAS  PubMed  Google Scholar 

  • Suenaga H, Goto M, Furukawa K (2001a) Emergence of multifunctional oxygenase activities by random priming recombination. J Biol Chem 276:22500–22506

    Article  CAS  PubMed  Google Scholar 

  • Suenaga H, Mitsuoka M, Ura Y, Watanabe T, Furukawa K (2001b) Directed evolution of biphenyl dioxygenase: emergence of enhanced degradation capacity for benzene, toluene, and alkylbenzenes. J Bacteriol 183:5441–5444

    Article  CAS  PubMed  Google Scholar 

  • Suenaga H, Nishi A, Watanabe T, Sakai M, Furukawa K (1999) Engineering a hybrid pseudomonad to acquire 3,4-dioxygenase activity for polychlorinated biphenyls. J Biosci Bioeng 87:430–435

    Article  CAS  Google Scholar 

  • Suenaga H, Watanabe T, Sato M, Ngadiman, Furukawa K (2002) Alteration of regiospecificity in biphenyl dioxygenase by active-site engineering. J Bacteriol 184:3682–3688

    Article  CAS  PubMed  Google Scholar 

  • Suzuki K, Ogawa N, Miyashita K (2001) Expression of 1,2-halobenzoate dioxygenase genes (cbdSABC) involved in the degradation of benzoate and 2-halobenzoate in Burkholderia sp. TH2. Gene 262:137–145

    Article  CAS  PubMed  Google Scholar 

  • Taguchi K, Motoyama M, Kudo T (2004) Multiplicity of 2,3-dihydroxybiphenyl dioxygenase genes in the Gram-positive polychlorinated biphenyl degrading bacterium Rhodococcus rhodochrous K37. Biosci Biotechnol Biochem 68:787–795

    Article  CAS  PubMed  Google Scholar 

  • Taira K, Hayase N, Arimura N, Yamashita S, Miyazaki T, Furukawa K (1988) Cloning and nucleotide sequence of the 2,3-dihydroxybiphenyl dioxygenase gene from the PCB-degrading strain of Pseudomonas paucimobilis Q1. Biochemistry 27:3990–3996

    CAS  PubMed  Google Scholar 

  • Takeda H, Yamada A, Miyauchi K, Masai E, Fukuda M (2004) Characterization of transcriptional regulatory genes for biphenyl degradation in Rhodococcus sp. strain RHA1. J Bacteriol 186:2134–2146

    Article  CAS  PubMed  Google Scholar 

  • Tandlich R, Brezna B, Dercova K (2001) The effect of terpenes on the biodegradation of polychlorinated biphenyls by Pseudomonas stutzeri. Chemosphere 44:1547–1555

    Article  CAS  PubMed  Google Scholar 

  • Toussaint A, Merlin C, Monchy S, Benotmane MA, Leplae R, Mergeay M, Springael D (2003) The biphenyl- and 4-chlorobiphenyl-catabolic transposon Tn4371, a member of a new family of genomic islands related to IncP and Ti plasmids. Appl Environ Microbiol 69:4837–4845

    Article  CAS  PubMed  Google Scholar 

  • Trefault N, de la Iglesia R, Molina A, Manzano M, Ledger T, Perez-Pantoja D, Sanchez M, Stuardo M, Gonzalez B (2004) Genetic organization of the catabolic plasmid pJP4 from Ralstonia eutropha JMP134 (pJP4) reveals mechanisms of adaptation to chloroaromatic pollutants and evolution of specialized chloroaromatic degradation pathways. Environ Microbiol 6:655–668

    Article  CAS  PubMed  Google Scholar 

  • Triska J, Kuncova G, Mackova M, Novakova H, Paasivirta J, Lahtipera M, Vrchotova N (2004) Isolation and identification of intermediates from biodegradation of low chlorinated biphenyls (Delor-103). Chemosphere 54:725–733

    Article  CAS  PubMed  Google Scholar 

  • Tsoi TV, Plotnikova EG, Cole JR, Guerin WF, Bagdasarian M, Tiedje JM (1999) Cloning, expression, and nucleotide sequence of the Pseudomonas aeruginosa 142 ohb genes coding for oxygenolytic ortho dehalogenation of halobenzoates. Appl Environ Microbiol 65:2151–2162

    Google Scholar 

  • Vaillancourt FH, Labbe G, Drouin NM, Fortin PD, Eltis LD (2002) The mechanism-based inactivation of 2,3-dihydroxybiphenyl 1,2-dioxygenase by catecholic substrates. J Biol Chem 277:2019–2027

    Article  CAS  PubMed  Google Scholar 

  • Vaillancourt FH, Haro M, Drouin N, Karim Z, Maaroufi H, Eltis L (2003) Characterization of extradiol dioxygenases from a polychlorinated biphenyl-degrading strain that possess higher specificities for chlorinated metabolites. J Bacteriol 185:1253–1260

    Article  CAS  PubMed  Google Scholar 

  • Vedler E, Koiv V, Heinaru A (2000) Analysis of the 2,4-dichlorophenoxyacetic acid-degradative plasmid pEST4011 of Achromobacter xylosooxidans subsp denitrificans strain EST4002. Gene 255:281–288

    Article  CAS  PubMed  Google Scholar 

  • Vollmer MD, Schlömann M (1995) Conversion of 2-chloro-cis,cis-muconate and its metabolites 2-chloro- and 5-chloromuconolactone by chloromuconate cycloisomerase of pJP4 and pAC27. J Bacteriol 177:2938–2941

    CAS  PubMed  Google Scholar 

  • Vollmer MD, Fischer P, Knackmuss H-J, Schlömann M (1994) Inability of muconate cycloisomerases to cause dehalogenation during conversion of 2-chloro-cis,cis-muconate. J Bacteriol 176:4366–4375

    CAS  PubMed  Google Scholar 

  • Watanabe T, Fujihara H, Furukawa K (2003) Characterization of the second LysR-type regulator in the biphenyl-catabolic gene cluster of Pseudomonas pseudoalcaligenes KF707. J Bacteriol 185:3575–3582

    Article  CAS  PubMed  Google Scholar 

  • Watanabe T, Inoue R, Kimura N, Furukawa K (2000) Versatile transcription of biphenyl catabolic bph operon in Pseudomonas pseudoalcaligenes KF707. J Biol Chem 275:31016–31023

    Article  CAS  PubMed  Google Scholar 

  • Worsey M, Williams PA (1975) Metabolism of toluene and xylenes by Pseudomonas putida (arvilla) mt-2: evidence for a new function of the TOL plasmid. J Bacteriol 124:7–13

    CAS  PubMed  Google Scholar 

  • Yamada A, Kishi H, Sugiyama K, Hatta T, Nakamura K, Masai E, Fukuda M (1998) Two nearly identical aromatic compound hydrolase genes in a strong polychlorinated biphenyl degrader, Rhodococcus sp. strain RHA1. Appl Environ Microbiol 64:2006–2012

    CAS  PubMed  Google Scholar 

  • Yang G, Liang P-H, Dunaway-Mariano D (1994) Evidence of nucleophilic catalysis in the aromatic substitution reaction catalyzed by (4-chlorobenzoyl) coenzyme A dehalogenase. Biochemistry 33:8527–8531

    CAS  PubMed  Google Scholar 

  • Zaitsev GM, Karasevich YN (1984) Utilization of 2-chlorobenzoic acid by Pseudomonas cepacia. Mikrobiologiya 53:75–80

    CAS  Google Scholar 

  • Zielinski M, Backhaus S, Hofer B (2002) The principal determinants for the structure of the substrate-binding pocket are located within a central core of a biphenyl dioxygenase alpha subunit. Microbiology 148:2439–2448

    CAS  PubMed  Google Scholar 

  • Zielinski M, Kahl S, Hecht HJ, Hofer B (2003) Pinpointing biphenyl dioxygenase residues that are crucial for substrate interaction. J Bacteriol 185:6976–6980

    Article  CAS  PubMed  Google Scholar 

  • Zylstra GJ, Kim E (1997) Aromatic hydrocarbon degradation by Sphingomonas yanoikuyae B1. J Ind Microbiol Biotechnol 19:408–414

    Article  CAS  Google Scholar 

  • Zylstra GJ, McCombie WR, Gibson DT, Finette BA (1988) Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon. Appl Environ Microbiol 54:1498–1503

    CAS  PubMed  Google Scholar 

Download references

Acknowledgements

The work of D.H.P. in biodegradation is supported by grants EVK1-CT-1999-00023, QLK3-CT-2000-00731 and ICA4-CT-2002-10011 from the EU and by the DFG-European Graduate College 653 contract. Critical reading of the manuscript by Lotte Gabriel-Jürgens and Peter Golyshin is gratefully acknowledged

Author information

Affiliations

  1. Department of Environmental Microbiology, German Research Center for Biotechnology, Mascheroder Weg 1, 38124, Braunschweig, Germany

    Dietmar H. Pieper

Authors
  1. Dietmar H. Pieper
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Dietmar H. Pieper.

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Pieper, D.H. Aerobic degradation of polychlorinated biphenyls. Appl Microbiol Biotechnol 67, 170–191 (2005). https://doi.org/10.1007/s00253-004-1810-4

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00253-004-1810-4

Keywords

  • PCBs
  • Chlorocatechol
  • Biphenyl Dioxygenase
  • Muconate
  • Extradiol Dioxygenases