Genetics and Biochemistry of Biphenyl and PCB Biodegradation

  • Loreine Agulló
  • Dietmar H. Pieper
  • Michael SeegerEmail author
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Microorganisms are crucial for the removal of polychlorinated biphenyls (PCBs) from polluted environments. Microbial anaerobic dehalogenation of highly and moderately chlorinated biphenyls generates the subsequent less chlorinated congeners. Microbial aerobic degradation performed by enzymes of the biphenyl (bph) upper and lower pathways oxidizes moderately and low chlorinated biphenyls. These enzymes and their substrate specificities are discussed in Sect. 2.1. Biphenyl 2,3-dioxgenases (BDOs) are key enzymes of biphenyl pathways, which determine substrate range and extent of PCB degradation. In addition, the specificity of subsequent enzymes is also crucial for productive metabolism. Specific native and engineered BDOs possess a wide range of substrates, which permit their application for synthesis of fine organic chemicals including novel bioactive compounds. The metabolism of PCBs is described in detail for some model organisms, and the genetic organization of gene clusters of model organisms is described in Sect. 2.2. The sequenced genomes of some PCB-metabolizing organisms including the model strains Burkholderia xenovorans LB400 and Rhodococcus jostii RHA1 improve the understanding of their overall metabolism, physiology, and evolution as described in Sect. 2.3. This has also allowed a better evaluation into genome and proteome-wide defenses against PCB toxicity, which is summarized in Sect. 2.4. However, our knowledge on enzymes and genes involved in PCB metabolism is still rather fragmentary and an overview of the diversity of enzymes reported and mosaic routes is given in Sect. 2.5. Finally, strategies to optimize microorganisms for improved PCB degradation and bioremediation processes are discussed in Sects. 2.6 and 2.7.



M.S. gratefully acknowledges support from the grants FONDECYT (1070507, 1020221, 1110992, 1151174, 7020221, 7070174, 7080148, 7090079, and 7100027), USM (130522, 130836, 130948, 131109, 131342, 131562), MILENIO P04/007-F (MIDEPLAN), and CONICYT-BMBF. D.P. gratefully acknowledges support from the grant EU GOCE 003998 (BIOTOOL) and BACSIN.


  1. Adebusoye SA, Picardal FW, Ilori MO, Amund OO (2008) Evidence of aerobic utilization of di-ortho-substituted trichlorobiphenyls as growth substrates by Pseudomonas sp. SA-6 and Ralstonia sp. SA-4. Environ Microbiol 10:1165–1174PubMedCrossRefPubMedCentralGoogle Scholar
  2. Adrian L, Rahnenführer J, Gobom J, Hölscher T (2007) Identification of a chlorobenzene reductive dehalogenase in Dehalococcoides sp. strain CBDB1. Appl Environ Microbiol 73(23):7717–7724PubMedPubMedCentralCrossRefGoogle Scholar
  3. Adrian L, Dudková V, Demnerová K, Bedard DL (2009) Dehalococcoides sp. strain CBDB1 extensively dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260. Appl Environ Microbiol 75: 4516–4524PubMedPubMedCentralCrossRefGoogle Scholar
  4. Agulló L, Cámara B, Martínez P, Latorre V, Seeger M (2007) Response to (chloro)biphenyls of the polychlorobiphenyl-degrader Burkholderia xenovorans LB400 involves stress proteins also induced by heat shock and oxidative stress. FEMS Microbiol Lett 267:167–175PubMedCrossRefPubMedCentralGoogle Scholar
  5. Agulló L, Romero-Silva MJ, Domenech M, Seeger M (2017) p-Cymene promotes its catabolism through the p-cymene and the p-cumate pathways, activates a stress response and reduces the biofilm formation in Burkholderia xenovorans LB400. PLoS One 12(1):e0169544. Scholar
  6. Arora A, Nair MG, Strasburg GM (1998) Antioxidant activities of isoflavones and their biological metabolites in a liposomal system. Arch Biochem Biophys 356:133–141PubMedCrossRefPubMedCentralGoogle Scholar
  7. Bae M, Kim E (2000) Association of a common reductase with multiple aromatic terminal dioxygenases in Sphingomonas yanoikuyae strain B1. J Microbiol 38:40–43Google Scholar
  8. Baker P, Carere J, Seah SY (2011) Probing the molecular basis of substrate specificity, stereospecificity, and catalysis in the class II pyruvate aldolase, BphI. Biochemistry 50:3559–3569PubMedCrossRefPubMedCentralGoogle Scholar
  9. Barriault D, Sylvestre M (1999) Catalytic activity of Pseudomonas putida strain G7 naphthalene 1,2-dioxygenase on biphenyl. Int Biodeterior Biodegrad 44:33–37CrossRefGoogle Scholar
  10. 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 145:2821–2834PubMedCrossRefPubMedCentralGoogle Scholar
  11. Bedard DL, Ritalahti KM, Loffler FE (2007) The Dehalococcoides population in sediment-free mixed cultures metabolically dechlorinates the commercial polychlorinated biphenyl mixture Aroclor 1260. Appl Environ Microbiol 73:2513–2521PubMedPubMedCentralCrossRefGoogle Scholar
  12. Bhowmik S, Horsman GP, Bolin JT, Eltis LD (2007) The molecular basis for inhibition of BphD, a C–C bond hydrolase involved in polychlorinated biphenyls degradation: large 3-substituents prevent tautomerization. J Biol Chem 282:36377–36385PubMedCrossRefPubMedCentralGoogle Scholar
  13. 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 270:29229–29235PubMedCrossRefPubMedCentralGoogle Scholar
  14. 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 63:427–434PubMedPubMedCentralGoogle Scholar
  15. Bopp L (1986) Degradation of highly chlorinated PCBs by Pseudomonas strain LB400. J Ind Microbiol 1:23–29CrossRefGoogle Scholar
  16. 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 6:842–850PubMedCrossRefPubMedCentralGoogle Scholar
  17. Cámara B, Seeger M, González M, Standfuss-Gabisch C, Kahl S, Hofer B (2007) Generation of a hybrid dioxygenase showing improved oxidation of polychlorobiphenyls by a widely applicable approach. Appl Environ Microbiol 73:2682–2689PubMedPubMedCentralCrossRefGoogle Scholar
  18. Carere J, Baker P, Seah S (2011) Investigating the molecular determinants for substrate channeling in BphI – BphJ, an aldolase – dehydrogenase complex from the polychlorinated biphenyls degradation pathway. Biochemistry 50:8407–8416PubMedCrossRefPubMedCentralGoogle Scholar
  19. Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agulló L, Reyes VL, Hauser L, Córdova M, Gomez L, González M, Land M, Lao V, Larimer F, LiPuma JJ, Mahenthiralingam E, Malfatti SA, Marx CJ, Parnell JJ, Ramette A, Richardson P, Seeger M, Smith D, Spilker T, Sul WJ, Tsoi TV, Ulrich LE, Zhulin IB, Tiedje JM (2006) Burkholderia xenovorans LB400 harbors a multi-replicon, 9.73-Mbp genome shaped for versatility. Proc Natl Acad Sci USA 103:15280–15287PubMedCrossRefPubMedCentralGoogle Scholar
  20. Chavez FP, Lünsdorf H, Jerez CA (2004) Growth of polychlorinated-biphenyl-degrading bacteria in the presence of biphenyl and chlorobiphenyls generates oxidative stress and massive accumulation of inorganic polyphosphate. Appl Environ Microbiol 70:3064–3072PubMedPubMedCentralCrossRefGoogle Scholar
  21. Chirino B, Strahsburger E, Agulló L, González M, Seeger M (2013) Genomic and functional analyses of the 2-aminophenol catabolic pathway and partial conversion of its substrate into picolinic acid in Burkholderia xenovorans LB400. PLoS ONE 8:e75746PubMedPubMedCentralCrossRefGoogle Scholar
  22. Correa PA, Lin L, Just CL, Hu D, Hornbuckle KC, Schnoor JL, Van Aken B (2010) The effects of individual PCB congeners on the soil bacterial community structure and the abundance of biphenyl dioxygenase genes. Environ Int 36(8):901–906PubMedCrossRefPubMedCentralGoogle Scholar
  23. Cutter LA, Watts JEM, Sowers KR, May HD (2001) Identification of a microorganism that links its growth to the reductive dechlorination of 2,3,5,6-chlorobiphenyl. Environ Microbiol 3:699–709PubMedCrossRefPubMedCentralGoogle Scholar
  24. 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 9:934–939PubMedCrossRefPubMedCentralGoogle Scholar
  25. Demaneche S, Meyer C, Micoud J, Louwagie M, Willison JC, Jouanneau Y (2004) Identification and functional analysis of two aromatic-ring-hydroxylating dioxygenases from a Sphingomonas strain that degrades various polycyclic aromatic hydrocarbons. Appl Environ Microbiol 70:6714–6725PubMedPubMedCentralCrossRefGoogle Scholar
  26. Denef VJ, Patrauchan MA, Florizone C, Park J, Tsoi TV, Verstraete W, Tiedje JM, Eltis LD (2005) Growth substrate- and phase-specific expression of biphenyl, benzoate, and C1 metabolic pathways in Burkholderia xenovorans LB400. J Bacteriol 187:7996–8005PubMedPubMedCentralCrossRefGoogle Scholar
  27. Drinker CK, Warren MF, Bennet GA (1937) The problem of possible systemic effects from certain chlorinated hydrocarbons. J Ind Hyg Toxicol 19:283–311Google Scholar
  28. Dunwell JM, Culham A, Carter C, Sos-Aguirre C, Goodenough PW (2001) Evolution of functional diversity in the cupin superfamily. Trends Biochem Sci 26:740–746PubMedCrossRefPubMedCentralGoogle Scholar
  29. Eltis LD, Bolin JT (1996) Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178:5930–5937PubMedPubMedCentralCrossRefGoogle Scholar
  30. Erickson BD, Mondello FJ (1993) Enhanced biodegradation of polychlorinated biphenyls after site-directed mutagenesis of a biphenyl dioxygenase gene. Appl Environ Microbiol 59:3858–3862PubMedPubMedCentralGoogle Scholar
  31. Faroon O, Jones D, de Rosa C (2001) Effects of polychlorinated biphenyls on the nervous system. Toxicol Ind Health 16:305–333CrossRefGoogle Scholar
  32. Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Haggblom MM (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075–2081PubMedCrossRefPubMedCentralGoogle Scholar
  33. Ferraro D, Daniel J, Brown EN, Yu CL, Parales RE, Gibson DT, Ramaswamy S (2007) Structural investigations of the ferredoxin and terminal oxygenase components of the biphenyl 2,3-dioxygenase from Sphingobium yanoikuyae B1. BMC Struct Biol 9:10CrossRefGoogle Scholar
  34. Fortin PD, Horsman G, Yang H, Eltis LD (2006) A glutathione S-transferase catalyzes the dehalogenation of inhibitory metabolites of polychlorinated biphenyls. J Bacteriol 188:4424–4430PubMedPubMedCentralCrossRefGoogle Scholar
  35. Fortin PD, Lo ATF, Haro MA, Kaschabek SR, Reineke W, Eltis LD (2005) Evolutionarily divergent extradiol dioxygenases possess higher specificities for polychlorinated biphenyl metabolites. J Bacteriol 187:415–421PubMedPubMedCentralCrossRefGoogle Scholar
  36. Furukawa K, Miyazaki T (1986) Cloning of a gene cluster encoding biphenyl and chlorobiphenyl degradation in Pseudomonas pseudoalcaligenes. J Bacteriol 166:392–398PubMedPubMedCentralCrossRefGoogle Scholar
  37. Furukawa K, Hirose J, Suyama A, Zaiki T, Hayashida S (1993) Gene components responsible for discrete substrate specificity in the metabolism of biphenyl (bph operon) and toluene (tod operon). J Bacteriol 175:5224–5232PubMedPubMedCentralCrossRefGoogle Scholar
  38. Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98(11):4781–4794PubMedCrossRefPubMedCentralGoogle Scholar
  39. Fuentes S, Ding GC, Cárdenas F, Smalla K, Seeger M (2015) Assessing environmental drivers of microbial communities in estuarine soils of the Aconcagua River in Central Chile. FEMS Microbiol Ecol 91:fiv110. Scholar
  40. Fuentes S, Barra B, Caporaso JG, Seeger M (2016) From rare to dominant: a fine-tuned soil bacterial bloom during petroleum hydrocarbon bioremediation. Appl Environ Microbiol 82(3):888–896PubMedPubMedCentralCrossRefGoogle Scholar
  41. Furukawa K (2000) Biochemical and genetic bases of microbial degradation of polychlorinated biphenyls (PCBs). J Gen Appl Microbiol 46:283–296PubMedCrossRefPubMedCentralGoogle Scholar
  42. Gerlt JA, Babbitt PC (2001) Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu Rev Biochem 70:209–246PubMedPubMedCentralCrossRefGoogle Scholar
  43. Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243PubMedCrossRefPubMedCentralGoogle Scholar
  44. Gilmartin N, Ryan D, Sherlock O, Dowling DN (2003) BphK shows dechlorination activity against 4-chlorobenzoate, an end-product of bph-promoted degradation of PCBs. FEMS Microbiol Lett 222:251–255PubMedCrossRefPubMedCentralGoogle Scholar
  45. Gomes H, Dias-Ferreira C, Ribeiro A (2013) Overview of in situ and ex situ remediation technologies for PCB-contaminated soils and sediments and obstacles for full-scale application. Sci Total Environ 445-–446:237–260PubMedCrossRefPubMedCentralGoogle Scholar
  46. Gomez-Gutiérrez A, Garnacho E, Bayona JM, Albaigés J (2007) Assessment of the Mediterranean sediments contamination by persistent organic pollutants. Environ Pollut 148:396–408PubMedCrossRefPubMedCentralGoogle Scholar
  47. Goncalves E, Hara H, Miyazawa D, Davies J, Eltis LD, Mohn WW (2006) Transcriptomic assessment of isoenzymes in the biphenyl pathway of Rhodococcus sp. strain RHA1. Appl Environ Microbiol 72:6283–6193CrossRefGoogle Scholar
  48. 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 177:20–26PubMedPubMedCentralCrossRefGoogle Scholar
  49. Harayama S, Rekik M (1989) Bacterial aromatic ring-cleavage enzymes are classified into two different gene families. J Biol Chem 264:15328–15333PubMedPubMedCentralGoogle Scholar
  50. Hatta T, Mukerjee-Dhar G, Damborsky J, Kiyohara H, Kimbara K (2003) Characterization of a novel thermostable Mn(II)-dependent 2,3-dihydroxybiphenyl 1,2-dioxygenase from a polychlorinated biphenyl- and naphthalene-degrading Bacillus sp JF8. J Biol Chem 278:21483–21492PubMedCrossRefPubMedCentralGoogle Scholar
  51. 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 172:1160–1164PubMedPubMedCentralCrossRefGoogle Scholar
  52. Hiraoka Y, Yamada T, Tone K, Futaesaku Y, Kimbara K (2002) Flow cytometry analysis of changes in the DNA content of the polychlorinated biphenyl degrader Comamonas testosteroni TK102: effect of metabolites on cell-cell separation. Appl Environ Microbiol 68:5104–5112PubMedPubMedCentralCrossRefGoogle Scholar
  53. 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 65:2163–2169PubMedPubMedCentralGoogle Scholar
  54. Hu J, Qian M, Zhang Q, Cui J, Yu C, Su X et al (2015) Sphingobium fuliginis HC3: a novel and robust isolated biphenyl- and polychlorinated biphenyls-degrading bacterium without dead-end intermediates accumulation. PLoS ONE 10(4):e0122740. Scholar
  55. Iwasaki T, Miyauchi K, Masai E, Fukuda M (2006) Multiple-subunit genes of the aromatic-ring-hydroxylating dioxygenase play an active role in biphenyl and polychlorinated biphenyl degradation in Rhodococcus sp. strain RHA1. Appl Environ Microbiol 72:5396–5402PubMedPubMedCentralCrossRefGoogle Scholar
  56. Jakoncic J, Jouanneau Y, Meyer C, Stojanoff V (2007) The catalytic pocket of the ring-hydroxylating dioxygenase from Sphingomonas CHY-1. Biochem Biophys Res Commun 352:861–866PubMedCrossRefPubMedCentralGoogle Scholar
  57. Jouanneau Y, Meyer C (2006) Purification and characterization of an arene cis-dihydrodiol dehydrogenase endowed with broad substrate specificity toward polycyclic aromatic hydrocarbon dihydrodiols. Appl Environ Microbiol 72:4726–4734PubMedPubMedCentralCrossRefGoogle Scholar
  58. 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 69:6688–6697PubMedPubMedCentralCrossRefGoogle Scholar
  59. 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 176:4269–4276PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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 179:3936–3943PubMedPubMedCentralCrossRefGoogle Scholar
  61. Kumamaru T, Suenaga H, Mitsuoka M, Watanabe T, Furukawa K (1998) Enhanced degradation of polychlorinated biphenyls by directed evolution of biphenyl dioxygenase. Nat Biotechnol 16:663–666PubMedCrossRefPubMedCentralGoogle Scholar
  62. Lauby-Secretan B, Loomis D, Grosse Y, El Ghissassi F, Bouvard V, Benbrahim-Tallaa L, Guha N, Baan R, Mattock H, Straif K et al (2013) Carcinogenicity of polychlorinated biphenyls and polybrominated biphenyls. Lancet Oncol 14:287–288PubMedCrossRefPubMedCentralGoogle Scholar
  63. Larkin MJ, Allen CCR, Kulakov LA, Lipscomb DA (1999) Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp strain NCIMB12038. J Bacteriol 181:6200–6204PubMedPubMedCentralGoogle Scholar
  64. Leigh MB, Pellizari VH, Uhlík O, Sutka R, Rodrigues J, Ostrom NE, Zhou J, Tiedje JM (2007) Biphenyl-utilizing bacteria and their functional genes in a pine root zone contaminated with polychlorinated biphenyls (PCBs). ISME J 1:134–148PubMedCrossRefPubMedCentralGoogle Scholar
  65. Liang Y, Meggo R, Hu D, Schnoor JL, Mattes TE (2014) Enhanced polychlorinated biphenyl removal in a switchgrass rhizosphere by bioaugmentation with Burkholderia xenovorans LB400. Ecol Eng 71:215–222PubMedPubMedCentralCrossRefGoogle Scholar
  66. 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 6:11–17CrossRefGoogle Scholar
  67. Lunt D, Evans WC (1970) The microbial metabolism of biphenyl. Biochem J 118:54–55CrossRefGoogle Scholar
  68. Martínez P, Agulló L, Hernández M, Seeger M (2007) Chlorobenzoate inhibits growth and induces stress proteins in the PCB-degrading bacterium Burkholderia xenovorans LB400. Arch Microbiol 188:289–297PubMedCrossRefGoogle Scholar
  69. 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 61:2079–2085PubMedPubMedCentralGoogle Scholar
  70. Mayes BA, McConnell EE, Neal BH, Brunner MJ, Hamilton SB, Sullivan TM, Peters AC, Ryan MJ, Toft JD, Singer AW, Brown JF, Menton RG, Moore JA (1998) Comparative carcinogenicity in Sprague-Dawley rats of the polychlorinated biphenyl mixtures aroclors 1016, 1242, 1254, and 1260. Toxicol Sci 41:62–76PubMedPubMedCentralGoogle Scholar
  71. 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 179:1924–1930PubMedPubMedCentralCrossRefGoogle Scholar
  72. McGuinness MC, Mazurkiewicz V, Brennan E, Dowling DN (2007) Dechlorination of pesticides by a specific bacterial glutathione S-transferase, BphK LB400: potential for bioremediation. Eng Life Sci 7(6):611–615CrossRefGoogle Scholar
  73. 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 185:2944–2951PubMedPubMedCentralCrossRefGoogle Scholar
  74. McLeod MP, Warren RL, Hsiao WW, Araki N, Myhre M, Fernandes C, Miyazawa D, Wong W, Lillquist AL, Wang D, Dosanjh M, Hara H, Petrescu A, Morin RD, Yang G, Stott JM, Schein JE, Shin H, Smailus D, Siddiqui AS, Marra MA, Jones SJ, Holt R, Brinkman FS, Miyauchi K, Fukuda M, Davies JE, Mohn WW, Eltis LD (2006) The complete genome of Rhodococcus sp. RHA1 provides insights into a catabolic powerhouse. Proc Natl Acad Sci USA 103:15582–15587PubMedCrossRefPubMedCentralGoogle Scholar
  75. Méndez V, Agulló L, González M, Seeger M (2011) The homogentisate and homoprotocatechuate central pathways are involved in 3- and 4-hydroxyphenylacetate degradation by Burkholderia xenovorans LB400. PLoS ONE 6:e17583PubMedPubMedCentralCrossRefGoogle Scholar
  76. Méndez V (2017) Molecular mechanisms of the adaptive response of Burkholderia xenovorans LB400 to oxidative stress induced by oxidants exposure and aromatic metabolism. Biotechnology PhD thesis, Universidad Técnica Federico Santa María & Pontificia Universidad Catolica de Valparaiso, Valparaiso, ChileGoogle Scholar
  77. Mondello FJ (1989) Cloning and expression in Escherichia coli of Pseudomonas strain LB400 genes encoding polychlorinated biphenyl degradation. J Bacteriol 171:1725–1732PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 63:3096–3103PubMedPubMedCentralGoogle Scholar
  79. 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 262:790–799PubMedCrossRefPubMedCentralGoogle Scholar
  80. Mukerjee-Dhar G, Shimura M, Miyazawa D, Kimbara K, Hatta T (2005) bph genes of the thermophilic PCB degrader, Bacillus sp. JF8: characterization of the divergent ring-hydroxylating dioxygenase and hydrolase genes upstream of the Mn-dependent BphC. Microbiology 151:4139–4151PubMedCrossRefPubMedCentralGoogle Scholar
  81. Müller JA, Rosner BM, von Abendroth G, Meshulam-Simon G, McCarty PL, Spormann AM (2004) Molecular identification of the catabolic vinyl chloride reductase from Dehalococcoides sp. strain VS and its environmental distribution. Appl Environ Microbiol 70:4880–4888PubMedPubMedCentralCrossRefGoogle Scholar
  82. Neumann A, Wohlfarth G, Diekert G (1996) Purification and characterization of tetrachloroethene reductive dehalogenase from Dehalospirillum multivorans. J Biol Chem 271:16515–16519PubMedCrossRefPubMedCentralGoogle Scholar
  83. Nojiri H, Nam JW, Kosaka M, Morii KI, Takemura T, Furihata K, Yamane H, Omori T (1999) Diverse oxygenations catalyzed by carbazole 1,9a-dioxygenase from Pseudomonas sp strain CA10. J Bacteriol 181:3105–3113PubMedPubMedCentralGoogle Scholar
  84. Novakova M, Mackova M, Antosova Z, Viktorova J, Szekeres M, Demnerova K, Macek T (2010) Cloning the bacterial bphC gene into Nicotiana tabacum to improve the efficiency of phytoremediation of polychlorinated biphenyls. Bioeng Bugs 1(6):419–423PubMedPubMedCentralCrossRefGoogle Scholar
  85. 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 147:31–41PubMedCrossRefPubMedCentralGoogle Scholar
  86. Ollis DL, Cheah E, Cygler M, Dijkstra B, Frolow F, Franken SM, Harel M, Remington SJ, Silman I, Schrag J, Sussman JL, Verschueren KHG, Goldman A (1992) The alpha/beta hydrolase fold. Protein Eng 5:197–211PubMedCrossRefPubMedCentralGoogle Scholar
  87. Overwin H, González M, Méndez V, Seeger M, Wray V, Hofer B (2012) Dioxygenation of the biphenyl dioxygenation product. Appl Environ Microbiol 78:4529–4532PubMedPubMedCentralCrossRefGoogle Scholar
  88. Overwin H, González M, Méndez V, Cárdenas F, Seeger M, Hofer B (2015a) Stepwise conversion of flavonoids by engineered dioxygenases and dehydrogenase: characterization of novel biotransformation products. Enzym Microb Technol 81:63–71CrossRefGoogle Scholar
  89. Overwin H, Standfuß-Gabisch C, González M, Méndez V, Seeger M, Reichelt J, Wray V, Hofer B (2015b) Permissivity of the biphenyl specific aerobic bacterial metabolic pathway towards analogues with various steric requirements. Microbiology 161:1844–1856PubMedCrossRefPubMedCentralGoogle Scholar
  90. Overwin H, González M, Méndez V, Seeger M, Wray V, Hofer B (2016) An aryl dioxygenase shows remarkable double dioxygenation capacity for diverse bis-aryl compounds, provided they are carbocyclic. Appl Microbiol Biotechnol 100:8053–8061. Scholar
  91. Payne RB, Fagervold SK, May HD, Sowers KR (2013) Remediation of polychlorinated biphenyl impacted sediment by concurrent bioaugmentation with anaerobic halorespiring and aerobic degrading bacteria. Environ Sci Technol 47(8):3807–3815PubMedPubMedCentralCrossRefGoogle Scholar
  92. Palma-Fleming H, Cornejo C, González M, Pérez V, González M, Gutierrez E, Sericano JL, Seeger M (2008) Polycyclic aromatic hydrocarbons and polychlorinated biphenyls from the coastal reef of Valdivia and Valparaíso region Chile. J Chil Chem Soc 53:1393–1398CrossRefGoogle Scholar
  93. Parnell JJ, Park J, Denef V, Tsoi T, Hashsham S, Quensen J III, Tiedje JM (2006) Coping with polychlorinated biphenyl (PCB) toxicity: physiological and genome-wide responses of Burkholderia xenovorans LB400 to PCB-mediated stress. Appl Environ Microbiol 72:6607–6614PubMedPubMedCentralCrossRefGoogle Scholar
  94. 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 125:35–40PubMedCrossRefPubMedCentralGoogle Scholar
  95. Pentyala SN, Rebecchi M, Mishra S, Rahman A, Stefen R, Rebecchi J, Kodavanti PS (2011) Polychlorinates biphenyls: In situ bioremediation from the environment. GR Reddy, SJF Flora, and RM Basha (ed.) Environ Pollut Ecol Hum Hlth, Narosa Publishing House, New Delhi, India, Chapter 1:249–262Google Scholar
  96. Pieper DH, Seeger M (2008) Bacterial metabolism of polychlorinated biphenyls. J Mol Microbiol Biotechnol 15:121–138PubMedCrossRefPubMedCentralGoogle Scholar
  97. Ponce BL, Latorre VK, González M, Seeger M (2011) Antioxidant compounds improved PCB-degradation by B. xenovorans strain LB400. Enzym Microb Technol 49:509–516CrossRefGoogle Scholar
  98. 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 67:3333–3339PubMedPubMedCentralCrossRefGoogle Scholar
  99. Reineke W (1998) Development of hybrid strains for the mineralization of chloroaromatics by patchwork assembly. Annu Rev Microbiol 52:287–331PubMedCrossRefPubMedCentralGoogle Scholar
  100. Rogers JE, Gibson DT (1977) Purification and properties of cis-toluene dihydrodiol dehydrogenase from Pseudomonas putida. J Bacteriol 130:1117–1124PubMedPubMedCentralGoogle Scholar
  101. Romero-Silva MJ, Méndez V, Agulló L, Seeger M (2013) Genomic and functional analyses of the gentisate and protocatechuate ring-cleavage pathways and related 3-hydroxybenzoate and 4-hydroxybenzoate peripheral pathways in Burkholderia xenovorans LB400. PLoS ONE 8:e56038PubMedPubMedCentralCrossRefGoogle Scholar
  102. Ruder AM, Hein MJ, Hopf NB, Waters MA (2014) Mortality among 24,865 workers exposed to polychlorinated biphenyls (PCBs) in three electrical capacitor manufacturing plants: a ten-year update. Int J Hyg Environ Health 217:176–187PubMedCrossRefPubMedCentralGoogle Scholar
  103. Ruzzini AC, Bhowmik S, Yam KC, Ghosh S, Bolin JT, Eltis LD (2013) The lid domain of the MCP hydrolase DxnB2 contributes to the reactivity toward recalcitrant PCB metabolites. Biochemistry 52(33):5685–5695PubMedPubMedCentralCrossRefGoogle Scholar
  104. Saavedra JM, Acevedo F, González M, Seeger M (2010) Mineralization of PCBs by the genetically modified strain Cupriavidus necator JMS34 and its application for bioremediation of PCBs in soil. Appl Microbiol Biotechnol 87(4):1543–1554PubMedCrossRefPubMedCentralGoogle Scholar
  105. Seah SY, Ke J, Denis G, Horsman GP, Fortin PD, Whiting CJ, Eltis LD (2007) Characterization of a C–C bond hydrolase from Sphingomonas wittichii RW1 with novel specificities towards polychlorinated biphenyl metabolites. J Bacteriol 189:4038–4045PubMedPubMedCentralCrossRefGoogle Scholar
  106. 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 275:15701–15708PubMedCrossRefPubMedCentralGoogle Scholar
  107. Seah SYK, Labbe G, Kaschabek SR, Reifenrath F, Reineke W, Eltis LD (2001) Comparative specificities of two evolutionarily divergent hydrolases involved in microbial degradation of polychlorinated biphenyls. J Bacteriol 183:1511–1516PubMedPubMedCentralCrossRefGoogle Scholar
  108. Seeger M, Timmis KN, Hofer B (1995a) 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 133:259–264PubMedCrossRefPubMedCentralGoogle Scholar
  109. Seeger M, Timmis KN, Hofer B (1995b) Conversion of chlorobiphenyls into phenylhexadienoates and benzoates by the enzymes of the upper pathway for polychlorobiphenyl degradation encoded by the bph locus of Pseudomonas sp. strain LB400. Appl Environ Microbiol 61:2654–2658PubMedPubMedCentralGoogle Scholar
  110. Seeger M, Cámara B, Hofer B (2001) Dehalogenation, denitration, dehydroxylation, and angular attack on substituted biphenyls and related compounds by a biphenyl dioxygenase. J Bacteriol 183:3548–3555PubMedPubMedCentralCrossRefGoogle Scholar
  111. 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 65:3614–3621PubMedPubMedCentralGoogle Scholar
  112. Seeger M, González M, Cámara B, Muñoz 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 69:5045–5050PubMedPubMedCentralCrossRefGoogle Scholar
  113. Seo J, Kang S, Kim M, Han J, Hur H-G (2011) Flavonoids biotransformation by bacterial non-heme dioxygenases, biphenyl and naphthalene dioxygenase. Appl Microbiol Biotechnol 91:219–228PubMedCrossRefPubMedCentralGoogle Scholar
  114. Sikkema J, de Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222PubMedPubMedCentralGoogle Scholar
  115. Singer AC, Gilbert ES, Luepromchai E, Crowley DE (2000) Bioremediation of polychlorinated biphenyl-contaminated soil using carvone and surfactant-grown bacteria. Appl Microbiol Biotechnol 54(6):838–843PubMedCrossRefPubMedCentralGoogle Scholar
  116. Sowers K, May HD (2013) In situ treatment of PCBs by anaerobic microbial dechlorination in aquatic sediment: are we there yet? Curr Opin Biotechnol 24(3):482–488PubMedCrossRefPubMedCentralGoogle Scholar
  117. 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 175:1674–1681PubMedPubMedCentralCrossRefGoogle Scholar
  118. 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 185:5269–5274PubMedPubMedCentralCrossRefGoogle Scholar
  119. 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 87:430–435PubMedCrossRefPubMedCentralGoogle Scholar
  120. Suenaga H, Watanabe T, Sato M, Ngadiman FK (2002) Alteration of regiospecificity in biphenyl dioxygenase by active-site engineering. J Bacteriol 184:3682–3688PubMedPubMedCentralCrossRefGoogle Scholar
  121. 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 68:787–795CrossRefGoogle Scholar
  122. Taguchi K, Motoyama M, Iida T, Kudo T (2007) Polychlorinated biphenyl/biphenyl degrading gene clusters in Rhodococcus sp. K37, HA99, and TA431 are different from well-known bph gene clusters of Rhodococci. Biosci Biotechnol Biochem 71:1136–1144PubMedCrossRefPubMedCentralGoogle Scholar
  123. 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 186:2134–2146PubMedPubMedCentralCrossRefGoogle Scholar
  124. Taylor PM, Medd JM, Schoenborn L, Hodgson B, Janssen PH (2002) Detection of known and novel genes encoding aromatic ring- hydroxylating dioxygenases in soils and in aromatic hydrocarbon-degrading bacteria. FEMS Microbiol Lett 216:61–66PubMedCrossRefPubMedCentralGoogle Scholar
  125. 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 69:4837–4845PubMedPubMedCentralCrossRefGoogle Scholar
  126. Triscari-Barberi T, Simone D, Calabrese FM, Attimonelli M, Hahn KR, Amoako KK, Turner RJ, Fedi S, Zannonia D (2012) Genome sequence of the polychlorinated-biphenyl degrader Pseudomonas pseudoalcaligenes KF707. J Bacteriol 194(16):4426–4427PubMedPubMedCentralCrossRefGoogle Scholar
  127. Tu C, Teng Y, Luo Y, Li X, Sun X, Li Z, Liu W, Christie P (2011) Potential for biodegradation of polychlorinated biphenyls (PCBs) by Sinorhizobium meliloti. J Hazard Mater 186(2–3):1438–1444PubMedCrossRefPubMedCentralGoogle Scholar
  128. 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 277:2019–2027CrossRefPubMedPubMedCentralGoogle Scholar
  129. Vezina J, Barriault D, Sylvestre M (2007) Family shuffling of soil DNA to change the regiospecificity of Burkholderia xenovorans LB400 biphenyl dioxygenase. J Bacteriol 189:779–788PubMedCrossRefPubMedCentralGoogle Scholar
  130. Watanabe T, Inoue R, Kimura N, Furukawa K (2000) Versatile transcription of biphenyl catabolic bph operon in Pseudomonas pseudoalcaligenes KF707. J Biol Chem 275:31016–31023Google Scholar
  131. Witzig R, Junca H, Hecht HJ, Pieper DH (2006) Assessment of toluene/biphenyl dioxygenase gene diversity in benzene-polluted soils: links between benzene biodegradation and genes similar to those encoding isopropylbenzene dioxygenases. Appl Environ Microbiol 72:3504–3514PubMedPubMedCentralCrossRefGoogle Scholar
  132. Wu Q, Watts JE, Sowers KR, May HD (2002) Identification of a bacterium that specifically catalyzes the reductive dechlorination of polychlorinated biphenyls with doubly flanked chlorines. Appl Environ Microbiol 68:807–812PubMedPubMedCentralCrossRefGoogle Scholar
  133. Xu Y, Yu M, Shen A (2016) Complete genome sequence of the polychlorinated biphenyl degrader Rhodococcus sp. WB1. Genome Announc 4(5):e00996–e00916PubMedPubMedCentralCrossRefGoogle Scholar
  134. Xu L, Teng Y, Li ZG, Norton JM, Luo YM (2010) Enhanced removal of polychlorinated biphenyls from alfalfa rhizosphere soil in a field study: the impact of a rhizobial inoculum. Sci Total Environ 408(5):1007–1013PubMedCrossRefPubMedCentralGoogle Scholar
  135. 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 64:2006–2012PubMedPubMedCentralGoogle Scholar
  136. Yang X, Liu X, Xie F, Zhang G, Qian S (2007) Characterization and functional analysis of a novel gene cluster involved in biphenyl degradation in Rhodococcus sp. strain R04. J Appl Microbiol 103:2214–2224PubMedCrossRefPubMedCentralGoogle Scholar
  137. Yu C, Liu W, Ferraro D, Brown E, Parales JV, Ramaswamy S, Zylstra GJ, Gibson DT, Parales RE (2007) Purification, characterization and crystallization of the components of a biphenyl dioxygenase system from Sphingobium yanoikuyae B1. J Ind Microbiol Biotechnol 34:311–324PubMedCrossRefPubMedCentralGoogle Scholar
  138. Zielinski M, Kahl S, Standfuss-Gabisch C, Cámara B, Seeger M, Hofer B (2006) Generation of novel-substrate-accepting biphenyl dioxygenases through segmental random mutagenesis and identification of residues involved in enzyme specificity. Appl Environ Microbiol 72:2191–2199PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • Loreine Agulló
    • 1
  • Dietmar H. Pieper
    • 2
  • Michael Seeger
    • 1
    Email author
  1. 1.Laboratorio de Microbiología Molecular y Biotecnología Ambiental, Department of Chemistry and Center for Nanotechnology and Systems Biology and Centro de BiotecnologíaUniversidad Técnica Federico Santa MaríaValparaísoChile
  2. 2.Microbial Interactions and Processes Research GroupHZI – Helmholtz Centre for Infection ResearchBraunschweigGermany

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