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Genetics and Biochemistry of Biphenyl and PCB Biodegradation

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Aerobic Utilization of Hydrocarbons, Oils, and Lipids

Part of the book series: Handbook of Hydrocarbon and Lipid Microbiology ((HHLM))

Abstract

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.

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References

  • 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 10:1165–1174

    Article  CAS  PubMed  Google Scholar 

  • 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):7717–7724

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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: 4516–4524

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 267:167–175

    Article  PubMed  CAS  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0169544

    Article  PubMed  PubMed Central  Google Scholar 

  • Arora A, Nair MG, Strasburg GM (1998) Antioxidant activities of isoflavones and their biological metabolites in a liposomal system. Arch Biochem Biophys 356:133–141

    Article  CAS  PubMed  Google Scholar 

  • Bae M, Kim E (2000) Association of a common reductase with multiple aromatic terminal dioxygenases in Sphingomonas yanoikuyae strain B1. J Microbiol 38:40–43

    CAS  Google Scholar 

  • 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 50:3559–3569

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  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

    Article  CAS  PubMed  Google Scholar 

  • 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 73:2513–2521

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 282:36377–36385

    Article  CAS  PubMed  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 

  • 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

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bopp L (1986) Degradation of highly chlorinated PCBs by Pseudomonas strain LB400. J Ind Microbiol 1:23–29

    Article  CAS  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  CAS  Google Scholar 

  • 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 73:2682–2689

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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 50:8407–8416

    Article  CAS  PubMed  Google Scholar 

  • 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 103:15280–15287

    Article  PubMed  PubMed Central  Google Scholar 

  • 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 70:3064–3072

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e75746

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):901–906

    Article  CAS  PubMed  Google Scholar 

  • 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 3:699–709

    Article  CAS  PubMed  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 

  • 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 70:6714–6725

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 187:7996–8005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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

    CAS  Google Scholar 

  • Dunwell JM, Culham A, Carter C, Sos-Aguirre C, Goodenough PW (2001) Evolution of functional diversity in the cupin superfamily. Trends Biochem Sci 26:740–746

    Article  CAS  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

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

    Article  Google Scholar 

  • Fennell DE, Nijenhuis I, Wilson SF, Zinder SH, Haggblom MM (2004) Dehalococcoides ethenogenes strain 195 reductively dechlorinates diverse chlorinated aromatic pollutants. Environ Sci Technol 38:2075–2081

    Article  CAS  PubMed  Google Scholar 

  • 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 9:10

    Article  CAS  Google Scholar 

  • Fortin PD, Horsman G, Yang H, Eltis LD (2006) A glutathione S-transferase catalyzes the dehalogenation of inhibitory metabolites of polychlorinated biphenyls. J Bacteriol 188:4424–4430

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 187:415–421

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 175:5224–5232

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fuentes S, Méndez V, Aguila P, Seeger M (2014) Bioremediation of petroleum hydrocarbons: catabolic genes, microbial communities, and applications. Appl Microbiol Biotechnol 98(11):4781–4794

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1093/femsec/fiv110

    Article  CAS  PubMed  Google Scholar 

  • 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):888–896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Furukawa K (2000) Biochemical and genetic bases of microbial degradation of polychlorinated biphenyls (PCBs). J Gen Appl Microbiol 46:283–296

    Article  CAS  PubMed  Google Scholar 

  • Gerlt JA, Babbitt PC (2001) Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu Rev Biochem 70:209–246

    Article  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 

  • 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 222:251–255

    Article  CAS  PubMed  Google Scholar 

  • 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-–446:237–260

    Article  PubMed  CAS  Google Scholar 

  • Gomez-Gutiérrez A, Garnacho E, Bayona JM, Albaigés J (2007) Assessment of the Mediterranean sediments contamination by persistent organic pollutants. Environ Pollut 148:396–408

    Article  PubMed  CAS  Google Scholar 

  • 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 72:6283–6193

    Article  CAS  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harayama S, Rekik M (1989) Bacterial aromatic ring-cleavage enzymes are classified into two different gene families. J Biol Chem 264:15328–15333

    CAS  PubMed  Google Scholar 

  • 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 278:21483–21492

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:5104–5112

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1371/journal.pone.0122740

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 72:5396–5402

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 352:861–866

    Article  CAS  PubMed  Google Scholar 

  • 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 72:4726–4734

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • 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 14:287–288

    Article  CAS  PubMed  Google Scholar 

  • Larkin MJ, Allen CCR, Kulakov LA, Lipscomb DA (1999) Purification and characterization of a novel naphthalene dioxygenase from Rhodococcus sp strain NCIMB12038. J Bacteriol 181:6200–6204

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 1:134–148

    Article  CAS  PubMed  Google Scholar 

  • 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 71:215–222

    Article  PubMed  PubMed Central  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

    Article  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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 188:289–297

    Article  PubMed  CAS  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  PubMed Central  Google Scholar 

  • 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 41:62–76

    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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):611–615

    Article  CAS  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  PubMed Central  Google Scholar 

  • 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 103:15582–15587

    Article  PubMed  PubMed Central  Google Scholar 

  • 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:e17583

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • 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, Chile

    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

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  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 

  • 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 151:4139–4151

    Article  CAS  PubMed  Google Scholar 

  • 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 70:4880–4888

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Neumann A, Wohlfarth G, Diekert G (1996) Purification and characterization of tetrachloroethene reductive dehalogenase from Dehalospirillum multivorans. J Biol Chem 271:16515–16519

    Article  CAS  PubMed  Google Scholar 

  • 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 181:3105–3113

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):419–423

    Article  PubMed  PubMed Central  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

    Article  CAS  PubMed  Google Scholar 

  • 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 5:197–211

    Article  CAS  PubMed  Google Scholar 

  • Overwin H, González M, Méndez V, Seeger M, Wray V, Hofer B (2012) Dioxygenation of the biphenyl dioxygenation product. Appl Environ Microbiol 78:4529–4532

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 81:63–71

    Article  CAS  Google Scholar 

  • 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 161:1844–1856

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1007/s00253-016-7570-0

    Article  CAS  PubMed  Google Scholar 

  • 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):3807–3815

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 53:1393–1398

    Article  Google Scholar 

  • 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 72:6607–6614

    Article  CAS  PubMed  PubMed Central  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 

  • 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 1:249–262

    Google Scholar 

  • Pieper DH, Seeger M (2008) Bacterial metabolism of polychlorinated biphenyls. J Mol Microbiol Biotechnol 15:121–138

    Article  CAS  PubMed  Google Scholar 

  • Ponce BL, Latorre VK, González M, Seeger M (2011) Antioxidant compounds improved PCB-degradation by B. xenovorans strain LB400. Enzym Microb Technol 49:509–516

    Article  CAS  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  PubMed Central  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 

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

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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:e56038

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 217:176–187

    Article  CAS  PubMed  Google Scholar 

  • 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):5685–5695

    Article  CAS  PubMed  Google Scholar 

  • 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):1543–1554

    Article  CAS  PubMed  Google Scholar 

  • 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 189:4038–4045

    Article  CAS  PubMed  PubMed Central  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 

  • 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 183:1511–1516

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 133:259–264

    Article  CAS  PubMed  Google Scholar 

  • 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 61:2654–2658

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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 183:3548–3555

    Article  CAS  PubMed  PubMed Central  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  PubMed Central  Google Scholar 

  • 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 69:5045–5050

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 91:219–228

    Article  CAS  PubMed  Google Scholar 

  • Sikkema J, de Bont JAM, Poolman B (1995) Mechanisms of membrane toxicity of hydrocarbons. Microbiol Rev 59:201–222

    CAS  PubMed  PubMed Central  Google Scholar 

  • 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):838–843

    Article  CAS  PubMed  Google Scholar 

  • 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):482–488

    Article  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

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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  PubMed Central  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  PubMed  Google Scholar 

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

    Article  CAS  PubMed  PubMed Central  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 

  • 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 71:1136–1144

    Article  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  PubMed Central  Google Scholar 

  • 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 216:61–66

    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  PubMed Central  Google Scholar 

  • 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):4426–4427

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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):1438–1444

    Article  CAS  PubMed  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 

  • Vezina J, Barriault D, Sylvestre M (2007) Family shuffling of soil DNA to change the regiospecificity of Burkholderia xenovorans LB400 biphenyl dioxygenase. J Bacteriol 189:779–788

    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

    Google Scholar 

  • 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 72:3504–3514

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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 68:807–812

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xu Y, Yu M, Shen A (2016) Complete genome sequence of the polychlorinated biphenyl degrader Rhodococcus sp. WB1. Genome Announc 4(5):e00996–e00916

    Article  PubMed  PubMed Central  Google Scholar 

  • 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):1007–1013

    Article  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  PubMed Central  Google Scholar 

  • 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 103:2214–2224

    Article  CAS  PubMed  Google Scholar 

  • 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 34:311–324

    Article  CAS  PubMed  Google Scholar 

  • 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 72:2191–2199

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

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.

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  1. Laboratorio de Microbiología Molecular y Biotecnología Ambiental, Department of Chemistry and Center for Nanotechnology and Systems Biology and Centro de Biotecnología, Universidad Técnica Federico Santa María, Valparaíso, Chile

    Loreine Agulló & Michael Seeger

  2. Microbial Interactions and Processes Research Group, HZI – Helmholtz Centre for Infection Research, Braunschweig, Germany

    Dietmar H. Pieper

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  1. Loreine Agulló
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  2. Dietmar H. Pieper
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  3. Michael Seeger
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Correspondence to Michael Seeger .

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  1. Centro Nacional de Biotecnología, CSIC, Madrid, Spain

    Fernando Rojo

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Agulló, L., Pieper, D.H., Seeger, M. (2019). Genetics and Biochemistry of Biphenyl and PCB Biodegradation. In: Rojo, F. (eds) Aerobic Utilization of Hydrocarbons, Oils, and Lipids. Handbook of Hydrocarbon and Lipid Microbiology . Springer, Cham. https://doi.org/10.1007/978-3-319-50418-6_30

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