Phylogenomics of Aerobic Bacterial Degradation of Aromatics

  • D. Pérez-Pantoja
  • R. Donoso
  • H. Junca
  • B. González
  • Dietmar H. PieperEmail author
Reference work entry
Part of the Handbook of Hydrocarbon and Lipid Microbiology book series (HHLM)


Aromatic compounds are widely distributed in nature. They are found as lignin components, aromatic amino acids, and xenobiotic compounds, among others. Microorganisms, mostly bacteria, degrade an impressive variety of such chemical structures. Various aerobic aromatic catabolic pathways have been reported in bacteria, which typically consist of activation of the aromatic ring through oxygenases or CoA ligases and ring cleavage of di- or trihydroxylated intermediates or dearomatized CoA derivatives. We survey almost 900 sequenced bacterial genomes available in 2008 for the presence of genes encoding key enzymes of aromatic metabolic pathways, including ring-cleavage enzymes as well as enzymes activating aromatics or dearomatizing CoA derivatives. The metabolic diversity is discussed from two angles: the spread of such key activities among different bacterial phyla and the overall metabolic potential of members of bacterial genera.


  1. Altenschmidt U, Fuchs G (1992) Novel aerobic 2-aminobenzoate metabolism. Purification and characterization of 2-aminobenzoate-CoA ligase, localisation of the genes on a 8-kbp plasmid, and cloning and sequencing of the genes from a denitrifying Pseudomonas sp. Eur J Biochem 205:721–727PubMedCrossRefGoogle Scholar
  2. Ampe F, Lindley ND (1996) Flux limitations in the ortho pathway of benzoate degradation of Alcaligenes eutrophus: metabolite overflow and induction of the meta pathway at high substrate concentrations. Microbiology 142:1807–1817PubMedCrossRefGoogle Scholar
  3. Aoki K, Konohana T, Shinke R, Nishira H (1984) Two catechol 1,2-dioxygenases from aniline-assimilating bacterium, Frateuria species ANA-18. Agric Biol Chem 48:2097–2104Google Scholar
  4. Arias-Barrau E, Olivera ER, Luengo JM, Fernandez C, Galan B, Garcia JL, Diaz E, Minambres B (2004) The homogentisate pathway: a central catabolic pathway involved in the degradation of L-phenylalanine, L-tyrosine, and 3-hydroxyphenylacetate in Pseudomonas putida. J Bacteriol 186:5062–5077PubMedPubMedCentralGoogle Scholar
  5. Arias-Barrau E, Sandoval A, Naharro G, Olivera ER, Luengo JM (2005) A two-component hydroxylase involved in the assimilation of 3-hydroxyphenyl acetate in Pseudomonas putida. J Biol Chem 280:26435–26447PubMedGoogle Scholar
  6. 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 175:4631–4640PubMedPubMedCentralCrossRefGoogle Scholar
  7. Ballou DP, Entsch B, Cole LJ (2005) Dynamics involved in catalysis by single-component and two-component flavin-dependent aromatic hydroxylases. Biochem Biophys Res Commun 338:590–598PubMedCrossRefGoogle Scholar
  8. Beil S, Mason JR, Timmis KN, Pieper DH (1998) Identification of chlorobenzene dioxygenase sequence elements involved in dechlorination of 1,2,4,5-tetrachlorobenzene. J Bacteriol 180:5520–5528PubMedPubMedCentralGoogle Scholar
  9. Beltrametti F, Marconi AM, Bestetti G, Colombo C, Galli E, Ruzzi M, Zennaro E (1997) Sequencing and functional analysis of styrene catabolism genes from Pseudomonas fluorescens ST. Appl Environ Microbiol 63:2232–2239PubMedPubMedCentralGoogle Scholar
  10. Bosch R, GarciaValdes E, Moore ERB (1999a) Genetic characterization and evolutionary implications of a chromosomally encoded naphthalene-degradation upper pathway from Pseudomonas stutzeri AN10. Gene 236:149–157PubMedCrossRefGoogle Scholar
  11. Bosch R, Moore ERB, GarciaValdes E, Pieper DH (1999b) Nah W, a novel, inducible salicylate hydroxylase involved in mineralization of naphthalene by Pseudomonas stutzeri AN10. J Bacteriol 181:2315–2322PubMedPubMedCentralGoogle Scholar
  12. Buder R, Fuchs G (1989) 2-Aminobenzoyl-CoA monooxygenase/reductase, a novel type of flavoenzyme. Purification and some properties of the enzyme. Eur J Biochem 185:629–635PubMedCrossRefGoogle Scholar
  13. Cai M, Xun LY (2002) Organization and regulation of pentachlorophenol-degrading genes in Sphingobium chlorophenolicum ATCC 39723. J Bacteriol 184:4672–4680PubMedPubMedCentralCrossRefGoogle Scholar
  14. Cámara B, Bielecki P, Kaminski F, dos Santos VM, Plumeier I, Nikodem P, Pieper DH (2007) A gene cluster involved in degradation of substituted salicylates via ortho cleavage in Pseudomonas sp. strain MT1 encodes enzymes specifically adapted for transformation of 4-methylcatechol and 3-methylmuconate. J Bacteriol 189:1664–1674PubMedCrossRefPubMedCentralGoogle Scholar
  15. Cao B, Geng A, Loh K (2008) Induction of ortho- and meta-cleavage pathways in Pseudomonas in biodegradation of high benzoate concentration: MS identification of catabolic enzymes. Appl Microbiol Biotechnol 81:99–107PubMedCrossRefGoogle Scholar
  16. Chain PS, Denef VJ, Konstantinidis KT, Vergez LM, Agullo L, Reyes VL, Hauser L, Cordova M, Gomez L, Gonzalez 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
  17. Chang HK, Mohseni P, Zylstra GJ (2003) Characterization and regulation of the genes for a novel anthranilate 1,2-dioxygenase from Burkholderia cepacia DBO1. J Bacteriol 185:5871–5881PubMedPubMedCentralCrossRefGoogle Scholar
  18. Daane LL, Harjono I, Barns SM, Launen LA, Palleroni NJ, Häggblom MM (2002) PAH-degradation by Paenibacillus spp. and description of Paenibacillus naphthalenovorans sp. Nov., a naphthalene- degrading bacterium from the rhizosphere of salt marsh plants. Int J Syst Evol Microbiol 52:131–139PubMedCrossRefGoogle Scholar
  19. Dehmel U, Engesser K-H, Timmis KN, Dwyer DF (1995) Cloning, nucleotide sequence, and expression of the gene encoding a novel dioxygenase involved in metabolism of carboxydiphenyl ehters in Pseudomonas pseudoalcaligenes POB310. Arch Microbiol 163:35–41PubMedCrossRefGoogle Scholar
  20. Denef VJ, Park J, Tsoi TV, Rouillard JM, Zhang H, Wibbenmeyer JA, Verstraete W, Gulari E, Hashsham SA, Tiedje JM (2004) Biphenyl and benzoate metabolism in a genomic context: outlining genome-wide metabolic networks in Burkholderia xenovorans LB400. Appl Environ Microbiol 70:4961–4970PubMedPubMedCentralCrossRefGoogle Scholar
  21. Denef VJ, Klappenbach JA, Patrauchan MA, Florizone C, Rodrigues JL, Tsoi TV, Verstraete W, Eltis LD, Tiedje JM (2006) Genetic and genomic insights into the role of benzoate-catabolic pathway redundancy in Burkholderia xenovorans LB400. Appl Environ Microbiol 72:585–595PubMedPubMedCentralCrossRefGoogle Scholar
  22. Deng D, Li X, Fang X, Sun G (2007) Characterization of two components of the 2-naphthoate monooxygenase system from Burkholderia sp. strain JT1500. FEMS Microbiol Lett 273:22–27PubMedCrossRefGoogle Scholar
  23. Diaz E, Ferrandez A, Prieto MA, Garcia J (2001) Biodegradation of aromatic compounds by Escherichia coli. Microbiol Mol Biol Rev 65:523–569PubMedPubMedCentralCrossRefGoogle Scholar
  24. Duarte M, Jauregui R, Vilchez-Vargas R, Junca H, Pieper DH (2014) AromaDeg, a novel database for phylogenomics of aerobic degradation of aromatics. Database bau118Google Scholar
  25. Duffner FM, Muller R (1998) A novel phenol hydroxylase and catechol 2,3-dioxygenase from the thermophilic Bacillus thermoleovorans strain A2: nucleotide sequence and analysis of the genes. FEMS Microbiol Lett 161:37–45PubMedCrossRefGoogle Scholar
  26. Dunwell JM, Khuri S, Gane PJ (2000) Microbial relatives of the seed storage proteins of higher plants: conservation of structure and diversification of function during evolution of the cupin superfamily. Microbiol Mol Biol Rev 64:153–179PubMedPubMedCentralCrossRefGoogle Scholar
  27. Eaton RW (1996) p-Cumate catabolic pathway in Pseudomonas putida F1: cloning and characterization of DNA carrying the cmt operon. J Bacteriol 178:1351–1362PubMedPubMedCentralCrossRefGoogle Scholar
  28. Eaton RW, Ribbons DW (1982) Metabolism of dibutylphthalate and phthalate by Micrococcus sp. strain 12B. J Bacteriol 151:48–57PubMedPubMedCentralGoogle Scholar
  29. Eby DM, Beharry ZM, Coulter ED, Kurtz DM, Neidle EL (2001) Characterization and evolution of anthranilate 1,2-dioxygenase from Acinetobacter sp. strain ADP1. J Bacteriol 183:109–118PubMedPubMedCentralCrossRefGoogle Scholar
  30. Edgar RC (2004) MUSCLE: a multiple sequence alignment method with reduced time and space complexity. BMC Bioinforma 5:113CrossRefGoogle Scholar
  31. Eltis LD, Bolin JT (1996) Evolutionary relationships among extradiol dioxygenases. J Bacteriol 178:5930–5937PubMedPubMedCentralCrossRefGoogle Scholar
  32. Enroth C, Huang W, Waters S, Neujahr H, Lindqvist Y, Schneider G (1994) Crystallization and preliminary X-ray analysis of phenol hydroxlase from Trichosporon cutaneum. J Mol Biol 238:128–130PubMedCrossRefGoogle Scholar
  33. Eulberg D, Golovleva LA, Schlomann M (1997) Characterization of catechol catabolic genes from Rhodococcus erythropolis 1CP. J Bacteriol 179:370–381PubMedPubMedCentralCrossRefGoogle Scholar
  34. 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 180:2522–2530PubMedPubMedCentralGoogle Scholar
  35. Gerlt JA, Babbitt PC (2001) Divergent evolution of enzymatic function: mechanistically diverse superfamilies and functionally distinct suprafamilies. Annu Rev Biochem 70:209–246PubMedPubMedCentralCrossRefGoogle Scholar
  36. Gibson DT, Parales RE (2000) Aromatic hydrocarbon dioxygenases in environmental biotechnology. Curr Opin Biotechnol 11:236–243PubMedCrossRefPubMedCentralGoogle Scholar
  37. Gonzalez JM, Mayer F, Moran MA, Hodson RE, Whitman WB (1997) Sagittula stellata gen. Nov., sp. Nov., a lignin-transforming bacterium from a coastal environment. Int J Syst Bacteriol 47:773–780PubMedCrossRefGoogle Scholar
  38. Haigler BE, Johnson GR, Suen WC, Spain JC (1999) Biochemical and genetic evidence for meta-ring cleavage of 2,4,5-trihydroxytoluene in Burkholderia sp. strain DNT. J Bacteriol 181:965–972PubMedPubMedCentralGoogle Scholar
  39. 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
  40. Hawumba JF, Brözel VS, Theron J (2007) Cloning and characterization of a 4-hydroxyphenylacetate 3-hydroxylase from the thermophile Geobacillus sp. PA-9. Curr Microbiol 55:480–484PubMedCrossRefGoogle Scholar
  41. Hiromoto T, Fujiwara S, Hosokawa K, Yamaguchi H (2006) Crystal structure of 3-hydroxybenzoate hydroxylase from Comamonas testosteroni has a large tunnel for substrate and oxygen access to the active site. J Mol Biol 364:878–896PubMedCrossRefGoogle Scholar
  42. Huang Y, Zhao KX, Shen XH, Chaudhry MT, Jiang CY, Liu SJ (2006) Genetic characterization of the resorcinol catabolic pathway in Corynebacterium glutamicum. Appl Environ Microbiol 72:7238–7245PubMedPubMedCentralCrossRefGoogle Scholar
  43. Iida T, Nakamura K, Izumi A, Mukouzaka Y, Kudo T (2006) Isolation and characterization of a gene cluster for dibenzofuran degradation in a new dibenzofuran-utilizing bacterium, Paenibacillus sp. strain YK5. Arch Microbiol 184:305–315PubMedCrossRefGoogle Scholar
  44. Ishiyama D, Vujaklija D, Davies J (2004) Novel pathway of salicylate degradation by Streptomyces sp. strain WA46. Appl Environ Microbiol 70:1297–1306PubMedPubMedCentralCrossRefGoogle Scholar
  45. Ismail W, El-Said Mohamed M, Wanner BL, Datsenko KA, Eisenreich W, Rohdich F, Bacher A, Fuchs G (2003) Functional genomics by NMR spectroscopy. Phenylacetate catabolism in Escherichia coli. Eur J Biochem 270:3047–3054PubMedCrossRefGoogle Scholar
  46. 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
  47. Jimenez JI, Minambres B, Garcia JL, Diaz E (2002) Genomic analysis of the aromatic catabolic pathways from Pseudomonas putida KT2440. Environ Microbiol 4:824–841PubMedCrossRefGoogle Scholar
  48. Jones RM, Pagmantidis V, Williams PA (2000) sal genes determining the catabolism of salicylate esters are part of a supraoperonic cluster of catabolic genes in Acinetobacter sp. strain ADP1. J Bacteriol 182:2018–2025PubMedPubMedCentralCrossRefGoogle Scholar
  49. Junca H, Plumeier I, Hecht HJ, Pieper DH (2004) Difference in kinetic behaviour of catechol 2,3-dioxygenase variants from a polluted environment. Microbiology 150:4181–4187PubMedCrossRefGoogle Scholar
  50. Kasai D, Masai E, Miyauchi K, Katayama Y, Fukuda M (2004) Characterization of the 3-O-methylgallate dioxygenase gene and evidence of multiple 3-O-methylgallate catabolic pathways in Sphingomonas paucimobilis SYK-6. J Bacteriol 186:4951–4959PubMedPubMedCentralCrossRefGoogle Scholar
  51. Kasai D, Masai E, Miyauchi K, Katayama Y, Fukuda M (2005) Characterization of the gallate dioxygenase gene: three distinct ring cleavage dioxygenases are involved in syringate degradation by Sphingomonas paucimobilis SYK-6. J Bacteriol 187:5067–5074PubMedPubMedCentralCrossRefGoogle Scholar
  52. Kim SH, Miyatake H, Hisano T, Iwasaki W, Ebihara AKM (2007) Crystallization and preliminary X-ray analysis of the oxygenase component (HpaB) of 4-hydroxyphenylacetate 3-monooxygenase from Thermus thermophilus HB8. Acta Crystallogr Sect F Struct Biol Cryst Commun 63:556–559PubMedPubMedCentralCrossRefGoogle Scholar
  53. Kurnasov O, Jablonski L, Polanuyer B, Dorrestein P, Begley T, Osterman A (2003) Aerobic tryptophan degradation pathway in bacteria: novel kynurenine formamidase. FEMS Microbiol Lett 227:219–227PubMedCrossRefGoogle Scholar
  54. Laurie AD, Lloyd-Jones G (1999) Conserved and hybrid meta-cleavage operons from PAH-degrading Burkholderia RP007. Biochem Biophys Res Commun 262:308–314PubMedCrossRefGoogle Scholar
  55. Leahy JG, Batchelor PJ, Morcomb SM (2003) Evolution of the soluble diiron monooxygenases. FEMS Microbiol Rev 27:449–479CrossRefPubMedPubMedCentralGoogle Scholar
  56. Lee SH, Ka JO, Cho JC (2008) Members of the phylum Acidobacteria are dominant and metabolically active in rhizosphere soil. FEMS Microbiol Lett 285:263–269PubMedCrossRefGoogle Scholar
  57. 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 61:549–555PubMedPubMedCentralGoogle Scholar
  58. Martin VJJ, Mohn WW (1999) A novel aromatic-ring-hydroxylating dioxygenase from the diterpenoid-degrading bacterium Pseudomonas abietaniphila BKME-9. J Bacteriol 181:2675–2682PubMedPubMedCentralGoogle Scholar
  59. Martin VJ, Mohn WW (2000) Genetic investigation of the catabolic pathway for degradation of abietane diterpenoids by Pseudomonas abietaniphila BKME-9. J Bacteriol 182:3784–3793PubMedPubMedCentralCrossRefGoogle Scholar
  60. 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
  61. Miyauchi K, Adachi Y, Nagata Y, Takagi M (1999) Cloning and sequencing of a novel meta-cleavage dioxygenase gene whose product is involved in degradation of gamma-hexachlorocyclohexane in Sphingomonas paucimobilis. J Bacteriol 181:6712–6719PubMedPubMedCentralGoogle Scholar
  62. Miyazawa D, Mukerjee-Dhar G, Shimura M, Hatta T, Kimbara K (2004) Genes for Mn(II)-dependent NahC and Fe(II)-dependent NahH located in close proximity in the thermophilic naphthalene and PCB degrader, Bacillus sp. JF8: cloning and characterization. Microbiology 150:993–1004PubMedCrossRefGoogle Scholar
  63. Moonen MJ, Synowsky SA, van den Berg WA, Westphal AH, Heck AJ, van den Heuvel RH, Fraaije MW, van Berkel WJ (2008) Hydroquinone dioxygenase from Pseudomonas fluorescens ACB: a novel member of the family of nonheme-iron(II)-dependent dioxygenases. J Bacteriol 190:5199–5209PubMedPubMedCentralCrossRefGoogle Scholar
  64. Moran MA, Buchan A, González JM, Heidelberg JF, Whitman WB, Kiene RP, Henriksen JR, King GM, Belas R, Fuqua C, Brinkac L, Lewis M, Johri S, Weaver B, Pai G, Eisen JA, Rahe E, Sheldon WM, Ye W, Miller TR, Carlton J, Rasko DA, Paulsen IT, Ren Q, Daugherty SC, Deboy RT, Dodson RJ, Durkin AS, Madupu R, Nelson WC, Sullivan SA, Rosovitz MJ, Haft DH, Selengut J, Ward N (2004) Genome sequence of Silicibacter pomeroyi reveals adaptations to the marine environment. Nature 432:910–913PubMedCrossRefPubMedCentralGoogle Scholar
  65. Muraki T, Taki M, Hasegawa Y, Iwaki H, Lau PCK (2003) Prokaryotic homologs of the eukaryotic 3-hydroxyanthranilate 3,4-dioxygenase and 2-amino-3-carboxymuconate-6-semialdehyde decarboxylase in the 2-nitrobenzoate degradation pathway of Pseudomonas fluorescens strain KU-7. Appl Environ Microbiol 69:1564–1572PubMedPubMedCentralCrossRefGoogle Scholar
  66. Nakano H, Wieser M, Hurh B, Kawai T, Yoshida T, Yamane T, Nagasawa T (1999) Purification, characterization and gene cloning of 6-hydroxynicotinate 3-monooxygenase from Pseudomonas fluorescens TN5. Eur J Biochem 260:120–126PubMedCrossRefGoogle Scholar
  67. Nogales J, Canales A, Jimenez-Barbero J, Garcia JL, Diaz E (2005) Molecular characterization of the gallate dioxygenase from Pseudomonas putida KT2440. The prototype of a new subgroup of extradiol dioxygenases. J Biol Chem 280:35382–35390PubMedCrossRefGoogle Scholar
  68. Nogales J, Palsson B, Thiele I (2008) A genome-scale metabolic reconstruction of Pseudomonas putida KT2440: iJN746 as a cell factory. BMC Syst Biol 2:79PubMedPubMedCentralCrossRefGoogle Scholar
  69. Nomura Y, Nakagawa M, Ogawa N, Harashima S, Oshima Y (1992) Genes in PHT plasmid encoding the initial degradation pathway of phthalate in Pseudomonas putida. J Ferm Bioeng 74:333–344CrossRefGoogle Scholar
  70. Nordin K, Unell M, Jansson JK (2005) Novel 4-chlorophenol degradation gene cluster and degradation route via hydroxyquinol in Arthrobacter chlorophenolicus A6. Appl Environ Microbiol 71:6538–6544PubMedPubMedCentralGoogle Scholar
  71. Nurk A, Kasak L, Kivisaar M (1991) Sequence of the gene (pheA) encoding phenol monooxygenae from Pseudomonas sp. EST1001: expression in Escherichia coli and Pseudomonas putida. Gene 102:13–18PubMedPubMedCentralGoogle Scholar
  72. Park HS, Kim HS (2000) Identification and characterization of the nitrobenzene catabolic plasmids pNB1 and pNB2 in Pseudomonas putida HS12. J Bacteriol 182:573–580PubMedPubMedCentralCrossRefGoogle Scholar
  73. Peng X, Misawa N, Harayama S (2003) Isolation and characterization of thermophilic Bacilli degrading cinnamic, 4-coumaric, and ferulic acids. Appl Environ Microbiol 69:1417–1427PubMedPubMedCentralCrossRefGoogle Scholar
  74. 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 185:1534–1542PubMedPubMedCentralCrossRefGoogle Scholar
  75. Pérez-Pantoja D, De la Iglesia R, Pieper DH, Gonzalez B (2008) Metabolic reconstruction of aromatic compounds degradation from the genome of the amazing pollutant-degrading bacterium Cupriavidus necator JMP134. FEMS Microbiol Rev 32:736–794PubMedCrossRefGoogle Scholar
  76. Pinyakong O, Habe H, Yoshida T, Nojiri H, Omori T (2003) Identification of three novel salicylate 1-hydroxylases involved in the phenanthrene degradation of Sphingobium sp. strain P2. Biochem Biophys Res Commun 301:350–357PubMedCrossRefGoogle Scholar
  77. Rabus R (2005) Functional genomics of an anaerobic aromatic-degrading denitrifying bacterium, strain EbN1. Appl Microbiol Biotechnol 68:580–587PubMedCrossRefGoogle Scholar
  78. Rascher A, Hu Z, Buchanan GO, Reid R, Hutchinson CR (2005) Insights into the biosynthesis of the benzoquinone ansamycins geldanamycin and herbimycin, obtained by gene sequencing and disruption. Appl Environ Microbiol 71:4862–4871PubMedPubMedCentralCrossRefGoogle Scholar
  79. Roper DI, Cooper RA (1990) Subcloning and nucleotide sequence of the 3,4-dihydroxyphenylacetate (homoprotocatechuate) 2,3-dioxygenase gene from Escherichia coli C. FEBS Lett 275:53–57PubMedCrossRefGoogle Scholar
  80. 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 93:421–427PubMedCrossRefGoogle Scholar
  81. Sakai M, Ezaki S, Suzuki N, Kurane R (2005) Isolation and characterization of a novel polychlorinated biphenyl-degrading bacterium, Paenibacillus sp. KBC101. Appl Microbiol Biotechnol 68:111–116PubMedCrossRefGoogle Scholar
  82. Sanchez MA, Gonzalez B (2007) Genetic characterization of 2,4,6-trichlorophenol degradation in Cupriavidus necator JMP134. Appl Environ Microbiol 73:2769–2776PubMedPubMedCentralCrossRefGoogle Scholar
  83. Sanchez-Perez G, Mira A, Nyiro G, Pasić L, Rodriguez-Valera F (2008) Adapting to environmental changes using specialized paralogs. Trends Genet 24:154–158PubMedCrossRefGoogle Scholar
  84. Sasoh M, Masai E, Ishibashi S, Hara H, Kamimura N, Miyauchi K, Fukuda M (2006) Characterization of the terephthalate degradation genes of Comamonas sp. strain E6. Appl Environ Microbiol 72:1825–1832PubMedPubMedCentralCrossRefGoogle Scholar
  85. Sato S, Ouchiyama N, Kimura T, Nojiri H, Yamane H, Omori T (1997a) Cloning of genes involved in carbazole degradation of Pseudomonas sp. strain CA10: nucleotide sequences of genes and characterization of meta-cleavage enzymes and hydrolase. J Bacteriol 179:4841–4849PubMedPubMedCentralCrossRefGoogle Scholar
  86. Sato SI, Nam JW, Kasuga K, Nojiri H, Yamane H, Omori T (1997b) Identification and characterization of genes encoding carbazole 1,9a-dioxygenase in Pseudomonas sp. strain CA10. J Bacteriol 179:4850–4858PubMedPubMedCentralCrossRefGoogle Scholar
  87. 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 3:81–91PubMedCrossRefGoogle Scholar
  88. Seto M, Masai E, Ida M, Hatta T, Kimbara K, Fukuda M, Yano K (1995) Multiple polychlorinated biphenyl transformation systems in the gram-positive bacterium Rhodococcus sp. strain RHA1. Appl Environ Microbiol 61:4510–4513PubMedPubMedCentralGoogle Scholar
  89. Shashirekha S, Uma L, Subramanian G (1997) Phenol degradation by the marine cyanobacterium Phormidium valderianum BDU 30501. J Ind Microbiol Biotechnol 19:130–133CrossRefGoogle Scholar
  90. Shimura M, MukerjeeDhar G, Kimbara K, Nagato H, Kiyohara H, Hatta T (1999) Isolation and characterization of a thermophilic Bacillus sp. JF8 capable of degrading polychlorinated biphenyls and naphthalene. FEMS Microbiol Lett 178:87–93PubMedCrossRefGoogle Scholar
  91. Smith DJ, Park J, Tiedje JM, Mohn WW (2007) A large gene cluster in Burkholderia xenovorans encoding abietane diterpenoid catabolism. J Bacteriol 189:6195–6204PubMedPubMedCentralCrossRefGoogle Scholar
  92. Stingley RL, Khan AA, Cerniglia CE (2004a) Molecular characterization of a phenanthrene degradation pathway in Mycobacterium vanbaalenii PYR-1. Biochem Biophys Res Commun 322:133–146PubMedCrossRefGoogle Scholar
  93. Stingley RL, Brezna B, Khan AA, Cerniglia CE (2004b) Novel organization of genes in a phthalate degradation operon of Mycobacterium vanbaalenii PYR-1. Microbiology 150:3749–3761PubMedCrossRefGoogle Scholar
  94. Sugimoto K, Senda T, Aoshima H, Masai E, Fukuda M, Mitsui Y (1999) Crystal structure of an aromatic ring opening dioxygenase LigAB, a protocatechuate 4,5-dioxygenase, under aerobic conditions. Structure 7:953–965CrossRefGoogle Scholar
  95. Suske WA, Held M, Schmid A, Fleischmann T, Wubbolts MG, Kohler HPE (1997) Purification and characterization of 2-hydroxybiphenyl 3-monooxygenase, a novel NADH-dependent, FAD-containing aromatic hydroxylase from Pseudomonas azelaica HBP1. J Biol Chem 272:24257–24265CrossRefGoogle Scholar
  96. Tago K, Sato J, Takesa H, Kawagishi H, Hayatsu M (2005) Characterization of methylhydroquinone-metabolizing oxygenase genes encoded on plasmid in Burkholderia sp. NF100. J Biosci Bioeng 100:517–523CrossRefGoogle Scholar
  97. 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
  98. Takenaka S, Murakami S, Shinke R, Hatakeyama K, Yukawa H, Aoki K (1997) Novel genes encoding 2-aminophenol 1,6-dioxygenase from Pseudomonas species AP-3 growing on 2-aminophenol and catalytic properties of the purified enzyme. J Biol Chem 272:14727–14732CrossRefGoogle Scholar
  99. Takeo M, Yasukawa T, Abe Y, Niihara S, Maeda Y, Negoro S (2003) Cloning and characterization of a 4-nitrophenol hydroxylase gene cluster from Rhodococcus sp. PN1. J Biosci Bioeng 95:139–145PubMedCrossRefGoogle Scholar
  100. Tamura K, Dudley J, Nei M, Kumar S (2007) MEGA4: molecular evolutionary genetic analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599CrossRefPubMedGoogle Scholar
  101. Tao Y, Fishman A, Bentley WE, Wood TK (2004) Altering toluene 4-monooxygenase by active-site engineering for the synthesis of 3-methoxycatechol, methoxyhydroquinone, and methylhydroquinone. J Bacteriol 186:4705–4713PubMedPubMedCentralCrossRefGoogle Scholar
  102. Thotsaporn K, Sucharitakul J, Wongratana J, Suadee C, Chaiyen P (2004) Cloning and expression of p-hydroxyphenylacetate 3-hydroxylase from Acinetobacter baumannii: evidence of the divergence of enzymes in the class of two-protein component aromatic hydroxylases. Biochim Biophys Acta 1680:60–66PubMedCrossRefGoogle Scholar
  103. van Berkel WJ, Kamerbeek NM, Fraaije MW (2006) Flavoprotein monooxygenases, a diverse class of oxidative biocatalysts. J Biotechnol 124:670–689CrossRefPubMedPubMedCentralGoogle Scholar
  104. van der Geize R, Dijkhuizen L (2004) Harnessing the catabolic diversity of rhodococci for environmental and biotechnological applications. Curr Opin Microbiol 7:255–261PubMedCrossRefGoogle Scholar
  105. Vetting MW, Wackett LP, Que L, Lipscomb JD, Ohlendorf DH (2004) Crystallographic comparison of manganese- and iron-dependent homoprotocatechuate 2,3-dioxygenases. J Bacteriol 186:1945–1958PubMedPubMedCentralCrossRefGoogle Scholar
  106. Wang YZ, Zhou Y, Zylstra GJ (1995) Molecular analysis of isophthalate and terephthalate degradation by Comamonas testosteroni YZW-D. Environ Health Perspect 103:9–12PubMedPubMedCentralGoogle Scholar
  107. Williams PA, Murray K (1974) Metabolism of benzoate and the methylbenzoates by Pseudomonas putida (arvilla) mt-2: evidence for the existence of a TOL plasmid. J Bacteriol 120:416–423PubMedPubMedCentralGoogle Scholar
  108. 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
  109. Xu L, Resing K, Lawson SL, Babbitt PC, Copley SD (1999) Evidence that pcpA encodes 2,6-dichlorohydroquinone dioxygenase, the ring cleavage enzyme required for pentachlorophenol degradation in Sphingomonas chlorophenolica strain ATCC 39723. Biochemistry 38:7659–7669PubMedCrossRefPubMedCentralGoogle Scholar
  110. Yen KM, Gunsalus IC (1982) Plasmid gene organization: naphthalene/salicylate oxidation. Proc Natl Acad Sci USA 79:874–878PubMedCrossRefGoogle Scholar
  111. Yoshida M, Oikawa T, Obata H, Abe K, Mihara H, Esaki N (2007) Biochemical and genetic analysis of the gamma-resorcylate (2,6-dihydroxybenzoate) catabolic pathway in Rhizobium sp. strain MTP-10005: identification and functional analysis of its gene cluster. J Bacteriol 189:1573–1581PubMedCrossRefGoogle Scholar
  112. Zaar A, Gescher J, Eisenreich W, Bacher A, Fuchs G (2004) New enzymes involved in aerobic benzoate metabolism in Azoarcus evansii. Mol Microbiol 54:223–238PubMedCrossRefGoogle Scholar
  113. Zylstra GJ, McCombie WR, Gibson DT, Finette BA (1988) Toluene degradation by Pseudomonas putida F1: genetic organization of the tod operon. Appl Environ Microbiol 54:1498–1503PubMedPubMedCentralGoogle Scholar

Copyright information

© Springer Nature Switzerland AG 2019

Authors and Affiliations

  • D. Pérez-Pantoja
    • 1
  • R. Donoso
    • 2
  • H. Junca
    • 3
  • B. González
    • 2
  • Dietmar H. Pieper
    • 4
    Email author
  1. 1.Departamento de Bioquímica y Biología Molecular, Facultad de Ciencias BiológicasUniversidad de ConcepciónConcepciónChile
  2. 2.Facultad de Ingeniería y CienciasUniversidad Adolfo IbáñezSantiagoChile
  3. 3.Research Group Microbial Ecology: Metabolism, Genomics and EvolutionMicrobiomas FoundationChiaColombia
  4. 4.Microbial Interactions and Processes Research GroupHZI – Helmholtz Centre for Infection ResearchBraunschweigGermany

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