Antonie van Leeuwenhoek

, Volume 71, Issue 1–2, pp 159–178 | Cite as

Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds

  • Jan Roelof van der Meer


Chlorobenzenes are substrates not easily metabolized by existing bacteria in the environment. Specific strains, however, have been isolated from polluted environments or in laboratory selection procedures that use chlorobenzenes as their sole carbon and energy source. Genetic analysis indicated that these bacteria have acquired a novel combination of previously existing genes. One of these gene clusters contains the genes for an aromatic ring dioxy-genase and a dihydrodiol dehydrogenase. The other contains the genes for a chlorocatechol oxidative pathway. Comparison of such gene clusters with those from other aromatics degrading bacteria reveals that this process of recombining or assembly of existing genetic material must have occurred in many of them. Similarities of gene functions between pathways suggest that incorporation of existing genetic material has been the most important mechanism of expanding a metabolic pathway. Only in a few cases a horizontal expansion, that is acqui sition of gene functions to accomodate a wider range of substrates which are then all transformed in one central pathway, is observed on the genetic level. Evidence is presented indicating that the assembly process may trigger a faster divergence of nearby gene sequences. Further ‘fine-tuning’, for example by developing a proper regulation, is then the next step in the adaptation.

aromatic pathways chlorobenzenes evolution genes plasmids pseudomonas 


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  1. Aldrich TL, Frantz B, Gill JF, Kilbane JJ & Chakrabarty AM (1987) Cloning and complete nucleotide sequence determination of the catB gene encoding cis, cis-muconate lactonizing enzyme. Gene 52: 185–195Google Scholar
  2. Amabile-Cuevas CF & Chicurel ME (1992) Bacterial plasmids and gene flux. Cell 70: 189–199Google Scholar
  3. Assinder SJ, Demarco P, Osborne DJ, Poh CL, Shaw LE, Winson MK & Williams PA (1993) A comparison of the multiple alleles of xylS carried by TOL plasmids pWW53 and pDK1 and its implications for their evolutionary relationship. J. Gen. Microbiol. 139: 557–568Google Scholar
  4. Asturias JA, Diaz E & Timmis KN (1995) The evolutionary relationship of biphenyl dioxygenase from gram-positive Rhodococcus globerulus P6 to multicomponent dioxygenases from gram-negative bacteria. Gene 156: 11–18Google Scholar
  5. 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: 4631–4640Google Scholar
  6. Brenner V, Arensdorf JJ & Focht DD (1994) Genetic construction of PCB degraders. Biodegradation 5: 359–378Google Scholar
  7. Cairns J, Overbaugh J & Miller S (1988) The origin of mutants. Nature (London) 335: 142–145Google Scholar
  8. Carrington B, Lowe A, Shaw LE & Williams PA (1994) The lower pathway operon for benzoate catabolism in biphenyl-utilizing Pseudomonas sp. strain IC and the nucleotide sequence of the bphE gene for catechol 2,3-dioxygenase. Microbiology UK 140: 499–508Google Scholar
  9. Cerdan P, Rekik M & Harayama S (1995) Substrate specificity differences between two catechol 2,3-dioxygenases encoded by the TOL and NAH plasmids from Pseudomonas putida. Eur. J. Biochem. 229: 113–118Google Scholar
  10. Clarke PH (1984) The evolution of degradative pathways. In: Gibson DT (Ed) Microbial degradation of organic compounds (pp 11–27). Marcel Dekker, Inc., New YorkGoogle Scholar
  11. Coco WM, Rothmel RK, Henikoff S & Chakrabarty AM (1993) Nucleotide sequence and initial functional characterization of the clcR gene encoding a LysR family activator of the clcABD chlorocatechol operon in Pseudomonas putida. J. Bacteriol. 175: 417–427Google Scholar
  12. Dagley S (1986) Biochemistry of aromatic hydrocarbon degradation in pseudomonads. In: Sokatch JR (Ed) The Bacteria, Vol 10 (pp 527–555). Academic Press, Inc., New YorkGoogle Scholar
  13. Danganan CE, Ye RW, Daubaras DL, Xun L & Chakrabarty AM (1994) Nucleotide sequence and functional analysis of the genes encoding 2,4,5-trichlorophenoxyacetic acid oxygenase in Pseudomonas cepacia AC1100. Appl. Environ. Microbiol. 60: 4100–4106Google Scholar
  14. Daubaras DL, Hershberger CD, Kitano K & Chakrabarty AM (1995) Sequence analysis of a gene cluster involved in metabolism of 2,4,5-trichlorophenoxyacetic acid by Burkholderia cepacia AC1100. Appl. Environ. Microbiol. 61: 1279–1289Google Scholar
  15. De Jong E, Field JA, Spinnler H-E, Wijnberg JBPA & de Bont JAM (1994) Significant biogenesis of chlorinated aromatics by fungi in natural environments. Appl. Environ. Microbiol. 60: 264–270Google Scholar
  16. Dehmel U, Engesser KH, Timmis KN & Dwyer DF (1995) Cloning, nucleotide sequence, and expression of the gene encoding a novel dioxygenase involved in metabolism of carboxydiphenyl ethers in Pseudomonas pseudoalcaligenes POB310. Arch. Microbiol. 163: 35–41Google Scholar
  17. Denome SA, Stanley DC, Olson ES & Young KD (1993) Metabolism of dibenzothiophene and naphthalene in Pseudomonas strains: complete DNA sequence of an upper naphthalene catabolic pathway. J. Bacteriol. 175: 6890–6901Google Scholar
  18. Devereux J, Haeberli P & Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12: 387–395Google Scholar
  19. DiMarco AA, Averhoff B & Ornston LN (1993a) Identification of the transcriptional activator pobR and characterization of its role in the expression of pobA, the structural gene for p-hydroxybenzoate hydroxylase in Acinetobacter calcoaceticus. J. Bacteriol. 175: 4499–4506Google Scholar
  20. DiMarco AA, Averhoff BA, Kim EE & Ornston LN (1993b) Evolutionary divergence of pobA, the structural gene encoding p-hydroxybenzoate hydroxylase in an Acinetobacter calcoaceticus strain well-suited for genetic analysis. Gene 125: 25–33Google Scholar
  21. Dimri GP, Rudd KE, Morgan MK, Bayat H & Ferro-Luzzi Ames G (1992) Physical mapping of repetitive extragenic palindromic sequences in Escherichia coli and phylogenetic distribution among Escherichia coli strains and other enteric bacteria. J. Bacteriol. 174: 4583–4593Google Scholar
  22. Drake JW (1991) Spontaneous mutation. Annu. Rev. Genet. 25: 124–146Google Scholar
  23. Eaton RW (1994) Organization and evolution of naphthalene catabolic pathways: sequence of the DNA encoding 2-hydroxychromene-2-carboxylate isomerase and trans-o-hydroxybenzylidenepyruvate hydratase-aldolase from the NAH7 plasmid. J. Bacteriol. 176: 7757–7762Google Scholar
  24. Eaton RW & Chapman PJ (1992) Bacterial metabolism of naphthalene — construction and use of recombinant bacteria to study ring cleavage of 1,2-dihydroxynaphthalene and subsequent reactions. J. Bacteriol. 174: 7542–7554Google Scholar
  25. Eaton RW & Timmis KN (1986) Spontaneous deletion of a 20-kilo-base DNA segment carrying genes specifying isopropylbenzene metabolism in Pseudomonas putida RE204. J. Bacteriol. 168: 428–430Google Scholar
  26. Echols H & Goodman MF (1991) Fidelity mechanisms in DNA replication. Annu. Rev. Biochem. 60: 477–511Google Scholar
  27. Ehrt S, Schirmer F & Hillen W (1995) Expression of phenol hydroxylase and catechol 1,2-dioxygenase is differentially regulated in Acinetobacter calcoaceticus. EMBL/GenBank Accession nr. Z36909Google Scholar
  28. Elsemore DA & Ornston LN (1995) Unusual ancestry of dehydratases associated with quinate catabolism in Acinetobacter calcoaceticus. J. Bacteriol. 177: 5971–5978Google Scholar
  29. Erickson BD & Mondello FJ (1992) Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400. J. Bacteriol. 174: 2903–2912Google Scholar
  30. Fernandez S, Shingler V & de Lorenzo V (1994) Cross-regulation by XylR and DmpR activators of Pseudomonas putida suggests that transcriptional control of biodegradative operons evolves independently of catabolic genes. J. Bacteriol. 176: 5052–5058Google Scholar
  31. Foster PL (1993) Adaptive mutation: the uses of adversity. Annu. Rev. Microbiol. 47: 467–504Google Scholar
  32. Frantz B & Chakrabarty AM (1986) Degradative plasmids in Pseudomonas. In: Sokatch JR (Ed) The biology of Pseudomonas, Vol 10 (pp 295–323). Academic Press, Inc., New YorkGoogle Scholar
  33. Frantz B & Chakrabarty AM (1987) Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. Proc. Natl. Acad. Sci. USA 84: 4460–4464Google Scholar
  34. Frazee RW, Livingston DM, LaPorte DC & Lipscomb JD (1993) Cloning, sequencing, and expression of the Pseudomonas putida protocatechuate 3,4-dioxygenase genes. J. Bacteriol. 175:6194–6202Google Scholar
  35. Fukuda M, Yasukochi Y, Kikuchi Y, Nagata Y, Kimbara K, Horiuchi H, Takagi M & Yano K (1994) Identification of the bphA and bphB genes of Pseudomonas sp. strain KKS102 involved in the degradation of biphenyl and polychlorinated biphenyls. Biochem. Biophys. Res. Comm. 202: 850–856Google Scholar
  36. Furukawa K (1994) Molecular genetics and evolutionary relationship of PCB-degrading bacteria. Biodegradation 5: 289–300Google Scholar
  37. Furukawa K, Arimura N & Miyazaki T (1987) Nucleotide sequence of the 2,3-dihydroxybiphenyl dioxygenase gene of Pseudomonas pseudoalcaligenes. J. Bacteriol. 169: 427–429Google Scholar
  38. Galas DJ & Chandler M (1989) Bacterial insertion sequences. In: Berg DE & Howe MM (Ed) Mobile DNA (pp 109–163). American Society for Microbiology, Washington, D. C.Google Scholar
  39. Gerischer U & Ornston LN (1995) Spontaneous mutations in pcaH and-G, structural genes for protocatechuate 3,4-dioxygenase in Acinetobacter calcoaceticus. J. Bacteriol. 177: 1336–1347Google Scholar
  40. Gibson DT, Zylstra GJ & Chauhan S (1990) Biotransformations catalyzed by toluene dioxygenase from Pseudomonas putida F1. In: Silver S, Chakrabarty AM, Iglewski B & Kaplan S (Ed) Pseudomonas: biotransformations, pathogenesis and evolving biotechnology (pp 121–133). American Society for Microbiology, WashingtonGoogle Scholar
  41. Gregg-Jolly LA & Ornston LN (1990) Recovery of DNA from the Acinetobacter calcoaceticus chromosome by gap repair. J. Bacteriol. 172: 6169–72Google Scholar
  42. Gregg-Jolly LA & Ornston LN (1994) Properties of Acinetobacter calcoaceticus recA and its contribution to intracellular gene conversion. Mol. Microbiol. 12: 985–992Google Scholar
  43. Gribble GW (1992) Naturally occurring organohalogen compounds — a survey. J. Nat. Prod. 55: 1353–1395Google Scholar
  44. Grindley NDF & Reed RR (1985) Transpositional recombination in prokaryotes. Annu. Rev. Biochem. 54: 863–896Google Scholar
  45. Haak B, Fetzner S & Lingens F (1995) Cloning, nucleotide sequence, and expression of the plasmid-encoded genes for the twocomponent 2-halobenzoate 1,2-dioxygenase from Pseudomonas cepacia 2CBS. J. Bacteriol. 177: 667–675Google Scholar
  46. Han S, Eltis LD, Timmis KN, Muchmore SW & Bolin JT (1995) Crystal structure of the biphenyl-cleaving extradiol dioxygenase from a PCB-degrading pseudomonad. Science 270: 976–980Google Scholar
  47. Harayama S (1994) Codon usage patterns suggest independent evolution of two catabolic operons on toluene-degradative plasmid TOL pWW0 of Pseudomonas putida. J. Mol. Evol. 38: 328–335Google Scholar
  48. Harayama S, Kok M & Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 46: 565–601Google Scholar
  49. Harayama S & Rekik M (1989) Bacterial aromatic ring-cleavage enzymes are classified into two different gene families. J. Biol. Chem. 264: 15328–15333Google Scholar
  50. Harayama S & Rekik M (1990) The meta cleavage operon of TOL degradative plasmid pWW0 comprises 13 genes. Mol. Gen. Genet. 221: 113–120Google Scholar
  51. Harayama S & Rekik M (1993) Comparison of the nucleotide sequences of the meta-cleavage pathway genes of TOL plasmid pWW0 from Pseudomonas putida with other meta-cleavage genes suggests that both single and multiple nucleotide substitutions contribute to enzyme evolution. Mol. Gen. Genet. 239: 81–89Google Scholar
  52. Harayama S, Rekik M, Bairoch A, Neidle EL & Ornston LN (1991) Potential DNA slippage structures acquired during evolutionary divergence of Acinetobacter calcoaceticus chromosomal ben ABC and Pseudomonas putida TOL pWW0 plasmid xylXYZ, genes encoding benzoate dioxygenases. J. Bacteriol. 173: 7540–7548Google Scholar
  53. Harayama S, Rekik M, Wasserfallen A & Bairoch A (1987) Evolutionary relationships between catabolic pathways for aromatics: conservation of gene order and nucleotide sequences of catechol oxidation genes of pWW0 and NAH7 plasmids. Mol. Gen. Genet. 210: 241–247Google Scholar
  54. Harris RS, Longerich S & Rosenberg SM (1994) Recombination in adaptive mutation. Science 264: 258–260Google Scholar
  55. Hartnett C, Neidle EL, Ngai K-L & Ornston LN (1990) DNA sequences of genes encoding Acinetobacter calcoaceticus protocatechuate 3,4-dioxygenase: evidence indicating shuffling of genes and of DNA sequences within genes during their evolutionary divergence. J. Bacteriol. 172: 956–966Google Scholar
  56. Hartnett GB & Ornston LN (1994) Acquisition of apparent DNA slippage structures during extensive evolutionary divergence of pcaD and catD genes encoding identical catalytic activities in Acinetobacter calcoaceticus. Gene 142: 23–29Google Scholar
  57. Herrmann H, Muller C, Schmidt I, Mahnke J, Petruschka L & Hahnke K (1995) Localization and organization of phenol degradation genes of Pseudomonas putida strain H. Mol. Gen. Genet. 247: 240–246Google Scholar
  58. Hirose J, Kimura N, Suyama A, Kobayashi A, Hayashida S & Furukawa K (1994) Functional and structural relationship of various extradiol aromatic ring-cleavage dioxygenases of Pseudomonas origin. FEMS Microbiol. Lett. 118: 273–277Google Scholar
  59. Hoeijmakers J (1993) Nucleotide excision repair. 1. From E. coli to yeast. Trends Genet. 9: 173–177Google Scholar
  60. Hofer B, Eltis LD, Dowling DN & Timmis KN (1993) Genetic analysis of a Pseudomonas locus encoding a pathway for biphenyl/polychlorinated biphenyl degradation. Gene 130: 47–55Google Scholar
  61. Horn JM, Harayama S & Timmis KN (1991) DNA sequence determination of the TOL plasmid (pWWO) xylGFJ genes of Pseudomonas putida: implications for the evolution of aromatic catabolism. Mol. Microbiol. 5: 2459–2474Google Scholar
  62. Houghton JE, Brown TM, Appel AJ, Hughes EJ & Ornston LN (1995) Discontinuities in the evolution of Pseudomonas putida cat genes. J. Bacteriol. 177: 401–412Google Scholar
  63. Inouye S, Asai Y, Nakazawa A & Nakazawa T (1986) Nucleotide sequence of a DNA segment promoting transcription in Pseudomonas putida. J. Bacteriol. 166: 739–745Google Scholar
  64. Inouye S, Nakazawa A & Nakazawa T (1983) Molecular cloning of regulatory gene xyIR and operator-promoter regions of the xylABC and xylDEGF operons of the TOL plasmid. J. Bacteriol. 155: 1192–1199Google Scholar
  65. Irie S, Doi S, Yorifuji T, Takagi M & Yano K (1987) Nucleotide sequencing and characterization of the genes encoding benzene oxidation enzymes of Pseudomonas putida. J. Bacteriol. 169: 5174–5179Google Scholar
  66. Janssen DB, van der Ploeg JR & Pries F (1994) Genetics and biochemistry of 1,2-dichloroethane degradation. Biodegradation 5: 249–257Google Scholar
  67. Ka JO, Holben WE & Tiedje JM (1994a) Genetic and phenotypic diversity of 2,4-dichlorophenoxyacetic acid (2,4-D)-degrading bacteria isolated from 2,4-D-treated field soils. Appl. Environ. Microbiol. 60: 1106–1115Google Scholar
  68. Ka JO, Holben WE & Tiedje JM (1994b) Use of gene probes to aid in recovery and identification of functionally dominant 2,4-dichlorophenoxyacetic acid-degrading populations in soil. Appl. Environ. Microbiol. 60: 1116–1120Google Scholar
  69. Kasak L, Horak R, Nurk A, Talvik K & Kivisaar M (1993) Regulation of the catechol 1,2-dioxygenase-and phenol monooxygenaseencoding pheBA operon in Pseudomonas putida PaW85. J. Bacteriol. 175: 8038–42Google Scholar
  70. Kasberg T, Daubaras DL, Chakrabarty AM, Kinzelt D & Reineke W (1995) Evidence that operons tcb, tfd, and clc encode maleylacetate reductase, the fourth enzyme of the modified ortho pathway. J. Bacteriol. 177: 3885–3889Google Scholar
  71. Kaschabek SR & Reineke W (1995) Maleylacetate reductase of Pseudomonas sp. strain B13: specificity of substrate conversion and halide elimination. J. Bacteriol. 1774: 320–325Google Scholar
  72. Kikuchi Y, Nagata Y, Hinata M, Kimbara K, Fukuda M, Yano K & Takagi M (1994a) Identification of the bphA4 gene encoding ferredoxin reductase involved in biphenyl and polychlorinated biphenyl degradation in Pseudomonas sp. strain KKS102. J. Bacteriol. 176: 1689–1694Google Scholar
  73. Kikuchi Y, Yasukochi Y, Nagata Y, Fukuda M & Takagi M (1994b) 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: 4269–4276Google Scholar
  74. Kim E & Zylstra GJ (1995) Molecular and biochemical characterization of two meta-cleavage dioxygenases involved in biphenyl and m-xylene degradation by Beijerinckia sp. strain B1. J. Bacteriol. 177: 3095–3103Google Scholar
  75. Kimbara K, Hashimoto T, Fukuda M, Koana T, Takagi M, Oishi M & Yano K (1989) Cloning and sequencing of two tandem genes involved in degradation of 2,3-dihydroxybiphenyl to benzoic acid the polychlorinated biphenyl-degrading soil bacterium Pseudomonas sp. strain KKS102. J. Bacteriol. 171: 2740–2747Google Scholar
  76. Kivisaar M, Kasak L & Nurk A (1991) Sequence of the plasmidencoded catechol 1,2-dioxygenase-expressing gene, pheB, of phenol-degrading Pseudomonas sp. strain EST1001. Gene 98: 15–20Google Scholar
  77. Kivisaar MA, Habicht JK & Heinaru AL (1989) Degradation of phenol and m-toluate in Pseudomonas sp. strain EST1001 and its Pseudomonas putida transconjugants is determined by a multiplasmid system. J. Bacteriol. 171: 5111–5116Google Scholar
  78. Kowalchuk GA, Gregg JL & Ornston LN (1995) Nucleotide sequences transferred by gene conversion in the bacterium Acinetobacter calcoaceticus. Gene 153: 111–115Google Scholar
  79. Kröckel L & Focht DD (1987) Construction of chlorobenzene-utilizing recombinants by progenitive manifestation of a rare event. Appl. Environ. Microbiol. 53: 2470–2475Google Scholar
  80. Kukor JJ & Olsen RH (1991) Genetic organization and regulation of a meta-cleavage pathway for catechols produced from catabolism of toluene, benzene, phenol and cresols by Pseudomonas pickettii PKO1. J. Bacteriol. 173: 4587–4594Google Scholar
  81. Kukor JJ & Olsen RH (1992) Complete nucleotide sequence of tbuD, the gene encoding phenol/ cresol hydroxylase from Pseudomonas pickettii PKO1, and functional analysis of the encoded enzyme. J. Bacteriol. 174: 6518–6526Google Scholar
  82. Kukor JJ, Olsen RH & Siak J-S (1989) Recruitment of a chromosomally encoded maleylacetate reductase for degradation of 2,4-dichlorophenoxyacetic acid by plasmid pJP4. J. Bacteriol. 171: 3385–3390Google Scholar
  83. Kurkela S, Lehväslaiho H, Palva ET & Teeri TH (1988) Cloning, nucleotide sequence and characterization of genes encoding naphthalene dioxygenase of Pseudomonas putida strain NCIB9816. Gene 73: 355–362Google Scholar
  84. Lau PCK, Bergeron H, Labbe D, Wang Y, Brousseau R & Gibson DT (1994) Sequence and expression of the todGIH genes involved in the last three steps of toluene degradation by Pseudomonas putida F1. Gene 146: 7–13Google Scholar
  85. Levine JG, Schaaper RM & DeMarini DM (1994) Complex frameshift mutations mediated by plasmid pKM101: mutational mechanisms deduced from 4-aminobiphenyl-induced mutation spectra in Salmonella. Genetics 136: 731–46Google Scholar
  86. Louws FJ, Fulbright DW, Stephens CT & de Bruijn FJ (1994) Specific genomic fingerprints of phytopathogenic Xanthomonas and Pseudomonas pathovars and strains generated with repetitive sequences and PCR. Appl. Environ. Microbiol. 60: 2286–2295Google Scholar
  87. Marques S & Ramos JL (1993) Transcriptional control of the Pseudomonas putida TOL plasmid catabolic pathways. Mol. Microbiol. 9: 923–929Google Scholar
  88. Masai E, Yamada A, Healy JM, Hatta T, Kimbara K, Fukuda M & Yano K (1995) Characterization of biphenyl catabolic genes of gram-positive polychlorinated biphenyl degrader Rhodococcus sp. strain RHA1. Appl. Environ. Microbiol. 61: 2079–2085Google Scholar
  89. Mason JR & Cammack R (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu. Rev. Microbiol. 46: 277–305Google Scholar
  90. Matrubutham U & Harker AR (1994) Analysis of duplicated gene sequences associated with tfdR and tfdS in Alcaligenes eutrophus JMP134. J. Bacteriol. 176: 2348–2353Google Scholar
  91. Menn FM, Zylstra GJ & Gibson DT (1991) Location and sequence of the todF gene encoding 2-hydroxy-6-oxohepta-2,4-dienoate hydrolase. Gene 104: 91–94Google Scholar
  92. Mermod N, Ramos JL, Bairoch A & Timmis KN (1987) The xylS gene positive regulator of TOL plasmid pWW0: identification, sequence analysis and overproduction leading to constitutive expression of meta cleavage operon. Mol. Gen. Genet. 207: 349–354Google Scholar
  93. Modrich P (1991) Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25: 229–253Google Scholar
  94. Mokross H, Schmidt E & Reineke W (1990) Degradation of 3-chlorobiphenyl by in vivo constructed hybrid peudomonads. FEMS Microbiol. Lett. 71: 179–186Google Scholar
  95. Nakai C, Kagamiyama H & Nozaki M (1983) Complete nucleotide sequence of the metapyrocatechase gene on the TOL plasmid of Pseudomonas putida mt-2. J. Biol. Chem. 258: 2923–2938Google Scholar
  96. Nakatsu C, Ng J, Singh R, Straus N & Wyndham C (1991) Chlorobenzoate catabolic transposon Tn5271 is a composite class I element with flanking class II insertion sequences. Proc. Natl. Acad. Sci. USA 88: 8312–8316Google Scholar
  97. Nakatsu CH, Straus NA & Wyndham RC (1995) The nucleotide sequence of the Tn5271 3-chlorobenzoate 3,4-dioxygenase genes (cbaAB) unites the class IA oxygenases in a single lineage. Microbiology UK 141: 485–495Google Scholar
  98. Nakatsu CH & Wyndham RC (1993) Cloning and expression of the transposable chlorobenzoate 3,4-dioxygenase genes of Alcaligenes sp. strain BR60. Appl. Environ. Microbiol. 59: 3625–3633Google Scholar
  99. Nakazawa T, Inouye S & Nakazawa A (1990) Regulatory systems for expression of xyl genes on the TOL plasmid. In: Silver S, Chakrabarty AM, Iglewski B & Kaplan S (Ed) Pseudomonas: biotransformations, pathogenesis and evolving biotechnology (pp 133–141). American Society for Microbioloy, WashingtonGoogle Scholar
  100. Negoro S, Kato K, Fujiyama K & Okada H (1994) The nylon oligomer biodegradation system of Flavobacterium and Pseudomonas. Biodegradation 5: 185–194Google Scholar
  101. Neidle E, Hartnett C, Ornston LN, Bairoch A, Rekik M & Harayama S (1992) Cis-diol dehydrogenases encoded by the TOL pWW0 plasmid xylL gene and the Acinetobacter calcoaceticus chromosomal benD gene are members of the short-chain alcohol dehydrogenase superfamily. Eur. J. Biochem. 204: 113–120Google Scholar
  102. Neidle EL, Hartnett C, Bonitz S & Ornston LN (1988) DNA sequence of the Acinetobacter calcoaceticus catechol 1,2-dioxygenase I structural gene catA: evidence for evolutionary divergence of intradiol dioxygenases by acquisition of DNA sequence repetitions. J. Bacteriol. 170: 4874–4880Google Scholar
  103. Neidle EL, Hartnett C & Ornston LN (1989) Characterization of Acinetobacter calcoaceticus catM, a repressor gene homologous in sequence to transcriptional activator genes. J. Bacteriol. 171: 5410–5421Google Scholar
  104. Neidle EL, Hartnett C, Ornston LN, Bairoch A, Rekik M & Harayama S (1991) Nucleotide sequences of the Acinetobacter calcoaceticus benABC genes for benzoate 1,2-dioxygenase reveal evolutionary relationships among multicomponent oxygenases. J. Bacteriol. 173: 5385–5395Google Scholar
  105. Nishino SF, Spain JC, Belcher LA & Litchfield CD (1992) Chlorobenzene degradation by bacteria isolated from contaminated groundwater. Appl. Environ. Microbiol. 58: 1719–1726Google Scholar
  106. 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. Ferment. Bioeng. 74: 333–344Google Scholar
  107. Nordlund I, Powlowski J & Shingler V (1990) Complete nucleotide sequence and polypeptide analysis of multicomponent phenol hydroxylase from Pseudomonas sp. strain CF600. J. Bacteriol. 172: 6826–6833Google Scholar
  108. Nurk A, Kasak L & Kivisaar M (1991) Sequence of the gene (pheA) encoding phenol monooxygenase from Pseudomonas sp. EST1001: Expression in Escherichia coli and Pseudomonas putida. Gene 102: 13–18Google Scholar
  109. Oltmanns RH, Rast HG & Reineke W (1988) Degradation of 1,4-dichlorobenzene by constructed and enriched strains. Appl. Microbiol. Biotechnol. 28: 609–616Google Scholar
  110. Orser CS & Lange CC (1994) Molecular analysis of pentachlorophenol degradation. Biodegradation 5: 277–288Google Scholar
  111. Orser CS, Lange CC, Xun L, Zahrt TC & Schneider BJ (1993) Cloning, sequence analysis, and expression of the Flavobacterium pentachlorophenol-4-monooxygenase gene in Escherichia coli. J. Bacteriol. 175: 411–416Google Scholar
  112. Parke D (1995) Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens. J. Bacteriol. 177: 3808–3817Google Scholar
  113. Parsek MR, Kivisaar M & Chakrabarty AM (1995) Differential DNA bending introduced by the Pseudomonas putida LysR-type regulator. Mol. Microbiol. 15: 819–828Google Scholar
  114. Parsek MR, Shinabarger DL, Rothmel RK & Chakrabarty AM (1992) Roles of CatR and cis,cis-muconate in activation of the catBC operon, which is involved in benzoate degradation in Pseudomonas putida. J. Bacteriol. 174: 7798–7806Google Scholar
  115. Pearson DJ & Lipman WR (1988) Improved tools for biological sequence analysis. Proc. Natl. Acad. Sci. USA 85: 2444–2448Google Scholar
  116. Perez-Martin J & de Lorenzo V (1995a) Integration host factor (IHF) suppresses promiscuous activation of the σ 54-dependent promoter Pu of Pseudomonas putida. Proc. Natl. Acad. Sci. USA 92: 7277–7281Google Scholar
  117. Perez-Martin J & de Lorenzo V (1995b) The σ 54-dependent promoter Ps of the TOL plasmid of Pseudomonas putida requires HU for transcriptional activation in vivo by XylR. J. Bacteriol. 177: 3758–3763Google Scholar
  118. Perkins EJ, Gordon MP, Caceres O & Lurquin PF (1990) Organization and sequence analysis of the 2,4-dichlorophenol hydroxylase and dichlorocatechol oxidative operons of plasmid pJP4. J. Bacteriol. 172: 2351–2359Google Scholar
  119. Powlowski J & Shingler V (1994) Genetics and biochemistry of phenol degradation by Pseudomonas sp. CF600. Biodegradation 5: 219–236Google Scholar
  120. Pries F, van den Wijngaard AJ, Bos R, Pentenga M & Janssen DB (1994) The role of spontaneous cap domain mutations in haloalkane dehalogenase specificity and evolution. J. Biol. Chem. 269: 17490–17494Google Scholar
  121. Ramos JL, Stolz A, Reineke W & Timmis KN (1986) Altered effector specificities in regulators of gene expression: TOL plasmid xylS mutants and their use to engineer expansion of the range of aromatics degraded by bacteria. Proc. Natl. Acad. Sci. USA 83: 8467–8471Google Scholar
  122. Ramos JL & Timmis KN (1987) Experimental evolution of catabolic pathways of bacteria. Microbiol. Sci. 4: 228–237Google Scholar
  123. Ramos JL, Wasserfallen A, Rose K & Timmis KN (1987) Redesigning metabolic routes: manipulation of TOL plasmid pathway for catabolism of alkylbenzoates. Science 235: 593–596Google Scholar
  124. Reineke W & Knackmuss H-J (1984) Microbial metabolism of haloaromatics: isolation and properties of a chlorobenzenedegrading bacterium. Appl. Environ. Microbiol. 47: 395–402Google Scholar
  125. Rojo F, Pieper DH, Engesser K-H, Knackmuss H-J & Timmis KN (1987) Assemblage of ortho cleavage route for simultaneous degradation of chloro-and methylaromatics. Science 238: 1395–1398Google Scholar
  126. Romero-Arroyo CE, Schell MA, Gaines III GL & Neidle EL (1995) catM encodes a LysR-type transcriptional activator regulating catechol degradation in Acinetobacter calcoaceticus. J. Bacteriol. 177: 5891–5898Google Scholar
  127. Sander P, Wittich R-M, Fortnagel P, Wilkes H & Francke W (1991) Degradation of 1,2,4-trichloro-and 1,2,4,5-tetrachlorobenzene by Pseudomonas strains. Appl. Environ. Microbiol. 57: 1430–1440Google Scholar
  128. Sayler GS, Hooper SW, Layton AC & King JMH (1990) Catabolic plasmids of environmental and ecological significance. Microb. Ecol. 19: 1–20Google Scholar
  129. Schaaper RM, Danforth BN & Glickman BW (1986) Mechanisms of spontaneous mutagenesis: an analysis of the spectrum of spontaneous mutation in the Escherichia coli lacI gene. J. Mol. Biol. 189: 273–284Google Scholar
  130. Schaaper RM & Dunn RL (1987) Spectra of spontaneous mutations in Escherichia coli strains defective in mismatch correction: the nature of in vivo DNA replication errors. Proc. Natl. Acad. Sci. USA 84: 6220–6224Google Scholar
  131. Schell MA (1985) Transcriptional control of the nah and sal hydrocarbon-degradation operons by the nahR gene product. Gene 36: 301–309Google Scholar
  132. Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47: 597–626Google Scholar
  133. Schell MA & Sukordhaman M (1989) Evidence that the transcription activator encoded by the Pseudomonas putida nahR gene is evolutionarily related to the transcription activators encoded by the Rhizobium nodD genes. J. Bacteriol. 171: 1952–1959Google Scholar
  134. Schlömann M (1994) Evolution of chlorocatechol catabolic pathways. Conclusions to be drawn from comparisons of lactone hydrolases. Biodegradation 5: 301–321Google Scholar
  135. Schlömann M, Schmidt E & Knackmuss H-J (1990) Different types of dienelactone hydrolase in 4-fluorobenzoate-utilizing bacteria. J. Bacteriol. 172: 5112–5118Google Scholar
  136. Schraa G, Boone ML, Jetten MSM, van Neerven ARW, Colberg PJ & Zehnder AJB (1986) Degradation of 1,4-dichlorobenzene by Alcaligenes sp. strain A175. Appl. Environ. Microbiol. 52: 1374–1381Google Scholar
  137. Shanley MS, Harrison A, Parales RE, Kowalchuk G, Mitchell DJ & Ornston LN (1994) Unusual G+C content and codon usage in catIJF, a segment of the ben-cat supra-operonic cluster in the Acinetobacter calcoaceticus chromosome. Gene 138: 59–65Google Scholar
  138. Shingler V, Bartilson M & Moore T (1993) Cloning and nucleotide sequence of the gene encoding the positive regulator (dmpR) of the phenol catabolic pathway encoded by pVI150 and identification of DmpR as a member of the NtrC family of transcriptional activators. J. Bacteriol. 175: 1596–1604Google Scholar
  139. Shingler V, Powlowski J & Marklund U (1992) Nucleotide sequence and functional analysis of the complete phenol/3,4-dimethylphenol catabolic pathway of Pseudomonas sp. strain CF600. J. Bacteriol. 174: 711–724Google Scholar
  140. Simon MJ, Osslund TD, Saunders R, Ensley BD, Suggs S, Harcourt A, Suen W-C, Cruden DL, Gibson DT & Zylstra GJ (1993) Sequences of genes encoding naphthalene dioxygenase in Pseudomonas putida strains G7 and NCIB 9816-4. Gene 127: 31–37Google Scholar
  141. Spain JC & Nishino SF (1987) Degradation of 1,4-dichlorobenzene by a Pseudomonas sp. Appl. Environ. Microbiol. 53: 1010–1019Google Scholar
  142. Stern MJ, Ferro-Luzzi Ames G, Smith NH, Robinson EC & Higgins CF (1984) Repetitive extragenic palindromic sequences: a major component of the bacterial genome. Cell 37: 1015–1026Google Scholar
  143. Streber WR, Timmis KN & Zenk MH (1987) Analysis, cloning, and high-level expression of 2,4-dichlorophenoxyacetate monooxygenase gene tfdA of Alcaligenes eutrophus. J. Bacteriol. 169: 2950–2955Google Scholar
  144. Summers DK (1994) The origins and consequences of genetic instability in prokaryotes. Dev. Biol. Stand. 83: 7–11Google Scholar
  145. Suzuki M, Hayakawa T, Shaw JP, Rekik M & Harayama S (1991) Primary structures of xylene monooxygenase: similarities to and differences from the alkane hydroxylation system. J. Bacteriol. 173: 1690–1695Google Scholar
  146. Taira K, Hirose J, Hayashida S & Furukawa K (1992) Analysis of bph operon from the polychlorinated biphenyl-degrading strain of Pseudomonas pseudoalcaligenes KF707. J. Biol. Chem. 267: 4844–4853Google Scholar
  147. Takizawa N, Kaida N, Torigoe S, Moritani T, Sawada T, Satoh S & Kiyohara H (1994) Identification and characterization of genes encoding polycyclic aromatic hydrocarbon dioxygenase and polycyclic aromatic hydrocarbon dihydrodiol dehydrogenase in Pseudomonas putida OUS82. J. Bacteriol. 176: 2444–2449Google Scholar
  148. Tan H-M & Fong KP-Y (1993) Molecular analysis of the plasmidborne bed gene cluster from Pseudomonas putida ML2 and cloning of the cis-benzene dihydrodiol dehydrogenase gene. Can. J. Microbiol. 39: 357–362Google Scholar
  149. Terzaghi E & O'Hara M (1990) Microbial plasticity. The relevance to microbial ecology. Adv. Microbial Ecol. 11: 431–460Google Scholar
  150. Timmis KN, Rojo F & Ramos JL (1990) Design of new pathways for the catabolism of environmental pollutants. Adv. Appl. Biotechnol. 4: 61–82Google Scholar
  151. van der Meer JR, de Vos WM, Harayama S & Zehnder AJB (1992) Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol. Rev. 56: 677–694Google Scholar
  152. van der Meer JR, Eggen RIL, Zehnder AJB & de Vos WM (1991a) Sequence analysis of the Pseudomonas sp. strain P51 tcb gene cluster, which encodes metabolism of chlorinated catechols: evidence for specialization of catechol 1,2-dioxygenases for chlorinated substrates. J. Bacteriol. 173: 2425–2434Google Scholar
  153. van der Meer JR, Frijters ACJ, Leveau JHJ, Eggen RIL, Zehnder AJB & de Vos WM (1991b) Characterization of the Pseudomonas sp. strain P51 gene tcbR, a LysR-type transcriptional activator of the tcbCDEF chlorocatechol oxidative operon, and analysis of the regulatory region. J. Bacteriol. 173: 3700–3708Google Scholar
  154. van der Meer JR, Roelofsen W, Schraa G & Zehnder AJB (1987) Degradation of low concentrations of dichlorobenzenes and 1,2,4-trichlorobenzene by Pseudomonas sp. strain P51 in nonsterile soil columns. FEMS Microbiol. Ecol. 45: 333–341Google Scholar
  155. van der Meer JR, van Neerven ARW, de Vries EJ, de Vos WM & Zehnder AJB (1991c) Cloning and characterization of plasmidencoded genes for the degradation of 1,2-dichloro-, 1,4-dichloro-, and 1,2,4-trichlorobenzene of Pseudomonas sp. strain P51. J. Bacteriol. 173: 6–15Google Scholar
  156. van der Meer JR, Zehnder AJB & de Vos WM (1991d) Identification of a novel composite transposable element, Tn5280, carrying chlorobenzene dioxygenase genes of Pseudomonas sp. strain P51. J. Bacteriol. 173: 7077–7083Google Scholar
  157. van Houten B (1990) Nucleotide excision repair in Escherichia coli. Microbiol. Rev. 54: 18–51Google Scholar
  158. Vollmer MD, Fischer P, Knackmuss HJ & Schlömann M (1994) Inability of muconate cycloisomerases to cause dehalogenation during conversion of 2-chloro-cis,cis-muconate. J. Bacteriol. 1768: 4366–4375Google Scholar
  159. Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol. Rev. 48: 60–93Google Scholar
  160. Wang L, Helmann JD & Winans SC (1992) The A.tumefaciens transcriptional activator OccR causes a bend at a target promoter, which is partially relaxed by a plant tumor metabolite. Cell 69: 659–667Google Scholar
  161. Wang Y, Rawlings M, Gibson DT, Labbe D, Bergeron H, Brousseau R & Lau PC (1995) Identification of a membrane protein and a truncated LysR-type regulator associated with the toluene degradation pathway in Pseudomonas putida F1. Mol. Gen. Genet. 246: 570–579Google Scholar
  162. Werlen C, Kohler H-PE & van der Meer JR (1996) The broad substrate chlorobenzene dioxygenase and cis-chlorobenzene dihydrodiol dehydrogenase of Pseudomonas sp. strain P51 are linked evolutionarily to the enzymes for benzene and toluene degradation. J. Biol. Chem. 271: 4009–4016Google Scholar
  163. Williams PA & Sayers JR (1994) The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas. Biodegradation 5: 195–218Google Scholar
  164. Woodgate R & Sedgwick SG (1992) Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues. Mol. Microbiol. 6: 2213–2218Google Scholar
  165. Wyndham RC, Cashore AE, Nakatsu CH & Peel MC (1994) Catabolic transposons. Biodegradation 5: 323–342Google Scholar
  166. Yen K-M & Serdar CM (1988) Genetics of naphthalene catabolism in pseudomonads. CRC Crit. Rev. Microbiol. 15: 247–268Google Scholar
  167. You I-S & Ghosal D (1995) Genetic and molecular analysis of a regulatory region of the herbicide 2,4-dichlorophenoxyacetate catabolic plasmid pJP4. Mol. Microbiol. 16: 321–331Google Scholar
  168. You I-S, Ghosal D & Gunsalus IC (1988) Nucleotide sequence of plasmid NAH7 gene nahR and DNA binding of the nahR product. J. Bacteriol. 120: 5409–5415Google Scholar
  169. — (1991) Nucleotide sequence analysis of the Pseudomonas putida PpG7 salicylate hydroxylase gene (nahG) and its 3'-flanking region. Biochemistry 30: 1635–1641Google Scholar
  170. Zylstra GJ & Gibson DT (1989) Toluene degradation by Pseudomonas putida F1. J. Biol. Chem. 264: 14940–14946Google Scholar

Copyright information

© Kluwer Academic Publishers 1997

Authors and Affiliations

  • Jan Roelof van der Meer
    • 1
  1. 1.Department of MicrobiologySwiss Federal Institute for Environmental Science and Technology, EAWAGDuebendorfSwitzerland

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