Skip to main content
SpringerLink
Log in

Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds

  • Published:
Antonie van Leeuwenhoek Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • 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: 185–195

    Google Scholar 

  • Amabile-Cuevas CF & Chicurel ME (1992) Bacterial plasmids and gene flux. Cell 70: 189–199

    Google Scholar 

  • 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: 557–568

    Google Scholar 

  • 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: 11–18

    Google Scholar 

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

    Google Scholar 

  • Brenner V, Arensdorf JJ & Focht DD (1994) Genetic construction of PCB degraders. Biodegradation 5: 359–378

    Google Scholar 

  • Cairns J, Overbaugh J & Miller S (1988) The origin of mutants. Nature (London) 335: 142–145

    Google Scholar 

  • 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: 499–508

    Google Scholar 

  • 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: 113–118

    Google Scholar 

  • Clarke PH (1984) The evolution of degradative pathways. In: Gibson DT (Ed) Microbial degradation of organic compounds (pp 11–27). Marcel Dekker, Inc., New York

    Google Scholar 

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

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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: 4100–4106

    Google Scholar 

  • 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: 1279–1289

    Google Scholar 

  • 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: 264–270

    Google Scholar 

  • 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: 35–41

    Google Scholar 

  • 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: 6890–6901

    Google Scholar 

  • Devereux J, Haeberli P & Smithies O (1984) A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 12: 387–395

    Google Scholar 

  • 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: 4499–4506

    Google Scholar 

  • 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: 25–33

    Google Scholar 

  • 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: 4583–4593

    Google Scholar 

  • Drake JW (1991) Spontaneous mutation. Annu. Rev. Genet. 25: 124–146

    Google Scholar 

  • 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: 7757–7762

    Google Scholar 

  • 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: 7542–7554

    Google Scholar 

  • 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: 428–430

    Google Scholar 

  • Echols H & Goodman MF (1991) Fidelity mechanisms in DNA replication. Annu. Rev. Biochem. 60: 477–511

    Google Scholar 

  • 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. Z36909

  • Elsemore DA & Ornston LN (1995) Unusual ancestry of dehydratases associated with quinate catabolism in Acinetobacter calcoaceticus. J. Bacteriol. 177: 5971–5978

    Google Scholar 

  • Erickson BD & Mondello FJ (1992) Nucleotide sequencing and transcriptional mapping of the genes encoding biphenyl dioxygenase, a multicomponent polychlorinated-biphenyl-degrading enzyme in Pseudomonas strain LB400. J. Bacteriol. 174: 2903–2912

    Google Scholar 

  • 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: 5052–5058

    Google Scholar 

  • Foster PL (1993) Adaptive mutation: the uses of adversity. Annu. Rev. Microbiol. 47: 467–504

    Google Scholar 

  • 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 York

    Google Scholar 

  • 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: 4460–4464

    Google Scholar 

  • Frazee RW, Livingston DM, LaPorte DC & Lipscomb JD (1993) Cloning, sequencing, and expression of the Pseudomonas putida protocatechuate 3,4-dioxygenase genes. J. Bacteriol. 175:6194–6202

    Google Scholar 

  • 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: 850–856

    Google Scholar 

  • Furukawa K (1994) Molecular genetics and evolutionary relationship of PCB-degrading bacteria. Biodegradation 5: 289–300

    Google Scholar 

  • Furukawa K, Arimura N & Miyazaki T (1987) Nucleotide sequence of the 2,3-dihydroxybiphenyl dioxygenase gene of Pseudomonas pseudoalcaligenes. J. Bacteriol. 169: 427–429

    Google Scholar 

  • 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 

  • Gerischer U & Ornston LN (1995) Spontaneous mutations in pcaH and-G, structural genes for protocatechuate 3,4-dioxygenase in Acinetobacter calcoaceticus. J. Bacteriol. 177: 1336–1347

    Google Scholar 

  • 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, Washington

    Google Scholar 

  • Gregg-Jolly LA & Ornston LN (1990) Recovery of DNA from the Acinetobacter calcoaceticus chromosome by gap repair. J. Bacteriol. 172: 6169–72

    Google Scholar 

  • Gregg-Jolly LA & Ornston LN (1994) Properties of Acinetobacter calcoaceticus recA and its contribution to intracellular gene conversion. Mol. Microbiol. 12: 985–992

    Google Scholar 

  • Gribble GW (1992) Naturally occurring organohalogen compounds — a survey. J. Nat. Prod. 55: 1353–1395

    Google Scholar 

  • Grindley NDF & Reed RR (1985) Transpositional recombination in prokaryotes. Annu. Rev. Biochem. 54: 863–896

    Google Scholar 

  • 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: 667–675

    Google Scholar 

  • 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: 976–980

    Google Scholar 

  • 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: 328–335

    Google Scholar 

  • Harayama S, Kok M & Neidle EL (1992) Functional and evolutionary relationships among diverse oxygenases. Annu. Rev. Microbiol. 46: 565–601

    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

    Google Scholar 

  • Harayama S & Rekik M (1990) The meta cleavage operon of TOL degradative plasmid pWW0 comprises 13 genes. Mol. Gen. Genet. 221: 113–120

    Google Scholar 

  • 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: 81–89

    Google Scholar 

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

    Google Scholar 

  • 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: 241–247

    Google Scholar 

  • Harris RS, Longerich S & Rosenberg SM (1994) Recombination in adaptive mutation. Science 264: 258–260

    Google Scholar 

  • 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: 956–966

    Google Scholar 

  • 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: 23–29

    Google Scholar 

  • 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: 240–246

    Google Scholar 

  • 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: 273–277

    Google Scholar 

  • Hoeijmakers J (1993) Nucleotide excision repair. 1. From E. coli to yeast. Trends Genet. 9: 173–177

    Google Scholar 

  • 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: 47–55

    Google Scholar 

  • 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: 2459–2474

    Google Scholar 

  • Houghton JE, Brown TM, Appel AJ, Hughes EJ & Ornston LN (1995) Discontinuities in the evolution of Pseudomonas putida cat genes. J. Bacteriol. 177: 401–412

    Google Scholar 

  • Inouye S, Asai Y, Nakazawa A & Nakazawa T (1986) Nucleotide sequence of a DNA segment promoting transcription in Pseudomonas putida. J. Bacteriol. 166: 739–745

    Google Scholar 

  • 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: 1192–1199

    Google Scholar 

  • 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: 5174–5179

    Google Scholar 

  • Janssen DB, van der Ploeg JR & Pries F (1994) Genetics and biochemistry of 1,2-dichloroethane degradation. Biodegradation 5: 249–257

    Google Scholar 

  • 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: 1106–1115

    Google Scholar 

  • 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: 1116–1120

    Google Scholar 

  • 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: 8038–42

    Google Scholar 

  • 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: 3885–3889

    Google Scholar 

  • Kaschabek SR & Reineke W (1995) Maleylacetate reductase of Pseudomonas sp. strain B13: specificity of substrate conversion and halide elimination. J. Bacteriol. 1774: 320–325

    Google Scholar 

  • 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: 1689–1694

    Google Scholar 

  • 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: 4269–4276

    Google Scholar 

  • 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: 3095–3103

    Google Scholar 

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

    Google Scholar 

  • 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: 15–20

    Google Scholar 

  • 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: 5111–5116

    Google Scholar 

  • Kowalchuk GA, Gregg JL & Ornston LN (1995) Nucleotide sequences transferred by gene conversion in the bacterium Acinetobacter calcoaceticus. Gene 153: 111–115

    Google Scholar 

  • Kröckel L & Focht DD (1987) Construction of chlorobenzene-utilizing recombinants by progenitive manifestation of a rare event. Appl. Environ. Microbiol. 53: 2470–2475

    Google Scholar 

  • 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: 4587–4594

    Google Scholar 

  • 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: 6518–6526

    Google Scholar 

  • 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: 3385–3390

    Google Scholar 

  • 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: 355–362

    Google Scholar 

  • 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: 7–13

    Google Scholar 

  • 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: 731–46

    Google Scholar 

  • 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: 2286–2295

    Google Scholar 

  • Marques S & Ramos JL (1993) Transcriptional control of the Pseudomonas putida TOL plasmid catabolic pathways. Mol. Microbiol. 9: 923–929

    Google Scholar 

  • 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: 2079–2085

    Google Scholar 

  • Mason JR & Cammack R (1992) The electron-transport proteins of hydroxylating bacterial dioxygenases. Annu. Rev. Microbiol. 46: 277–305

    Google Scholar 

  • Matrubutham U & Harker AR (1994) Analysis of duplicated gene sequences associated with tfdR and tfdS in Alcaligenes eutrophus JMP134. J. Bacteriol. 176: 2348–2353

    Google Scholar 

  • 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: 91–94

    Google Scholar 

  • 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: 349–354

    Google Scholar 

  • Modrich P (1991) Mechanisms and biological effects of mismatch repair. Annu. Rev. Genet. 25: 229–253

    Google Scholar 

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

    Google Scholar 

  • 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: 2923–2938

    Google Scholar 

  • 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: 8312–8316

    Google Scholar 

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

    Google Scholar 

  • 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: 3625–3633

    Google Scholar 

  • 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, Washington

    Google Scholar 

  • Negoro S, Kato K, Fujiyama K & Okada H (1994) The nylon oligomer biodegradation system of Flavobacterium and Pseudomonas. Biodegradation 5: 185–194

    Google Scholar 

  • 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: 113–120

    Google Scholar 

  • 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: 4874–4880

    Google Scholar 

  • 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: 5410–5421

    Google Scholar 

  • 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: 5385–5395

    Google Scholar 

  • Nishino SF, Spain JC, Belcher LA & Litchfield CD (1992) Chlorobenzene degradation by bacteria isolated from contaminated groundwater. Appl. Environ. Microbiol. 58: 1719–1726

    Google Scholar 

  • 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: 333–344

    Google Scholar 

  • 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: 6826–6833

    Google Scholar 

  • 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: 13–18

    Google Scholar 

  • Oltmanns RH, Rast HG & Reineke W (1988) Degradation of 1,4-dichlorobenzene by constructed and enriched strains. Appl. Microbiol. Biotechnol. 28: 609–616

    Google Scholar 

  • Orser CS & Lange CC (1994) Molecular analysis of pentachlorophenol degradation. Biodegradation 5: 277–288

    Google Scholar 

  • 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: 411–416

    Google Scholar 

  • Parke D (1995) Supraoperonic clustering of pca genes for catabolism of the phenolic compound protocatechuate in Agrobacterium tumefaciens. J. Bacteriol. 177: 3808–3817

    Google Scholar 

  • Parsek MR, Kivisaar M & Chakrabarty AM (1995) Differential DNA bending introduced by the Pseudomonas putida LysR-type regulator. Mol. Microbiol. 15: 819–828

    Google Scholar 

  • 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: 7798–7806

    Google Scholar 

  • Pearson DJ & Lipman WR (1988) Improved tools for biological sequence analysis. Proc. Natl. Acad. Sci. USA 85: 2444–2448

    Google Scholar 

  • 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: 7277–7281

    Google Scholar 

  • 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: 3758–3763

    Google Scholar 

  • 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: 2351–2359

    Google Scholar 

  • Powlowski J & Shingler V (1994) Genetics and biochemistry of phenol degradation by Pseudomonas sp. CF600. Biodegradation 5: 219–236

    Google Scholar 

  • 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: 17490–17494

    Google Scholar 

  • 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: 8467–8471

    Google Scholar 

  • Ramos JL & Timmis KN (1987) Experimental evolution of catabolic pathways of bacteria. Microbiol. Sci. 4: 228–237

    Google Scholar 

  • Ramos JL, Wasserfallen A, Rose K & Timmis KN (1987) Redesigning metabolic routes: manipulation of TOL plasmid pathway for catabolism of alkylbenzoates. Science 235: 593–596

    Google Scholar 

  • Reineke W & Knackmuss H-J (1984) Microbial metabolism of haloaromatics: isolation and properties of a chlorobenzenedegrading bacterium. Appl. Environ. Microbiol. 47: 395–402

    Google Scholar 

  • 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: 1395–1398

    Google Scholar 

  • 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: 5891–5898

    Google Scholar 

  • 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: 1430–1440

    Google Scholar 

  • Sayler GS, Hooper SW, Layton AC & King JMH (1990) Catabolic plasmids of environmental and ecological significance. Microb. Ecol. 19: 1–20

    Google Scholar 

  • 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: 273–284

    Google Scholar 

  • 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: 6220–6224

    Google Scholar 

  • Schell MA (1985) Transcriptional control of the nah and sal hydrocarbon-degradation operons by the nahR gene product. Gene 36: 301–309

    Google Scholar 

  • Schell MA (1993) Molecular biology of the LysR family of transcriptional regulators. Annu. Rev. Microbiol. 47: 597–626

    Google Scholar 

  • 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: 1952–1959

    Google Scholar 

  • Schlömann M (1994) Evolution of chlorocatechol catabolic pathways. Conclusions to be drawn from comparisons of lactone hydrolases. Biodegradation 5: 301–321

    Google Scholar 

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

    Google Scholar 

  • 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: 1374–1381

    Google Scholar 

  • 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: 59–65

    Google Scholar 

  • 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: 1596–1604

    Google Scholar 

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

    Google Scholar 

  • 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: 31–37

    Google Scholar 

  • Spain JC & Nishino SF (1987) Degradation of 1,4-dichlorobenzene by a Pseudomonas sp. Appl. Environ. Microbiol. 53: 1010–1019

    Google Scholar 

  • 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: 1015–1026

    Google Scholar 

  • 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: 2950–2955

    Google Scholar 

  • Summers DK (1994) The origins and consequences of genetic instability in prokaryotes. Dev. Biol. Stand. 83: 7–11

    Google Scholar 

  • 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: 1690–1695

    Google Scholar 

  • 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: 4844–4853

    Google Scholar 

  • 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: 2444–2449

    Google Scholar 

  • 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: 357–362

    Google Scholar 

  • Terzaghi E & O'Hara M (1990) Microbial plasticity. The relevance to microbial ecology. Adv. Microbial Ecol. 11: 431–460

    Google Scholar 

  • Timmis KN, Rojo F & Ramos JL (1990) Design of new pathways for the catabolism of environmental pollutants. Adv. Appl. Biotechnol. 4: 61–82

    Google Scholar 

  • van der Meer JR, de Vos WM, Harayama S & Zehnder AJB (1992) Molecular mechanisms of genetic adaptation to xenobiotic compounds. Microbiol. Rev. 56: 677–694

    Google Scholar 

  • 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: 2425–2434

    Google Scholar 

  • 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: 3700–3708

    Google Scholar 

  • 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: 333–341

    Google Scholar 

  • 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: 6–15

    Google Scholar 

  • 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: 7077–7083

    Google Scholar 

  • van Houten B (1990) Nucleotide excision repair in Escherichia coli. Microbiol. Rev. 54: 18–51

    Google Scholar 

  • 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: 4366–4375

    Google Scholar 

  • Walker GC (1984) Mutagenesis and inducible responses to deoxyribonucleic acid damage in Escherichia coli. Microbiol. Rev. 48: 60–93

    Google Scholar 

  • 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: 659–667

    Google Scholar 

  • 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: 570–579

    Google Scholar 

  • 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: 4009–4016

    Google Scholar 

  • Williams PA & Sayers JR (1994) The evolution of pathways for aromatic hydrocarbon oxidation in Pseudomonas. Biodegradation 5: 195–218

    Google Scholar 

  • Woodgate R & Sedgwick SG (1992) Mutagenesis induced by bacterial UmuDC proteins and their plasmid homologues. Mol. Microbiol. 6: 2213–2218

    Google Scholar 

  • Wyndham RC, Cashore AE, Nakatsu CH & Peel MC (1994) Catabolic transposons. Biodegradation 5: 323–342

    Google Scholar 

  • Yen K-M & Serdar CM (1988) Genetics of naphthalene catabolism in pseudomonads. CRC Crit. Rev. Microbiol. 15: 247–268

    Google Scholar 

  • 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: 321–331

    Google Scholar 

  • 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: 5409–5415

    Google Scholar 

  • — (1991) Nucleotide sequence analysis of the Pseudomonas putida PpG7 salicylate hydroxylase gene (nahG) and its 3'-flanking region. Biochemistry 30: 1635–1641

    Google Scholar 

  • Zylstra GJ & Gibson DT (1989) Toluene degradation by Pseudomonas putida F1. J. Biol. Chem. 264: 14940–14946

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Department of Microbiology, Swiss Federal Institute for Environmental Science and Technology, EAWAG, Ueberlandstrasse 133, CH-8600, Duebendorf, Switzerland

    Jan Roelof van der Meer

Authors
  1. Jan Roelof van der Meer
    View author publications

    You can also search for this author in PubMed Google Scholar

Rights and permissions

Reprints and permissions

About this article

Cite this article

van der Meer, J.R. Evolution of novel metabolic pathways for the degradation of chloroaromatic compounds. Antonie Van Leeuwenhoek 71, 159–178 (1997). https://doi.org/10.1023/A:1000166400935

Download citation

  • Issue Date:

  • DOI: https://doi.org/10.1023/A:1000166400935

Search

Navigation