Skip to main content
Log in

Evolutionary relationships between catabolic pathways for aromatics: Conservation of gene order and nucleotide sequences of catechol oxidation genes of pWW0 and NAH7 plasmids

  • Published:
Molecular and General Genetics MGG Aims and scope Submit manuscript

Summary

TOL plasmid pWW0 and plasmid NAH7 encode catabolic enzymes required for oxidative degradation of toluene and naphthalene, respectively. The gene order of the catabolic operon of NAH7 for salicylate oxidation was determined to be: promoter-nahG (the structural gene for salicylate hydroxylase)-nahH (catechol 2,3-dioxygenase)-nahI (hydroxymuconic semialdehyde dehydrogenase)-nahN (hydroxymuconic semialdehyde hydrolase)-nahL (2-oxopent-4-enoate hydratase). This order is identical to that of the isofunctional genes of TOL plasmid pWW0. The complete nucleotide sequence of nahH was determined and compared with that of xylE, the isofunctional gene of TOL plasmid pWW0. There were 20% and 16% differences in their nucleotide and amino acid sequences, respectively. The homology between the NAH7 and TOL pWW0 plasmids ends upstream of the Shine-Dalgarno sequences of nahH and xylE, but the homology continues downstream of these genes. This observation suggested that genes for the catechol oxidative enzymes of NAH7 and TOL pWW0 were derived from a common ancestral sequence which was transferred as a discrete segment of DNA between plasmids.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

References

  • Babiuk LA, Paul EA (1970) The use of fluorescein isothiocyanate in the determination of the bacterial biomass of grassland soil. Can J Microbiol 16:57–62

    Google Scholar 

  • Bayley SA, Morris DW, Broda P (1979) The relationship of degradative and resistance plasmids of Pseudomonas belonging to the same incompatibility group. Nature 280:338–339

    Google Scholar 

  • Benson S, Shapiro J (1978) TOL is a broad-host range plasmid. J Bacteriol 135:278–280

    Google Scholar 

  • Cane PA, Williams PA (1986) A restriction map of naphthalene catabolic plasmid pWW60-1 and the location of some of its catabolic genes. J Gen Microbiol 132:2919–2929

    Google Scholar 

  • Catterall FA, Sala-Trepat JM, Williams PA (1971) The coexistence of two pathways for the metabolism of 2-hydroxymuconic semialdehyde in a naphthalene-grown Pseudomonad. Biochem Biophys Res Commun 43:463–469

    Google Scholar 

  • Chakrabarty AM, Friello DA, Bopp LH (1978) Transposition of plasmid DNA segments specifying hydrocarbon degradation and their expression in various microorganisms. Proc Natl Acad Sci USA 75:3109–3112

    Google Scholar 

  • Chen EY, Seeburg DH (1985) Supercoil sequencing: a fast and simple method for sequencing plasmid DNA. DNA 4:165–170

    Google Scholar 

  • Clarke PH, Ornston LN (1975) Metabolic pathways and regulation: 1. In: Clarke PH, Richmond MH (eds) Genetics and biochemistry of Pseudomonas. John Wiley & Sons, London, pp 191–261

    Google Scholar 

  • Doolittle RF (1979) Protein evolution. In: Neurath H, Hill RL (eds) The proteins, vol IV. Academic Press, New York, pp 1–118

    Google Scholar 

  • Dunn NW, Gunsalus IC (1973) Transmissible plasmid coding early enzymes of naphthalene oxidation in Pseudomonas putida. J Bacteriol 114:974–979

    Google Scholar 

  • Ensley BD, Gibson DT (1983) Naphthalene dioxygenase: purification and properties of a terminal oxygenase component. J Bacteriol 155:505–511

    Google Scholar 

  • Farrell R, Chakrabarty AM (1979) Degradative plasmids: Molecular nature and mode of evolution. In: Timmis KN, Pühler A (eds) Plasmids of medical, environmental and commercial importance. Elsevier/North-Holland Biomedical, Amsterdam, pp 97–109

    Google Scholar 

  • Franklin FCH, Bagdasarian M, Bagdasarian MM, Timmis KN (1981) Molecular and functional analysis of the TOL plasmid pWW0 from Pseudomonas putida and cloning of genes for the entire regulated aromatic ring meta-cleavage pathway. Proc Natl Acad Sci USA 78:7458–7462

    Google Scholar 

  • Franklin FCH, Lehrbach PR, Lurz R, Rueckert B, Bagdasarian M, Timmis KN (1983) Localization and functional analysis of transposon mutations in regulatory genes of the TOL catabolic pathway. J Bacteriol 154:676–685

    Google Scholar 

  • Hagström A (1984) Aquatic bacteria: measurements and significance of growth. In: Klug MJ, Reddy CA (eds) Current perspectives in microbial ecology. American Society for Microbiology, Washington, DC, pp 495–501

    Google Scholar 

  • Hansen JB, Olsen RH (1978) Isolation of large bacterial plasmids and characterization of the P2 compatibility group plasmids pMG1 and pMG5. J Bacteriol 135:227–238

    Google Scholar 

  • Harayama S, Lehrbach PR, Timmis KN (1984) Transposon mutagenesis analysis of meta-cleavage pathway operon genes of the TOL plasmid of Pseudomonas putida mt-2. J Bacteriol 160:251–255

    Google Scholar 

  • Harayama S, Rekik M, Timmis KN, (1986a) Genetic analysis of a relaxed substrate specificity aromatic ring dioxygenase, toluate 1,2-dioxygenase, encoded by TOL plasmid pWW0 of Pseudomonas putida. Mol Gen Genet 202:226–234

    Google Scholar 

  • Harayama S Leppik RA, Rekik M, Mermod N, Lehrbach PR, Reineke W, Timmis KN (1986b) Gene order of the TOL catabolic plasmid upper pathway operon and oxidation of both toluene and benzyl alcohol by the xylA product. J Bacteriol 167:455–461

    Google Scholar 

  • Harayama S, Mermod N, Rekik M, Lehrbach, PR, Timmis KN (1987) Roles of the divergent branches of the meta-cleavage pathway in the degradation of benzoate and substituted benzoates. J Bacteriol 169:558–564

    Google Scholar 

  • Holmquist R (1972) Theoretical foundations for a quantitative approach to paleogenetics. Part I: DNA. J Mol Evol 1:115–133

    Google Scholar 

  • Inouye S, Nakazawa A, Nakazawa T (1981a) Molecular cloning of TOL genes xylB and xylE in Escherichia coli. J Bacteriol 145:1137–1143

    Google Scholar 

  • Inouye S, Nakazawa A, Nakazawa T (1981b) Molecular cloning of gene xylS of the TOL plasmid: evidence for positive regulation of the xylDEGF operon by xylS. J Bacteriol 148:413–418

    Google Scholar 

  • Inouye S, Nakazawa A, Nakazawa T (1983) Molecular cloning of regulatory gene xylR and operator-promoter regions of the xylABC and xylDEGF operons of the TOL plasmid. J Bacteriol 155:1192–1199

    Google Scholar 

  • Jacoby GA, Rogers JE, Jocob AE, Hedges RW (1978) Transposition of Pseudomonas toluene-degrading genes and expression in Escherichia coli. Nature 274:179–180

    Google Scholar 

  • Jeenes DJ, Williams PA (1982) Excision and integration of degradative pathway genes from TOL pWW0. J Bacteriol 150:188–194

    Google Scholar 

  • Kieny MP, Lathe R, Lecocq J-P (1983) New versatile cloning and sequencing vectors based on bacteriophage M13. Gene 26:91–99

    Google Scholar 

  • Kimura M (1977) Preponderance of synonymous changes as evidence for the neutral theory of molecular evolution. Nature 267:275–276

    Google Scholar 

  • Lehrbach PR, McGregor I, Ward JM, Broda P (1983) Molecular relationships between Pseudomonas Inc P-9 degradative plasmids TOL, NAH and SAL. Plasmid 10:164–174

    Google Scholar 

  • Lehrbach PR, Zeyer J, Reineke W, Knackmuss H-J, Timmis KN (1984) Enzyme recruitment in vitro: use of cloned genes to extend the range of haloaromatics degraded by Pseudomonas sp. strain B13. J Bacteriol 158:1025–1032

    Google Scholar 

  • Leisinger T (1983) Microorganisms and xenobiotic compounds. Experientia. 39:1183–1191

    Google Scholar 

  • Maniatis T, Fritsch EF, Sambrook J (1982) Molecular cloning. A laboratory manual. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Meulien P, Downing RG, Broda P (1981) Excision of the 40 kb segment of the TOL plasmid from Pseudomonas putida mt-2 involves direct repeats. Mol Gen Genet 184:97–101

    Google Scholar 

  • Miller JH (1972) Experiments in molecular genetics. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York

    Google Scholar 

  • Miyata T, Yasunaga T, Nishida T (1980) Nucleotide sequence divergence and functional constraint in mRNA evolution. Proc Natl Acad Sci USA 77:7328–7332

    Google Scholar 

  • Murray K, Duggleby CJ, Sala-Trepat JM, Williams PA (1972) The metabolism of benzoate and methylbenzoates via the meta-cleavage pathway by Pseudomonas arvilla mt-2. Eur J Biochem 28:301–310

    Google Scholar 

  • Nakai C, Kagamiyama H, Nozaki M, Nakazawa T, Inouye S, Ebina Y, Nakazawa A (1983) Complete nucleotide sequence of the metapyrocatechase gene on the TOL plasmid of Pseudomonas putida mt-2. J Biol Chem 258:2923–2928

    Google Scholar 

  • Nozaki M, Kagamiyama M, Hayaishi O (1963) Crystallization and some properties of metapyrocatechase. Biochem Biophys Res Commun 11:65–69

    Google Scholar 

  • Ornston LN, Yeh WK (1982) Recurring themes and repeated sequences in metabolic evolution. In: Chakrabarty AM (ed) Biodegradation and detoxification of environmental pollutants. CRC Press Inc, Boca Raton, Florida, pp 105–127

    Google Scholar 

  • Patel TR, Barnsley EA (1980) Naphthalene metabolism by Pseudomonads: purification and properties of 1,2-dihydroxynaphthalene oxygenase. J Bacteriol 143:668–673

    Google Scholar 

  • Patel TR, Gibson DT (1974) Purification and properties of (+)-cis-naphthalene naphthalene dihydrodiol dehydrogenase of Pseudomonas putida. J Bacteriol 119:879–888

    Google Scholar 

  • Pemberton JM (1983) Degradative plasmids. Int Rev Cytol 84:155–182

    Google Scholar 

  • Sala-Trepat JM, Evans WC (1971) The meta-cleavage of catechol by Azotobacter species. 4-oxalocrotonate pathway. Eur J Biochem 20:400–413

    Google Scholar 

  • Sanger F, Nicklen S, Coulson AR (1977) DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci USA 74:5463–5467

    Google Scholar 

  • Schell MA (1986) Homology between nucleotide sequences of promoter regions of nah and sal operons of NAH7 plasmid of Pseudomonas putida. Proc Natl Acad Sci USA 83:369–373

    Google Scholar 

  • Stanier RY, Palleroni NJ, Doudoroff M (1966) The aerobic pseudomonads: a taxonomic study. J Gen Microbiol 43:159–273

    Google Scholar 

  • Wigmore GJ, Bayly RC (1977) A partial order for genes determining enzymes of the meta-cleavage pathway in Pseudomonas putida. J Gen Microbiol 100:65–69

    Google Scholar 

  • Wilbur WJ (1985) Codon equilibrium I: testing for homogeneous equilibrium. J Mol Evol 21:169–181

    Google Scholar 

  • 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 120:416–423

    Google Scholar 

  • Wong CL, Dunn NW (1974) Transmissible plasmid coding for the degradation of benzoate and m-toluate in Pseudomonas arvilla mt-2. Genet Res 23:227–232

    Google Scholar 

  • Worsey MJ, Williams PA (1975) Metabolism of toluene and xylenes by Pseudomonas putida (arvilla) mt-2: evidence for a new function of the TOL plasmid. J Bacteriol 124:7–13

    Google Scholar 

  • Worsey MJ, Franklin FCH, Williams PA (1978) Regulation of the degradative pathway enzymes coded for by the TOL plasmid (pWW0) from Pseudomonas putida mt-2. J Bacteriol 134:757–764

    Google Scholar 

  • Yamamoto S, Katagiri M, Maeno H, Hayaishi O (1965) Salicylate hydroxylase, a monooxygenase requiring flavin adenine dinucleotide. J Biol Chem 240:3408–3413

    Google Scholar 

  • Yanisch-Perron C, Vieira J, Messing J (1985) Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene 33:103–119

    Google Scholar 

  • Yen K-M, Gunsalus IC (1982) Plasmid gene organization: naphthalene/salicylate oxidation. Proc Natl Acad Sci USA 79:874–878

    Google Scholar 

  • Yen K-M, Gunsalus IC (1985) Regulation of naphthalene catabolic genes of plasmid NAH7. J Bacteriol 162:1008–1013

    Google Scholar 

  • Zukowski MM, Gaffney DF, Speck D, Kaufmann M, Findeli A, Wisecup A, Lecocq J-P (1983) Chromogenic identification of genetic regulatory signals in Bacillus subtilis based on expression of a cloned Pseudomonas gene. Proc Natl Acad Sci USA 80:1101–1105

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by K. Isono

Rights and permissions

Reprints and permissions

About this article

Cite this article

Harayama, S., Rekik, M., Wasserfallen, A. et al. Evolutionary relationships between catabolic pathways for aromatics: Conservation of gene order and nucleotide sequences of catechol oxidation genes of pWW0 and NAH7 plasmids. Molec Gen Genet 210, 241–247 (1987). https://doi.org/10.1007/BF00325689

Download citation

  • Received:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00325689

Key words

Navigation