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. 1988 Oct;170(10):4874–4880. doi: 10.1128/jb.170.10.4874-4880.1988

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.

E L Neidle 1, C Hartnett 1, S Bonitz 1, L N Ornston 1
PMCID: PMC211532  PMID: 3170486

Abstract

The DNA sequence of a 1.6-kilobase-pair SalI-KpnI Acinetobacter calcoaceticus restriction fragment carrying catA, the structural gene for catechol 1,2-dioxygenase I, was determined. The 933-nucleotide gene encodes a protein product with a deduced molecular weight of 34,351. The similarly sized Pseudomonas clcA gene encodes catechol 1,2-dioxygenase II, an enzyme with relatively broad substrate specificity and relatively low catalytic efficiency. Comparison of the catA and clcA sequences demonstrated their common ancestry and suggested that acquisitions of direct and inverted sequence repetitions of 6 to 10 base pairs were frequent events in their evolutionary divergence. The catechol 1,2-dioxygenases proved to be evolutionarily homologous with the alpha and beta subunits of Pseudomonas protocatechuate 3,4-dioxygenase, and analysis of conserved residues in the intradiol dioxygenases revealed conserved histidyl and tyrosyl residues that are probably involved in the ligation of ferric ion in their active sites.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Aldrich T. L., Frantz B., Gill J. F., Kilbane J. J., Chakrabarty A. M. Cloning and complete nucleotide sequence determination of the catB gene encoding cis,cis-muconate lactonizing enzyme. Gene. 1987;52(2-3):185–195. doi: 10.1016/0378-1119(87)90045-x. [DOI] [PubMed] [Google Scholar]
  2. Chatterjee D. K., Chakrabarty A. M. Restriction mapping of a chlorobenzoate degradative plasmid and molecular cloning of the degradative genes. Gene. 1984 Feb;27(2):173–181. doi: 10.1016/0378-1119(84)90138-0. [DOI] [PubMed] [Google Scholar]
  3. Don R. H., Weightman A. J., Knackmuss H. J., Timmis K. N. Transposon mutagenesis and cloning analysis of the pathways for degradation of 2,4-dichlorophenoxyacetic acid and 3-chlorobenzoate in Alcaligenes eutrophus JMP134(pJP4). J Bacteriol. 1985 Jan;161(1):85–90. doi: 10.1128/jb.161.1.85-90.1985. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Dorn E., Knackmuss H. J. Chemical structure and biodegradability of halogenated aromatic compounds. Substituent effects on 1,2-dioxygenation of catechol. Biochem J. 1978 Jul 15;174(1):85–94. doi: 10.1042/bj1740085. [DOI] [PMC free article] [PubMed] [Google Scholar]
  5. Dorn E., Knackmuss H. J. Chemical structure and biodegradability of halogenated aromatic compounds. Two catechol 1,2-dioxygenases from a 3-chlorobenzoate-grown pseudomonad. Biochem J. 1978 Jul 15;174(1):73–84. doi: 10.1042/bj1740073. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Doten R. C., Ngai K. L., Mitchell D. J., Ornston L. N. Cloning and genetic organization of the pca gene cluster from Acinetobacter calcoaceticus. J Bacteriol. 1987 Jul;169(7):3168–3174. doi: 10.1128/jb.169.7.3168-3174.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  7. Frantz B., Chakrabarty A. M. Organization and nucleotide sequence determination of a gene cluster involved in 3-chlorocatechol degradation. Proc Natl Acad Sci U S A. 1987 Jul;84(13):4460–4464. doi: 10.1073/pnas.84.13.4460. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Holloway B. W., Morgan A. F. Genome organization in Pseudomonas. Annu Rev Microbiol. 1986;40:79–105. doi: 10.1146/annurev.mi.40.100186.000455. [DOI] [PubMed] [Google Scholar]
  9. Hou C. T., Lillard M. O., Schwartz R. D. Protocatechuate 3, 4-dioxygenase from Acinetobacter calcoaceticus. Biochemistry. 1976 Feb 10;15(3):582–588. doi: 10.1021/bi00648a020. [DOI] [PubMed] [Google Scholar]
  10. Iwaki M., Kagamiyama H., Nozaki M. The complete amino acid sequence of the beta-subunit of protocatechuate 3,4-dioxygenase from Pseudomonas aeruginosa. J Biochem. 1979 Oct;86(4):1159–1162. doi: 10.1093/oxfordjournals.jbchem.a132612. [DOI] [PubMed] [Google Scholar]
  11. Juni E. Genetics and physiology of Acinetobacter. Annu Rev Microbiol. 1978;32:349–371. doi: 10.1146/annurev.mi.32.100178.002025. [DOI] [PubMed] [Google Scholar]
  12. Kemp M. B., Hegeman G. D. Genetic control of the beta-ketoadipate pathway in Pseudomonas aeruginosa. J Bacteriol. 1968 Nov;96(5):1488–1499. doi: 10.1128/jb.96.5.1488-1499.1968. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Kohlmiller N. A., Howard J. B. The primary structure of the alpha subunit of protocatechuate 3,4-dioxygenase. I. Isolation and sequence of the tryptic peptides. J Biol Chem. 1979 Aug 10;254(15):7302–7308. [PubMed] [Google Scholar]
  14. Ludwig M. L., Weber L. D., Ballou D. P. Characterization of crystals of protocatechuate 3,4-dioxygenase from Pseudomonas cepacia. J Biol Chem. 1984 Dec 10;259(23):14840–14842. [PubMed] [Google Scholar]
  15. Marinus M. G. DNA methylation in Escherichia coli. Annu Rev Genet. 1987;21:113–131. doi: 10.1146/annurev.ge.21.120187.000553. [DOI] [PubMed] [Google Scholar]
  16. McCorkle G. M., Yeh W. K., Fletcher P., Ornston L. N. Repetitions in the NH2-terminal amino acid sequence of beta-ketoadipate enol-lactone hydrolase from Pseudomonas putida. J Biol Chem. 1980 Jul 10;255(13):6335–6341. [PubMed] [Google Scholar]
  17. Messing J., Crea R., Seeburg P. H. A system for shotgun DNA sequencing. Nucleic Acids Res. 1981 Jan 24;9(2):309–321. doi: 10.1093/nar/9.2.309. [DOI] [PMC free article] [PubMed] [Google Scholar]
  18. Neidle E. L., Ornston L. N. Benzoate and muconate, structurally dissimilar metabolites, induce expression of catA in Acinetobacter calcoaceticus. J Bacteriol. 1987 Jan;169(1):414–415. doi: 10.1128/jb.169.1.414-415.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Neidle E. L., Ornston L. N. Cloning and expression of Acinetobacter calcoaceticus catechol 1,2-dioxygenase structural gene catA in Escherichia coli. J Bacteriol. 1986 Nov;168(2):815–820. doi: 10.1128/jb.168.2.815-820.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. Neidle E. L., Shapiro M. K., Ornston L. N. Cloning and expression in Escherichia coli of Acinetobacter calcoaceticus genes for benzoate degradation. J Bacteriol. 1987 Dec;169(12):5496–5503. doi: 10.1128/jb.169.12.5496-5503.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Ngai K. L., Ornston L. N. Abundant expression of Pseudomonas genes for chlorocatechol metabolism. J Bacteriol. 1988 May;170(5):2412–2413. doi: 10.1128/jb.170.5.2412-2413.1988. [DOI] [PMC free article] [PubMed] [Google Scholar]
  22. Ngai K. L., Schlömann M., Knackmuss H. J., Ornston L. N. Dienelactone hydrolase from Pseudomonas sp. strain B13. J Bacteriol. 1987 Feb;169(2):699–703. doi: 10.1128/jb.169.2.699-703.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
  23. Ornston L. N., Yeh W. K. Origins of metabolic diversity: evolutionary divergence by sequence repetition. Proc Natl Acad Sci U S A. 1979 Aug;76(8):3996–4000. doi: 10.1073/pnas.76.8.3996. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Patel R. N., Hou C. T., Felix A., Lillard M. O. Catechol 1,2-dioxygenase from Acinetobacter calcoaceticus: purification and properties. J Bacteriol. 1976 Jul;127(1):536–544. doi: 10.1128/jb.127.1.536-544.1976. [DOI] [PMC free article] [PubMed] [Google Scholar]
  25. Sanger F., Nicklen S., Coulson A. R. DNA sequencing with chain-terminating inhibitors. Proc Natl Acad Sci U S A. 1977 Dec;74(12):5463–5467. doi: 10.1073/pnas.74.12.5463. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Satyshur K. A., Rao S. T., Lipscomb J. D., Wood J. M. Preliminary crystallographic study of protocatechuate 3,4-dioxygenase from Pseudomonas aeruginosa. J Biol Chem. 1980 Nov 10;255(21):10015–10016. [PubMed] [Google Scholar]
  27. Schmidt E., Knackmuss H. J. Chemical structure and biodegradability of halogenated aromatic compounds. Conversion of chlorinated muconic acids into maleoylacetic acid. Biochem J. 1980 Oct 15;192(1):339–347. doi: 10.1042/bj1920339. [DOI] [PMC free article] [PubMed] [Google Scholar]
  28. Shanley M. S., Neidle E. L., Parales R. E., Ornston L. N. Cloning and expression of Acinetobacter calcoaceticus catBCDE genes in Pseudomonas putida and Escherichia coli. J Bacteriol. 1986 Feb;165(2):557–563. doi: 10.1128/jb.165.2.557-563.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Shine J., Dalgarno L. Determinant of cistron specificity in bacterial ribosomes. Nature. 1975 Mar 6;254(5495):34–38. doi: 10.1038/254034a0. [DOI] [PubMed] [Google Scholar]
  30. Tautz D., Trick M., Dover G. A. Cryptic simplicity in DNA is a major source of genetic variation. Nature. 1986 Aug 14;322(6080):652–656. doi: 10.1038/322652a0. [DOI] [PubMed] [Google Scholar]
  31. Walsh T. A., Ballou D. P. Halogenated protocatechuates as substrates for protocatechuate dioxygenase from Pseudomonas cepacia. J Biol Chem. 1983 Dec 10;258(23):14413–14421. [PubMed] [Google Scholar]
  32. Whittaker J. W., Lipscomb J. D. 17O-water and cyanide ligation by the active site iron of protocatechuate 3,4-dioxygenase. Evidence for displaceable ligands in the native enzyme and in complexes with inhibitors or transition state analogs. J Biol Chem. 1984 Apr 10;259(7):4487–4495. [PubMed] [Google Scholar]
  33. Whittaker J. W., Lipscomb J. D., Kent T. A., Münck E. Brevibacterium fuscum protocatechuate 3,4-dioxygenase. Purification, crystallization, and characterization. J Biol Chem. 1984 Apr 10;259(7):4466–4475. [PubMed] [Google Scholar]
  34. Yanisch-Perron C., Vieira J., Messing J. Improved M13 phage cloning vectors and host strains: nucleotide sequences of the M13mp18 and pUC19 vectors. Gene. 1985;33(1):103–119. doi: 10.1016/0378-1119(85)90120-9. [DOI] [PubMed] [Google Scholar]
  35. Yeh W. K., Fletcher P., Ornston L. N. Evolutionary divergence of co-selected beta-ketoadipate enol-lactone hydrolases in Acinetobacter calcoaceticus. J Biol Chem. 1980 Jul 10;255(13):6342–6346. [PubMed] [Google Scholar]
  36. Yoshida R., Hori K., Fujiwara M., Saeki Y., Kagamiyama H. Nonidentical subunits of protocatechuate 3,4-dioxygenase. Biochemistry. 1976 Sep 7;15(18):4048–4053. doi: 10.1021/bi00663a020. [DOI] [PubMed] [Google Scholar]

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