Abstract
Recurring patterns of primary structure have been observed in enzymes that mediate sequential metabolic reactions in bacteria. The enzymes, muconolactone Δ-isomerase [(+)-4-hydroxy-4-carboxymethylisocrotonolactone Δ2-Δ3-isomerase, EC 5.3.3.4] and β-ketoadipate enol-lactone hydrolase [4-carboxymethylbut-3-enolide(1,4)enol-lactone-hydrolase, EC 3.1.1.24], have been coselected in bacterial populations because the isomerase can confer no nutritional advantage in the absence of the hydrolase. Similar amino acid sequences recur within the structure of the isomerase, and the amino-terminal amino acid sequence of the isomerase from Pseudomonas putida appears to be evolutionarily homologous with the corresponding sequence of a β-ketoadipate enol-lactone hydrolase from Acinetobacter calcoaceticus. One interpretation of the sequence repetitions is that they reflect tandem duplication mutations that took place early in the evolution of the proteins. According to this view, the mutations caused elongation of structural genes and the creation of duplicated genes as the metabolic pathways evolved. A review of the sequence data calls attention to a different hypothesis: repeated amino acid sequences were introduced in the course of the proteins' evolution by substitution of copies of DNA sequences into structural genes. Our observations are interpreted on the basis of a model proposing genetic exchange between misaligned DNA sequences. The model predicts that misalignments in one chromosomal region can influence the nature of mutations in another region. Thus, as often has been observed, the mutability of a base pair will be determined by its location in a DNA sequence. Furthermore, the intrachromosomal recombination of DNA sequences may account for complex genetic modifications that occur as new pathways evolve. The model provides an interpretation of an apparent paradox, the rapid creation of new metabolic traits by bacterial genomes that are remarkably resistant to genetic drift.
Keywords: enzymes, mutation, protein homology, protein sequences, recombination
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Selected References
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- Ambler R. P., Wynn M. The amino acid sequences of cytochromes c-551 from three species of Pseudomonas. Biochem J. 1973 Mar;131(3):485–498. doi: 10.1042/bj1310485. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anderson R. P., Roth J. R. Tandem genetic duplications in phage and bacteria. Annu Rev Microbiol. 1977;31:473–505. doi: 10.1146/annurev.mi.31.100177.002353. [DOI] [PubMed] [Google Scholar]
- Arnheim N., Hindenburg A., Begg G. S., Morgan F. J. Multiple genes for lysozyme in birds. Studies on black swan egg white lysozymes. J Biol Chem. 1973 Dec 10;248(23):8036–8042. [PubMed] [Google Scholar]
- Barker W. C., Ketcham L. K., Dayhoff M. O. A comprehensive examination of protein sequences for evidence of internal gene duplication. J Mol Evol. 1978 Feb 21;10(4):265–281. doi: 10.1007/BF01734217. [DOI] [PubMed] [Google Scholar]
- Cohen S. N. Transposable genetic elements and plasmid evolution. Nature. 1976 Oct 28;263(5580):731–738. doi: 10.1038/263731a0. [DOI] [PubMed] [Google Scholar]
- Crawford I. P. Gene rearrangements in the evolution of the tryptophan synthetic pathway. Bacteriol Rev. 1975 Jun;39(2):87–120. doi: 10.1128/br.39.2.87-120.1975. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Cánovas J. L., Stanier R. Y. Regulation of the enzymes of the beta-ketoadipate pathway in Moraxella calcoacetica. 1. General aspects. Eur J Biochem. 1967 May;1(3):289–300. doi: 10.1007/978-3-662-25813-2_40. [DOI] [PubMed] [Google Scholar]
- Dagley S. A biochemical approach to some problems of environmental pollution. Essays Biochem. 1975;11:81–138. [PubMed] [Google Scholar]
- Farabaugh P. J., Schmeissner U., Hofer M., Miller J. H. Genetic studies of the lac repressor. VII. On the molecular nature of spontaneous hotspots in the lacI gene of Escherichia coli. J Mol Biol. 1978 Dec 25;126(4):847–857. doi: 10.1016/0022-2836(78)90023-2. [DOI] [PubMed] [Google Scholar]
- Fitch W. M. Aspects of molecular evolution. Annu Rev Genet. 1973;7:343–380. doi: 10.1146/annurev.ge.07.120173.002015. [DOI] [PubMed] [Google Scholar]
- Hegeman G. D., Rosenberg S. L. The evolution of bacterial enzyme systems. Annu Rev Microbiol. 1970;24:429–462. doi: 10.1146/annurev.mi.24.100170.002241. [DOI] [PubMed] [Google Scholar]
- Hood J. M., Fowler A. V., Zabin I. On the evolution of beta-galactosidase. Proc Natl Acad Sci U S A. 1978 Jan;75(1):113–116. doi: 10.1073/pnas.75.1.113. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Horowitz N. H. On the Evolution of Biochemical Syntheses. Proc Natl Acad Sci U S A. 1945 Jun;31(6):153–157. doi: 10.1073/pnas.31.6.153. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jensen R. A. Enzyme recruitment in evolution of new function. Annu Rev Microbiol. 1976;30:409–425. doi: 10.1146/annurev.mi.30.100176.002205. [DOI] [PubMed] [Google Scholar]
- Jones D., Sneath P. H. Genetic transfer and bacterial taxonomy. Bacteriol Rev. 1970 Mar;34(1):40–81. doi: 10.1128/br.34.1.40-81.1970. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kabat E. A., Wu T. T., Bilofsky H. Variable region genes for the immunoglobulin framework are assembled from small segments of DNA--a hypothesis. Proc Natl Acad Sci U S A. 1978 May;75(5):2429–2433. doi: 10.1073/pnas.75.5.2429. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kleckner N. Translocatable elements in procaryotes. Cell. 1977 May;11(1):11–23. doi: 10.1016/0092-8674(77)90313-0. [DOI] [PubMed] [Google Scholar]
- Meagher R. B. Purification and partial amino acid sequence of the cyanogen bromide fragments of muconolactone isomerase from Pseudomonas putida. Biochim Biophys Acta. 1977 Sep 27;494(1):33–47. doi: 10.1016/0005-2795(77)90132-5. [DOI] [PubMed] [Google Scholar]
- Ornston L. N., Parke D. Evolution of catabolic pathways. Biochem Soc Trans. 1976;4(3):468–472. doi: 10.1042/bst0040468. [DOI] [PubMed] [Google Scholar]
- Ornston L. N. The conversion of catechol and protocatechuate to beta-ketoadipate by Pseudomonas putida. IV. Regulation. J Biol Chem. 1966 Aug 25;241(16):3800–3810. [PubMed] [Google Scholar]
- Patel R. N., Mazumdar S., Ornston L. N. Beta-ketoadipate enol-lactone hydrolases I and II from Acinetobacter calcoaceticus. J Biol Chem. 1975 Aug 25;250(16):6567–6567. [PubMed] [Google Scholar]
- Patel R. N., Meagher R. B., Ornston L. N. Relationships among enzymes of the beta-ketoadipate pathway. IV. Muconolactone isomerase from Acinetobacter calcoaceticus and Pseudomonas putida. J Biol Chem. 1974 Dec 10;249(23):7410–7419. [PubMed] [Google Scholar]
- Seidman J. G., Leder A., Nau M., Norman B., Leder P. Antibody diversity. Science. 1978 Oct 6;202(4363):11–17. doi: 10.1126/science.99815. [DOI] [PubMed] [Google Scholar]
- Yeh W. K., Davis G., Fletcher P., Ornston L. N. Homologous amino acid sequences in enzymes mediating sequential metabolic reactions. J Biol Chem. 1978 Jul 25;253(14):4920–4923. [PubMed] [Google Scholar]
