Evolutionary flux of potentially bldA-dependent Streptomyces genes containing the rare leucine codon TTA
- 353 Downloads
Previous studies have shown that one of the six leucine codons, UUA, is rare in Streptomyces, and that, while the gene for the UUA-specific tRNA, bldA, can generally be inactivated in diverse streptomycetes without impairing vegetative growth, bldA mutants are typically defective in reproductive aerial growth and in antibiotic production. Here, four complete genome sequences and 143 gene clusters for antibiotic biosynthesis from diverse streptomycetes were analysed in order to evaluate the evolution and function of genes whose possession of TTA codons makes them dependent on bldA. It was deduced that the last common ancestor of the four sequenced genomes, possibly 220 million years ago, already possessed the bldA system, together with perhaps 200 TTA-containing target genes. Some 33 of these genes are retained by the modern descendants, though only three of them retain a TTA in all occurrences. Nearly all of these 33, as well as many of the TTA-containing genes with orthologues in two or three of the four genomes, have the same location on the chromosomes as in their common ancestor. However, the majority of TTA-containing genes (61% overall in the four genomes) are species-specific, and were probably acquired by comparatively recent horizontal gene transfer. Most of these genes are of unknown function, and it is likely that many of them confer specialised ecological benefits. On the other hand, one class of species-specific, functionally recognisable, horizontally acquired genes—the gene clusters for antibiotic production—very often contain TTA codons; and nearly half of them have TTA codons in their pathway-specific regulatory genes.
KeywordsSporulation Antibiotic production Translational regulation Comparative genomics Codon usage
We thank Mervyn Bibb and Diversa Corporation for allowing us access to the genome sequence of S. venezuelae, and Professor Alan Ward for information on the dating of the point of divergence of the strains with sequenced genomes. KFC is a John Innes Foundation Emeritus Fellow.
- Bentley SD, Chater KF, Cerdeno-Tarraga AM, Challis GL, Thomson NR, James KD, Harris DE, Quail MA, Kieser H, Harper D, Bateman A, Brown S, Chandra G, Chen CW, Collins M, Cronin A, Fraser A., Goble A, Hidalgo J, Hornsby T, Howarth S, Huang CH, Kieser T, Larke L, Murphy L, Oliver K, O’Neil S, Rabbinowitsch E, Rajandream MA, Rutherford K, Rutter S, Seeger K, Saunders D, Sharp S, Squares R, Squares S, Taylor K, Warren T, Wietzorrek A, Woodward J, Barrell BG, Parkhill J, Hopwood DA (2002) Complete genome sequence of the model actinomycete Streptomyces coelicolor A3(2). Nature 417:141–147PubMedCrossRefGoogle Scholar
- Böger P (1975) Photosynthese in globaler Sicht. Naturwiss Rundsch 28:429–435Google Scholar
- Chater KF, Chandra G (2008) The use of the rare UUA codon to define “expression space” for genes involved in secondary metabolism, development and environmental adaptation in Streptomyces. J Microbiol (in press)Google Scholar
- Li W, Wu J, Tao W, Zhao C, Wang Y, He X, Chandra G, Zhou X, Deng Z, Chater KF, Tao M (2007) A genetic and bioinformatic analysis of Streptomyces coelicolor genes containing TTA codons, possible targets for regulation by a developmentally significant tRNA. FEMS Microbiol Lett 266:20–28PubMedCrossRefGoogle Scholar
- Stajich JE, Block D, Boulez K, Brenner SE, Chervitz SA, Dagdigian C, Fuellen G, Gilbert JG, Korf I, Lapp H, Lehvaslaiho H, Matsalla C, Mungall CJ, Osborne BI, Pocock MR, Schattner P, Senger M, Stein LD, Stupka E, Wilkinson MD, Birney E (2002) The Bioperl toolkit: perl modules for the life sciences. Genome Res 12:1611–1618PubMedCrossRefGoogle Scholar
- Tao WF, Wu J, Deng ZX, Tao MF (2007) Cloning of bldAa and the effect on morphological differentiation and avermectins production in Streptomyces avermitilis NRRL8165. Wei Sheng Wu Xue Bao 47:34–38, ChineseGoogle Scholar