1887

Abstract

A codon-profile strategy was used to predict gene expression levels in . Predicted highly expressed (PHE) genes included those encoding glycolytic and fermentative enzymes, sugar-conversion systems and carbohydrate-transporters. Additionally, some genes required for infection that are involved in oxidative metabolism and hydrogen peroxide production were PHE. Low expression values were predicted for genes encoding specific regulatory proteins like two-component systems and competence genes. Correspondence analysis localized 484 ORFs which shared a distinctive codon profile in the right horn. These genes had a mean G+C content (33·4 %) that was lower than the bulk of the genome coding sequences (39·7 %), suggesting that many of them were acquired by horizontal transfer. Half of these genes (242) were pseudogenes, ORFs shorter than 80 codons or without assigned function. The remaining genes included several virulence factors, such as capsular genes, , , , , choline-binding proteins, and functions related to DNA acquisition, such as restriction-modification systems and . In order to compare predicted translation rate with the relative amounts of mRNA for each gene, the codon adaptation index (CAI) values were compared with microarray fluorescence intensity values following hybridization of labelled RNA from laboratory-grown cultures. High mRNA amounts were observed in 32·5 % of PHE genes and in 64 % of the 25 genes with the highest CAI values. However, high relative amounts of RNA were also detected in 10·4 % of non-PHE genes, such as those encoding fatty acid metabolism enzymes and proteases, suggesting that their expression might also be regulated at the level of transcription or mRNA stability under the conditions tested. The effects of codon bias and mRNA amount on different gene groups in are discussed.

Loading

Article metrics loading...

/content/journal/micro/10.1099/mic.0.27097-0
2004-07-01
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/micro/150/7/mic1502313.html?itemId=/content/journal/micro/10.1099/mic.0.27097-0&mimeType=html&fmt=ahah

References

  1. Andersson S. G. E., Sharp P. M. 1996; Codon usage in the Mycobacterium tuberculosis complex. Microbiology 142:915–925 [CrossRef]
    [Google Scholar]
  2. Auzat I., Chapuy-Regaud S., Le Bras G., Dos Santos D., Ogunniyi A. D., Le Thomas I., Garel J. R., Paton J. C., Trombe M. C. 1999; The NADH oxidase of Streptococcus pneumoniae: its involvement in competence and virulence. Mol Microbiol 34:1018–1028 [CrossRef]
    [Google Scholar]
  3. Berge M., Garcia P., Iannelli F., Prere M. F., Granadel C., Polissi A., Claverys J. P. 2001; The puzzle of zmpB and extensive chain formation, autolysis defect and non-translocation of choline-binding proteins in Streptococcus pneumoniae. Mol Microbiol 39:1651–1660 [CrossRef]
    [Google Scholar]
  4. Chastanet A., Prudhomme M., Claverys J. P., Msadek T. 2001; Regulation of Streptococcus pneumoniae clp genes and their role in competence development and stress survival. J Bacteriol 183:7295–7307 [CrossRef]
    [Google Scholar]
  5. Chavancy G., Garel J. P. 1981; Does quantitative tRNA adaptation to codon content in mRNA optimize the ribosomal translation efficiency? Proposal for a translation system model. Biochimie 63:187–195 [CrossRef]
    [Google Scholar]
  6. Dagkessamanskaia A., Moscoso M., Guiral S., Overweg K., Reuter M., Wells J. M., Claverys J. P., Hénard V. 2004; Interconnection of competence, stress and CiaR regulons in Streptococus pneumoniae: competence triggers stationary phase autolysis of ciaR mutant cells. Mol Micro 51:1071–1086 [CrossRef]
    [Google Scholar]
  7. Dopazo J., Mendoza A., Herrero J. & 13 other authors; 2001; Annotated draft genomic sequence from a Streptococcus pneumoniae type 19F clinical isolate. Micro Drug Resist 7:99–125 [CrossRef]
    [Google Scholar]
  8. Dos Reis M., Wernisch L., Savva R. 2003; Unexpected correlations between gene expression and codon usage bias from microarray data for the whole Escherichia coli K-12 genome. Nucleic Acids Res 31:6976–6985 [CrossRef]
    [Google Scholar]
  9. Duane P. G., Rubins J. B., Weisel H. R., Janoff E. N. 2000; Identification of hydrogen peroxide as a Streptococcus pneumoniae toxin for rat alveolar epithelial cells. Infect Immun 61:4392–4397
    [Google Scholar]
  10. Giard J. C., Rince A., Capiaux H., Auffray Y., Hartke A. 2000; Inactivation of the stress- and starvation-inducible gls24 operon has a pleiotropic effect on cell morphology, stress sensitivity, and gene expression in Enterococcus faecalis. J Bacteriol 182:4512–4520 [CrossRef]
    [Google Scholar]
  11. Grosjean H., Sankoff D., Jou W. M., Fiers W., Cedergren R. J. 1978; Bacteriophage MS2 RNA: a correlation between the stability of the codon : anticodon interaction and the choice of code words. J Mol Evol 12:113–119 [CrossRef]
    [Google Scholar]
  12. Hoskins J., Alborn W. E., Arnold J. & 37 other authors; 2001; Genome of the bacterium Streptococcus pneumoniae strain R6. J Bacteriol 183:5709–5717 [CrossRef]
    [Google Scholar]
  13. Ikemura T. 1981; Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol 146:1–21 [CrossRef]
    [Google Scholar]
  14. Jakubovics N. S., Jenkinson H. F. 2001; Out of the iron age: new insights into the critical role of manganese homeostasis in bacteria. Microbiology 147:1709–1718
    [Google Scholar]
  15. Karlin S., Mrazek J. 2000; Predicted highly expressed genes of diverse prokaryotic genomes. J Bacteriol 182:5238–5250 [CrossRef]
    [Google Scholar]
  16. Karlin S., Mrazek J., Campbell A., Kaiser D. 2001; Characterization of highly expressed genes of four fast-growing bacteria. J Bacteriol 183:5025–5040 [CrossRef]
    [Google Scholar]
  17. Kronigsberg W., Codson G. N. 1983; Evidence for use of rare codons in the dnaG gene and other regulatory genes of Escherichia coli. Proc Natl Acad Sci U S A 80:687–691 [CrossRef]
    [Google Scholar]
  18. Kurland C. G. 1991; Codon bias and gene expression. FEBS Lett 285:165–169 [CrossRef]
    [Google Scholar]
  19. Martin B., Prudhomme M., Alloing G., Granadel C., Claverys J. P. 2000; Cross-regulation of competence pheromone production and export in the early control of transformation in Streptococcus pneumoniae. Mol Microbiol 38:867–878 [CrossRef]
    [Google Scholar]
  20. McInerney J. O. 1998; GCUA (General Codon usage Analysis. Bioinformatics 14:372–373 [CrossRef]
    [Google Scholar]
  21. Médigue C., Rouxel T., Vigier P., Hénaut A., Danchin A. 1991; Evidence for horizontal gene transfer in Escherichia coli speciation. . J Mol Biol 222:851–856 [CrossRef]
    [Google Scholar]
  22. Morrison D. A., Baker M. F. 1979; Competence for genetic transformation in pneumococcus depends on synthesis of a small set of proteins. Nature 282:215–217 [CrossRef]
    [Google Scholar]
  23. Overweg K., Pericone C. D., Verhoef G. G., Weiser J. N., Meiring H. D., De Jong A. P., De Groot R., Hermans P. W. 2000; Differential protein expression in phenotypic variants of Streptococcus pneumoniae. Infect Immun 68:4604–4610 [CrossRef]
    [Google Scholar]
  24. Paton J. C., Andrew P. W., Boulnois G. J., Mitchell T. J. 1993; Molecular analysis of the pathogenicity of Streptococcus pneumoniae: the role of pneumococcal proteins. Annu Rev Microbiol 47:89–115 [CrossRef]
    [Google Scholar]
  25. Pericone C. D., Overweg K., Hermans P. W. M., Weiser J. N. 2000; Inhibitory and bactericidal effects of hydrogen peroxide production by Streptococcus pneumoniae on other inhabitants of the upper respiratory tract. Infect Immun 68:3990–3997 [CrossRef]
    [Google Scholar]
  26. Sharp P. M. 1991; Determinants of DNA sequence divergence between Escherichia coli and Salmonella typhimurium: codon usage, map position, and concerted evolution. J Mol Evol 33:23–33 [CrossRef]
    [Google Scholar]
  27. Sharp P. M., Li W. 1987a; The codon adaptation index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 15:1281–1295 [CrossRef]
    [Google Scholar]
  28. Sharp P. M., Li W. H. 1987b; The rate of synonymous substitution in enterobacterial genes is inversely related to codon usage bias. Mol Biol Evol 4:222–230
    [Google Scholar]
  29. Spellerberg B., Cundell D. R., Sandros J., Pearce B. J., Idanpaan-Heikkila I., Rosenow C., Masure H. R. 1996; Pyruvate oxidase, as a determinant of virulence in Streptococcus pneumoniae. Mol Microbiol 19:803–813 [CrossRef]
    [Google Scholar]
  30. Tettelin H., Nelson K. E., Paulsen I. T. & 36 other authors; 2001; Complete genome sequence of a virulent isolate of Streptococcus pneumoniae. Science 293:498–506 [CrossRef]
    [Google Scholar]
  31. Tseng H. J., McEwan A. G., Paton J. C., Jennings M. P. 2002; Virulence of Streptococcus pneumoniae: PsaA mutants are hypersensitive to oxidative stress. Infect Immun 70:1635–1639 [CrossRef]
    [Google Scholar]
  32. Wilkins J. C., Homer K. A., Beighton D. 2002; Analysis of Streptococcus mutans proteins modulated by culture under acidic conditions. Appl Environ Microbiol 68:2382–2390 [CrossRef]
    [Google Scholar]
  33. Wright F. 1990; The ‘effective number of codons' used in a gene. Gene 87:23–29 [CrossRef]
    [Google Scholar]
  34. Yesilkaya H., Kadioglu A., Gingles N., Alexander J. E., Mitchell T. J., Andrew P. W. 2000; Role of manganese-containing superoxide dismutase in oxidative stress and virulence of Streptococcus pneumoniae. Infect Immun 68:2819–2826 [CrossRef]
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.27097-0
Loading
/content/journal/micro/10.1099/mic.0.27097-0
Loading

Data & Media loading...

Supplements

Supplementary material 1

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error