1887

Abstract

Synonymous codon usage in the complete genome of was investigated. The moderate A+T-richness of the genome (G+C=39 mol%) is reflected in the overall synonymous codon usage but the frequencies of some codons cannot be explained by simple mutational biases. A low level of heterogeneity among genes was observed, but this does not appear to be due to varying mutational bias or translational selection. Some of the heterogeneity was due to amino acid composition variation among the encoded proteins, and some may be attributable to recent acquisition of genes from other species. Since codon usage is not dominated by biased mutation patterns, the absence of evidence for translationally mediated selection among synonymous codons is striking. This has implications with regard to the life history of this species, and in particular suggests that strains are not subject to periods of competitive exponential growth. Despite the lack of selected codon usage, base composition immediately after the translation initiation site is skewed, consistent with selection against secondary structure formation in this region.

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2000-04-01
2024-10-08
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References

  1. Akopyants N. S., Eaton K. A., Berg D. E. 1995; Adaptive mutation and cocolonization during Helicobacter pylori infection of gnotobiotic piglets. Infect Immun 63:116–121
    [Google Scholar]
  2. Andersson S. G. E., Sharp P. M. 1996a; Codon usage and base composition in Rickettsia prowazeckii. J Mol Evol 42:525–536 [CrossRef]
    [Google Scholar]
  3. Andersson S. G. E., Sharp P. M. 1996b; Codon usage in the Mycobacterium tuberculosis complex. Microbiology 142:915–925 [CrossRef]
    [Google Scholar]
  4. Beji A., Vincent P., Dachis I., Husson M. O., Cortol A., Leclerc H. 1989; Evidence of gastritis with several Helicobacter pylori strains. Lancet 2:1402–1405
    [Google Scholar]
  5. Berg D. E., Gilman R. H., Lelwala-Guruge J.9 other authors 1997; Helicobacter pylori populations in Peruvian patients. Clin Infect Dis 25:996–1002 [CrossRef]
    [Google Scholar]
  6. Berg O. G., Kurland C. G. 1997; Growth rate-optimised tRNA abundance and codon usage. J Mol Biol 270:544–550 [CrossRef]
    [Google Scholar]
  7. Blaser M. J. 1992; Helicobacter pylori – its role in disease. Clin Infect Dis 15:386–393 [CrossRef]
    [Google Scholar]
  8. Blaser M. J. 1997; Heterogeneity of Helicobacter pylori. Eur J Gastroenterol Hepatol 9:S3–S6 [CrossRef]
    [Google Scholar]
  9. Blattner F. R., Plunkett G. I., Bloch A.14 other authors 1997; The complete genome sequence of Escherichia coli K-12. Science 277:1453–1462 [CrossRef]
    [Google Scholar]
  10. Borodovsky M., McIninch J. D. 1993; Parallel gene recognition for both DNA strands. Comput Chem 17:123–133 [CrossRef]
    [Google Scholar]
  11. Bulmer M. 1987; Coevolution of codon usage and transfer RNA abundance. Nature 325:728–730 [CrossRef]
    [Google Scholar]
  12. Bulmer M. 1990; The effect of context on synonymous codon usage genes with low codon usage bias. Nucleic Acids Res 18:2869–2873 [CrossRef]
    [Google Scholar]
  13. Bulmer M. 1991; The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–907
    [Google Scholar]
  14. Cao P., Cover T. L. 1997; High-level genetic diversity in the vapD chromosomal region of Helicobacter pylori. J Bacteriol 179:2852–2856
    [Google Scholar]
  15. Covacci A., Falkow S., Berg D. E., Rappuoli R. 1997; Did the inheritance of a pathogenicity island modify the virulence of Helicobacter pylori?. Trends Microbiol 5:205–208 [CrossRef]
    [Google Scholar]
  16. Eyre-Walker A., Bulmer M. 1993; Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res 21:4599–4603 [CrossRef]
    [Google Scholar]
  17. Fleischmann R. D., Adams M. D., White O.37 other authors 1995; Whole-genome random sequencing and assembly of Haemophilus influenzae Rd. Science 269:496–512 [CrossRef]
    [Google Scholar]
  18. Francino M. P., Ochman H. 1997; Strand asymmetries in DNA evolution. Trends Genet 13:240–245 [CrossRef]
    [Google Scholar]
  19. Fujimoto S., Marshall B., Blaser M. J. 1994; PCR-based restriction fragment length polymorphism typing of Helicobacter pylori. J Clin Microbiol 32:331–334
    [Google Scholar]
  20. Go M. F., Kapur V., Graham D. Y., Musser J. M. 1996; Population genetic analysis of Helicobacter pylori by multilocus enzyme electrophoresis: extensive allelic diversity and recombinational population structure. J Bacteriol 178:3934–3938
    [Google Scholar]
  21. Göttke M. U., Groody J. M., Loo V., Fallone C. A., Barkum A. N., Beech R. N. 1996; Panmyctic population structure due to frequent recombination in Helicobacter pylori. Gut 39:A121 [CrossRef]
    [Google Scholar]
  22. Gouy M., Gautier C. 1982; Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res 10:7055–7074 [CrossRef]
    [Google Scholar]
  23. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. 1981; Codon catalog usage is a genome strategy modulated for gene expressivity. Nucleic Acids Res 9:r43–r74
    [Google Scholar]
  24. Greenacre M. J. 1984 Theory and Applications of Correspondence Analysis London: Academic Press;
    [Google Scholar]
  25. Hazell S. L., Andrews R. H., Mitchell H. M., Daskalopoulos G. 1997; Genetic relationship among isolates of Helicobacter pylori: evidence for the existence of a Helicobacter pylori species-complex. FEMS Microbiol Lett 150:27–32 [CrossRef]
    [Google Scholar]
  26. Ikemura T. 1981a; 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]
  27. Ikemura T. 1981b; Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes: a proposal for a synonymous codon choice that is optimal for the E. coli translational system. J Mol Biol 151:389–409 [CrossRef]
    [Google Scholar]
  28. Kerr A. R. W., Peden J. F., Sharp P. M. 1997; Systematic base composition variation around the genome of Mycoplasma genitalium, but not Mycoplasma pneumoniae. Mol Microbiol 25:1177–1179
    [Google Scholar]
  29. Kitamoto N., Nakamoto H., Katai A., Takahara N., Nakata H., Tamaki H., Tanaka T. 1998; Heterogeneity of protein profiles of Helicobacter pylori isolated from individual patients. Helicobacter 3:152–162 [CrossRef]
    [Google Scholar]
  30. Kunst F., Ogasawara N., Moszer I.148 other authors 1997; The complete genome sequence of the gram-positive bacterium Bacillus subtilis. Nature 390:249–256 [CrossRef]
    [Google Scholar]
  31. Kurland C. G. 1993; Major codon preference: theme and variations. Biochem Soc Trans 21:841–846
    [Google Scholar]
  32. Lafay B., Lloyd A. T., McLean M. J., Devine K. M., Sharp P. M., Wolfe K. H. 1999; Proteome composition and codon usage in spirochaetes: species-specific and DNA strand-specific mutational biases. Nucleic Acids Res 27:1642–1649 [CrossRef]
    [Google Scholar]
  33. Lawrence J. G., Ochman H. 1997; Amelioration of bacterial genomes: rates of change and exchange. J Mol Evol 44:383–397 [CrossRef]
    [Google Scholar]
  34. Lobry J. R., Gautier C. 1994; Hydrophobicity, expressivity and aromaticity are the major trends of amino-acid usage in 999 Escherichia coli chromosome-encoded genes. Nucleic Acids Res 22:3174–3180 [CrossRef]
    [Google Scholar]
  35. Lloyd A. T., Sharp P. M. 1992; codons: a microcomputer program for codon usage analysis. J Hered 83:239–240
    [Google Scholar]
  36. McInerney J. O. 1997; Prokaryotic genome evolution as assessed by multivariate analysis of codon usage patterns. Microb Comp Genomics 2:1–10 [CrossRef]
    [Google Scholar]
  37. McInerney J. O. 1998; Replicational and transcriptional selection on codon usage in Borrelia burgdorferi. Proc Natl Acad Sci USA 95:10698–10703 [CrossRef]
    [Google Scholar]
  38. McLean M. J., Wolfe K. H., Devine K. M. 1998; Base composition skews, replication orientation, and gene orientation in 12 prokaryote genomes. J Mol Evol 47:691–696 [CrossRef]
    [Google Scholar]
  39. Marshall D. G., Dundon W. G., Beesley S. M., Smyth C. J. 1998; Helicobacter pylori – a conundrum of genetic diversity. Microbiology 144:2925–2939 [CrossRef]
    [Google Scholar]
  40. Maynard Smith M., Smith N. H. 1998; Detecting recombination from gene trees. Mol Biol Evol 15:590–599 [CrossRef]
    [Google Scholar]
  41. Ohama T., Muto A., Osawa S. 1990; Role of GC-biased mutation pressure on synonymous codon choice in Micrococcus luteus, a bacterium with a high genomic GC-content. Nucleic Acids Res 18:1565–1569 [CrossRef]
    [Google Scholar]
  42. Ohkubo S., Muto A., Kawauchi Y., Yamao F., Osawa S. 1987; The ribosomal protein gene cluster of Mycoplasma capricolum. Mol Gen Genet 210:314–322 [CrossRef]
    [Google Scholar]
  43. Olsen G. J., Woese C. R., Overbeek R. 1994; The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 176:1–6
    [Google Scholar]
  44. Owen R. J., Desai M., Figura N., Bayeli P. F., Di Gregorio L., Russi M., Musmanno R. A. 1993; Comparisons between degree of histological gastritis and DNA fingerprints, cytotoxicity and adhesivity of Helicobacter pylori from different gastric sites. Eur J Epidemiol 9:315–321 [CrossRef]
    [Google Scholar]
  45. Perrière G., Lobry J. R., Thioulouse J. 1996; Correspondence discriminant analysis: a multivariate method for comparing classes of protein and nucleic acid sequences. Comput Appl Biosci 12:519–524
    [Google Scholar]
  46. Post L. E., Nomura M. 1980; DNA sequences from the str operon of Escherichia coli. J Biol Chem 255:4660–4666
    [Google Scholar]
  47. Salaün L., Audibert C., Le Gay G., Burucoa C., Fauchère J. L., Picard B. 1998; Panmictic structure of Helicobacter pylori demonstrated by the comparative study of six genetic markers. FEMS Microbiol Lett 161:231–239 [CrossRef]
    [Google Scholar]
  48. Salzberg S. L., Delcher A. L., Kasif S., White O. 1998; Microbial gene identification using interpolated Markov models. Nucleic Acids Res 26:544–548 [CrossRef]
    [Google Scholar]
  49. Sharp P. M., Li W.-H. 1986a; Codon usage in regulatory genes in Escherichia coli does not reflect selection for ‘‘rare’’ codons. Nucleic Acids Res 14:7737–7749 [CrossRef]
    [Google Scholar]
  50. Sharp P. M., Li W.-H. 1986b; An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38 [CrossRef]
    [Google Scholar]
  51. Sharp P. M., Stenico M., Peden J. F., Lloyd A. T. 1993; Codon usage: mutational bias, translational selection, or both?. Biochem Soc Trans 21:835–841
    [Google Scholar]
  52. Shields D. C., Sharp P. M. 1987; Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Res 15:8023–8040 [CrossRef]
    [Google Scholar]
  53. Shields D. C., Sharp P. M., Higgins D. G., Wright F. 1988; ‘‘Silent’’ sites in Drosophila genes are not neutral: evidence of selection among synonymous codons. Mol Biol Evol 5:704–716
    [Google Scholar]
  54. Stormo G. D., Schneider T. D., Gold L. M. 1982; Characterization of translational initiation sites in E. coli. Nucleic Acids Res 10:2971–2996 [CrossRef]
    [Google Scholar]
  55. Suerbaum S., Maynard Smith J., Bapumia K., Morelli G., Smith N. H., Kunstmann E., Dyrek I., Achtman M. 1998; Free recombination within Helicobacter pylori. Proc Natl Acad Sci USA 95:12619–12624 [CrossRef]
    [Google Scholar]
  56. Taylor D. N., Blaser M. J. 1991; The epidemiology of Helicobacter pylori. Epidemiol Rev 13:42–59
    [Google Scholar]
  57. Taylor N. S., Fox J. G., Akopyants N. S.8 other authors 1995; Long-term colonization with single and multiple strains of Helicobacter pylori assessed by DNA-fingerprinting. J Clin Microbiol 33:918–923
    [Google Scholar]
  58. Tomb J.-F., White O., Kerlavage A. R.39 other authors 1997; The complete genome sequence of the gastric pathogen Helicobacter pylori. Nature 388:539–547 [CrossRef]
    [Google Scholar]
  59. Wright F. 1990; The ‘effective number of codons’ used in a gene. Gene 87:23–29 [CrossRef]
    [Google Scholar]
  60. Wright F., Bibb M. J. 1992; Codon usage in the G+C-rich Streptomyces genome. Gene 113:55–65 [CrossRef]
    [Google Scholar]
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