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Volume 142, Issue 4

Codon usage in the complex Free

Abstract

The usage of alternative synonymous codons in (and genes has been investigated. This species is a member of the high-G + C Gram-positive bacteria, with a genomic G + C content around 65 mol%. This G + C-richness is reflected in a strong bias towards C- and Gending codons for every amino acid: overall, the G + C content at the third positions of codons is 83%. However, there is significant variation in codon usage patterns among genes, which appears to be associated with gene expression level. From the variation among genes, putative optimal codons were identified for 15 amino acids. The degree of bias towards optimal codons in an gene is correlated with that in homologues from and . The set of selectively favoured codons seems to be quite highly conserved between and another high-G + C Gram-positive bacterium, Corynebacterium , even though the genome and overall codon usage of the latter are much less G + C-rich.

  • Received:
  • Accepted:
  • Revised:
  • Published Online:
Keyword(s): codon usage , intein , molecular evolution and Mycobacterium tuberculosis
© Society for General Microbiology 1996
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1996-04-01
2024-04-18
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References

  1. Aldovini A., Husson R.N., Young R.A. The uraA locus and homologous recombination in Mycobacterium bovis BCG. J Bacteriol 1993; 175:7282–7289
     [Google Scholar]
  2. Altschul S.F., Gish W., Miller W., Myers E.W., Lipman D.J. Basic local alignment search tool. J Mol Biol 1990; 215:403–410
     [Google Scholar]
  3. Andersen A.B., Hansen E.B. Structure and mapping of antigenic domains of protein antigen b, a 38, 000-molecular-weight protein of Mycobacterium tuberculosis. Infect Immun 1989; 57:2481–2488
     [Google Scholar]
  4. Andersen A.B., Hansen E.B. Cloning of the lysA gene from Mycobacterium tuberculosis. Gene 1993; 124:105–109
     [Google Scholar]
  5. Andersen A.B., Andersen P., Ljungqvist L. Structure and function of a 40, 000-molecular-weight protein antigen of Mycobacterium tuberculosis. Infect Immun 1992; 60:2317–2323
     [Google Scholar]
  6. Andersson S.G.E., Kurland C.G. Codon preferences in free-living microorganisms. Microbiol Rev 1990; 54:198–210
     [Google Scholar]
  7. Baird P.N., Hall L.M.C., Coates A.R.M. Cloning and sequence analysis of the 10 kDa antigen gene of Mycobacterium tuberculosis. J Gen Microbiol 1989; 135:931–939
     [Google Scholar]
  8. Banerjee A., Dubnau E., Quemard A., Balasubramanian V., Um K.S., Wilson T., Collins D., De Lisle G., Jacobs W.R. Jr inhA, a gene encoding a target for isoniazid and ethionamide in Mycobacterium tuberculosis. Science 1994; 263:227–230
     [Google Scholar]
  9. Bergh S., Cole S.T. MycDB: an integrated mycobacterial database. Mol Microbiol 1994; 12:517–534
     [Google Scholar]
  10. Bloom B.R., Murray C.J.L. Tuberculosis - commentary on a reemergent killer. Science 1992; 257:1055–1064
     [Google Scholar]
  11. Carlin N.I., Lofdahl S., Magnusson M. Monoclonal antibodies specific for elongation factor Tu and complete nucleotide sequence of the tuf gene in Mycobacterium tuberculosis. Infect Immun 1992; 60:3136–3142
     [Google Scholar]
  12. Cirillo J.D., Weisbrod T.R., Banerjee A., Bloom B.R., Jacobs W.R. Jr Genetic determination of the meso-diaminopimelate biosynthetic pathway of mycobacteria. J Bacteriol 1994a; 176:4424–4429
     [Google Scholar]
  13. Cirillo J.D., Weisbrod T.R., Pascopella L., Bloom B.R., Jacobs W.R. Jr Isolation and characterization of the aspartokinase and aspartate semialdehyde dehydrogenase operon from mycobacteria. Mol Microbiol 1994b; 11:629–639
     [Google Scholar]
  14. Coates A.R.M., Shinnick T.M., Ellis R.J. Chaperonin nomenclature. Mol Microbiol 1993; 8:787
     [Google Scholar]
  15. Cockerill F.R., Uhl J.R., Temesgen Z., Zhang Y., Stockman L., Roberts G.D., Williams D.L., Kline B.C. Rapid identification of a point mutation of the Mycobacterium tuberculosis catalase-peroxidase (katG) gene associated with isoniazid resistance. J Infect Dis 1995; 171:240–245
     [Google Scholar]
  16. Collins M.E., Patki A., Wall S., Nolan A., Goodger J., Woodward M.J., Dale J.W. Cloning and characterization of the gene for the ‘ 19 kDa ’ antigen of Mycobacterium bovis. J Gen Microbiol 1990; 136:1429–1436
     [Google Scholar]
  17. Coque J.-J., R., Malumbres M., Martin J.F., Liras P. Analysis of the codon usage of the cephamycin C producer Nocardia lactamdurans. FEMS Microbiol Lett 1993; 110:91–96
     [Google Scholar]
  18. Curran J.F., Yarus M. Rates of aa-tRNA selection at 29 sense codons in vivo. J Mol Biol 1989; 209:65–77
     [Google Scholar]
  19. Davis E.O., Sedgwick S.G., Colston M.J. Novel structure of the recA locus of Mycobacterium tuberculosis implies processing of the gene product. J Bacteriol 1991; 173:5653–5662
     [Google Scholar]
  20. Davis E.O., Thangaraj H.S., Brooks P.C., Colston M.J. Evidence of selection for protein introns in the recAs of pathogenic mycobacteria. EMBO J 1994; 13:699–703
     [Google Scholar]
  21. Eikmanns B.J. Identification, sequence analysis, and expression of a Corynebacterium glutamicum gene cluster encoding the three glycolytic enzymes glyceraldehyde-3-phosphate dehydrogenase, 3-phosphoglycerate kinase, and triose phosphate isomerase. J Bacteriol 1992; 174:6076–6086
     [Google Scholar]
  22. Garbe T., Jones C., Charles I., Dougan G., Young D.B. Cloning and characterization of the aroA gene from Mycobacterium tuberculosis. J Bacteriol 1990; 172:6774–6782
     [Google Scholar]
  23. Garbe T., Servos S., Hawkins A., Dimitriadis G., Young D., Dougan G., Charles I. The Mycobacterium tuberculosis shikimate pathway genes: evolutionary relationship between biosynthetic and catabolic 3-dehydroquinases. Mol & Gen Genet 1991; 228:385–392
     [Google Scholar]
  24. Gouy M., Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Rit 1982; 10:7055–7074
     [Google Scholar]
  25. Gouy M., Gautier C., Attimonelli M., Lanave C., Di Paola G. acnuc - a portable retrieval system for nucleic acid sequence databases: logical and physical designs and usage. Comput Appl Biosci 1985; 1:167–172
     [Google Scholar]
  26. Grange J.M., Gibson J., Osborn T.W., Collins C.H., Yates M.D. What is BCG. Tubercle 1983; 64:129–139
     [Google Scholar]
  27. Grantham R., Gautier C., Gouy M., Jacobzone M., Mercier R. Codon catalog usage is a genomic strategy modulated for gene expressivity. Nucleic Acids Res 1981; 9:r43–r74
     [Google Scholar]
  28. Greenacre M.J. Theory and Applications of Correspondence Analysis 1984 London: Academic Press;
     [Google Scholar]
  29. Hall B.G., Sharp P.M. Molecular population genetics of Escherichia coli: DNA sequence diversity at the celC, err, and gutB loci of natural isolates. Mol Biol Evol 1992; 9:654–665
     [Google Scholar]
  30. Holm L. Codon usage and gene expression. Nucleic Acids Res 1986; 14:3075–3087
     [Google Scholar]
  31. Honore N., Bergh S., Chanteau S., Doucet-Populaire F., Eiglmeier K., Garnier T., Georges C., Launois P., Limpaiboon T., Newton S., Niang K., del Portillo P., Ramesh G.R., Reddi P., Ridel P.R., Sittisombut N., Wu-Hunter S., Cole S.T. Nucleotide sequence of the first cosmid from the Mycobacterium leprae genome project: structure and function of the Rif-Str regions. Mol Microbiol 1993; 7:207–214
     [Google Scholar]
  32. Ikemura T. 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 1981; 151:389–409
     [Google Scholar]
  33. Kong T.H., Coates A.R.M., Butcher P.D., Hickman C.J., Shinnick T.M. Mycobacterium tuberculosis expresses two chaperonin-60 homologs. Troc Natl Acad Sci USA 1993; 90:2608–2612
     [Google Scholar]
  34. Labuda D., Grosjean H., Striker G., Porschke D. Codon-anticodon and anticodon-anticodon interaction - evaluation of equilibrium and kinetic parameters of complexes involving a G-U wobble. Biochim Biophys Acta 1982; 698:230–236
     [Google Scholar]
  35. Leao S.C., Rocha C.L., Murillo L.A., Parra C.A., Patarroyo M.E. A species-specific nucleotide sequence of Mycobacterium tuberculosis encodes a protein that exhibits hemolytic activity when expressed in Escherichia coli. Infect Immun 1995; 63:4301–4306
     [Google Scholar]
  36. Lloyd A.T., Sharp P.M. codons: a microcomputer program for codon usage analysis. J Hered 1992; 83:239–240
     [Google Scholar]
  37. Malumbres M., Gil J.A., Martin J.F. Codon preference in corynebacteria. Gene 1993; 134:15–24
     [Google Scholar]
  38. Mathur M., Kolattukudy P.E. Molecular cloning and sequencing of the gene for mycocerosic acid synthase, a novel fatty acid elongating multifunctional enzyme, from Mycobacterium tuberculosis var. bovis Bacillus Calmette-Guerin. J Biol Chem 1992; 267:19388–19395
     [Google Scholar]
  39. Medigue G., Rouxel T., Vigier P., Henaut A., Danchin A. Evidence for horizontal gene transfer in Escherichia coli spéciation. J Mol Biol 1991; 222:851–856
     [Google Scholar]
  40. Merino E., Baibas P., Puente J.L., Bolivar F. Antisense overlapping open reading frames in genes from bacteria to humans. Nucleic Acids Res 1994; 22:1903–1908
     [Google Scholar]
  41. Miller L.P., Crawford J.T., Shinnick T.M. The rpoB gene of Mycobacterium tuberculosis. Antimicrob Agents Chemother 1994; 38:805–811
     [Google Scholar]
  42. Mizrahi V., Huberts P., Dawes S.S., Dudding L.R. A PCR method for the sequence analysis of the gyrA, polA and rnhA gene segments from mycobacteria. Gene 1993; 136:287–290
     [Google Scholar]
  43. Nair J., Rouse D.A., Bai G.H., Morris S.L. The rpsL gene and streptomycin resistance in single and multiple drug-resistant strains of Mycobacterium tuberculosis. Mol Microbiol 1993; 10:521–527
     [Google Scholar]
  44. Norman E., De Smet K.A., Stoker N.G., Ratledge C., Wheeler P.R., Dale J.W. Lipid synthesis in mycobacteria: characterization of the biotin carboxyl carrier protein genes from Mycobacterium leprae and M. tuberculosis. J Bacteriol 1994; 176:2525–2531
     [Google Scholar]
  45. O'Connor S.P., Rumschlag H.S., Mayer L.W. Nucleotide sequence of the gene encoding the 35-kDa protein of Mycobacterium tuberculosis. Rat Microbiol 1990; 141:407–423
     [Google Scholar]
  46. Ohama T., Muto A., Osawa S. Role of GC-biased mutation pressure on synonymous codon choice in Micrococcus luteus, a bacterium with a high genomic GC-content. Nucleic Acids Res 1990; 18:1565–1569
     [Google Scholar]
  47. Ohara N., Kimura M., Higashi Y., Yamada T. Isolation and amino acid sequence of the 30S ribosomal protein SI 9 from Mycobacterium bovis BCG. FEBS Lett 1993a; 331:9–14
     [Google Scholar]
  48. Ohara N., Kimura M., Wada N., Yamada T. Cloning and sequencing of the gene encoding the ribosomal L7/L12-like protein of Mycobacterium bovis BCG. Nucleic Acids Res 1993b; 21:3579
     [Google Scholar]
  49. Ohkubo S., Muto A., Kawauchi Y., Yamao F., Osawa S. The ribosomal protein gene cluster of Mycoplasma capricolum. Mol & Gen Genet 1987; 210:314–322
     [Google Scholar]
  50. Olsen G.J., Woese C.R., Overbeek R. The winds of (evolutionary) change: breathing new life into microbiology. J Bacteriol 1994; 176:1–6
     [Google Scholar]
  51. Osawa S., Jukes T.H., Watanabe K., Muto A. Recent evidence for evolution of the genetic code. Microbiol Rev 1992; 56:229–264
     [Google Scholar]
  52. Perler F.B., Davis E.O., Dean G.E., Gimble F.S., Jack W.E., Neff N., Noren G.J., Thorner J., Belfort M. Protein-splicing elements: inteins and exteins - a definition of terms and recommended nomenclature. Nucleic Acids Rtfj 1994; 22:1125–1127
     [Google Scholar]
  53. Plunkett G., Burland V., Daniels D.L., Blattner F.R. Analysis of the Escherichia coli genome III DNA sequence of the region from 87-2 to 89-2 minutes. Nucleic Acids Res 1993; 21:3391–3398
     [Google Scholar]
  54. Sharp P.M. Does the ‘non-coding’ strand code. Nucleic Acids Res 1985; 13:1389–1397
     [Google Scholar]
  55. Sharp P.M., Devine K.M. Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do ‘prefer’ optimal codons. Nucleic Acids Rw 1989; 17:5029–5039
     [Google Scholar]
  56. Sharp P.M., Li W.-H. The Codon Adaptation Index - a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res 1987; 15:1281–1295
     [Google Scholar]
  57. Sharp P.M., Cowe E., Higgins D.G., Shields D.G., Wolfe K.H., Wright F. Codon usage patterns in Escherichia coli, Bacillus subtilis, Saccharomyces cerevisiae, Schizosaccharomyces pombe, Drosophila melanogaster and Homo sapiens: a review of the considerable within-species diversity. Nucleic Acids Res 1988; 16:8207–8211
     [Google Scholar]
  58. Sharp P.M., Higgins D.G., Shields D.G., Devine K.M., Hoch J.A. Bacillus subtilis gene sequences. In Genetics and Biotechnology of Bacilli 1990 Edited by Zukowski M.M., Ganesan A.T., Hoch J.A. San Diego: Academic Press; pp 89–98
     [Google Scholar]
  59. Sharp P.M., Stenico M., Peden J.F., Lloyd A.T. Codon usage: mutational bias, translational selection, or both. Biochem Soc Trans 1993; 21:835–841
     [Google Scholar]
  60. Shields D.C. Switches in species-specific codon preferences: the influence of mutation biases. J Mol Evol 1990; 31:71–80
     [Google Scholar]
  61. Shields D.C., Sharp P.M. Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Res 1987; 15:8023–8040
     [Google Scholar]
  62. Shinnick T.M. The 65-kilodalton antigen of Mycobacterium tuberculosis. J Bacteriol 1987; 169:1080–1088
     [Google Scholar]
  63. Stelandre M., Bosseloir Y., De Bruyn J., Maes P., Content J. Cloning and sequence analysis of the gene encoding an NADP-dependent alcohol dehydrogenase in Mycobacterium bovis BCG. Gene 1992; 121:79–86
     [Google Scholar]
  64. Takiff H.E., Salazar L., Guerrero C., Philipp W., Huang W.M., Kreiswirth B., Cole S.T., Jacobs W.R. Jr, Telenti A. Cloning and nucleotide sequence of Mycobacterium tuberculosis gyrA and gyrB genes and detection of quinolone resistance mutations. Antimicrob Agents Chemother 1994; 38:773–780
     [Google Scholar]
  65. Thole J.E.R., Keulen W.J., Kolk A.H.J., Groothuis D.G., Berwald L.G., Tiesjema R.H., Van Embden J.D.A. Characterization, sequence determination, and immunogenicity of a 64-kilodalton protein of Mycobacterium bovis BCG expressed in Escherichia coli K-12. Infect Immun 1987; 55:1466–1475
     [Google Scholar]
  66. Thomas L.K., Dix D.B., Thompson R.C. Codon choice and gene expression: synonymous codons differ in their ability to direct aminoacylated-transfer RNA binding to ribosomes in vitro. Troc Natl Acad Sei USA 1988; 85:4242–4246
     [Google Scholar]
  67. Thompson J.D., Higgins D.G., Gibson T.J. clustal w - improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Rw 1994; 22:4673–4680
     [Google Scholar]
  68. Timm J., Van Rompaey I., Tricot C., Massaer M., Haeseleer F., Fauconnier A., Stalon V., Bollen A., Jacobs P. Molecular cloning, characterization and purification of ornithine carbamoyl-transferase from Mycobacterium bovis BCG. Mol & Gen Genet 1992; 234:475–480
     [Google Scholar]
  69. Wada K.-n., Wada Y., Ishibashi F., Gojobori T., Ikemura T. Codon usage tabulated from the GenBank genetic sequence data. Nucleic Acids Rîj 1992; 20:2111–2118
     [Google Scholar]
  70. Wright F. The ‘effective number of codons ’ used in a gene. Gene 1990; 87:23–29
     [Google Scholar]
  71. Wright F., Bibb M.J. Codon usage in the G + C-rich Streptomyces genome. Gent 1992; 113:55–65
     [Google Scholar]
  72. Yamaguchi R., Matsuo K., Yamazaki A., Nagai S., Terasaka K., Yamada T. Immunogenic protein MPB57 from Mycobacterium bovis BCG: molecular cloning, nucleotide sequence and expression. FEBS Lett 1988; 240:115–117
     [Google Scholar]
  73. Yang F., Lu G., Rubin H. Isolation of ribonucleotide reductase from Mycobacterium tuberculosis and cloning, expression, and purification of the large subunit. J Bacteriol 1994; 176:6738–6743
     [Google Scholar]
  74. Young D., Lathigra R., Hendrix R., Sweetser D., Young R.A. Stress proteins are immune targets in leprosy and tuberculosis. Proc Natl Acad Sci USA 1988; 85:4267–4270
     [Google Scholar]
  75. Young D.B., Kaufmann S.H.E., Hermans P.W.M., Thole J.E.R. Mycobacterial protein antigens: a compilation. Mol Microbiol 1992; 6:133–145
     [Google Scholar]
  76. Zhang Y., Lathigra R., Garbe T., Catty D., Young D. Genetic analysis of superoxide dismutase, the 23 kilodalton antigen of Mycobacterium tuberculosis. Mol Microbiol 1991; 5:381–391
     [Google Scholar]
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Codon usage in the Mycobacterium tuberculosis complex
Microbiology 142, 915 (1996); https://doi.org/10.1099/00221287-142-4-915
/content/journal/micro/10.1099/00221287-142-4-915
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