Skip to main content
PMC home page
Nucleic Acids Research logoLink to Nucleic Acids Research
. 1994 Mar 25;22(6):929–936. doi: 10.1093/nar/22.6.929

Divergence in codon usage of Lactobacillus species.

P H Pouwels 1, J A Leunissen 1
PMCID: PMC307911  PMID: 8152923

Abstract

We have analyzed codon usage patterns of 70 sequenced genes from different Lactobacillus species. Codon usage in lactobacilli is highly biased. Both inter-species and intra-species heterogeneity of codon usage bias was observed. Codon usage in L. acidophilus is similar to that in L. helveticus, but dissimilar to that in L. bulgaricus, L. casei, L. pentosus and L. plantarum. Codon usage in the latter three organisms is not significantly different, but is different from that in L. bulgaricus. Inter-species differences in codon usage can, at least in part, be explained by differences in mutational drift. L. bulgaricus shows GC drift, whereas all other species show AT drift. L. acidophilus and L. helveticus rarely use NNG in family-box (a set of synonymous) codons, in contrast to all other species. This result may be explained by assuming that L. acidophilus and L. helveticus, but not other species examined, use a single tRNA species for translation of family-box codons. Differences in expression level of genes are positively correlated with codon usage bias. Highly expressed genes show highly biased codon usage, whereas weakly expressed genes show much less biased codon usage. Codon usage patterns at the 5'-end of Lactobacillus genes is not significantly different from that of entire genes. The GC content of codons 2-6 is significantly reduced compared with that of the remainder of the gene. The possible implications of a reduced GC content for the control of translation efficiency are discussed.

Full text

PDF
929

Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Andersson S. G., Kurland C. G. Codon preferences in free-living microorganisms. Microbiol Rev. 1990 Jun;54(2):198–210. doi: 10.1128/mr.54.2.198-210.1990. [DOI] [PMC free article] [PubMed] [Google Scholar]
  2. Bennetzen J. L., Hall B. D. Codon selection in yeast. J Biol Chem. 1982 Mar 25;257(6):3026–3031. [PubMed] [Google Scholar]
  3. Boot H. J., Kolen C. P., van Noort J. M., Pouwels P. H. S-layer protein of Lactobacillus acidophilus ATCC 4356: purification, expression in Escherichia coli, and nucleotide sequence of the corresponding gene. J Bacteriol. 1993 Oct;175(19):6089–6096. doi: 10.1128/jb.175.19.6089-6096.1993. [DOI] [PMC free article] [PubMed] [Google Scholar]
  4. Curran J. F., Yarus M. Rates of aminoacyl-tRNA selection at 29 sense codons in vivo. J Mol Biol. 1989 Sep 5;209(1):65–77. doi: 10.1016/0022-2836(89)90170-8. [DOI] [PubMed] [Google Scholar]
  5. Devereux J., Haeberli P., Smithies O. A comprehensive set of sequence analysis programs for the VAX. Nucleic Acids Res. 1984 Jan 11;12(1 Pt 1):387–395. doi: 10.1093/nar/12.1part1.387. [DOI] [PMC free article] [PubMed] [Google Scholar]
  6. Dreyfus M. What constitutes the signal for the initiation of protein synthesis on Escherichia coli mRNAs? J Mol Biol. 1988 Nov 5;204(1):79–94. doi: 10.1016/0022-2836(88)90601-8. [DOI] [PubMed] [Google Scholar]
  7. Eyre-Walker A., Bulmer M. Reduced synonymous substitution rate at the start of enterobacterial genes. Nucleic Acids Res. 1993 Sep 25;21(19):4599–4603. doi: 10.1093/nar/21.19.4599. [DOI] [PMC free article] [PubMed] [Google Scholar]
  8. Gold L. Posttranscriptional regulatory mechanisms in Escherichia coli. Annu Rev Biochem. 1988;57:199–233. doi: 10.1146/annurev.bi.57.070188.001215. [DOI] [PubMed] [Google Scholar]
  9. Gouy M., Gautier C. Codon usage in bacteria: correlation with gene expressivity. Nucleic Acids Res. 1982 Nov 25;10(22):7055–7074. doi: 10.1093/nar/10.22.7055. [DOI] [PMC free article] [PubMed] [Google Scholar]
  10. Grantham R., Gautier C., Gouy M., Mercier R., Pavé A. Codon catalog usage and the genome hypothesis. Nucleic Acids Res. 1980 Jan 11;8(1):r49–r62. doi: 10.1093/nar/8.1.197-c. [DOI] [PMC free article] [PubMed] [Google Scholar]
  11. Grosjean H., Fiers W. Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene. 1982 Jun;18(3):199–209. doi: 10.1016/0378-1119(82)90157-3. [DOI] [PubMed] [Google Scholar]
  12. Gruss A., Ehrlich S. D. The family of highly interrelated single-stranded deoxyribonucleic acid plasmids. Microbiol Rev. 1989 Jun;53(2):231–241. doi: 10.1128/mr.53.2.231-241.1989. [DOI] [PMC free article] [PubMed] [Google Scholar]
  13. Hensel R., Mayr U., Stetter K. O., Kandler O. Comparative studies of lactic acid dehydrogenases in lactic acid bacteria. I. Purification and kinetics of the allosteric L-lactic acid dehydrogenase from Lactobacillus casei ssp. casei and Lactobacillus curvatus. Arch Microbiol. 1977 Feb 4;112(1):81–93. doi: 10.1007/BF00446658. [DOI] [PubMed] [Google Scholar]
  14. Higgins D. G. Sequence ordinations: a multivariate analysis approach to analysing large sequence data sets. Comput Appl Biosci. 1992 Feb;8(1):15–22. doi: 10.1093/bioinformatics/8.1.15. [DOI] [PubMed] [Google Scholar]
  15. Hyde J. E., Sims P. F. Anomalous dinucleotide frequencies in both coding and non-coding regions from the genome of the human malaria parasite Plasmodium falciparum. Gene. 1987;61(2):177–187. doi: 10.1016/0378-1119(87)90112-0. [DOI] [PubMed] [Google Scholar]
  16. Ikemura T. Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol. 1985 Jan;2(1):13–34. doi: 10.1093/oxfordjournals.molbev.a040335. [DOI] [PubMed] [Google Scholar]
  17. Ikemura T. Correlation between the abundance of Escherichia coli transfer RNAs and the occurrence of the respective codons in its protein genes. J Mol Biol. 1981 Feb 15;146(1):1–21. doi: 10.1016/0022-2836(81)90363-6. [DOI] [PubMed] [Google Scholar]
  18. Looman A. C., Bodlaender J., Comstock L. J., Eaton D., Jhurani P., de Boer H. A., van Knippenberg P. H. Influence of the codon following the AUG initiation codon on the expression of a modified lacZ gene in Escherichia coli. EMBO J. 1987 Aug;6(8):2489–2492. doi: 10.1002/j.1460-2075.1987.tb02530.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  19. Muto A., Osawa S. The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci U S A. 1987 Jan;84(1):166–169. doi: 10.1073/pnas.84.1.166. [DOI] [PMC free article] [PubMed] [Google Scholar]
  20. 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 Mar 25;18(6):1565–1569. doi: 10.1093/nar/18.6.1565. [DOI] [PMC free article] [PubMed] [Google Scholar]
  21. Osawa S., Jukes T. H., Muto A., Yamao F., Ohama T., Andachi Y. Role of directional mutation pressure in the evolution of the eubacterial genetic code. Cold Spring Harb Symp Quant Biol. 1987;52:777–789. doi: 10.1101/sqb.1987.052.01.087. [DOI] [PubMed] [Google Scholar]
  22. Osawa S., Muto A., Ohama T., Andachi Y., Tanaka R., Yamao F. Prokaryotic genetic code. Experientia. 1990 Dec 1;46(11-12):1097–1106. doi: 10.1007/BF01936919. [DOI] [PubMed] [Google Scholar]
  23. Pedersen S. Escherichia coli ribosomes translate in vivo with variable rate. EMBO J. 1984 Dec 1;3(12):2895–2898. doi: 10.1002/j.1460-2075.1984.tb02227.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
  24. Pittet A. C., Hottinger H. Sequence of a hexameric tRNA gene cluster associated with rRNA genes in Lactobacillus bulgaricus. Nucleic Acids Res. 1989 Jun 26;17(12):4873–4873. [PMC free article] [PubMed] [Google Scholar]
  25. Projan S. J., Novick R. Comparative analysis of five related Staphylococcal plasmids. Plasmid. 1988 May;19(3):203–221. doi: 10.1016/0147-619x(88)90039-x. [DOI] [PubMed] [Google Scholar]
  26. Rodier F., Gabarro-Arpa J., Ehrlich R., Reiss C. Key for protein coding sequences identification: computer analysis of codon strategy. Nucleic Acids Res. 1982 Jan 11;10(1):391–402. doi: 10.1093/nar/10.1.391. [DOI] [PMC free article] [PubMed] [Google Scholar]
  27. Saul A., Battistutta D. Codon usage in Plasmodium falciparum. Mol Biochem Parasitol. 1988 Jan 1;27(1):35–42. doi: 10.1016/0166-6851(88)90022-9. [DOI] [PubMed] [Google Scholar]
  28. Scherer G. F., Walkinshaw M. D., Arnott S., Morré D. J. The ribosome binding sites recognized by E. coli ribosomes have regions with signal character in both the leader and protein coding segments. Nucleic Acids Res. 1980 Sep 11;8(17):3895–3907. doi: 10.1093/nar/8.17.3895. [DOI] [PMC free article] [PubMed] [Google Scholar]
  29. Sharp P. M., Cowe E., Higgins D. G., Shields D. C., 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 Sep 12;16(17):8207–8211. doi: 10.1093/nar/16.17.8207. [DOI] [PMC free article] [PubMed] [Google Scholar]
  30. Sharp P. M., Devine K. M. Codon usage and gene expression level in Dictyostelium discoideum: highly expressed genes do 'prefer' optimal codons. Nucleic Acids Res. 1989 Jul 11;17(13):5029–5039. doi: 10.1093/nar/17.13.5029. [DOI] [PMC free article] [PubMed] [Google Scholar]
  31. 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 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
  32. Shepherd J. C. From primeval message to present-day gene. Cold Spring Harb Symp Quant Biol. 1983;47(Pt 2):1099–1108. doi: 10.1101/sqb.1983.047.01.124. [DOI] [PubMed] [Google Scholar]
  33. Shields D. C., Sharp P. M. Synonymous codon usage in Bacillus subtilis reflects both translational selection and mutational biases. Nucleic Acids Res. 1987 Oct 12;15(19):8023–8040. doi: 10.1093/nar/15.19.8023. [DOI] [PMC free article] [PubMed] [Google Scholar]
  34. Sueoka N. Directional mutation pressure and neutral molecular evolution. Proc Natl Acad Sci U S A. 1988 Apr;85(8):2653–2657. doi: 10.1073/pnas.85.8.2653. [DOI] [PMC free article] [PubMed] [Google Scholar]
  35. Trifonov E. N. Translation framing code and frame-monitoring mechanism as suggested by the analysis of mRNA and 16 S rRNA nucleotide sequences. J Mol Biol. 1987 Apr 20;194(4):643–652. doi: 10.1016/0022-2836(87)90241-5. [DOI] [PubMed] [Google Scholar]
  36. Vidgrén G., Palva I., Pakkanen R., Lounatmaa K., Palva A. S-layer protein gene of Lactobacillus brevis: cloning by polymerase chain reaction and determination of the nucleotide sequence. J Bacteriol. 1992 Nov;174(22):7419–7427. doi: 10.1128/jb.174.22.7419-7427.1992. [DOI] [PMC free article] [PubMed] [Google Scholar]
  37. Wright F., Bibb M. J. Codon usage in the G+C-rich Streptomyces genome. Gene. 1992 Apr 1;113(1):55–65. doi: 10.1016/0378-1119(92)90669-g. [DOI] [PubMed] [Google Scholar]
  38. de Smit M. H., van Duin J. Control of prokaryotic translational initiation by mRNA secondary structure. Prog Nucleic Acid Res Mol Biol. 1990;38:1–35. doi: 10.1016/s0079-6603(08)60707-2. [DOI] [PubMed] [Google Scholar]

Articles from Nucleic Acids Research are provided here courtesy of Oxford University Press

RESOURCES