Journal of Molecular Evolution

, Volume 75, Issue 1–2, pp 34–42 | Cite as

Transfer RNA Gene Numbers may not be Completely Responsible for the Codon Usage Bias in Asparagine, Isoleucine, Phenylalanine, and Tyrosine in the High Expression Genes in Bacteria

  • Siddhartha Sankar Satapathy
  • Malay Dutta
  • Alak Kumar Buragohain
  • Suvendra Kumar Ray


It is generally believed that the effect of translational selection on codon usage bias is related to the number of transfer RNA genes in bacteria, which is more with respect to the high expression genes than the whole genome. Keeping this in the background, we analyzed codon usage bias with respect to asparagine, isoleucine, phenylalanine, and tyrosine amino acids. Analysis was done in seventeen bacteria with the available gene expression data and information about the tRNA gene number. In most of the bacteria, it was observed that codon usage bias and tRNA gene number were not in agreement, which was unexpected. We extended the study further to 199 bacteria, limiting to the codon usage bias in the two highly expressed genes rpoB and rpoC which encode the RNA polymerase subunits β and β′, respectively. In concordance with the result in the high expression genes, codon usage bias in rpoB and rpoC genes was also found to not be in agreement with tRNA gene number in many of these bacteria. Our study indicates that tRNA gene numbers may not be the sole determining factor for translational selection of codon usage bias in bacterial genomes.


Codon usage bias Gene expression Translational selection tRNA gene number 



We thank Dr. Supek, the Rudjer Boskovic Institute, Croatia, for providing information for retrieving transcriptome data from the NCBI. We extend our thanks to Mrs. Madhusmita Dash, Qr. No. C-83, Tezpur University, for writing the C program for rank calculation. We also thank Dr. B.R. Powdel, Darang College, Tezpur, for his comments on the manuscript. We thank the two anonymous reviewers for their helpful comments on the previous version of this manuscript.

Supplementary material

239_2012_9524_MOESM1_ESM.doc (700 kb)
Supplementary material 1 (DOC 700 kb)
239_2012_9524_MOESM2_ESM.doc (58 kb)
Supplementary material 2 (DOC 57 kb)


  1. Arnold HH, Keith G (1977) The nucleotide sequence of phenylalanine tRNA from Bacillus subtilis. Nucl Acids Res 4:2821–2829PubMedCrossRefGoogle Scholar
  2. Bossi L, Roth JR (1980) The influence of codon context on genetic code translation. Nature 286:123–127PubMedCrossRefGoogle Scholar
  3. Bulmer M (1987) Coevolution of codon usage and tRNA abundance. Nature 325:728–730PubMedCrossRefGoogle Scholar
  4. Bulmer M (1991) The selection–mutation–drift theory of synonymous codon usage. Genetics 129:897–907PubMedGoogle Scholar
  5. Chen SL, Lee W, Hottes AK, Shapiro L, McAdams HH (2004) Codon usage between genomes is constrained by genome wide mutational processes. Proc Natl Acad Sci USA 101:3480–3485PubMedCrossRefGoogle Scholar
  6. Dong H, Nilsson L, Kurland CG (1996) Co-variation of tRNA abundance and codon usage in Escherichia coli at different growth rates. J Mol Biol 260:649–663PubMedCrossRefGoogle Scholar
  7. dos Reis M, Wernisch L (2009) Estimating translational selection in eukaryotic genomes. Mol Biol Evol 26:451–461PubMedCrossRefGoogle Scholar
  8. Duret L (2000) tRNA gene number and codon usage in the C. elegans genome are co-adapted for optimal translation of highly expressed genes. Trends Genet 16:287–289PubMedCrossRefGoogle Scholar
  9. Ermolaeva MD (2001) Synonymous codon usage in bacteria. Curr Issues Mol Biol 3:91–97PubMedGoogle Scholar
  10. Fedorov A, Saxonov S, Gilbert W (2002) Regularities of context-dependent codon bias in eukaryotic genes. Nucl Acids Res 30:1192–1197PubMedCrossRefGoogle Scholar
  11. Francino MP, Ochman H (1997) Strand asymmetries in DNA evolution. Trends Genet 13:240–245PubMedCrossRefGoogle Scholar
  12. Gelfand MS, Koonin EV (1997) Avoidance of palindromic words in bacterial and archaeal genomes: a close connection with restriction enzymes. Nucl Acids Res 25:2430–2439PubMedCrossRefGoogle Scholar
  13. Gouy M (1987) Codon contexts in enterobacterial and coliphage genes. Mol Biol Evol 4:426–444PubMedGoogle Scholar
  14. Gouy M, Gautier C (1982) Codon usage in bacteria: correlation with gene expressivity. Nucl Acids Res 10:7055–7074PubMedCrossRefGoogle Scholar
  15. Grosjean H, Fiers W (1982) Preferential codon usage in prokaryotic genes: the optimal codon-anticodon interaction energy and the selective codon usage in efficiently expressed genes. Gene 18:199–209PubMedCrossRefGoogle Scholar
  16. Harada F, Nishimura S (1972) Possible anticodon sequences of tRNAhis, tRNAasn, and tRNAasp from Escherichia coli B. Universal presence of nucleoside Q in the first position of the anticodon of these transfer ribonucleic acids. Biochemistry 11:301–308PubMedCrossRefGoogle Scholar
  17. Hershberg R, Petrov DA (2009) General rules for optimal codon choice. PLoS Genet 5:e1000556PubMedCrossRefGoogle Scholar
  18. Hershberg R, Petrov DA (2010) Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6:e1001115PubMedCrossRefGoogle Scholar
  19. Higgs PG, Ran W (2008) Coevolution of codon usage and tRNA genes leads to alternative stable states of biased codon usage. Mol Biol Evol 25:2279–2291PubMedCrossRefGoogle Scholar
  20. Hildebrand F, Meyer A, Eyre-Walker A (2010) Evidence of selection upon genomic GC-content in bacteria. PLoS Genet 6:e1001107PubMedCrossRefGoogle Scholar
  21. Ikemura T (1981) 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 151:389–409PubMedCrossRefGoogle Scholar
  22. Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34PubMedGoogle Scholar
  23. Ishihama Y, Schmidt T, Rappsilber J, Mann M, Hartl FU, Kerner MJ, Frishman D (2008) Protein abundance profiling of the Escherichia coli cytosol. BMC Genomics 9:102PubMedCrossRefGoogle Scholar
  24. Kanaya S, Yamada Y, Kudo Y, Ikemura T (1999) Studies of codon usage and tRNA genes of 18 unicellular organisms and quantification of Bacillus subtilis tRNAs: gene expression level and species specific diversity of codon usage based on multivariate analysis. Gene 238:143–155PubMedCrossRefGoogle Scholar
  25. Karlin S, Campbell AM, Mrázek J (1998) Comparative DNA analysis across diverse genomes. Annu Rev Genet 32:185–225PubMedCrossRefGoogle Scholar
  26. Lowe TM, Eddy SR (1997) tRNAscan-SE: a program for improved detection of transfer RNA genes in genome sequences. Nucl Acid Res 25:955–964Google Scholar
  27. Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169PubMedCrossRefGoogle Scholar
  28. Osawa S, Jukes TH, Watanabe K, Muto A (1992) Recent evidence for evolution of the genetic code. Microbiol Rev 56:229–264PubMedGoogle Scholar
  29. Percudani R, Pavesi A, Ottonello S (1997) Transfer RNA gene redundancy and translational selection in Saccharomyces cerevisiae. J Mol Biol 268:322–330PubMedCrossRefGoogle Scholar
  30. Ran W, Higgs PG (2010) The influence of anticodon–codon interactions and modified bases on codon usage bias in bacteria. Mol Biol Evol 27:2129–2140PubMedCrossRefGoogle Scholar
  31. Rocha EPC (2004) Codon usage bias from tRNA’s point of view, redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14:2279–2286PubMedCrossRefGoogle Scholar
  32. Rocha EPC, Feil EJ (2010) Mutational patterns cannot explain genome composition: are there any neutral sites in the genomes of bacteria? PLoS Genet 6:e1001104PubMedCrossRefGoogle Scholar
  33. Salser W (1969) The influence of the reading context upon the suppression of nonsense codons. Mol Gen Genet 105:125–130PubMedCrossRefGoogle Scholar
  34. Sharp PM, Li WH (1986a) An evolutionary perspective on synonymous codon usage in unicellular organisms. J Mol Evol 24:28–38PubMedCrossRefGoogle Scholar
  35. Sharp PM, Li WH (1986b) Codon usage in regulatory genes in Escherichia coli does not reflect selection for “rare” codons. Nucl Acids Res 14:7737–7749PubMedCrossRefGoogle Scholar
  36. Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE (2005) Variation in the strength of selected codon usage bias among bacteria. Nucl Acids Res 33:1141–1153PubMedCrossRefGoogle Scholar
  37. Shpaer EG (1986) Constraints on codon context in Escherichia coli genes. Their possible role in modulating the efficiency of translation. J Mol Biol 188:555–564PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2012

Authors and Affiliations

  • Siddhartha Sankar Satapathy
    • 1
  • Malay Dutta
    • 1
  • Alak Kumar Buragohain
    • 2
  • Suvendra Kumar Ray
    • 2
  1. 1.Departments of Computer Science and EngineeringTezpur UniversityTezpurIndia
  2. 2.Departments of Molecular Biology and BiotechnologyTezpur UniversityTezpurIndia

Personalised recommendations