Skip to main content

Advertisement

Log in

Selection on GGU and CGU Codons in the High Expression Genes in Bacteria

  • Original Article
  • Published:
Journal of Molecular Evolution Aims and scope Submit manuscript

Abstract

The fourfold degenerate site (FDS) in coding sequences is important for studying the effect of any selection pressure on codon usage bias (CUB) because nucleotide substitution per se is not under any such pressure at the site due to the unaltered amino acid sequence in a protein. We estimated the frequency variation of nucleotides at the FDS across the eight family boxes (FBs) defined as Um(g), the unevenness measure of a gene g. The study was made in 545 species of bacteria. In many bacteria, the Um(g) correlated strongly with Nc′—a measure of the CUB. Analysis of the strongly correlated bacteria revealed that the U-ending codons (GGU, CGU) were preferred to the G-ending codons (GGG, CGG) in Gly and Arg FBs even in the genomes with G+C % higher than 65.0. Further evidence suggested that these codons can be used as a good indicator of selection pressure on CUB in genomes with higher G+C %.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Subscribe and save

Springer+ Basic
€32.70 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price includes VAT (Finland)

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

Abbreviations

CUB:

Codon usage bias

FB(s):

Family box(es)

FDS:

Fourfold degenerate site

References

  • Antezana MA, Kreitman M (1999) The nonrandom location of synonymous codons suggests that reading frame-independent forces have patterned codon preferences. J Mol Evol 49:36–43

    Article  CAS  PubMed  Google Scholar 

  • Botzman M, Margalit H (2011) Variation in global codon usage bias among prokaryotic organisms is associated with their lifestyles. Genome Biol 12:R109

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bulmer M (1990) The effect of context on synonymous codon usage in genes with low codon usage bias. Nucleic Acids Res 18:2869–2873

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bulmer M (1991) The selection-mutation-drift theory of synonymous codon usage. Genetics 129:897–907

    PubMed Central  CAS  PubMed  Google Scholar 

  • Chen SL, Lee W, Hotts AK, Shapiro L, McAdams HH (2004) Codon usage between genomes is constrained by genome wide mutational processes. Proc Natl Acad Sci USA 101:3480–3485

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Emery LR, Sharp PM (2011) Impact of translational selection on codon usage bias in the archaeon methanococcus maripaludis. Biol Lett 7:131–135

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ermolaeva MD (2001) Synonymous codon usage in bacteria. Curr Issues Mol Biol 3:91–97

    CAS  PubMed  Google Scholar 

  • Francino MP, Ochman H (1997) Strand asymmetries in DNA evolution. Trends Genet 13:240–245

    Article  CAS  PubMed  Google Scholar 

  • Francino MP, Ochman H (2001) Deamination as the basis of strand-asymmetric evolution in transcribed Escherichia coli sequences. Mol Biol Evol 18:1147–1150

    Article  CAS  PubMed  Google Scholar 

  • Genin S (2010) Molecular traits controlling host range and adaptation to plants in Ralstonia solanacearum. New Phytol 187:920–928

    Article  PubMed  Google Scholar 

  • Ghaemmaghami S, Huh WK, Bower K, Howson RW, Belle A, Dephoure N, O’Shea EK, Weissman JS (2003) Global analysis of protein expression in yeast. Nature 425:737–741

    Article  CAS  PubMed  Google Scholar 

  • Goldberg JB (2000) Pseudomonas: global bacteria. Trends Microbiol 8:55–57

    Article  CAS  PubMed  Google Scholar 

  • Grocock RJ, Sharp PM (2002) Synonymous codon usage in Pseudomonas aeruginosa PA01. Gene 289:131–139

    Article  CAS  PubMed  Google Scholar 

  • 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 18:199–209

    Article  CAS  PubMed  Google Scholar 

  • Grosjean H, de Crécy-Lagard V, Marck C (2010) Deciphering synonymous codons in the three domains of life: coevolution with specific tRNA modification enzymes. FEBS Lett 584:252–264

    Article  CAS  PubMed  Google Scholar 

  • Hershberg R, Petrov DA (2009) General rules for optimal codon choice. PLoS Genet 5:e1000556

    Article  PubMed Central  PubMed  Google Scholar 

  • Hershberg R, Petrov DA (2010) Evidence that mutation is universally biased towards AT in bacteria. PLoS Genet 6:e1001115

    Article  PubMed Central  PubMed  Google Scholar 

  • Higgs PG (2009) A four-column theory for the origin of the genetic code: tracing the evolutionary pathways that gave rise to an optimized code. Biol Direct 4:16

    Article  PubMed Central  PubMed  Google Scholar 

  • 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 151:389–409

    Article  CAS  PubMed  Google Scholar 

  • Ikemura T (1985) Codon usage and tRNA content in unicellular and multicellular organisms. Mol Biol Evol 2:13–34

    CAS  PubMed  Google Scholar 

  • 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 9:102

    Article  PubMed Central  PubMed  Google Scholar 

  • Jia W, Higgs PG (2008) Codon usage in mitochondrial genomes: distinguishing context-dependent mutation from translational selection. Mol Biol Evol 25:339–351

    Article  CAS  PubMed  Google Scholar 

  • Karlin S, Campbell AM, Mrázek J (1998) Comparative DNA analysis across diverse genomes. Annu Rev Genet 32:185–225

    Article  CAS  PubMed  Google Scholar 

  • Lobry JR, Sueoka N (2002) Asymmetric directional mutation pressures in bacteria. Genome Biol 3:1–14

    Article  Google Scholar 

  • Mann HB, Whitney DR (1947) On a test of whether one of two random variables is stochastically larger than the other. Ann Math Stat 18:50–60

    Article  Google Scholar 

  • McInerney JO (1998) Replicational and transcriptional selection on codon usage in Borrelia burgdorferi. Proc Natl Acad Sci USA 95:10698–10703

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Murphy FV, Ramakrishnan V (2004) Structure of a purine–purine wobble base pair in the decoding center of the ribosome. Nat Struct Mol Biol 11:1251–1252

    Article  CAS  PubMed  Google Scholar 

  • Muto A, Osawa S (1987) The guanine and cytosine content of genomic DNA and bacterial evolution. Proc Natl Acad Sci USA 84:166–169

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Novembre JA (2002) Accounting for background nucleotide composition when measuring codon usage bias. Mol Biol Evol 19:1390–1394

    Article  CAS  PubMed  Google Scholar 

  • Novoa EM, Pavon-Eternod M, Pan T, de Pouplana LR (2012) A role for tRNA modifications in genome structure and codon usage. Cell 149:202–213

    Article  CAS  PubMed  Google Scholar 

  • Ochman H (2003) Neutral mutations and neutral substitutions in bacterial genomes. Mol Biol Evol 20:2091–2096

    Article  CAS  PubMed  Google Scholar 

  • Osawa S, Jukes TH, Watanabe K, Muto A (1992) Recent evidence for evolution of the genetic code. Microbiol Rev 56:229–264

    PubMed Central  CAS  PubMed  Google Scholar 

  • Palidwor GA, Perkins TJ, Xia X (2010) A general model of codon bias due to GC mutational bias. PLoS One 5:e13431

    Article  PubMed Central  PubMed  Google Scholar 

  • Palmeira L, Guéguen L, Lobry JR (2006) UV-targeted dinucleotides are not depleted in light-exposed prokaryotic genomes. Mol Biol Evol 23:2214–2219

    Article  CAS  PubMed  Google Scholar 

  • Peden JF (1999) Analysis of codon usage. PhD Thesis, University of Nottingham

  • Powdel BR, Borah M, Ray SK (2010) Strand-specific mutational bias influences codon usage of weakly expressed genes in Escherichia coli. Genes Cells 15:773–782

    Article  CAS  PubMed  Google Scholar 

  • Ran W, Higgs PG (2010) The influence of anticodon-codon interactions and modified bases on codon usage bias in bacteria. Mol Biol Evol 27:2129–2140

    Article  CAS  PubMed  Google Scholar 

  • Rocha EPC (2004) Codon usage bias from tRNA’s point of view, redundancy, specialization, and efficient decoding for translation optimization. Genome Res 14:2279–2286

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Rocha EPC, Feil EJ (2010) Mutational patterns cannot explain genome composition: are there any neutral sites in the genomes of bacteria? PLoS Genet 6:e1001104

    Article  PubMed Central  PubMed  Google Scholar 

  • Rocha EPC, Danchin A, Viari A (1999) Universal replication biases in bacteria. Mol Microbiol 32:11–16

    Article  CAS  PubMed  Google Scholar 

  • Satapathy SS, Dutta M, Buragohain AK, Ray SK (2012) 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. J Mol Evol 75:34–42

    Article  CAS  PubMed  Google Scholar 

  • Sharp PM, Bailes E, Grocock RJ, Peden JF, Sockett RE (2005) Variation in the strength of selected codon usage bias among bacteria. Nucleic Acids Res 33:1141–1153

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sharp PM, Li WH (1987) The codon adaptation index—a measure of directional codon usage bias, and its potential application. Nucleic Acids Res 15:1281–1295

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Stadler M, Fire A (2011) Wobble base-pairing slows in vivo translation elongation in metazoans. RNA 17:2063–2073

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sueoka N (1962) On the genetic basis of variation and heterogeneity of DNA base composition. Proc Natl Acad Sci USA 48:582–592

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Sueoka N (1995) Intrastrand parity rules of DNA base composition and usage biases of synonymous codons. J Mol Evol 40:318–325

    Article  CAS  PubMed  Google Scholar 

  • Suzuki H, Brown CJ, Forney LJ, Top EM (2008) Comparison of correspondence analysis methods for synonymous codon usage in bacteria. DNA Res 15:357–365

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wald N, Alroy M, Botzman M, Margalit H (2012) Codon usage bias in prokaryotic pyrimidine-ending codons is associated with the degeneracy of the encoded amino acids. Nucl Acids Res 40:7074–7083

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wang B, Shao Z-Q, Xu Y, Liu J, Liu Y, Hang Y-Y, Chen J-Q (2011) Optimal codon identities in bacteria: implications from the conflicting results of two different methods. PLoS One 6:e22714

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Wright F (1990) The effective number of codons used in a gene. Gene 87:23–29

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We are extremely thankful to several scientists and colleagues such as EPC Rocha (Institut Pasteur, Farnce), F. Supek (Ruđer Bošković Institute, Zagreb, Croatia), M. dos Reis (University College, London), A. Goel (DuPont, Hyderabad), S. K. Kar (KIIT, Bhubaneswar), and V. J. Baruah (Tezpur University, Tezpur) for their helpful sugegstions on the manuscript. We are extremely grateful to the anonymous reviewers for their critical comments on the work which helped us in improving the quality of the manuscript. SKR is thankful to DBT, Govt. of India for the Bioinformatics Infrastructure Facility at Tezpur University. We also thank Mala Dutta (Gauhati University, Guwahati) for her comment on the English writing of the manuscript.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Suvendra Kumar Ray.

Electronic supplementary material

Below is the link to the electronic supplementary material.

239_2013_9596_MOESM1_ESM.tif

Supplementary Fig. 1. A four panel figure presenting in- and off-frame tri-nucleotide frequency analysis in rpoB and rpoC genes. Figure 1 presents comparison of the in- frame and off- frame tri-nucleotides GGU, GGG, CGU and CGG frequencies in rpoB/C genes in five different genome G+C groups (i) very high, 65.0 ≤ G+C %; (ii) high, 55.0 ≤ G+C % < 65.0; (iii) moderate, 45.0 ≤ G+C % < 55.0; (iv) low, 35.0 ≤ G+C % < 45.0; and (v) very low, G+C % < 35.0. Within each group, four bacteria (as analyzed in Fig. 2) that exhibited strong Pearson r(Um(g), Nc′) were considered. It is evident in the Fig. 1 that the abundance values of in-frame GGU/CGU triplets are different from that in off-frame1 and off-frame2. Similarly, the abundance values of in-frame GGG/CGG triplets are different from that in off-frame1 and off-frame2. This study suggests that selection of GGU and CGU codons in the high expression genes is not due to general selection of these triplets in coding regions. (TIFF 110 kb)

Supplementary material 2 (XLS 44 kb)

Supplementary material 3 (DOC 1104 kb)

Supplementary material 4 (DOC 507 kb)

Supplementary material 5 (DOC 366 kb)

Supplementary material 6 (DOC 157 kb)

Rights and permissions

Reprints and permissions

About this article

Cite this article

Satapathy, S.S., Powdel, B.R., Dutta, M. et al. Selection on GGU and CGU Codons in the High Expression Genes in Bacteria. J Mol Evol 78, 13–23 (2014). https://doi.org/10.1007/s00239-013-9596-6

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00239-013-9596-6

Keywords

Navigation