Variation in the strength of selected codon usage bias among bacteria

Abstract

Among bacteria, many species have synonymous codon usage patterns that have been influenced by natural selection for those codons that are translated more accurately and/or efficiently. However, in other species selection appears to have been ineffective. Here, we introduce a population genetics-based model for quantifying the extent to which selection has been effective. The approach is applied to 80 phylogenetically diverse bacterial species for which whole genome sequences are available. The strength of selected codon usage bias, S, is found to vary substantially among species; in 30% of the genomes examined, there was no significant evidence that selection had been effective. Values of S are highly positively correlated with both the number of rRNA operons and the number of tRNA genes. These results are consistent with the hypothesis that species exposed to selection for rapid growth have more rRNA operons, more tRNA genes and more strongly selected codon usage bias. For example, Clostridium perfringens, the species with the highest value of S, can have a generation time as short as 7 min.

Figure 1

Phylogenetic relationships of the 80 bacterial genomes analysed. Species codes are given in Table 1.

Figure 2

G+C content at the three codon positions within the dnaA gene, compared with the G+C content of the genome as a whole, for 79 bacterial genomes (no dnaA homologue has been found in W.glossinidia). Positions 1, 2 and 3 are indicated by open circles, open triangles and filled circles, respectively. The third position is strongly influenced by G+C bias; the first two positions are also influenced, implying an effect on amino acid composition (68).

Figure 3

Selected codon usage bias (S) and genomic G+C bias for 80 bacterial species. Genomic G+C bias is estimated by the overall GC3_S. Open circles denote species where the S-value is not greater than found among randomly selected genes; filled triangles denote three Clostridium species.

Figure 4

Ribosomal RNA operon copy number and tRNA gene number for 80 bacterial species. Symbols are as in Figure 3.

Figure 5

Selected codon usage bias (S) and ribosomal RNA operon copy number for 80 bacterial species. Symbols are as in Figure 3.

Figure 6

Selected codon usage bias (S) and tRNA gene number for 80 bacterial species. Symbols are as in Figure 3.

Figure 7

Comparison of two estimates of selected codon usage bias: x-axis values are taken from this paper, y-axis values from dos Reis et al. (62). Values significantly greater than zero in the dos Reis et al. analysis are shown as circles; values significantly greater than zero in our analysis are shown as filled symbols.