Translation Comes First: Ancient and Convergent Selection of Codon Usage Bias Across Prokaryotic Genomes.

Codon usage is the outcome of different evolutionary processes and can inform us about the conditions in which organisms live and evolve. Here, we present R_ENC', which is an improvement to the original S index developed by dos Reis et al. (2004). Our index is less sensitive to G+C content, which greatly affects synonymous codon usage in prokaryotes, making it better suited to detect selection acting on codon usage. We used R_ENC' to estimate the extent of selected codon usage bias in 1800 genomes representing 26 prokaryotic phyla. We found that Gammaproteobacteria, Betaproteobacteria, Actinobacteria, and Firmicutes are the phyla/subphyla showing more genomes with selected codon usage bias. In particular, we found that several lineages within Gammaproteobacteria and Firmicutes show a similar set of functional terms enriched in genes under selected codon usage bias, indicating convergent evolution. We also show that selected codon usage bias tends to evolve in genes coding for the translation machinery before other functional GO terms. Finally, we discuss the possibility to use R_ENC' to predict whether lineages evolved in copiotrophic or oligotrophic environments.