In each genome, synonymous codons are used with different frequencies; this general phenomenon is known as codon usage bias. It has been previously recognised that codon usage bias could affect the cellular fitness and might be associated with the ecology of microbial organisms. In this exploratory study, we investigated the relationship between codon usage bias, lifestyles (thermophiles vs. mesophiles; pathogenic vs. non-pathogenic; halophilic vs. non-halophilic; aerobic vs. anaerobic and facultative) and habitats (aquatic, terrestrial, host-associated, specialised, multiple) of 615 microbial organisms (544 bacteria and 71 archaea). Principal component analysis revealed that species with given phenotypic traits and living in similar environmental conditions have similar codon preferences, as represented by the relative synonymous codon usage (RSCU) index, and similar spectra of tRNA availability, as gauged by the tRNA gene copy number (tGCN). Moreover, by measuring the average tRNA adaptation index (tAI) for each genome, an index that can be associated with translational efficiency, we observed that organisms able to live in multiple habitats, including facultative organisms, mesophiles and pathogenic bacteria, are characterised by a reduced translational efficiency, consistently with their need to adapt to different environments. Our results show that synonymous codon choices might be under strong translational selection, which modulates the choice of the codons to differently match tRNA availability, depending on the organism’s lifestyle needs. To our knowledge, this is the first large-scale study that examines the role of codon bias and translational efficiency in the adaptation of microbial organisms to the environment in which they live.

In each genome, some codons are favored over others by selection likely because they are translated more efficiently and accurately. The selectively favored codons tend to correspond to the most highly expressed tRNAs. It has been recognized that this codon usage bias can influence the cellular fitness and that might be associated with the lifestyle of the organism. To test the impact of environments on genome evolution we studied the codon usage bias of 615 prokaryotes. We found that the extent of codon usage corresponds to the environment in witch the prokaryotes live. In particular, measuring the degree of codon usage bias by the tRNA adaptation index (tAI), we obtained that organisms living in a specialized habitat have high extents of codon usage bias, consistent with their need to adapt efficiently to specific environmental constraints. Differently, organisms able to live in multiple habitats exhibit low codon usage bias as they need to adapt to various physical and chemical conditions. Our results suggest the importance of co-evolution between tRNA availability and codon usage of an organism, in relation with the environmental adaptation.