Translational Selection for Speed Is Not Sufficient to Explain Variation in Bacterial Codon Usage Bias

Genome Biol Evol. 2018 Feb 1;10(2):562-576. doi: 10.1093/gbe/evy018.

Abstract

Increasing growth rate across bacteria strengthens selection for faster translation, concomitantly increasing the total number of tRNA genes and codon usage bias (CUB: enrichment of specific synonymous codons in highly expressed genes). Typically, enriched codons are translated by tRNAs with higher gene copy numbers (GCN). A model of tRNA-CUB coevolution based on fast growth-associated selection on translational speed recapitulates these patterns. A key untested implication of the coevolution model is that translational selection should favor higher tRNA GCN for more frequently used amino acids, potentially weakening the effect of growth-associated selection on CUB. Surprisingly, we find that CUB saturates with increasing growth rate across γ-proteobacteria, even as the number of tRNA genes continues to increase. As predicted, amino acid-specific tRNA GCN is positively correlated with the usage of corresponding amino acids, but there is no correlation between growth rate associated changes in CUB and amino acid usage. Instead, we find that some amino acids-cysteine and those in the NNA/G codon family-show weak CUB that does not increase with growth rate, despite large variation in the corresponding tRNA GCN. We suggest that amino acid-specific variation in CUB is not explained by tRNA GCN because GCN does not influence the difference between translation times of synonymous codons as expected. Thus, selection on translational speed alone cannot fully explain quantitative variation in overall or amino acid-specific CUB, suggesting a significant role for other functional constraints and amino acid-specific codon features.

Keywords: amino acid usage; effective number of codons; growth rate; rRNA copy number; tRNA gene copy number.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Amino Acids / genetics
  • Bacteria / genetics*
  • Bacteria / growth & development
  • Codon*
  • Evolution, Molecular
  • Gene Dosage
  • Gene Expression Regulation, Bacterial
  • Protein Biosynthesis*
  • RNA, Bacterial / genetics*
  • RNA, Ribosomal / genetics*
  • RNA, Transfer / genetics*
  • Selection, Genetic

Substances

  • Amino Acids
  • Codon
  • RNA, Bacterial
  • RNA, Ribosomal
  • RNA, Transfer