The evolutionary dynamics of tRNA-gene copy number and codon-use in E. coli.

Michael J. McDonald, Chih-Hung Chou, Krishna BS Swamy, Hsien-Da Huang, Jun-Yi Leu

The introduction of foreign DNA by Lateral Gene Transfer (LGT) can quickly and drastically alter genome composition. Problems can arise if the genes introduced by LGT use codons that are not suited to the host's translational machinery. Here we investigate compensatory adaptation of E. coli in response to the introduction of large volumes of codons that are rarely used by the host genome. We analyze genome sequences from the E. coli/Shigella complex, and find that certain tRNA genes are present in multiple copies in two pathogenic Shigella and O157:H7 subgroups of E. coli. Furthermore, we show that the codons that correspond to these multi-copy number tRNA genes are enriched in the high copy number Selfish Genetic Elements (SGE's) in Shigella and laterally introduced genes in O157:H7. We analyze the duplicate copies and find evidence for the selective retention of tRNA genes introduced by LGT in response to the changed codon content of the genome. These data support a model where the relatively rapid influx of LGT genes and SGE's introduces a large number of genes maladapted to the host's translational machinery. Under these conditions, it becomes advantageous for the host to retain tRNA genes that are required for the incorporation of amino acids at these codons. Subsequently, the increased number of copies of these specific tRNA genes adjusts the cellular tRNA pool to the demands set by global shifts in codon usage.