Abstract
Prokaryote genome evolution is characterized by the frequent gain of genes through horizontal gene transfer (HGT). For a gene, being horizontally transferred can represent a strong change in its genomic and physiological context. If the codon usage of a transferred gene deviates from that of the receiving organism, the fitness benefits it provides can be reduced due to a mismatch with the expression machinery. Consequently, transferred genes with a deviating codon usage can be selected against or elicit evolutionary responses that enhance their integration, such as gene amelioration and compensatory evolution. Within bacterial species, the extent and relative importance of these different mechanisms has never been considered altogether. In this study, a phylogeny-based method was used to investigate the occurrence of these different evolutionary responses in Pseudomonas aeruginosa. Selection on codon usage of genes acquired through HGT was observed over evolutionary time, with the overall codon usage converging towards that of the core genome. Gene amelioration, through the accumulation of synonymous mutations after HGT, did not seem to systematically affect transferred genes. This pattern therefore seemed to be mainly driven by selective retention of transferred genes with an initial codon usage similar to that of the core genes. Additionally, variation in the copy number of tRNA genes was often associated with the acquisition of genes for which the observed variation could enhance their expression. This provides evidence that compensatory evolution might be an important mechanism for the integration of horizontally transferred genes.
Highlights
Horizontal gene transfer (HGT) strongly contributes to bacterial evolution and is a key mechanism for a quick adaptation to environmental challenges
This phylogeny indicated a structure consisting of two large clades, with 61 strains belonging to the clade containing reference strain PAO1 and 32 strains belonging to the clade containing reference strain PA14 (Fig. 1)
We showed that there was selection on codon usage of genes acquired through HGT, with their codon usage converging toward that of the core genome over evolutionary time
Summary
Horizontal gene transfer (HGT) strongly contributes to bacterial evolution and is a key mechanism for a quick adaptation to environmental challenges. The frequent uptake of foreign genetic material leads to numerous genes being found in certain genomes of a bacterial species, but not in all. This set of dispersed genes, the accessory genome, is highly dynamic and is shaped by frequent gene gains and losses [1]. A new gene is incorporated into the accessory genome if – after initial acquisition – it replicates itself within the receiving organism and is vertically inherited. Long-term retention of a gene will depend on its effect on the fitness of the receiving organism, which is often dependent on the environmental and genomic context. There is a high probability that it will be subsequently lost due to natural selection [2].
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