Slightly beneficial genes are retained by evolving Horizontal Gene Transfer despite selfish elements

Abstract

Horizontal gene transfer (HGT) is a key component of bacterial evolution, which in concert with gene loss can result in rapid changes in gene content. While HGT can evidently aid bacteria to adapt to new environments, it also carries risks since bacteria may pick up selfish genetic elements (SGEs). Here, we use modeling to study how bacterial growth rates are affected by HGT of slightly beneficial genes, if bacteria can evolve HGT to improve their growth rates, and when HGT is evolutionarily maintained in light of harmful SGEs. We find that we can distinguish between four classes of slightly beneficial genes: indispensable, enrichable, rescuable, and unrescuable genes. Rescuable genes - genes that confer small fitness benefits and are lost from the population in the absence of HGT -- can be collectively retained by a bacterial community that engages in HGT. While this gene-sharing cannot evolve in well-mixed cultures, it does evolve in a spatially structured population such as a biofilm. Although HGT does indeed enable infection by harmful SGEs, HGT is nevertheless evolutionarily maintained by the hosts, explaining the stable coexistence and co-evolution of bacteria and SGEs.