Dynamics of bacterial insertion sequences: can transposition bursts help the elements persist?

Abstract

Abstract Background Currently there is no satisfactory explanation for why bacterial insertion sequences (ISs) widely occur across prokaryotes despite being mostly harmful to their host genomes. Rates of horizontal gene transfer are likely to be too low to maintain ISs within a population. IS-induced beneficial mutations may be important for both prevalence of ISs and microbial adaptation to changing environments but may be too rare to sustain IS elements in the long run. Environmental stress can induce elevated rates of IS transposition activities; such episodes are known as ‘transposition bursts’. By examining how selective forces and transposition events interact to influence IS dynamics, this study asks whether transposition bursts can lead to IS persistence. Results We show through a simulation model that ISs are gradually eliminated from a population even if IS transpositions occasionally cause advantageous mutations. With beneficial mutations, transposition bursts create variation in IS copy numbers and improve cell fitness on average. However, these benefits are not usually sufficient to overcome the negative selection against the elements, and transposition bursts amplify the mean fitness effect which, if negative, simply accelerates the extinction of ISs. If down regulation of transposition occurs, IS extinctions are reduced while ISs still generate variation amongst bacterial genomes. Conclusions Transposition bursts do not help ISs persist in a bacterial population in the long run because most burst-induced mutations are deleterious and therefore not favoured by natural selection. However, bursts do create more genetic variation through which occasional advantageous mutations can help organisms adapt. Regulation of IS transposition bursts and stronger positive selection of the elements interact to slow down the burst-induced extinction of ISs.