Defence systems and horizontal gene transfer in bacteria

Abstract

Horizontal gene transfer (HGT) is a fundamental process in prokaryotic evolution, contributing significantly to diversification and adaptation. HGT is typically facilitated by mobile genetic elements (MGEs), such as conjugative plasmids and phages, which often impose fitness costs on their hosts. However, a considerable number of bacterial genes are involved in defence mechanisms that limit the propagation of MGEs, suggesting they may actively restrict HGT. In our study, we investigated whether defence systems limit HGT by examining the relationship between the HGT rate and the presence of 73 defence systems across 12 bacterial species. We discovered that only six defence systems, three of which were different CRISPR‐Cas subtypes, were associated with a reduced gene gain rate at the species evolution scale. Hosts of these defence systems tend to have a smaller pangenome size and fewer phage‐related genes compared to genomes without these systems. This suggests that these defence mechanisms inhibit HGT by limiting prophage integration. We hypothesize that the restriction of HGT by defence systems is species‐specific and depends on various ecological and genetic factors, including the burden of MGEs and the fitness effect of HGT in bacterial populations.

Evolution of the CRISPR-Cas9 defence system inMycoplasma gallisepticumfollowing colonization of a novel bird host

“…However, maintaining an active CRISPR-Cas undoubtedly incurs fitness costs. Such costs can arise, for instance, when CRISPR-Cas generates metabolic costs (Hall et al, 2021;Vale et al, 2015) and genetic conflicts (Hall et al, 2021;Vale et al, 2015) or when it is less effective at preventing infections than other defence processes (Stern et al 2010;Broniewski et al 2020;Watson et al 2024).CRISPR-Cas can also create a risk of self-targeting spacers (Stern et al, 2010;Wimmer & Beisel, 2020), and can prevent the acquisition of fitness-enhancing genes through horizontal gene transfer (HGT) (Alduhaidhawi et al, 2022;Bikard et al, 2012;Dimitriu et al, 2020;Kogay et al, 2024;Levin, 2010;Mackow et al, 2019;Palmer & Gilmore, 2010;Pursey et al, 2022;Wheatley & MacLean, 2021). The balance between the costs and benefits of maintaining an active CRISPR-Cas will therefore depend on CRISPR-Cas' contribution to the bacterium's global defence process, on its non-defence roles, and on the specific selective pressures exerted by different host environments.…”