Rapid evolutionary turnover of mobile genetic elements drives bacterial resistance to phages

Abstract

Although it is generally accepted that phages drive bacterial evolution, how these dynamics play out in the wild remains poorly understood. We found that susceptibility to viral killing in marine Vibrio is mediated by large and highly diverse mobile genetic elements. These phage defense elements display exceedingly fast evolutionary turnover, resulting in differential phage susceptibility among clonal bacterial strains while phage receptors remain invariant. Protection is cumulative, and a single bacterial genome can harbor 6 to 12 defense elements, accounting for more than 90% of the flexible genome among close relatives. The rapid turnover of these elements decouples phage resistance from other genomic features. Thus, resistance to phages in the wild follows evolutionary trajectories alternative to those predicted from laboratory-based evolutionary experiments.

Microbial defenses against mobile genetic elements and viruses: Who defends whom from what?

“…Defense systems tend to be different across strains of a species [ 21 , 51 ] and are a significant part of the genetic differences between closely related strains of Vibrio spp. [ 8 ]. Why are defense systems so different among strains of a species?…”

“…Relative to microbial genomes, MGEs are more constrained in the number of genes they can carry, especially those packaged in viral particles. Yet, some also carry multiple defense systems [ 8 , 13 , 38 , 44 ], which may allow them to infect different hosts or fend off different MGEs.…”

“…In some cases, the advantage of the MGE defense system to the cell may be transient. Temperate phages that defend the cells from virulent phages are common [ 8 , 43 , 77 ] and provide a temporary relief to the host. But they may have little long-term impact in bacterial fitness if the victorious temperate phage is induced and lyses the cell.…”

“…In other contexts, these traits can be costly and, together with the costs of vertical and horizontal transfer, lower the host fitness [3]. As a result of these costs, MGEs rarely remain in genomes for long periods of time [4], and different strains tend to carry very different repertoires of prophages, plasmids, or transposable elements [5][6][7][8].…”

“…But the reality is much more complex and interesting because many of the systems found in bacterial genomes and once thought to be dedicated to the defense of the cell are actually encoded in MGEs. This includes systems encoded in temperate phages [8,[42][43][44][45], satellites [38,46,47], conjugative elements [13,[48][49][50], mobilizable plasmids [34], and genomic islands acquired by HGT [8,44,51]. For example, defense systems in Vibrio and in other species are a significant part of the species' accessory genome (12% to 20%) and are very frequently encoded in MGEs, many of which are poorly known [8].…”