How sequence populations persist inside bacterial genomes

Abstract

Compared to their eukaryotic counterparts, bacterial genomes are small and contain extremely tightly packed genes. Repetitive sequences are rare but not completely absent. One of the most common repeat families are REPINs. REPINs can replicate in the host genome and form populations that persist for millions of years. Here we model the interactions of these intragenomic sequence populations with the bacterial host. We first confirm well established results, in the presence and absence of horizontal gene transfer sequence populations either expand until they drive the host to extinction or the sequence population gets purged from the genome. We then show that a sequence population can be stably maintained, when each individual sequence provides a benefit that decreases with increasing sequence population size. Maintaining a sequence population of stable size also requires the replication of the sequence population to be costly to the host, otherwise the sequence population size will increase indefinitely. Surprisingly, in regimes with high horizontal gene transfer rates, the benefit conferred by the sequence population does not have to exceed the damage it causes to its host. Our analyses provide a plausible scenario for the persistence of sequence populations in bacterial genomes. We also hypothesize a limited biologically relevant parameter range for the provided benefit, which can be tested in future experiments.

Ancient Darwinian replicators nested within eubacterial genomes

“…This is because RAYT-encoded function does not mediate RAYT duplication. While the relationship between REPIN and RAYT most likely began as exploitative it appears to have evolved toward a mutualistic association (see below) – both in terms of the interaction between RAYT and host cell [15], and between RAYT and REPIN [14].…”

“…Examples of the latter are commonplace, yet the fate of selfish genetic elements is extinction, at least in bacterial genomes [9][10][11][12][13][14]. In order to persist long-term, selfish genetic elements must constantly infect new hosts.…”

Transposable elements drive the evolution of genome streamlining

“…Not all TEs are marked by these characteristics. For example, REPIN sequences ( r epetitive e xtragenic p alindromic sequences forming a hairp in ) take up many intergenic spaces in E. coli and Pseudomonas fluorescens SBW25 (Bertels & Rainey 2011; Park et al 2021). However, REPIN sequences do not move autonomously and are replicated by a single-copy transposase that has been vertically inherited for millions of years (Bertels & Rainey 2011).…”

“…At low transposition rates, these populations are clearly not yet in steady state, but appear to be going towards extinction. Coexistence is also possible in the well-mixed model, but only when the number of coding and non-coding genes is exactly the same (Park et al 2021).…”

“…To understand the relationship between TEs and genome architecture, it is necessary to consider mechanisms underpinning TE persistence. In asexual organisms the long-term fate of TEs within a given lineage is extinction (Park et al 2021). Opportunity for long-term persistence depends critically on ability to periodically invade new lineages via horizontal gene transfer (HGT) (Doolittle & Sapienza 1980; van Dijk et al 2020).…”