Prevalence and Dynamics of Genome Rearrangements in Bacteria and Archaea

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Abstract

The genetic material of bacteria and archaea is organized into various structures and set-ups, attesting that genome architecture is dynamic in these organisms. However, strong selective pressures are also acting to preserve genome organization, and it remains unclear how frequently genomes experience rearrangements and what mechanisms lead to these processes. Here, we assessed the dynamics and the drivers of genomic rearrangements across 121 microbial species. We show that synteny is highly conserved within most species, although several species present exceptionally flexible genomic layouts. Our results show a rather variable pace at which genomic rearrangements occur across bacteria and archaea, pointing to different selective constraints driving the accumulation of genomic changes across species. Importantly, we found that not only inversions but also translocations are highly enriched near the origin of replication ( Ori ), which suggests that many rearrangements may confer an adaptive advantage to the cell through the relocation of genes that benefit from gene dosage effects. Finally, our results support the view that mobile genetic elements—in particular transposable elements—are the main drivers of genomic translocations and inversions. Overall, our study shows that microbial species present largely stable genomic layouts and identifies key patterns and drivers of genome rearrangements in prokaryotes.

Significance statement

Bacterial and archaeal genomes display stable architectures which ensures the preservation of fundamental cellular processes. However, large genomic rearrangements occasionally occur. Although most of these events are thought to be highly deleterious, they have the potential to lead to adaptive events. Here, we examined the general trends of the dynamic of prokaryotic genomes by exploring the occurrence of genome rearrangements across a broad diversity of bacterial and archaeal species. We find that genomes remain highly syntenic in most species over short evolutionary timescales, although some species appear particularly dynamic. Rearrangements are strongly biased, and most gene blocks are relocated near the origin of replication. We also measured remarkably variables rates at which genome rearrangements occur across species, and transposons and other mobile genetic elements appear to be the main drivers of these variations. Overall, this study provides a comprehensive picture of the dynamic of genome architecture across many microbial species.

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