Replication-Dependent Organization Constrains Positioning of Long DNA Repeats in Bacterial Genomes

Bacterial genome organization is primarily driven by chromosomal replication from a single origin of replication. However, chromosomal rearrangements, which can disrupt such organization, are inevitable in nature. Long DNA repeats are major players mediating rearrangements, large and small, via homologous recombination. Since changes to genome organization affect bacterial fitness—and more so in fast-growing than slow-growing bacteria—and are under selection, it is reasonable to expect that genomic positioning of long DNA repeats is also under selection. To test this, we identified identical DNA repeats of at least 100 base pairs across ∼6,000 bacterial genomes and compared their distribution in fast- and slow-growing bacteria. We found that long identical DNA repeats are distributed in a non-random manner across bacterial genomes. Their distribution differs in the overall number, orientation, and proximity to the origin of replication, between fast- and slow-growing bacteria. We show that their positioning—which might arise from a combination of the processes that produce repeats and selection on rearrangements that recombination between repeat elements might cause—permits less disruption to the replication-dependent genome organization of bacteria compared with random suggesting it as a major constraint to positioning of long DNA repeats.