Core genes can have higher recombination rates than accessory genes within global microbial populations

Abstract

Recombination is essential to microbial evolution1-4, and is involved in the spread of antibiotic resistance, antigenic variation, and adaptation to the host niche5-8. Yet quantifying the impact of homologous recombination on different gene classes, which is critical to understanding how selection acts on variation to shape species diversity and genome structure, remains challenging. This is largely due to the dynamic nature of bacterial genomes, whose high intraspecies genome content diversity9 and complex phylogenetic relationships10-12 present difficulties for inferring rates of recombination, particularly for rare genes. In this work, we apply a computationally efficient, non-phylogenetic approach13,14 to measure homologous recombination rates in the core and accessory genome (genes present in all strains and only a subset of strains, respectively) using >100,000 whole genome sequences from 12 microbial species. Our analysis suggests that even well-resolved sequence clusters sampled from global populations interact with overlapping gene pools, which has implications for the role of population structure in genome evolution. We show that in a majority of species, core genes have shorter coalescence times and higher recombination rates than accessory genes, and that gene frequency is often positively correlated with increased recombination. Our results provide a new line of population genomic evidence supporting the hypothesis that core genes are under strong, purifying selection15-17, and indicate that homologous recombination may play a key role in increasing the efficiency of selection in those parts of the genome most conserved within each species.