Homologous recombination (HR) enables the exchange of genetic material between and within species. Recent studies suggest that this process plays a major role in the microevolution of microbial genomes, contributing to core genome homogenization and to the maintenance of cohesive population structures. However, we still have a very poor understanding of the possible adaptive roles of intraspecific HR and of the factors that determine its differential impact across clades and lifestyles. Here we used a unified methodological framework to assess HR in 338 complete genomes from 54 phylogenetically diverse and representative prokaryotic species, encompassing different lifestyles and a broad phylogenetic distribution. Our results indicate that lifestyle and presence of restriction-modification (RM) machineries are among the main factors shaping HR patterns, with symbionts and intracellular pathogens having the lowest HR levels. Similarly, the size of exchanged genomic fragments correlated with the presence of RM and competence machineries. Finally, genes exchanged by HR showed functional enrichments which could be related to adaptations to different environments and ecological strategies. Taken together, our results clarify the factors underlying HR impact and suggest important adaptive roles of genes exchanged through this mechanism. Our results also revealed that the extent of genetic exchange correlated with lifestyle and some genomic features. Moreover, the genes in exchanged regions were enriched for functions that reflected specific adaptations, supporting identification of HR as one of the main evolutionary mechanisms shaping prokaryotic core genomes.IMPORTANCE Microbial populations exchange genetic material through a process called homologous recombination. Although this process has been studied in particular organisms, we lack an understanding of its differential impact over the genome and across microbes with different life-styles. We used a common analytical framework to assess this process in a representative set of microorganisms. Our results uncovered important trends. First, microbes with different lifestyles are differentially impacted, with endosymbionts and obligate pathogens being those less prone to undergo this process. Second, certain genetic elements such as restriction-modification systems seem to be associated with higher rates of recombination. Most importantly, recombined genomes show the footprints of natural selection in which recombined regions preferentially contain genes that can be related to specific ecological adaptations. Taken together, our results clarify the relative contributions of factors modulating homologous recombination and show evidence for a clear a role of this process in shaping microbial genomes and driving ecological adaptations.

The group of J.A. is funded by grant CLG2015_66686-C3-03 from the Spanish Ministry of Economy and Competitiveness (MINECO), which is cofinanced with FEDER support from the European Union. P.G.-T. was an FPI-MINECO fellow associated with project CGL2012-39627-C03-01 (to J.A.). The T.G. group acknowledges support from the Spanish Ministry of Economy and Competitiveness (grants “Centro de Excelencia Severo Ochoa 2013-2017” SEV-2012-0208 and BFU2015-67107; cofounded by European Regional Development Fund [ERDF]); from the CERCA Program/Generalitat de Catalunya; from the Catalan Research Agency (AGAUR) (grant SGR857); and from the European Union’s Horizon 2020 research and innovation program under grant agreement ERC-2016-724173 (Marie Sklodowska-Curie grant agreement no. H2020-MSCA-ITN-2014-642095).