A global survey of prokaryotic genomes reveals the eco-evolutionary pressures driving horizontal gene transfer

Abstract Horizontal gene transfer, the exchange of genetic material through means other than reproduction, is a fundamental force in prokaryotic genome evolution. Genomic persistence of horizontally transferred genes has been shown to be influenced by both ecological and evolutionary factors. However, there is limited availability of ecological information about species other than the habitats from which they were isolated, which has prevented a deeper exploration of ecological contributions to horizontal gene transfer. Here we focus on transfers detected through comparison of individual gene trees to the species tree, assessing the distribution of gene-exchanging prokaryotes across over a million environmental sequencing samples. By analysing detected horizontal gene transfer events, we show distinct functional profiles for recent versus old events. Although most genes transferred are part of the accessory genome, genes transferred earlier in evolution tend to be more ubiquitous within present-day species. We find that co-occurring, interacting and high-abundance species tend to exchange more genes. Finally, we show that host-associated specialist species are most likely to exchange genes with other host-associated specialist species, whereas species found across different habitats have similar gene exchange rates irrespective of their preferred habitat. Our study covers an unprecedented scale of integrated horizontal gene transfer and environmental information, highlighting broad eco-evolutionary trends.