Protein secretion, DNA mobility and social conflict in microbial cooperation

Microbes engage in a remarkable array of cooperative behaviors, secreting shared proteins that are essential for foraging, shelter, microbial warfare and virulence. These proteins are costly, rendering populations of cooperators vulnerable to exploitation by non-producing cheaters arising by gene loss or migration. In such conditions, how can cooperation persist? Our model predicts that more mobile loci generate higher relatedness, and therefore allow the maintenance of more cooperative traits via kin selection. By analyzing bacterial genomes we observe a massive amount of horizontal transfer and show that this is the predominant mechanism of innovation in bacterial genomes. Additionally, this shows that we are far from knowing the diversity of functions encoded in the species. We confirm that genes coding for secreted proteins - the secretome – are very frequently lost and gained and are associated with mobile elements, supporting our major prediction that gene mobility drives bacterial cooperation. We demonstrate that mobile elements are in conflict with their chromosomal hosts over the chimeric ensemble’s social strategy, with mobile elements enforcing cooperation on their otherwise selfish hosts via the co-transfer of secretome genes with “mafia strategy” addictive systems. Such enforcement is nevertheless shaped by accommodation strategies that minimize the cost of infection by mobile elements. This analysis suggests that horizontal transfer promotes cooperation, as transmission increases local genetic relatedness at mobile loci and enforces cooperation on the resident genes. As a result, horizontal transfer promoted by agents such as plasmids, phages or integrons might drive microbial cooperation.