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Evolution of gene mobility: how mobile elements shape the function and sociality of microbial communities

Final Report Summary - EVOMOBILOME (Evolution of gene mobility: how mobile elements shape the function and sociality of microbial communities)

The project EVOMOBILOME developed an integrative identification and analysis of self-mobilizable elements to study the contributions of mobile genetic elements (MGEs) to the social evolution of bacteria. It used comparative genomics, phylogeny and population genetics techniques to detail how elements propagated and were maintained in populations.
First, we unraveled the determinants of the distribution of MGEs, and especially prophages and conjugative elements, in bacteria and how they affect genome repertoires. In particular, we identified a pervasive trend for the domestication of such elements by their bacterial host. We also investigated how defense functions worked to shape the interactions between these MGE and between them and the bacterial host. This showed that diversification of these systems change the genetic fluxes between elements in microbial communities, carving preferential routes of DNA transfer that are continuously changing. We then studied how genetic information, passing through defense mechanisms, integrates the genomes. We found that a few hotspots account for the majority of horizontally transferred genes in bacteria. Since, this suggests selection against integration of exogenous DNA in most regions of the bacterial chromosome, we studied the relative advantages of integrative MGEs relative to extra-chromosomal ones. We showed that the two types of elements have different advantages: the former tend to have a broader host range, whereas the latter diversify faster. At the end of this project, we obtained a much clearer view of the impact of self-mobilizable genetic elements in bacterial diversification.
The second aim of this project was to understand how secretion systems and their effectors were distributed in MGEs and how this drove gene mobility to promote social behavior (by way of the production of public goods). We demonstrated that genes encoding secreted proteins evolve fast and are over-represented in MGEs in most species, as we had shown before for E. coli. Our extensive studies on the distribution and evolution of secretion systems (and bacterial capsules proposed to affect secretion and horizontal transfer) in genomes and metagenomes allowed us to enquire on the roles of gene mobility and secretion in the social evolution of natural microbial populations. We observed, in confirmation of our initial hypothesis, that environmental structure affects the distribution of secreted proteins and secretion systems thus shaping bacterial social evolution.