Horizontal gene transfer, segregation loss, and the speed of microbial adaptation

Microbial adaptation is driven by the circulation of mobile genetic elements (MGEs) among bacteria. On the one hand, MGEs can be viewed as selfish genes that spread like infectious diseases in a host population. On the other hand, the horizontal transfer and the loss of these MGEs are often viewed as a form of sexual reproduction that reshuffles genetic diversity in a way that may sometimes be adaptive for bacteria cells. Here, we show how these 2 perspectives can be reconciled using a single unified framework capturing the dynamics of multiple, interacting MGEs. We apply this framework to study how interactions between MGEs affecting rates of horizontal gene transfer and segregation loss shape the short- and long-term evolutionary dynamics of MGEs and the bacteria population. We show that these interactions produce nonrandom MGE associations that can speed up or slow down microbial adaptation depending on the evolutionary conflicts between MGEs as well as between MGEs and their bacterial hosts. Moreover, we show how these interactions affect the evolutionary potential of the bacteria population. We discuss the implications of these predictions for the community response to environmental stressors such as antibiotic treatment or vaccination campaigns as well as the evolution of accessory genomes.