Conflicting selection alters the trajectory of molecular evolution in a tripartite bacteria–plasmid–phage interaction

Abstract

Bacteria engage in a complex network of ecological interactions, which includes mobile genetic elements ( MGE s) such as phages and plasmids. These elements play a key role in microbial communities as vectors of horizontal gene transfer but can also be important sources of selection for their bacterial hosts. In natural communities, bacteria are likely to encounter multiple MGE s simultaneously and conflicting selection among MGE s could alter the bacterial evolutionary response to each MGE . Here, we test the effect of interactions with multiple MGE s on bacterial molecular evolution in the tripartite interaction between the bacterium, Pseudomonas fluorescens , the lytic bacteriophage, SBW 25φ2, and conjugative plasmid, pQBR 103, using genome sequencing of experimentally evolved bacteria. We show that individually, both plasmids and phages impose selection leading to bacterial evolutionary responses that are distinct from bacterial populations evolving without MGE s, but that together, plasmids and phages impose conflicting selection on bacteria, constraining the evolutionary responses observed in pairwise interactions. Our findings highlight the likely difficulties of predicting evolutionary responses to multiple selective pressures from the observed evolutionary responses to each selective pressure alone. Understanding evolution in complex microbial communities comprising many species and MGE s will require that we go beyond studies of pairwise interactions.

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