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 (MGEs) 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 MGEs simultaneously and conflicting selection among MGEs could alter the bacterial evolutionary response to each MGE. Here, we test the effect of interactions with multiple MGEs on bacterial molecular evolution in the tripartite interaction between the bacterium, Pseudomonas fluorescens, the lytic bacteriophage, SBW25φ2, and conjugative plasmid, pQBR103, 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 MGEs, 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 MGEs will require that we go beyond studies of pairwise interactions.

Evolutionary pathways to antibiotic resistance are dependent upon environmental structure and bacterial lifestyle

“…These results suggest that the ancestral starting clone was already well adapted both to planktonic and biofilm lifestyles, likely because we had previously propagated the A. baumannii ATCC 17978 clone under identical drug-free conditions for 10 days leading to the fixation of mutations in three genes (Supplementary file 2). The absence of mutations specific to lifestyle in the absence of antibiotics and the acquisition of mutations specific to the growth mode under antibiotic pressure highlight different evolutionary responses to combined selective pressures that were not observed with each selective pressure alone (Harrison et al, 2017).…”

“…Together, our results demonstrate that bacterial lifestyle influences the evolutionary dynamics and targets of selection of AMR. Multiple selective pressures, particularly in the biofilm life cycle, may affect evolutionary dynamics and constrain the evolution of AMR if negative genetic correlations exist (Harrison et al, 2017). For instance, adeN mutations decrease biofilm formation and increase resistance by altering the adeN -controlled adeIJK efflux pump (Yoon et al, 2015), which could explain their prevalence in planktonic populations but not biofilm populations.…”

Genomic Signatures of Honey Bee Association in an Acetic Acid Symbiont

“…Movement and insertion of bacteriophage sequences in a genome can have profound effects on the evolution of that genome ( Casas and Maloy 2011 ; Koskella and Brockhurst 2014 ; Harrison et al. 2017 ).…”

The bacterial capsule is a gatekeeper for mobile DNA

“…Most of the works on MGE focus on the isolated effects of plasmids, phages, or other MGE. However, it is becoming increasingly evident that different types of MGE operate simultaneously and even coordinately sometimes [9][10][11], and new studies will help to gain a better understanding how MGE interactions affect bacterial evolution. Finally, this study also emphasizes the impact of the host range of different MGE on their potential effects on bacterial evolution.…”