Abstract
Bacteriophage shape the composition and function of microbial communities. Yet it remains difficult to predict the effect of phage on microbial interactions. Specifically, little is known about how phage influence mutualisms in networks of cross-feeding bacteria. We mathematically modeled the impacts of phage in a synthetic microbial community in which Escherichia coli and Salmonella enterica exchange essential metabolites. In this model, independent phage attack of either species was sufficient to temporarily inhibit both members of the mutualism; however, the evolution of phage resistance facilitated yields similar to those observed in the absence of phage. In laboratory experiments, attack of S. enterica with P22vir phage followed these modeling expectations of delayed community growth with little change in the final yield of bacteria. In contrast, when E. coli was attacked with T7 phage, S. enterica, the nonhost species, reached higher yields compared with no-phage controls. T7 infection increased nonhost yield by releasing consumable cell debris, and by driving evolution of partially resistant E. coli that secreted more carbon. Our results demonstrate that phage can have extensive indirect effects in microbial communities, that the nature of these indirect effects depends on metabolic and evolutionary mechanisms, and that knowing the degree of evolved resistance leads to qualitatively different predictions of bacterial community dynamics in response to phage attack.
Highlights
Bacteriophage significantly influence microbial community structure and function [1]
The pair forms an obligate mutualism in lactose minimal medium, as S. enterica cannot consume lactose and instead relies on acetate excreted by E. coli during overflow metabolism
We anticipated that phage resistance would evolve, making biomass reduction temporary. We found that both phage delayed community growth, but neither phage reduced final host yields and T7 infection of E. coli led to surprising changes in species ratios
Summary
Bacteriophage significantly influence microbial community structure and function [1]. The null hypothesis that phage infection will alter cooperative community biomass but not composition has several underlying assumptions that may not hold. It assumes that bacteria obtain nutrients directly from the secretions of bacterial partners. The pair forms an obligate mutualism in lactose minimal medium, as S. enterica cannot consume lactose and instead relies on acetate excreted by E. coli during overflow metabolism Grown under these conditions, these bacteria are a simple two-species cooperative community. We anticipated that phage resistance would evolve, making biomass reduction temporary We found that both phage delayed community growth, but neither phage reduced final host yields and T7 infection of E. coli led to surprising changes in species ratios
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