Phages indirectly maintain plant pathogen defense through regulation of the commensal microbiome

Many infectious diseases are associated with altered communities of bacteriophage viruses (phages). As parasites of bacteria, phages can regulate microbiome diversity and composition and may therefore affect disease susceptibility. Yet observational studies alone do not allow us to determine whether altered phage profiles are a contributor to disease risk, a response to infection, or simply an indicator of dysbiosis. To address this question, we used size-selective filtration to separate plant-associated microbial communities from their respective phages, then transplanted them together or separately onto tomato plants that we subsequently challenged with the bacterial pathogen Pseudomonas syringae. Microbial and phage communities together were more disease-protective than either component was alone, an effect that could not be explained by direct effects of phages on either P. syringae or the plant host. Moreover, the protective effect of phages was strongest when microbial and phage communities were isolated from neighboring field locations (allopatric phages), rather than from the same host plant (sympatric phages). This suggests a Goldilocks effect in which moderate rates of phage lysis maintain a microbiome community structure that is most resistant to pathogen invasion. Overall, our results support the idea that phage communities contribute to plant defenses by modulating the microbiome.