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

As parasites of bacteria, phages can regulate microbiome diversity and composition and may therefore affect susceptibility to pathogens and disease. Many infectious diseases are associated with altered bacteriophage communities, but observational studies alone do not allow us to determine when altered phage community composition is a contributor to disease risk, a response to infection, or simply an indicator of dysbiosis. To address this question directly, we used size-selective filtration to deplete plant-associated microbial communities of phages, then challenged plants with the bacterial pathogen Pseudomonas syringae. Plants with phage-depleted microbiomes were more susceptible to infection, an effect that could not be explained by direct effects of the phage communities on either P. syringae or the plant host. Moreover, the presence of phages was most impactful when the phage communities were isolated from neighboring field locations rather than from the same host plant as the bacteria, possibly suggesting that moderate rates of lysis maintain a 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.