RoL: FELS: EAGER: Disease resistance as a product of synergy between host immunity and the microbiome

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It is now well-established that the microbiome (the community of microbial species associated with a host organism) can increase host nutrient acquisition and protect against disease. Even so, which communities of bacteria will provide positive outcomes for their hosts cannot be reliably predicted. In large part, this is because there are seemingly infinite configurations of "healthy" microbiomes, making analysis of natural patterns difficult. Moreover, understanding of microbiome function is currently hampered by the complexity of host-microbe and microbe-microbe interactions underlying these positive outcomes. Despite this complexity, however, recent research suggests that general principles underlying microbiome-mediated protection against pathogen establishment and disease may be identifiable. The combination of new sequencing technologies and the development of new experimental systems presents a unique opportunity to begin disentangling the interactions between the microbiome and disease, and to examine the generality of microbiome-mediated protection across different host species. A starting point for such an undertaking focuses on a broad host range pathogen, for which evidence of microbiome-mediated protection currently exists across multiple hosts. Using two different plant-microbiome-pathogen systems (one with direct relevance to forestry management and the other to agriculture) as proof of concept, the current work aims to build a predictive framework for identifying microbial consortia that synergize with the host immune system to protect against disease. Building upon existing data from Bleeding Canker disease of Horse Chestnut trees and Bacterial Speck of Tomato plants, both of which are caused by pathovars of the bacterial pathogen, Pseudomonas syringae, this project will test the idea that there are general rules underlying microbiome-mediated protection that are applicable across systems. In each of these two systems, previous evidence has linked the diversity and composition of the phyllosphere (above ground) microbiome to pathogen colonization success and/or plant disease outcome. This project will use culture-independent sequencing data from the natural tree system to generate predictions about microbiome-mediated disease protection based on microbiome composition, diversity, and/or function. These predictions will then be tested using synthetic microbiomes in tomato plants, where the relative contributions of direct (microbe-microbe) and indirect (plant-mediated) effects in shaping microbiome-mediated protection can be experimentally quantified. By combining high-throughput seedling priming assays with a synthetic microbiome approach, the project seeks to identify disease protective community properties that synergize with plant defenses. The general principles of microbiome-mediated protection that this project seeks to uncover have the potential to be broadly applicable across systems, and inform predictions about protective microbial communities in human health and agriculture. The ultimate goal of the work is to be able to leverage these host-microbiome-pathogen interactions to attain robust and durable disease protection, and the results will aid in management of both agricultural and natural systems, and the development of probiotic treatment against plant disease.This award reflects NSF's statutory mission and has been deemed worthy of support through evaluation using the Foundation's intellectual merit and broader impacts review criteria.