Passaging phyllosphere microbial communities develop suppression towards bacterial speck disease in tomato

Microbial community-based disease management approaches have the potential to substitute or combine with currently employed strategies. Suppressive soils are great examples of microbial communities that suppress soilborne plant disease after severe outbreaks and are maintained over multiple years or crop cycles. While there are many suppressive soil examples, to our knowledge, there are no descriptions of disease suppressive phyllosphere communities. Therefore, we investigated whether a phyllosphere microbial community could be developed through a selective passaging method to suppress disease using the model pathosystem of Pseudomonas syringae pv. tomato (Pto) and tomato. Field tomato phyllosphere microbial communities were recovered, and spray transferred to greenhouse tomato plants, after which were inoculated with Pto. Disease severity was visually estimated, and the microbial communities were recovered to be independently applied to the next passage. Overall, greenhouse passaging resulted in an increase in disease severity for all passage lines from the initial passage, which peaked at passage 4-5, followed by a sharp decline until passage 9. The disease severity at passage 9 was also significantly lower than a non-passaged Pto only comparison. Heat-treatment of passage 9 communities resulted in elevated disease severity over several subsequent passages in the growth chamber, whereas the untreated community maintained low disease. Community-only passage lines (without Pto inclusion during passaging) did not show disease suppression after subsequent pathogen introduction. This work presents an experimental approach to develop phyllosphere microbial communities in the presence of a phytopathogen to enrich for a low disease phenotype and results in maintained disease suppression.