Succinate treatment reduces bacterial wilt disease and modulates the viable soil microbiota in tomato

Abstract Succinate is an intermediate of the tricarboxylic acid cycle and is well known for its role in energy metabolism. However, succinate is also involved in diverse cellular signaling processes in various organisms and may also play signaling roles in the plant microbiome. Previously, we showed that succinate acts as a public good in microbial syntrophy between an unculturable beneficiary and a helper bacterium, supporting the viability of energy-auxotrophic bacteria and their wide distribution in soil. In this study, we examined whether succinate treatment manages tomato bacterial wilt and modulates the viable soil microbiota. When tomato plants were treated with succinate together with an upland soil microbial fraction, bacterial wilt disease was significantly reduced. To assess the impact of exogenous succinate on bulk and rhizosphere soil microbiota, we performed microbiome analyses using propidium monoazide to focus on viable bacterial communities. Succinate treatment significantly increased microbial diversity in both bulk and rhizosphere soil microbiota, enriching Nocardioidaceae, Sphingomonadaceae, and Paenibacillaceae in bulk soil and Sphingomonadaceae and Erythrobacteraceae in the tomato rhizosphere. Based on microbiome data, we constructed a succinate-responsive synthetic community (SynCom) comprising six bacterial strains isolated from upland soil. Interestingly, the SynCom suppressed bacterial wilt only when co-applied with succinate in tomato plants. Our findings indicate that exogenous succinate can be used as a novel bioprotectant to manage bacterial wilt by enriching viable beneficial soil microbiota, offering a promising strategy for sustainable agriculture.