Ralstonia solanacearum (Rs), a soilborne phytopathogen, causes bacterial wilt disease in a broad range of hosts. Common approaches, for example, the direct reduction of the pathogen using classic single broad-spectrum probiotics, suffer from poor colonization efficiency, interference by resident microbiota, and nonnative-microorganism invasion. The soil microbiota plays an important role in plant health. Revealing the intrinsic linkage between the microbiome and the occurrence of disease and then applying it to agroecosystems for the precise control of soilborne diseases should be an effective strategy. Here, we surveyed the differences in the microbiome between healthy and diseased soils used for tomato planting across six climatic regions in China by using 16S rRNA amplicon and metagenomic sequencing. The roles of species associated with disease symptoms were further validated. Healthy soil possessed more diverse bacterial communities and more potential plant probiotics than diseased soil. Healthy soil simultaneously presented multiple strategies, including specifically antagonizing Rs, decreasing the gene expression of the type III secretion system of Rs, and competing for nutrition with Rs. Bacteria enriched in diseased samples promoted the progression of tomato bacterial wilt by strengthening the chemotaxis of pathogens. Therefore, Rs and its collaborators should be jointly combatted for disease suppression. Our research provides integrated insights into a multifaceted strategy for the biocontrol of tomato bacterial wilt based on the individual network of local microbiota. IMPORTANCE In the current work, the relationship between the soil microbiota and tomato bacterial wilt on a large scale offered us a comprehensive understanding of the disease. The delicate strategy of the microbiota in soil used for growing tomatoes to conquer the strong competitor, Rs, was revealed by microbiome research. The collaborators of Rs that coexist in a common niche with Rs strengthened our understanding of the pathogenesis of bacterial wilt. Bacteria enriched in healthy soil that antagonized pathogens with high specificity provide a novel view for ecofriendly probiotics mining. Our study offers new perspectives on soilborne-pathogen biocontrol in agroecosystems by decoding the rule of the natural ecosystem.
Keywords: Ralstonia solanacearum; multifaceted biocontrol; precision probiotics; soil microbiome.