Microbiome and volatile organic compound profiling of diseased soils and their association with tomato wilt caused by Ralstonia solanacearum

Soil volatile organic compounds (VOCs) are critical in suppressing soil-borne pathogens, yet their microbial origin, functional mechanisms, and contribution to disease suppression remain underexplored. This study investigated the role of VOCs in the disease-suppressive capacity of soils from two tomato monocropping regions against Ralstonia solanacearum , the causative agent of bacterial wilt. Among the disease-conductive and suppressive soils, suppressive soil showed the lowest disease incidence (0.37%) and pathogen load (9.6 × 10³ CFU/g), which was linked to potent soil VOC-mediated suppression of R. solanacearum growth and disease occurrence. GC-MS analysis identified 13 VOCs significantly related to disease index, including naphthalene, 2-undecanone, and humulene, which inhibited pathogen growth in vitro and promoted plant growth and defense enzymes (CAT, SOD). Amplicon sequencing revealed differences in microbial community diversity and composition between conductive and suppressive soils, with Streptomyces as a key disease-suppressive taxon. Isolation of 10 Streptomyces strains from suppressive soil confirmed their role in restoring VOC-mediated suppressiveness in sterilized soil, with strain Stre2 achieving 46.17% pathogen inhibition. Correlation, Procrustes, and variation partitioning analyses (VPA) demonstrated that soil physicochemical and microbial factors jointly shaped soil VOC composition, but bacterial communities also exerted a significant direct influence (11.1% unique contribution). Our findings demonstrate that disease-suppressive soils harness microbiota-derived VOCs to inhibit R. solanacearum and prime plant defenses, offering novel insights for sustainable pathogen management through microbial metabolite engineering.