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

Abstract Soil volatile organic compounds (VOCs) are critical for suppressing soil-borne pathogens, yet their microbial origins, functional mechanisms, and contributions 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 exhibited the lowest disease incidence (0.37%) and pathogen load (9.6 × 10 3 CFU/g), which was associated with strong soil VOC-mediated suppression of R. solanacearum growth and disease development. GC–MS analysis identified 13 VOCs significantly related to the disease index, including naphthalene, 2-undecanone, and humulene, which inhibited pathogen growth in vitro and promoted plant growth and defense enzymes (CAT and 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) showed that soil physicochemical and microbial factors together shaped the composition of soil VOCs, but bacterial communities also had a significant direct influence (11.1% unique contribution). Our results demonstrate that disease-suppressive soils utilize microbiota-derived VOCs to inhibit R. solanacearum and prime plant defenses, offering new insights for sustainable pathogen management through microbial metabolite engineering.