Microbial volatile humulene orchestrates plant-microbe alliance to establish disease-suppressive rhizosphere

Microbial volatile organic compounds (mVOCs) suppress growth and virulence traits of soil-borne pathogens, yet their ecological roles in disease suppression remain unclear. Here, we show that the sesquiterpene humulene from Streptomyces acts as a multifunctional regulator that suppresses bacterial wilt through coordinated inhibition of Ralstonia solanacearum, plant metabolic reprogramming, and rhizosphere microbiome modulation. We combined in vitro pathogen assays, pot experiments, microbiota transplantation, rhizosphere 16S rRNA profiling, root-exudate metabolomics, and plant and pathogen transcriptomics to investigate the direct and microbiome-mediated effects of humulene. Humulene reduced disease severity and pathogen abundance via a microbiome-dependent mechanism. Microbiota transplantation confirmed that the humulene-conditioned microbiome retains transferable disease-suppressiveness. Humulene also selectively enriched antagonistic Streptomyces, not by direct growth promotion, but by reprogramming tomato root exudation to produce lipid-derived petroselinic acid, which promoted Streptomyces growth, humulene production, and pathogen suppression. Root transcriptomics further revealed activation of lipid metabolic pathways involving alternative fatty acid desaturation and oxylipin signaling. Together, humulene functions as an ecological signal that integrates pathogen suppression, host lipid metabolism, and microbiome assembly to establish a disease-suppressive rhizosphere, enabling microbiome-informed control of bacterial wilt.