Three volatile organic compounds from a mangrove-derived Bacillus velezensis J64 inhibit Colletotrichum gloeosporioides via distinct transcriptional programs while preserving mango fruit quality under disease stress

Mango anthracnose, caused by Colletotrichum gloeosporioides , severely compromises fruit quality and leads to substantial postharvest losses, yet synthetic fungicides face mounting concerns over resistance and chemical residues. Mangrove ecosystems harbor microorganisms with unique metabolic adaptations under extreme environmental pressures, yet these habitats remain underexplored as sources of volatile organic compound (VOC)-producing biocontrol agents. From a mangrove-derived Bacillus velezensis J64, whole-genome sequencing revealed 4.01-Mb chromosome harboring genes encoding fatty acid β-oxidation and Radical SAM pathways for VOC biosynthesis, alongside multiple plant growth-promoting traits including siderophore production, phosphate solubilization, and indole-3-acetic acid synthesis. Volatilome profiling identified three structurally distinct VOCs: 2-nonanone (VOC1), 4-(pyrrolidin-2-ylcarbonyl)morpholine (VOC2), and 6,10-dimethylundecan-2-one (VOC3), a previously unreported antifungal compound. All three VOCs dose-dependently inhibited mycelial growth, compromised conidial membrane integrity as evidenced by SYTO-9/PI staining and cytoplasmic leakage, induced ultrastructural deformation, and suppressed appressorium formation, with potency VOC1 > VOC3 > VOC2. Comparative transcriptomics, with qPCR validation of representative genes involved in oxidative stress, chaperone function, and ribosome biogenesis, revealed distinct mechanisms: VOC1 downregulated MAPK signaling and proteostasis; VOC2 inhibited ribosome biogenesis and TCA cycle; VOC3 uniquely repressed mitochondrial biogenesis while inducing proteolytic stress, indicating complementary multi-target actions. In mango fruit trials, VOC fumigation reduced anthracnose lesions by 65.2–85.5%, preserved firmness (> 77%), and maintained or elevated total carotenoids. These findings establish mangrove-derived B. velezensis as a producer of chemically diverse VOCs with distinct transcriptional programs, and position mangrove habitats as promising underexplored sources of residue-free bio-preservatives that simultaneously suppress postharvest decay and safeguard fruit nutritional quality.