The Biocontrol Activity and Antifungal Mechanism of <i>Bacillus velezensis</i> GX0003742 Against Banana Anthracnose Revealed by Whole-Genome Sequencing and UPLC-MS Analysis

Banana (Musa spp.) is one of the most important economic crops worldwide. However, banana anthracnose caused by Colletotrichum musae severely affects banana yield and quality. In this study, a bacterial strain, Bacillus velezensis GX0003742, exhibiting strong antifungal activity against C. musae, was isolated from the rhizosphere soil of mangroves in an abandoned salt field in Beihai, Guangxi, China. B. velezensis GX0003742 exhibited broad-spectrum antifungal activity. Additionally, the strain displayed plant growth-promoting rhizobacteria traits. Biocontrol evaluation demonstrated that B. velezensis GX0003742 significantly delayed the onset of postharvest banana anthracnose and effectively preserved fruit quality. Furthermore, B. velezensis GX0003742 also exhibited protective effects on banana plants, reducing C. musae-induced damage while promoting plant growth and development. Whole-genome sequencing analysis revealed that B. velezensis GX0003742 has a genome size of 3,886,227 bp with a GC content of 47.29%. CAZyme annotation identified multiple genes encoding antifungal proteins, while antiSMASH analysis predicted the presence of biosynthetic gene clusters responsible for producing macrolactin H, bacillaene, bacillibactin, bacilysin, butirosin A/B, fengycin, difficidin, and surfactin. Comparative genomic analysis further revealed that GX0003742 harbors an abundant array of secondary metabolite biosynthetic gene clusters. B. velezensis GX0003742-derived active metabolites disrupted C. musae cell wall integrity, increased cell membrane permeability, and led to intracellular leakage. Additionally, these metabolites induced mitochondrial reactive oxygen species accumulation, causing oxidative damage to mitochondria. In conclusion, B. velezensis GX0003742 exhibits promising biocontrol potential against banana anthracnose through multiple antifungal mechanisms. Moreover, its diverse metabolic profile highlights its potential as a novel biocontrol agent, providing a feasible solution for the management of banana anthracnose.