Black Soldier Fly Gut Microbiota as a Green Alternative to Chemical Fungicides: Broad-Spectrum Biocontrol and Implications for Reducing Fungicide Environmental Loading

Abstract Plant diseases cause 20%–40% of global crop losses, a problem traditionally managed by chemical fungicides whose extensive use leads to widespread environmental contamination and potential human health risks. This underscores an urgent need for sustainable, low-environmental-impact alternatives. Black soldier fly (BSF)-mediated bioconversion of organic wastes offers a circular economy solution, producing frass with reported plant disease suppression potential; however, the underlying mechanisms remain largely unexplored. Here, we demonstrate that BSF frass exhibits in vitro broad-spectrum antifungal activity against major plant pathogens. We reveal that gut bacteria from BSF larvae, enriched in the frass during bioconversion, are the key drivers of this suppression. These bacteria employ two complementary mechanisms of action: volatile organic compounds (VOCs) exert long-distance effects, causing surface roughening and loss of turgidity of fungal hyphae, while liquid-phase secondary metabolites (LMs) result in intense disruption, leading to severe distortion and fragmentation of fungal cells. By isolating functional strains and constructing a synthetic microbial community (SynCom) based on their synergistic interactions, we develope a potent biocontrol agent. In potato trials, SynCom provides disease control comparable to raw frass for both black scurf and late blight, while achieving significantly greater reduction of rhizospheric Phytophthora infestans abundance (64% ± 13% vs 48% ± 15% with frass, p < 0.05). Our study identifies BSF gut bacteria as the key source of frass biocontrol capacity and validates the SynCom as an environmentally benign alternative to chemical fungicides, providing a sustainable solution that integrates agricultural disease management with organic waste recycling.