Offensive role of the Bacillus extracellular matrix in driving metabolite-mediated dialog and adaptive strategies with the fungus Botrytis

Bacterial-fungal interactions have traditionally been attributed to secondary metabolites, but the role of the bacterial extracellular matrix in shaping these relationships has remained unclear. Here, we demonstrate that the extracellular matrix protein TasA is a key mediator in the antagonistic interaction between Bacillus subtilis and Botrytis cinerea. TasA enables Bacillus to tightly adhere to fungal hyphae, disrupts the β-glucan layer, and compromises fungal cytoskeletal integrity synergistically with fengycin, which causes cytological damage. Additionally, TasA acts as a carrier for bacillaene, amplifying its fungistatic activity. In response, Botrytis mounts a multifaceted defense, enzymatically degrading fengycin, producing antibacterial oxylipins, and activating adaptive programs such as hyphal branching and chlamydospore formation. Our findings reveal the previously unrecognized role of extracellular matrix components in fungal suppression and the modulation of fungal adaptive responses. This study reveals the complex interplay between microbial aggression and defense, providing new insights into the ecological dynamics of microbial competition and coexistence.