Adaptation of Bacillus subtilis upon interaction with Setophoma terrestris results in loss of surfactin and plipastatin production

Metabolic exchange may define adaptation to the changes imposed by microbial interactions. We found that antifungal activity of cell-free supernatants of Bacillus subtilis ALBA01 is acquired after interacting with the soil fungus Setophoma terrestris (ST). Here we evaluated different traits of B. subtilis ALBA01 before (pre-ST) and after (post-ST) interacting with the fungus in co-cultures and inquired about the molecular mechanisms underlying this inter-kingdom interaction dependent antagonistic activity. Apart from the high fungal inhibition activity, we observed that the ability to form robust biofilms in vitro was a prevailing feature of post-ST and that biofilm formation was positively correlated to biocontrol efficacy. Moreover, nuclear magnetic resonance and mass spectrometry analysis revealed a differential metabolomics profile in post-ST variants, including the unexpected absence of surfactin or plipastatin production. Disruption of the srfAA gene implicated in surfactin synthesis resulted in an abolition of the ST-driven antifungal activity and ST growth inhibition levels similar to those observed for post-ST variants. The post-ST phenotype was stable after several passages on solid media, indicating that a mutation-based process underlies this phenotypic adaptation process. In fact, whole genome comparison revealed mutations that converge in genes of the ComQPXA quorum sensing system in post-ST variants. Altogether, our results suggest a role for a still unknown quorum sensing regulated pathway, which by classical antimicrobial lipopeptide abrogation mediates B. subtilis ALBA01 adaptive phenotypic variation and that may be responsible for the antagonistic behavior it exerts on S. terrestris.