Surfactin stimulated by pectin molecular patterns and root exudates acts as a key driver of Bacillus-plant mutualistic interaction

Bacillus velezensis is considered as model species belonging to the so-called B. subtilis complex that typically evolved to dwell in the soil rhizosphere niche and establish intimate association with plant roots. This bacterium provides protection to its natural host against diseases and represents one of the most promising biocontrol agents. However, the molecular basis of the cross-talk that this bacterium establishes with its natural host has been poorly investigated. We show here that these plant-associated bacteria have evolved some polymer-sensing system to perceive their host and that in response, they increase the production of the surfactin-type lipopeptide. Furthermore, we demonstrate that surfactin synthesis is favoured upon growth on root exudates and that this lipopeptide is a key component used by the bacterium to optimize biofilm formation, motility and early root colonization. In this specific nutritional context, the bacterium also modulates qualitatively the pattern of surfactin homologues co-produced in planta and mainly forms variants that are the most active at triggering plant immunity. Surfactin represents a shared good as it reinforces the defensive capacity of the host. Significance Statement Within the plant-associated microbiome, some bacterial species are of particular interest due to the disease protective effect they provide via direct pathogen suppression and/or stimulation of host immunity. While these biocontrol mechanisms are quite well characterized, we still poorly understand the molecular basis of the cross talk these beneficial bacteria initiate with their host. Here we show that the model species Bacillus velezensis stimulates production of the surfactin lipopeptide upon sensing pectin as cell surface molecular pattern and upon feeding on root exudates. Surfactin favors bacterial rhizosphere fitness on one hand and primes the plant immune system on the other hand. Our data therefore illustrate how both partners use this multifunctional compound as unique shared good to sustain mutualistic interaction.