Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus -Plant Mutualistic Interaction

Grégory Hoff (1, 2) , Anthony Arguelles Arias (2) , Farah Boubsi (2) , Jelena Pršić (2) , Thibault Meyer (2, 1) , Heba Ibrahim (3) , Sébastien Steels (2) , Patricio Luzuriaga (2) , Aurélien Legras (2) , Laurent Franzil (2) , Michelle Lequart-Pillon (4, 5) , Catherine Rayon (4, 5) , Victoria Osorio (6) , Edwin de Pauw (6) , Yannick Lara (7) , Estelle Deboever (8) , Barbara de Coninck (3) , Philippe Jacques (2) , Magali Deleu (8) , Emmanuel Petit (5, 9) , Olivier van Wuytswinkel (5, 4) , Marc Ongena (2)

1 LEM - Laboratoire d'Ecologie Microbienne - UMR 5557
2 BioEcoAgro - UMR transfrontalière INRAE 1158
3 KU Leuven - Catholic University of Leuven = Katholieke Universiteit Leuven
4 BioEcoAgro - Equipe 1 - Functioning and adaptation of the plant in interaction with its environment
5 BioEcoAgro BIOPI-UPJV
6 MolSys Research Unit [Liège]
7 Université de Liège
8 Laboratoire de Biophysique Moléculaire aux Interfaces
9 BioEcoAgro - Equipe 5 - Specialized Metabolites of Plant Origin

Bacillus velezensis is considered as a model species belonging to the socalled Bacillus subtilis complex that evolved typically to dwell in the soil rhizosphere niche and establish an 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 a polymer-sensing system to perceive their host and that, in response, they increase the production of the surfactintype lipopeptide. Furthermore, we demonstrate that surfactin synthesis is favored 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 coproduced in planta and forms mainly variants that are the most active at triggering plant immunity. Surfactin represents a shared good as it reinforces the defensive capacity of the host. IMPORTANCE 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 the production of the surfactin lipopeptide upon sensing pectin as a 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 a unique shared good to sustain a mutualistic interaction.

Mots clés: lipopeptides; plant cell wall polymers; plant immunity; molecular crosstalk; plant-microbe interactions

Domaines: Microbiologie et Parasitologie

Grégory Hoff, Anthony Arguelles Arias, Farah Boubsi, Jelena Pršić, Thibault Meyer, et al.. Surfactin Stimulated by Pectin Molecular Patterns and Root Exudates Acts as a Key Driver of the Bacillus -Plant Mutualistic Interaction. mBio, 2021, 12 (6), ⟨10.1128/mBio.01774-21⟩. ⟨hal-03522340⟩