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Abstract Beneficial rhizobacteria promote plant growth and protect plants against phytopathogens. Effective colonization on plant roots is critical for the rhizobacteria to exert beneficial activities. How bacteria migrate swiftly in the soil of semisolid or solid nature remains unclear. Here we report that sucrose, a disaccharide ubiquitously deployed by photosynthetic plants for fixed carbon transport and storage, and abundantly secreted from plant roots, promotes solid surface motility (SSM) and root colonization by Bacillus subtilis through a previously uncharacterized mechanism. Sucrose induces robust SSM by triggering a signaling cascade, first through extracellular synthesis of polymeric levan, which in turn stimulates strong production of surfactin and hyper-flagellation of the cells. B. subtilis poorly colonizes the roots of Arabidopsis thaliana mutants deficient in root-exudation of sucrose, while exogenously added sucrose selectively shapes the rhizomicrobiome associated with the tomato plant roots, promoting specifically bacilli and pseudomonad. We propose that sucrose activates a signaling cascade to trigger SSM and promote rhizosphere colonization by B. subtilis. Our findings also suggest a practicable approach to boost prevalence of beneficial Bacillus species in plant protection. 

Abstract InBacillus subtilis, robust biofilm formation requires large quantities of ferric iron. Here we show that this process requires preferential production of a siderophore precursor, 2,3-dihydroxybenzoate, instead of the siderophore bacillibactin. A large proportion of iron is associated extracellularly with the biofilm matrix. The biofilms are conductive, with extracellular iron potentially acting as electron acceptor. A relatively small proportion of ferric iron is internalized and boosts production of iron-containing enzymes involved in respiratory electron transfer and establishing strong membrane potential, which is key to biofilm matrix production. Our study highlights metabolic diversity and versatile energy generation strategies withinB. subtilisbiofilms.