Sucrose triggers a novel signaling cascade promoting Bacillus subtilis rhizosphere colonization

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.

Bacillus subtilis Colonization of Arabidopsis thaliana Roots Induces Multiple Biosynthetic Clusters for Antibiotic Production

“…To address this question systematically, we considered the overall effect of the plant host in regulating the transcription from four distinct promoters for B. subtilis antibiotics: surfactin, bacillaene, bacilysin, and plipastatin. As the population within B. subtilis biofilms and root associated communities is heterogeneous ( Lopez et al., 2009 ; Beauregard et al., 2013 ; Tian et al., 2021 ), we monitored the expression in the single-cell level relying on flow cytometry and imaging flow cytometry (IFC). The latter combines the power and speed of traditional flow cytometers with the resolution of a microscope.…”

Experimental evolution ofBacillus subtilisonArabidopsis thalianaroots reveals fast adaptation and improved root colonization in the presence of soil microbes

“…From an applied perspective, experimental evolution of B. subtilis on plant roots represents a novel approach for developing strains with enhanced root attachment capacities for agricultural use. However, a biofilmmotility tradeoff as observed here may be undesirable when developing biocontrol agents due to the growing evidence of motility as an important trait for bacterial root colonization in soil systems [16,61].…”

“…From an applied perspective, experimental evolution of B. subtilis on plant roots represents a novel approach for developing strains with enhanced root attachment capacities for agricultural use. However, a biofilmmotility tradeoff as observed here may be undesirable when developing biocontrol agents due to the growing evidence of motility as an important trait for bacterial root colonization in soil systems [16, 61]. The phenotypes associated with adaptation of B. subtilis to A. thaliana roots presented here as well as the accompanying evolutionary cost and the increased root colonization even in the presence of resident soil bacteria highlight the importance of considering the selective environment if evolving PGPR for biocontrol purposes.…”

“…This enhanced establishment on the root by Ev7.3 is not expected to be caused by altered antagonistic activities towards the community members. First, no major growing evidence of motility as an important trait for bacterial root colonization in soil systems [16,61].…”

Imaging flow cytometry reveals a dual role for exopolysaccharides in biofilms: To promote self-adhesion while repelling non-self-community members

“…Here, we used imaging flow cytometry to evaluate the roles of all major extracellular matrix components in microbial competition for floating biofilm (pellicle) formation. The population within B. subtilis biofilms and root associated communities is heterogeneous [14] , [34] , [35] , a heterogenicity which is affected by the production of the extracellular matrix. To overcome this fundamental property of biofilms, we monitored the effects of the extracellular matrix on the single cell level, relying on imaging flow cytometry.…”