Plant cell wall polysaccharides facilitate proliferation of soil-derived Flavobacterium spp.

Terrestrial Flavobacteria are highly enriched in root environments compared with their abundance in bulk soil, suggesting that they have evolved means to exploit the unique rhizosphere environment. While the specific mechanisms underlying this phenomenon are currently unclear, we hypothesize that the unique gliding motility of flavobacteria, combined with their capacity to degrade complex plant derived polysaccharides, facilitate their colonization and proliferation on root surfaces. In this study, we assessed the impact of complex plant cell wall carbohydrates (pectin, glucomannan and cellulose) on flavobacterial growth dynamics. We discovered that glucomannan and pectin drive significant directional expansion of two Flavobacterium strains even when grown on nutrient-rich media. No such response was found for other sugars, including monosaccharide pectin components (galacturonic acid and rhamnose). Pectin-facilitated flavobacterial proliferation was found to be dose dependent. Interestingly, pectin affected gliding velocity and colony density but did not significantly increase bacterial biomass production. Proteomic analysis of Flavobacterium johnsoniae revealed that pectin did not affect the expression of bacterial motility-gliding and secretion proteins (although several of these were not detected), but induced a specific set of SusC and D and TonB receptors associated with an outer membrane protein complex for polysaccharide uptake. Our results thus suggest that the enhanced gliding motility observed in response to pectin may be driven by a yet unknown regulator also involved in upregulation of TonB receptors. The capacity of selected terrestrial Flavobacterium strains to thrive in root ecosystems thus appears to be linked to identification and utilization of specific plant cell wall components.