Plant cell wall polysaccharides induce colony expansion of soil-derived Flavobacterium spp.

Flavobacterium is a genus of gram-negative bacteria, belonging to the Bacteriodetes phylum, characterized by a unique gliding motility. They are ubiquitous and often abundant in root microbiomes of various plants, but the factors contributing to this high abundance are currently unknown. In this study, we evaluate the effect of various plant-associated poly- and mono-saccharides on growth and colony expansion of two Flavobacterium strains (F. Johnsoniae, Flavobacterium sp. F52). Both strains were able to grow on pectin and other polysaccharides such as cellulose as a single carbon source. However, only pectin, a polysaccharide that is profuse in plant cell walls, enhanced colony expansion on solid surfaces even under high nutrient availability, suggesting a link between carbohydrate metabolism and gliding. Expansion on pectin was dose- and substrate-dependent, as it did not occur when bacteria were grown on the pectin monomers galacturonic acid and rhamnose. Using time-lapse microscopy, we demonstrated a bi-phasic expansion of F. johnsoniae on pectin: an initial phase of rapid expansion, followed by biomass production within the colonized area. Proteomics and gene expression analyses revealed significant induction of several carbohydrate metabolism related proteins when F. johnsoniae was grown on pectin, including selected operons of SusC/D, TonB-dependent glycan transport genes. Our results suggest a yet unknown linkage between specific glycan associated operons and flavobacterial motility. This may be associated with their capacity to rapidly glide along the root and metabolize plant cell wall carbohydrates, two characteristics that are crucial to rhizosphere competence.