There is increasing understanding that the plant root microbiome plays a pivotal role in plant health. A myriad of studies by our group and others have demonstrated that certain members of the Flavobacterium genus (phylum Bacteroidetes) are highly abundant in the rhizosphere of a wide array of plants, and that the relative abundance of these strains increases along the soil, rhizosphere, root-surface continuum. Furthermore, several strains of root-associated flavobacteria promote plant growth and/or confer resistance to plant pathogens, suggesting that they may be an important component of the root-associated microbiome. The high abundance of flavobacteria on plant roots suggests that these strains possess traits that enable them to compete and proliferate in this highly competitive environment; however, the specific mechanisms that confer rhizosphere competence in flavobacteria are currently an enigma. Several studies conducted in or lab collectively demonstrated that the unique Bacteroidetes gliding motility/type IX secretion system plays a pivotal role in both seed adhesion and plant root colonization, and indirect evidence suggest that this flavobacterial-root association is directly linked to induced plant resistance to foliar pathogens. Furthermore, through comparative genomics and a series of in-vitro proteomic-based analyses we determined that root-associated flavobacteria specialize in metabolism of specific plant cell wall glycans and that there is a direct link between gliding motility and metabolism of selected glycans. Collectively, the results presented here are unique in that they provide a comprehensive link between microbial ecology and bacterial physiology. We believe that uncovering this link is crucial for understanding plant-microbe interactions and for the development of plant growth promoting and biocontrol agents to address emerging challenges of global food security and environmental sustainability.