Cell-Surface and Periplasmic Deconstruction of Xylan by Oligotrophic Bacterium Caulobacter vibrioides

Bacterial species that inhabit diverse nutritional niches, such as plants, the human gut, and aquatic environments, exhibit common and unique molecular mechanisms for acquiring nutrients from plant polysaccharides like xylan. The oligotrophic bacterium Caulobacter vibrioides (Syn. Caulobacter crescentus) shows unique adaptations for growth in low-nutrient conditions and codes for a repertoire of genes that facilitate xylan utilisation as a carbon source. Investigation of xylan and xylan-derivative utilisation by C. vibrioides shows membrane-bound xylanase-mediated xylan deconstruction on the cell surface and further deconstruction of the xylo-oligosaccharides in the periplasm by xylosidases and other accessory enzymes. Proton motive force disruption studies suggest involvement of TonB-dependent transporters, Major Facilitator Superfamily transporters, or ATP-Binding Cassette transporters in the transport of xylo-oligosaccharides and other xylan-derivatives across the membranes of C. vibrioides. Results from our studies using enzyme assays and chromatographic analyses suggest that bacteria deconstruct xylan in a surface-bound manner leading to efficient uptake of xylo-oligosaccharides across the outer membrane, without loss of nutrients to the environment. This proposed model for C. vibrioides xylan utilisation highlights both unique and similar mechanistic features found in gut and plant pathogenic bacteria, advancing the molecular understanding of nutrient acquisition in oligotrophic Gram-negative bacteria.