Inter-Bacterial Communication through Exopolysaccharide Sensing

Our understanding of how bacteria communicate with one another via secreted exopolysaccharide (EPS) macromolecules is in its infancy, which stands in stark contrast to our understanding of quorum sensing via secreted small molecules. During early stages of forming a biofilm community, Pseudomonas aeruginosa (Pa) PAO1 can sense EPS trails of Psl deposited on a surface by previous Pa cells to orchestrate motility. This sensory signal is transduced into cyclic-di-guanylate monophosphate (cdGMP) second messengers, but none of the known receptors/adhesins that bind to Psl components have any roles in signal transduction. In this work, we show an unanticipated mechanism of EPS sensing based on continuous mechanochemical surveillance of Pa’s environment. This sensing is conducted via type IV pili (T4P) appendages pulling against cell-body localized adhesins, such as mannose-binding CdrA, which interacts with Psl trails. Using both bacterial-secreted Psl trails and glycopolymer-patterned surfaces, we found that Pa is capable of sensing EPS directly through T4P-powered ‘force spectroscopy’ of bonds formed between adhesins and specific EPS motifs. Whereas bacterial lifestyles are generally classified into free-swimming planktonic bacteria with low cdGMP, and sessile, biofilm bacteria with high cdGMP, we propose that these EPS trail interactions generate a hybrid, transitional planktonic-to-biofilm population with simultaneously elevated cdGMP, cAMP, and motility capable of following EPS trails. Our results demonstrate a generalizable mechanism of surface chemo-sensing through mechanosensitive appendages, facilitating spatiotemporal cell-cell communicative responses through motility and EPS.