C-di-GMP is Required for Swarming in E. coli: a Role for DgcO and Colanic Acid

Many bacteria use flagella to swim individually through bulk liquid, or swarm collectively over a semi-solid surface. In E. coli , c-di-GMP inhibits swimming via the effector protein YcgR. We show in this study that contrary to its effect on swimming, a certain threshold level of c-di-GMP is required for swarming. Gene expression profiles first indicated that several c-di-GMP synthases – dgcJ, dgcM, dgcO - were upregulated during swarming. Of these, we found DgcO to play a critical role. DgcO is reported to affect PGA (poly-β-1,6-N-acetylglucosamine) synthesis in E. coli . We show that DgcO also promotes production of colanic acid - one of the three major exopolysaccharides in E. coli , and that colanic acid has hitherto-unknown surfactant properties that are expected to aid swarming. Importance It is well-established that in bacteria, c-di-GMP inhibits flagella-driven motility at various points in the pathway. Concomitantly, elevated c-di-GMP levels induce the expression and synthesis of a variety of exopolysaccharides that enmesh the bacteria in a biofilm, thereby also interfering with flagella function. This study reports the surprising finding that in E. coli , the exopolysaccharide colanic acid is required to enable surface navigation and that the diguanylate cyclase DgcO is employed for this purpose. For surface navigation, there appears to be a sweet spot where c-di-GMP levels are just right to produce polysaccharides that can serve as surfactants and wetting agents rather than promote formation of biofilms.