c-di-GMP is required for swarming motility 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-{beta}-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. ImportanceIt 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.