c-di-GMP is required for swarming in E. coli, producing colanic acid that acts as surfactant.

Abstract

Many bacteria use flagella to swim individually through bulk liquid or swarm collectively over a semi-solid surface. In Escherichia 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, and dgcO-were upregulated during swarming. Of these, we found DgcO to play a critical role in promoting the production of colanic acid-one of the three major exopolysaccharides in E. coli. DgcO has been reported to increase poly-β-1,6-N-acetylglucosamine (PGA) synthesis in E. coli as well. We show 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 the flagella function. This study reports the surprising finding that, in Escherichia 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 the formation of biofilms.