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

Many bacteria use flagella to swim individually through bulk liquid or swarm collectively over a semi-solid surface. In <i>Escherichia coli</i>, 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<i>-dgcJ</i>, <i>dgcM</i>, and <i>dgcO</i>-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 <i>E. coli</i>. DgcO has been reported to increase poly-β-1,6-N-acetylglucosamine (PGA) synthesis in <i>E. coli</i> 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 <i>Escherichia coli</i>, 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.