Long-range alteration of the physical environment mediates cooperation betweenPseudomonas aeruginosaswarming colonies

Abstract

AbstractPseudomonas aeruginosamakes and secretes massive amounts of rhamnolipid surfactants that enable swarming motility over biogel surfaces. But how this rhamnolipids interact with biogels to assist swarming remains unclear. Here I use a combination of optical techniques across scales and genetically-engineered strains to demonstrate that rhamnolipids can induce agar gel swelling over distances > 10,000x the body size of an individual cell. The swelling front is on the micrometric scale, and is easily visible using shadowgraphy. Rhamnolipid transport is not restricted to the surface of the gel, but occurs through the whole thickness of the plate and, consequently, the spreading dynamics depends on the local thickness. Surprisingly, rhamnolipids can cross the whole gel and induce swelling on the opposite side of a two-face Petri dish. The swelling front delimits an area where the mechanical properties of the surface properties are modified: water wets the surface more easily, which increases the motility of individual bacteria and enables collective motility. A genetically-engineered mutant unable to secrete rhamnolipids (DrhlA), and therefore unable to swarm, is rescued from afar with rhamnolipids produced by a remote colony. These results exemplify the remarkable capacity of bacteria to change the physical environment around them and its ecological consequences.Significance statementLiving organisms have the ability to interact mechanically with their environment.Pseudomonas aeruginosa, a motile bacterium, can spread collectively on biogels, a behavior called swarming. Rhamnolipids, surfactant moleculesP. aeruginosamake and secrete, are required for swarming. Here, I demonstrate rhamnolipids not only physically alter the biogel in the vicinity of the secreting cells, but also over distances much greater than the bacterial cell size, through gel swelling. This long-distance physical alteration can even rescue a remote colony which would not produce rhamnolipids. This work illustrates the remarkable ability of bacteria to change the mechanical property of the world surrounding them.