High density waves of the bacterium Pseudomonas aeruginosa in propagating swarms result in efficient colonization of surfaces

Abstract

This work describes a new, to our knowledge, strategy of efficient colonization and community development where bacteria substantially alter their physical environment. Many bacteria move in groups, in a mode described as swarming, to colonize surfaces and form biofilms to survive external stresses, including exposure to antibiotics. One such bacterium is Pseudomonas aeruginosa, which is an opportunistic pathogen responsible for both acute and persistent infections in susceptible individuals, as exampled by those for burn victims and people with cystic fibrosis. Pseudomonas aeruginosa often, but not always, forms branched tendril patterns during swarming; this phenomena occurs only when bacteria produce rhamnolipid, which is regulated by population-dependent signaling called quorum sensing. The experimental results of this work show that P. aeruginosa cells propagate as high density waves that move symmetrically as rings within swarms toward the extending tendrils. Biologically justified cell-based multiscale model simulations suggest a mechanism of wave propagation as well as a branched tendril formation at the edge of the population that depends upon competition between the changing viscosity of the bacterial liquid suspension and the liquid film boundary expansion caused by Marangoni forces. Therefore, P. aeruginosa efficiently colonizes surfaces by controlling the physical forces responsible for expansion of thin liquid film and by propagating toward the tendril tips. The model predictions of wave speed and swarm expansion rate as well as cell alignment in tendrils were confirmed experimentally. The study results suggest that P. aeruginosa responds to environmental cues on a very short timescale by actively exploiting local physical phenomena to develop communities and efficiently colonize new surfaces.