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.

Swarming: Flexible Roaming Plans

“…The S. marcescens data show that serrawettin does not extract water from the agar, i.e., is not an osmolyte: the bacteria are clearly able to hydrate the colony independently of serrawettin, as evidenced by their robust motility within the zone of inoculation; they are simply unable to spread this water in the absence of serrawettin. (We sound a cautionary note in this regard when assuming that surfactants extract liquid from the substrate [58,59].) In B. subtilis, the complete lack of motility in the absence of surfactin could stem from an additional signaling function for surfactin, which includes the production of more flagella, as judged by poor flagellation of surfactantdeficient mutants (60) (22,57,62,63).…”

“…The movement of swarming bacteria displays spatiotemporal features of collective motion similar to those seen in these other swarming systems and is being increasingly used to study the general principles of emergent behavior (49,118). Features being modeled include colony expansion, pattern formation, and behavior of individuals within the swarm (11,12,58,(119)(120)(121)(122)(123)(124).…”

Preparation, Imaging, and Quantification of Bacterial Surface Motility Assays

“…We have developed a protocol for the detailed macroscopic analysis of bacterial swarms that provides in addition to swarm zone morphology and size (e.g., diameter), quantitative dynamic information regarding swarm expansion rate and bacterial or bioproduct density distribution 7 . Furthermore, this method can take advantage of available fluorescent proteins, luminescence, and dyes to obtain a comprehensive view of bacterial interactions 8 , as well as to track the synthesis of bioproducts (e.g., P. aeruginosa rhamnolipid 7,8 ) within a swarm.…”

Type IV pili interactions promote intercellular association and moderate swarming of Pseudomonas aeruginosa

“…Cell-to-cell alignment is an included feature of many of these computational models and an experimental measurement frequently used to characterize ordering of cells within populations (9,10). For example, assumption of higher alignment among cells to improve collective motion in model simulations was crucial to recreation of the density wave propagating with the velocity of the experimentally observed traveling wave in P. aeruginosa swarms (7). However, it…”