How does P. aeruginosa organize into microcolonies?
Biofilms have been previously compared to bacterial cities. It turns out there is an interesting connection to ‘rich-get-richer’ economics also. Much existing work has been done on factors impacting surface adhesion of cells that make up a biofilm, and it is known that P. aeruginosa secretes the Psl exopolysaccharide, which promotes surface attachment by acting as a ‘molecular glue’. The first step in the social organization of biofilms, however, is the formation of microcolonies, groups of <50 cells that seem to spontaneously aggregate and thereby nucleate the growth of the biofilm. Despite decades of work, it is not well understood precisely how individual surface-attached bacteria self-organize into microcolonies. In this manuscript, we identify a new role for Psl in early biofilm development using a recently developed cell-tracking algorithms to extract the motility history of every cell. By combining these techniques with fluorescent Psl staining and state-of-the-art computer simulations, we show that P. aeruginosa cells deposit trails of Psl as they move on a surface. This communally secreted, intersecting Psl web drastically influences the surface exploration strategy of subsequent cells that encounter these trails, dictating the probabilities of where cells go and how long they stay. In fact, our data quantitatively show that the web of secreted Psl ultimately leads to a steep distribution of surface visit frequencies (i.e. how often a given surface patch is visited by cells) that can be approximated by a power law, driven by large heterogeneities in the distribution of Psl. This constitutes one type of ‘Zipf’s law’ behavior, which is a form of ‘rich-get-richer’ phenomena in nature. Our results indicate that the bacterial community self-organizes in a manner analogous to a capitalist economic system, a ‘rich-get-richer’ mechanism of Psl accumulation that results in a small number of ‘elite’ cells extremely enriched in communally produced Psl. Using engineered strains with inducible Psl production at different rates, we show that local Psl levels determine post-division cell fates and that high local Psl levels ultimately allow ‘elite’ cells to serve as the founding population for initial microcolony development. The surface movements of bacteria have always seemed random and complex, but we now know what they are trying to do and find astonishingly quantitative agreement between our simple model and the observed behavior