Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms

Cell-tracking experiments and simulations show that the Psl exopolysaccharide deposited by Pseudomonas aeruginosa guides the surface motility of subsequent cells that encounter the Psl trails, generating a ‘rich-get-richer’ effect that leads to microcolony formation. A 'rich-get-richer' mechanism for biofilm formation How bacteria self-organize into microcolonies — the first step towards forming biofilms — is poorly understood. Here Gerard Wong and colleagues use a massively parallel cell-tracking algorithm to extract the motility history of every cell during colonization of a new surface. This system reveals that Pseudomonas aeruginosa deposits a trail of exopolysaccharide which influences the motility of any other cells that subsequently encounter it, generating a positive feedback that directs the cells to form a microcolony. The positive feedback observed here is analagous to the 'rich-get-richer' power law observed in wealth distribution. Bacterial biofilms are surface-associated, multicellular, morphologically complex microbial communities 1 , 2 , 3 , 4 , 5 , 6 , 7 . Biofilm-forming bacteria such as the opportunistic pathogen Pseudomonas aeruginosa are phenotypically distinct from their free-swimming, planktonic counterparts 7 , 8 , 9 , 10 . Much work has focused on factors affecting surface adhesion, and it is known that P. aeruginosa secretes the Psl exopolysaccharide, which promotes surface attachment by acting as ‘molecular glue’ 11 , 12 , 13 , 14 , 15 . However, how individual surface-attached bacteria self-organize into microcolonies, the first step in communal biofilm organization, is not well understood. Here we identify a new role for Psl in early biofilm development using a massively parallel cell-tracking algorithm to extract the motility history of every cell on a newly colonized surface 16 . By combining this technique with fluorescent Psl staining and computer simulations, we show that P. aeruginosa deposits a trail of Psl as it moves on a surface, which influences the surface motility of subsequent cells that encounter these trails and thus generates positive feedback. Both experiments and simulations indicate that the web of secreted Psl controls the distribution of surface visit frequencies, which can be approximated by a power law. This Pareto-type 17 behaviour indicates that the bacterial community self-organizes in a manner analogous to a capitalist economic system 18 , a ‘rich-get-richer’ mechanism of Psl accumulation that result