Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms

Abstract

Bacterial biofilms are surface-associated, multicellular, morphologically complex microbial communities1-7. Biofilm-forming bacteria such as the opportunistic pathogen7-10 Pseudomonas aeruginosa are phenotypically distinct from their free-swimming, planktonic counterparts. Much work has focused on factors impacting surface adhesion and it is known that P. aeruginosa secretes the Psl exopolysaccharide, which promotes surface attachment by acting as a ‘molecular glue’11-15. 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 via a search-engine based approach16. By combining these techniques 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 generate 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 Zipf's Law17 indicates that the bacterial community self-organizes in a manner analogous to a capitalist economic system18, 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, 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.

Vibrio cholerae biofilm growth program and architecture revealed by single-cell live imaging

“…We provide two here. For species with surface twitching motility, such as Pseudomonas aeruginosa, it is conceivable that surface-associated pressure might be relieved by surface motion, and, indeed, aggregation of motile P. aeruginosa is suggested to initiate biofilm formation rather than clonal growth from a single cell (13). However, in later stages of the process, a nonmotile subset of the P. aeruginosa cells forms the 3D stalk at the base of the biofilm (34).…”

Architectural transitions in Vibrio cholerae biofilms at single-cell resolution

“…In all contexts, biofilms can be difficult to control due to their resilience against chemical and physical stresses (12,13), including antibiotic treatment (14). Because of their ubiquity and their relevance to medicine and industry, the formation of biofilms has been studied intensively, with an emphasis on the genes, regulatory mechanisms, and transport properties that underlie transitions from planktonic growth to surface attachment (15)(16)(17), to proliferation and matrix secretion (2,18), and finally to dispersal (19,20). A basic understanding of several regulatory circuits and secreted matrix components governing biofilm formation has been developed (21)(22)(23)(24)(25).…”

Chemotaxis and autochemotaxis of self-propelling droplet swimmers

“…Thus, chemotaxis provides a mechanism of interindividual communication. Modeling such communication strategies is key to understanding the collective behavior of microorganisms (6)(7)(8) as well as flocks of animals like fire ants (9,10).…”