Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms

Kun Zhao, Boo Shan Tseng, Bernard Beckerman, Fan Jin, Maxsim L. Gibiansky, Joe J. Harrison, Erik Luijten, Matthew R. Parsek, Gerard C.L. Wong*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

191 Scopus citations

Abstract

Bacterial biofilms are surface-associated, multicellular, morphologically complex microbial communities. Biofilm-forming bacteria such as the opportunistic pathogen Pseudomonas aeruginosa are phenotypically distinct from their free-swimming, planktonic counterparts. 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'. 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. 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 behaviour indicates 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 becoming extremely enriched in communally produced Psl. Using engineered strains with inducible Psl production, we show that local Psl concentrations determine post-division cell fates and that high local Psl concentrations ultimately allow elite cells to serve as the founding population for initial microcolony development.

Original languageEnglish (US)
Pages (from-to)388-391
Number of pages4
JournalNature
Volume497
Issue number7449
DOIs
StatePublished - May 16 2013

ASJC Scopus subject areas

  • General

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