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Nature. 2013 May 16;497(7449):388-391. doi: 10.1038/nature12155. Epub 2013 May 8.

Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms.

Author information

1
Department of Bioengineering, University of California, Los Angeles, CA 90095.
2
Department of Microbiology, University of Washington, Seattle, WA 98195.
3
Department of Materials Science and Engineering, Northwestern University, Evanston, IL 60208.
4
CAS Key Laboratory of Soft Matter Chemistry, University of Science and Technology of China, Hefei, Anhui, 230026, P.R. China.
5
Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL 60208.
6
Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.
7
California NanoSystems Institute, University of California, Los Angeles, CA 90095.
#
Contributed equally

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.

PMID:
23657259
PMCID:
PMC4109411
DOI:
10.1038/nature12155
[Indexed for MEDLINE]
Free PMC Article

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