Publication Date:
2013-05-10
Description:
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.〈br /〉〈br /〉〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4109411/" target="_blank"〉〈img src="https://static.pubmed.gov/portal/portal3rc.fcgi/4089621/img/3977009" border="0"〉〈/a〉 〈a href="https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4109411/" target="_blank"〉This paper as free author manuscript - peer-reviewed and accepted for publication〈/a〉〈br /〉〈br /〉〈span class="detail_caption"〉Notes: 〈/span〉Zhao, Kun -- Tseng, Boo Shan -- Beckerman, Bernard -- Jin, Fan -- Gibiansky, Maxsim L -- Harrison, Joe J -- Luijten, Erik -- Parsek, Matthew R -- Wong, Gerard C L -- 1R01HL087920/HL/NHLBI NIH HHS/ -- P30 DK089507/DK/NIDDK NIH HHS/ -- R01 AI061396/AI/NIAID NIH HHS/ -- R01 AI077628/AI/NIAID NIH HHS/ -- R01 AI081983/AI/NIAID NIH HHS/ -- R01 AI097511/AI/NIAID NIH HHS/ -- R01 HL087920/HL/NHLBI NIH HHS/ -- R01AI077628/AI/NIAID NIH HHS/ -- R01AI081983/AI/NIAID NIH HHS/ -- R56AI061396/AI/NIAID NIH HHS/ -- England -- Nature. 2013 May 16;497(7449):388-91. doi: 10.1038/nature12155. Epub 2013 May 8.〈br /〉〈span class="detail_caption"〉Author address: 〈/span〉Department of Bioengineering, University of California, Los Angeles, California 90095, USA.〈br /〉〈span class="detail_caption"〉Record origin:〈/span〉 〈a href="http://www.ncbi.nlm.nih.gov/pubmed/23657259" target="_blank"〉PubMed〈/a〉
Keywords:
Algorithms
;
Bacterial Adhesion/physiology
;
Biofilms/*growth & development
;
Cell Tracking
;
Feedback, Physiological
;
Fluorescent Dyes
;
Polysaccharides, Bacterial/*metabolism
;
Pseudomonas aeruginosa/*cytology/*growth & development
;
Staining and Labeling
Print ISSN:
0028-0836
Electronic ISSN:
1476-4687
Topics:
Biology
,
Chemistry and Pharmacology
,
Medicine
,
Natural Sciences in General
,
Physics
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