title: Psl trails guide exploration and microcolony formation in Pseudomonas aeruginosa biofilms.
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.
authors: Department of Bioengineering, University of California, Los Angeles, CA 90095.
authors: Kun
authors: K
authors: Zhao
authors: Department of Microbiology, University of Washington, Seattle, WA 98195.
authors: Boo Shan
authors: BS
authors: Tseng
authors: Department of Materials Science and Engineering, Northwestern University, Evanston, IL 60208.
authors: Bernard
authors: B
authors: Beckerman
authors: CAS Key Laboratory of Soft Matter Chemistry, University of Science and Technology of China, Hefei, Anhui, 230026, P.R. China.
authors: Fan
authors: F
authors: Jin
authors: Department of Bioengineering, University of California, Los Angeles, CA 90095.
authors: Maxsim L
authors: ML
authors: Gibiansky
authors: Department of Microbiology, University of Washington, Seattle, WA 98195.
authors: Joe J
authors: JJ
authors: Harrison
authors: Department of Materials Science and Engineering, Northwestern University, Evanston, IL 60208.|Department of Engineering Sciences and Applied Mathematics, Northwestern University, Evanston, IL 60208.
authors: Erik
authors: E
authors: Luijten
authors: Department of Microbiology, University of Washington, Seattle, WA 98195.
authors: Matthew R
authors: MR
authors: Parsek
authors: Department of Bioengineering, University of California, Los Angeles, CA 90095.|Department of Chemistry and Biochemistry, University of California, Los Angeles, CA 90095.|California NanoSystems Institute, University of California, Los Angeles, CA 90095.
authors: Gerard C L
authors: GCL
authors: Wong
mesh_terms: D000465:Algorithms; D001422:Bacterial Adhesion / Q000502:physiology; D018441:Biofilms / Q000254:growth & development*; D058948:Cell Tracking; D025461:Feedback, Physiological; D005456:Fluorescent Dyes; D011135:Polysaccharides, Bacterial / Q000378:metabolism*; D011550:Pseudomonas aeruginosa / Q000166:cytology* / Q000254:growth & development*; D013194:Staining and Labeling
chemical_list: D005456:Fluorescent Dyes; D011135:Polysaccharides, Bacterial; C064841:exopolysaccharide, Pseudomonas
references: Annu Rev Microbiol. 2002;56:187-209
references: 12142477
references: mBio. 2010 Jun 29;1(3):
references: 20802825
references: Mol Microbiol. 2009 Aug;73(4):622-38
references: 19659934
references: Science. 2010 Oct 8;330(6001):197
references: 20929769
references: Microbes Infect. 2000 Jul;2(9):1051-60
references: 10967285
references: PLoS Pathog. 2009 Mar;5(3):e1000354
references: 19325879
references: Front Biosci. 2001 Aug 01;6:D890-7
references: 11487480
references: J Bacteriol. 2007 Nov;189(22):8353-6
references: 17631634
references: J Gen Microbiol. 1955 Dec;13(3):572-81
references: 13278508
references: Mol Microbiol. 2003 Oct;50(1):61-8
references: 14507363
references: Science. 1999 May 21;284(5418):1318-22
references: 10334980
references: Trends Microbiol. 2001 May;9(5):222-7
references: 11336839
references: Environ Microbiol. 2012 Aug;14(8):1913-28
references: 22176658
references: FEMS Microbiol Rev. 2012 Jul;36(4):893-916
references: 22212072
references: Mol Microbiol. 1998 Oct;30(2):295-304
references: 9791175
references: Microbiology (Reading). 2000 Oct;146 ( Pt 10):2409-2415
references: 11021917
references: J Bacteriol. 2006 Dec;188(23):8213-21
references: 16980452
references: Curr Protoc Microbiol. 2006 Jan;Chapter 1:Unit 1B.2
references: 18770573
references: J Bacteriol. 2004 Jul;186(14):4457-65
references: 15231777
references: PLoS Biol. 2007 Nov;5(11):e307
references: 18001153
references: Science. 1998 Apr 10;280(5361):295-8
references: 9535661
references: Biophys J. 2011 Jan 19;100(2):341-50
references: 21244830
references: Science. 2002 Feb 22;295(5559):1487
references: 11859186
references: Annu Rev Microbiol. 2000;54:49-79
references: 11018124
references: Gene. 1999 Feb 18;227(2):197-203
references: 10023058
references: Nature. 2000 Oct 12;407(6805):762-4
references: 11048725
references: J Bacteriol. 2007 Nov;189(22):7945-7
references: 17675377
references: Proc Natl Acad Sci U S A. 2001 Jun 5;98(12):6901-4
references: 11381130