Self-organization of bacterial biofilms is facilitated by extracellular DNA

Gloag, ES; Turnbull, L; Huang, A; Vallotton, P; Wang, H; Nolan, LM; Mililli, L; Hunt, C; Lu, J; Osvath, SR; Monahan, LG; Cavaliere, R; Charles, IG; Wand, MP; Gee, ML; Prabhakar, R; Whitchurch, CB

Self-organization of bacterial biofilms is facilitated by extracellular DNA

Gloag, ES Turnbull, L

Huang, A

Vallotton, P Wang, H Nolan, LM Mililli, L Hunt, C Lu, J Osvath, SR Monahan, LG

Cavaliere, R

Charles, IG

Wand, MP

Gee, ML Prabhakar, R Whitchurch, CB

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Publication Type:: Journal Article
Citation:: Proceedings of the National Academy of Sciences of the United States of America, 2013, 110 (28), pp. 11541 - 11546
Issue Date:: 2013-07-09

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Field	Value	Language
dc.contributor.author	Gloag, ES	en_US
dc.contributor.author	Turnbull, L https://orcid.org/0000-0002-9255-9033	en_US
dc.contributor.author	Huang, A https://orcid.org/0000-0002-7848-6755	en_US
dc.contributor.author	Vallotton, P	en_US
dc.contributor.author	Wang, H	en_US
dc.contributor.author	Nolan, LM	en_US
dc.contributor.author	Mililli, L	en_US
dc.contributor.author	Hunt, C	en_US
dc.contributor.author	Lu, J	en_US
dc.contributor.author	Osvath, SR	en_US
dc.contributor.author	Monahan, LG https://orcid.org/0000-0003-2933-9000	en_US
dc.contributor.author	Cavaliere, R https://orcid.org/0000-0002-4709-5081	en_US
dc.contributor.author	Charles, IG https://orcid.org/0000-0002-2423-1167	en_US
dc.contributor.author	Wand, MP https://orcid.org/0000-0003-2555-896X	en_US
dc.contributor.author	Gee, ML	en_US
dc.contributor.author	Prabhakar, R	en_US
dc.contributor.author	Whitchurch, CB https://orcid.org/0000-0003-2296-3791	en_US
dc.date.issued	2013-07-09	en_US
dc.identifier.citation	Proceedings of the National Academy of Sciences of the United States of America, 2013, 110 (28), pp. 11541 - 11546	en_US
dc.identifier.issn	0027-8424	en_US
dc.identifier.uri	http://hdl.handle.net/10453/24214
dc.description.abstract	Twitching motility-mediated biofilm expansion is a complex, multicellular behavior that enables the active colonization of surfaces by many species of bacteria. In this study we have explored the emergence of intricate network patterns of interconnected trails that form in actively expanding biofilms of Pseudomonas aeruginosa. We have used high-resolution, phase-contrast time-lapse microscopy and developed sophisticated computer vision algorithms to track and analyze individual cell movements during expansion of P. aeruginosa biofilms. We have also used atomic force microscopy to examine the topography of the substrate underneath the expanding biofilm. Our analyses reveal that at the leading edge of the biofilm, highly coherent groups of bacteria migrate across the surface of the semisolid media and in doing so create furrows along which following cells preferentially migrate. This leads to the emergence of a network of trails that guide mass transit toward the leading edges of the biofilm. We have also determined that extracellular DNA (eDNA) facilitates efficient traffic flow throughout the furrow network by maintaining coherent cell alignments, thereby avoiding traffic jams and ensuring an efficient supply of cells to the migrating front. Our analyses reveal that eDNA also coordinates the movements of cells in the leading edge vanguard rafts and is required for the assembly of cells into the "bulldozer" aggregates that forge the interconnecting furrows. Our observations have revealed that large-scale self-organization of cells in actively expanding biofilms of P. aeruginosa occurs through construction of an intricate network of furrows that is facilitated by eDNA.	en_US
dc.relation	http://purl.org/au-research/grants/nhmrc/GNT0571905
dc.relation.ispartof	Proceedings of the National Academy of Sciences of the United States of America	en_US
dc.relation.isbasedon	10.1073/pnas.1218898110	en_US
dc.subject.mesh	Biofilms	en_US
dc.subject.mesh	Pseudomonas aeruginosa	en_US
dc.subject.mesh	DNA, Bacterial	en_US
dc.title	Self-organization of bacterial biofilms is facilitated by extracellular DNA	en_US
dc.type	Journal Article
utslib.citation.volume	28	en_US
utslib.citation.volume	110	en_US
utslib.for	0605 Microbiology	en_US
pubs.embargo.period	Not known	en_US
pubs.organisational-group	/University of Technology Sydney
pubs.organisational-group	/University of Technology Sydney/Faculty of Science
pubs.organisational-group	/University of Technology Sydney/Faculty of Science/School of Mathematical and Physical Sciences
pubs.organisational-group	/University of Technology Sydney/Faculty of Science/School of Mathematical Sciences
pubs.organisational-group	/University of Technology Sydney/Strength - ithree - Institute of Infection, Immunity and Innovation
utslib.copyright.status	open_access
pubs.issue	28	en_US
pubs.publication-status	Published	en_US
pubs.volume	110	en_US

Abstract:

Twitching motility-mediated biofilm expansion is a complex, multicellular behavior that enables the active colonization of surfaces by many species of bacteria. In this study we have explored the emergence of intricate network patterns of interconnected trails that form in actively expanding biofilms of Pseudomonas aeruginosa. We have used high-resolution, phase-contrast time-lapse microscopy and developed sophisticated computer vision algorithms to track and analyze individual cell movements during expansion of P. aeruginosa biofilms. We have also used atomic force microscopy to examine the topography of the substrate underneath the expanding biofilm. Our analyses reveal that at the leading edge of the biofilm, highly coherent groups of bacteria migrate across the surface of the semisolid media and in doing so create furrows along which following cells preferentially migrate. This leads to the emergence of a network of trails that guide mass transit toward the leading edges of the biofilm. We have also determined that extracellular DNA (eDNA) facilitates efficient traffic flow throughout the furrow network by maintaining coherent cell alignments, thereby avoiding traffic jams and ensuring an efficient supply of cells to the migrating front. Our analyses reveal that eDNA also coordinates the movements of cells in the leading edge vanguard rafts and is required for the assembly of cells into the "bulldozer" aggregates that forge the interconnecting furrows. Our observations have revealed that large-scale self-organization of cells in actively expanding biofilms of P. aeruginosa occurs through construction of an intricate network of furrows that is facilitated by eDNA.

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http://hdl.handle.net/10453/24214