Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms

Turnbull, L; Toyofuku, M; Hynen, AL; Kurosawa, M; Pessi, G; Petty, NK; Osvath, SR; Cárcamo-Oyarce, G; Gloag, ES; Shimoni, R; Omasits, U; Ito, S; Yap, X; Monahan, LG; Cavaliere, R; Ahrens, CH; Charles, IG; Nomura, N; Eberl, L; Whitchurch, CB

Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms

Turnbull, L

Toyofuku, M Hynen, AL Kurosawa, M Pessi, G Petty, NK

Osvath, SR Cárcamo-Oyarce, G Gloag, ES Shimoni, R Omasits, U Ito, S Yap, X Monahan, LG

Cavaliere, R

Ahrens, CH Charles, IG

Nomura, N Eberl, L Whitchurch, CB

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Publication Type:: Journal Article
Citation:: Nature Communications, 2016, 7
Issue Date:: 2016-04-14

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Field	Value	Language
dc.contributor.author	Turnbull, L https://orcid.org/0000-0002-9255-9033	en_US
dc.contributor.author	Toyofuku, M	en_US
dc.contributor.author	Hynen, AL	en_US
dc.contributor.author	Kurosawa, M	en_US
dc.contributor.author	Pessi, G	en_US
dc.contributor.author	Petty, NK https://orcid.org/0000-0001-6528-9886	en_US
dc.contributor.author	Osvath, SR	en_US
dc.contributor.author	Cárcamo-Oyarce, G	en_US
dc.contributor.author	Gloag, ES	en_US
dc.contributor.author	Shimoni, R	en_US
dc.contributor.author	Omasits, U	en_US
dc.contributor.author	Ito, S	en_US
dc.contributor.author	Yap, X	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	Ahrens, CH	en_US
dc.contributor.author	Charles, IG https://orcid.org/0000-0002-2423-1167	en_US
dc.contributor.author	Nomura, N	en_US
dc.contributor.author	Eberl, L	en_US
dc.contributor.author	Whitchurch, CB https://orcid.org/0000-0003-2296-3791	en_US
dc.date.available	2016-03-02	en_US
dc.date.issued	2016-04-14	en_US
dc.identifier.citation	Nature Communications, 2016, 7	en_US
dc.identifier.uri	http://hdl.handle.net/10453/88350
dc.description.abstract	Many bacteria produce extracellular and surface-associated components such as membrane vesicles (MVs), extracellular DNA and moonlighting cytosolic proteins for which the biogenesis and export pathways are not fully understood. Here we show that the explosive cell lysis of a sub-population of cells accounts for the liberation of cytosolic content in Pseudomonas aeruginosa biofilms. Super-resolution microscopy reveals that explosive cell lysis also produces shattered membrane fragments that rapidly form MVs. A prophage endolysin encoded within the R- and F-pyocin gene cluster is essential for explosive cell lysis. Endolysin-deficient mutants are defective in MV production and biofilm development, consistent with a crucial role in the biogenesis of MVs and liberation of extracellular DNA and other biofilm matrix components. Our findings reveal that explosive cell lysis, mediated through the activity of a cryptic prophage endolysin, acts as a mechanism for the production of bacterial MVs.	en_US
dc.relation.ispartof	Nature Communications	en_US
dc.relation.isbasedon	10.1038/ncomms11220	en_US
dc.subject.mesh	Cell Membrane	en_US
dc.subject.mesh	Extracellular Space	en_US
dc.subject.mesh	Biofilms	en_US
dc.subject.mesh	Pseudomonas aeruginosa	en_US
dc.subject.mesh	Quinolones	en_US
dc.subject.mesh	Endopeptidases	en_US
dc.subject.mesh	Pyocins	en_US
dc.subject.mesh	DNA, Bacterial	en_US
dc.subject.mesh	Bacteriolysis	en_US
dc.subject.mesh	Stress, Physiological	en_US
dc.subject.mesh	Organelle Biogenesis	en_US
dc.title	Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms	en_US
dc.type	Journal Article
utslib.citation.volume	7	en_US
utslib.for	060106 Cellular Interactions (incl. Adhesion, Matrix, Cell Wall)	en_US
utslib.for	060103 Cell Development, Proliferation and Death	en_US
utslib.for	060503 Microbial Genetics	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/Strength - ithree - Institute of Infection, Immunity and Innovation
utslib.copyright.status	open_access
pubs.publication-status	Published	en_US
pubs.volume	7	en_US

Abstract:

Many bacteria produce extracellular and surface-associated components such as membrane vesicles (MVs), extracellular DNA and moonlighting cytosolic proteins for which the biogenesis and export pathways are not fully understood. Here we show that the explosive cell lysis of a sub-population of cells accounts for the liberation of cytosolic content in Pseudomonas aeruginosa biofilms. Super-resolution microscopy reveals that explosive cell lysis also produces shattered membrane fragments that rapidly form MVs. A prophage endolysin encoded within the R- and F-pyocin gene cluster is essential for explosive cell lysis. Endolysin-deficient mutants are defective in MV production and biofilm development, consistent with a crucial role in the biogenesis of MVs and liberation of extracellular DNA and other biofilm matrix components. Our findings reveal that explosive cell lysis, mediated through the activity of a cryptic prophage endolysin, acts as a mechanism for the production of bacterial MVs.

Please use this identifier to cite or link to this item:

http://hdl.handle.net/10453/49129