title: Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms.
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.
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Lynne
authors.initials: L
authors.lastname: Turnbull
authors.affiliation: Department of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan.|Department of Plant and Microbial Biology, University of Zurich, Zürich 8008, Switzerland.
authors.forename: Masanori
authors.initials: M
authors.lastname: Toyofuku
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Amelia L
authors.initials: AL
authors.lastname: Hynen
authors.affiliation: Department of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan.
authors.forename: Masaharu
authors.initials: M
authors.lastname: Kurosawa
authors.affiliation: Department of Plant and Microbial Biology, University of Zurich, Zürich 8008, Switzerland.
authors.forename: Gabriella
authors.initials: G
authors.lastname: Pessi
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Nicola K
authors.initials: NK
authors.lastname: Petty
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Sarah R
authors.initials: SR
authors.lastname: Osvath
authors.affiliation: Department of Plant and Microbial Biology, University of Zurich, Zürich 8008, Switzerland.
authors.forename: Gerardo
authors.initials: G
authors.lastname: Cárcamo-Oyarce
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Erin S
authors.initials: ES
authors.lastname: Gloag
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Raz
authors.initials: R
authors.lastname: Shimoni
authors.affiliation: Department of Biology, Institute of Molecular Systems Biology, ETH Zurich, Zürich 8093, Switzerland.
authors.forename: Ulrich
authors.initials: U
authors.lastname: Omasits
authors.affiliation: Department of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan.
authors.forename: Satoshi
authors.initials: S
authors.lastname: Ito
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Xinhui
authors.initials: X
authors.lastname: Yap
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Leigh G
authors.initials: LG
authors.lastname: Monahan
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Rosalia
authors.initials: R
authors.lastname: Cavaliere
authors.affiliation: Agroscope, Institute for Plant Production Sciences, Research Group Molecular Diagnostics, Genomics and Bioinformatics, &Swiss Institute of Bioinformatics (SIB), Wädenswil 8820, Switzerland.
authors.forename: Christian H
authors.initials: CH
authors.lastname: Ahrens
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Ian G
authors.initials: IG
authors.lastname: Charles
authors.affiliation: Department of Life and Environmental Sciences, University of Tsukuba, Tsukuba, Ibaraki 305-8572, Japan.
authors.forename: Nobuhiko
authors.initials: N
authors.lastname: Nomura
authors.affiliation: Department of Plant and Microbial Biology, University of Zurich, Zürich 8008, Switzerland.
authors.forename: Leo
authors.initials: L
authors.lastname: Eberl
authors.affiliation: The ithree institute, University of Technology Sydney, Ultimo, New South Wales 2007, Australia.
authors.forename: Cynthia B
authors.initials: CB
authors.lastname: Whitchurch
mesh_terms: D001433:Bacteriolysis / Q000187:drug effects; D018441:Biofilms / Q000187:drug effects; D002462:Cell Membrane / Q000187:drug effects / Q000378:metabolism*; D004269:DNA, Bacterial / Q000378:metabolism; D010450:Endopeptidases / Q000494:pharmacology; D005110:Extracellular Space / Q000378:metabolism; D001678:Organelle Biogenesis; D011550:Pseudomonas aeruginosa / Q000187:drug effects / Q000502:physiology*; D011709:Pyocins / Q000494:pharmacology; D015363:Quinolones / Q000494:pharmacology; D013312:Stress, Physiological / Q000187:drug effects
chemical_list: C407944:2-heptyl-3-hydroxy-4-quinolone; D004269:DNA, Bacterial; D011709:Pyocins; D015363:Quinolones; D010450:Endopeptidases; C001143:endolysin