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

Lynne Turnbull, Masanori Toyofuku (), Amelia L. Hynen, Masaharu Kurosawa, Gabriella Pessi, Nicola K. Petty, Sarah R. Osvath, Gerardo Cárcamo-Oyarce, Erin S. Gloag, Raz Shimoni, Ulrich Omasits, Satoshi Ito, Xinhui Yap, Leigh G. Monahan, Rosalia Cavaliere, Christian H. Ahrens, Ian G. Charles, Nobuhiko Nomura, Leo Eberl () and Cynthia B. Whitchurch ()
Additional contact information
Lynne Turnbull: The ithree institute, University of Technology Sydney
Masanori Toyofuku: University of Tsukuba
Amelia L. Hynen: The ithree institute, University of Technology Sydney
Masaharu Kurosawa: University of Tsukuba
Gabriella Pessi: University of Zurich
Nicola K. Petty: The ithree institute, University of Technology Sydney
Sarah R. Osvath: The ithree institute, University of Technology Sydney
Gerardo Cárcamo-Oyarce: University of Zurich
Erin S. Gloag: The ithree institute, University of Technology Sydney
Raz Shimoni: The ithree institute, University of Technology Sydney
Ulrich Omasits: Institute of Molecular Systems Biology, ETH Zurich
Satoshi Ito: University of Tsukuba
Xinhui Yap: The ithree institute, University of Technology Sydney
Leigh G. Monahan: The ithree institute, University of Technology Sydney
Rosalia Cavaliere: The ithree institute, University of Technology Sydney
Christian H. Ahrens: Agroscope, Institute for Plant Production Sciences, Research Group Molecular Diagnostics, Genomics and Bioinformatics, & Swiss Institute of Bioinformatics (SIB)
Ian G. Charles: The ithree institute, University of Technology Sydney
Nobuhiko Nomura: University of Tsukuba
Leo Eberl: University of Zurich
Cynthia B. Whitchurch: The ithree institute, University of Technology Sydney

Nature Communications, 2016, vol. 7, issue 1, 1-13

Abstract: 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.

Date: 2016
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DOI: 10.1038/ncomms11220

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