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, Cynthia B. Whitchurch

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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.

Original languageEnglish
Article number11220
JournalNature Communications
Volume7
DOIs
Publication statusPublished - 14 Apr 2016

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