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

Author

Listed:
  • Lynne Turnbull

    (The ithree institute, University of Technology Sydney)

  • Masanori Toyofuku

    (University of Tsukuba
    University of Zurich)

  • 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)

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.

Suggested Citation

  • 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 &, 2016. "Explosive cell lysis as a mechanism for the biogenesis of bacterial membrane vesicles and biofilms," Nature Communications, Nature, vol. 7(1), pages 1-13, September.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms11220
    DOI: 10.1038/ncomms11220
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    Cited by:

    1. Nuno M. Oliveira & James H. R. Wheeler & Cyril Deroy & Sean C. Booth & Edmond J. Walsh & William M. Durham & Kevin R. Foster, 2022. "Suicidal chemotaxis in bacteria," Nature Communications, Nature, vol. 13(1), pages 1-14, December.
    2. Qianbei Li & Zihao Ou & Jinduan Lin & Die Tang & Bairong He & Yuanyuan Wu & Xinyue Huang & Xixin Huang & Bingbing Ru & Qianwen Wang & Weirong Yao & Bo Situ & Lei Zheng, 2025. "Specific labeling of outer membrane vesicles with antibiotic-conjugated probe reveals early bacterial infections in blood," Nature Communications, Nature, vol. 16(1), pages 1-14, December.
    3. Arles Urrutia & Víctor A García-Angulo & Andrés Fuentes & Mauricio Caneo & Marcela Legüe & Sebastián Urquiza & Scarlett E Delgado & Juan Ugalde & Paula Burdisso & Andrea Calixto, 2020. "Bacterially produced metabolites protect C . elegans neurons from degeneration," PLOS Biology, Public Library of Science, vol. 18(3), pages 1-31, March.
    4. Steven J. Biller & M. Gray Ryan & Jasmine Li & Andrew Burger & John M. Eppley & Thomas Hackl & Edward F. DeLong, 2025. "Distinct horizontal gene transfer potential of extracellular vesicles versus viral-like particles in marine habitats," Nature Communications, Nature, vol. 16(1), pages 1-12, December.
    5. Diana P. Baquero & Guillaume Borrel & Anastasia Gazi & Camille Martin-Gallausiaux & Virginija Cvirkaite-Krupovic & Pierre-Henri Commere & Nika Pende & Stéphane Tachon & Anna Sartori-Rupp & Thibaut Dou, 2025. "Biogenesis of DNA-carrying extracellular vesicles by the dominant human gut methanogenic archaeon," Nature Communications, Nature, vol. 16(1), pages 1-13, December.

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