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A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria

Author

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  • Sandro Roier

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Franz G. Zingl

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Fatih Cakar

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Sanel Durakovic

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Paul Kohl

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Thomas O. Eichmann

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Lisa Klug

    (Institute of Biochemistry, Graz University of Technology, NAWI Graz, BioTechMed-Graz)

  • Bernhard Gadermaier

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Katharina Weinzerl

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Ruth Prassl

    (Institute of Biophysics, Medical University of Graz, BioTechMed-Graz)

  • Achim Lass

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Günther Daum

    (Institute of Biochemistry, Graz University of Technology, NAWI Graz, BioTechMed-Graz)

  • Joachim Reidl

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

  • Mario F. Feldman

    (University of Alberta)

  • Stefan Schild

    (Institute of Molecular Biosciences, University of Graz, NAWI Graz, BioTechMed-Graz)

Abstract

Bacterial outer membrane vesicles (OMVs) have important biological roles in pathogenesis and intercellular interactions, but a general mechanism of OMV formation is lacking. Here we show that the VacJ/Yrb ABC (ATP-binding cassette) transport system, a proposed phospholipid transporter, is involved in OMV formation. Deletion or repression of VacJ/Yrb increases OMV production in two distantly related Gram-negative bacteria, Haemophilus influenzae and Vibrio cholerae. Lipidome analyses demonstrate that OMVs from VacJ/Yrb-defective mutants in H. influenzae are enriched in phospholipids and certain fatty acids. Furthermore, we demonstrate that OMV production and regulation of the VacJ/Yrb ABC transport system respond to iron starvation. Our results suggest a new general mechanism of OMV biogenesis based on phospholipid accumulation in the outer leaflet of the outer membrane. This mechanism is highly conserved among Gram-negative bacteria, provides a means for regulation, can account for OMV formation under all growth conditions, and might have important pathophysiological roles in vivo.

Suggested Citation

  • Sandro Roier & Franz G. Zingl & Fatih Cakar & Sanel Durakovic & Paul Kohl & Thomas O. Eichmann & Lisa Klug & Bernhard Gadermaier & Katharina Weinzerl & Ruth Prassl & Achim Lass & Günther Daum & Joachi, 2016. "A novel mechanism for the biogenesis of outer membrane vesicles in Gram-negative bacteria," Nature Communications, Nature, vol. 7(1), pages 1-13, April.
    • Handle: RePEc:nat:natcom:v:7:y:2016:i:1:d:10.1038_ncomms10515
    DOI: 10.1038/ncomms10515
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    Cited by:

    1. Ruchika Dehinwal & Tata Gopinath & Richard D. Smith & Robert K. Ernst & Dieter M. Schifferli & Matthew K. Waldor & Francesca M. Marassi, 2024. "A pH-sensitive motif in an outer membrane protein activates bacterial membrane vesicle production," Nature Communications, Nature, vol. 15(1), pages 1-10, December.
    2. Shuai Gao & Lingyu Gao & Dailin Yuan & Xu’ai Lin & Stijn Veen, 2024. "Gonococcal OMV-delivered PorB induces epithelial cell mitophagy," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    3. Kyrie P. Grasekamp & Basile Beaud Benyahia & Najwa Taib & Bianca Audrain & Benjamin Bardiaux & Yannick Rossez & Nadia Izadi-Pruneyre & Maylis Lejeune & Xavier Trivelli & Zina Chouit & Yann Guerardel &, 2023. "The Mla system of diderm Firmicute Veillonella parvula reveals an ancestral transenvelope bridge for phospholipid trafficking," Nature Communications, Nature, vol. 14(1), pages 1-15, December.

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