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The cell envelope of Staphylococcus aureus selectively controls the sorting of virulence factors

Author

Listed:
  • Xuhui Zheng

    (New York University Grossman School of Medicine, New York)

  • Gerben Marsman

    (Max Planck Institute for Infection Biology)

  • Keenan A. Lacey

    (New York University Grossman School of Medicine, New York)

  • Jessica R. Chapman

    (New York University Grossman School of Medicine, New York)

  • Christian Goosmann

    (Max Planck Institute for Infection Biology)

  • Beatrix M. Ueberheide

    (New York University Grossman School of Medicine, New York
    New York University Grossman School of Medicine)

  • Victor J. Torres

    (New York University Grossman School of Medicine, New York)

Abstract

Staphylococcus aureus bi-component pore-forming leukocidins are secreted toxins that directly target and lyse immune cells. Intriguingly, one of the leukocidins, Leukocidin AB (LukAB), is found associated with the bacterial cell envelope in addition to secreted into the extracellular milieu. Here, we report that retention of LukAB on the bacterial cells provides S. aureus with a pre-synthesized active toxin that kills immune cells. On the bacteria, LukAB is distributed as discrete foci in two distinct compartments: membrane-proximal and surface-exposed. Through genetic screens, we show that a membrane lipid, lysyl-phosphatidylglycerol (LPG), and lipoteichoic acid (LTA) contribute to LukAB deposition and release. Furthermore, by studying non-covalently surface-bound proteins we discovered that the sorting of additional exoproteins, such as IsaB, Hel, ScaH, and Geh, are also controlled by LPG and LTA. Collectively, our study reveals a multistep secretion system that controls exoprotein storage and protein translocation across the S. aureus cell wall.

Suggested Citation

  • Xuhui Zheng & Gerben Marsman & Keenan A. Lacey & Jessica R. Chapman & Christian Goosmann & Beatrix M. Ueberheide & Victor J. Torres, 2021. "The cell envelope of Staphylococcus aureus selectively controls the sorting of virulence factors," Nature Communications, Nature, vol. 12(1), pages 1-16, December.
    • Handle: RePEc:nat:natcom:v:12:y:2021:i:1:d:10.1038_s41467-021-26517-z
    DOI: 10.1038/s41467-021-26517-z
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    References listed on IDEAS

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    1. L. Pasquina-Lemonche & J. Burns & R. D. Turner & S. Kumar & R. Tank & N. Mullin & J. S. Wilson & B. Chakrabarti & P. A. Bullough & S. J. Foster & J. K. Hobbs, 2020. "The architecture of the Gram-positive bacterial cell wall," Nature, Nature, vol. 582(7811), pages 294-297, June.
    2. Fredric Carlsson & Margaretha Stålhammar-Carlemalm & Klas Flärdh & Charlotta Sandin & Eric Carlemalm & Gunnar Lindahl, 2006. "Signal sequence directs localized secretion of bacterial surface proteins," Nature, Nature, vol. 442(7105), pages 943-946, August.
    3. Dennis Hanzelmann & Hwang-Soo Joo & Mirita Franz-Wachtel & Tobias Hertlein & Stefan Stevanovic & Boris Macek & Christiane Wolz & Friedrich Götz & Michael Otto & Dorothee Kretschmer & Andreas Peschel, 2016. "Toll-like receptor 2 activation depends on lipopeptide shedding by bacterial surfactants," Nature Communications, Nature, vol. 7(1), pages 1-11, November.
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