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Distant relatives of a eukaryotic cell-specific toxin family evolved a complement-like mechanism to kill bacteria

Author

Listed:
  • Hunter L. Abrahamsen

    (The University of Oklahoma Health Sciences Center)

  • Tristan C. Sanford

    (The University of Oklahoma Health Sciences Center)

  • Casie E. Collamore

    (The University of Oklahoma Health Sciences Center)

  • Bronte A. Johnstone

    (University of Melbourne
    University of Melbourne)

  • Michael J. Coyne

    (University of Chicago)

  • Leonor García-Bayona

    (University of Chicago)

  • Michelle P. Christie

    (University of Melbourne
    University of Melbourne)

  • Jordan C. Evans

    (The University of Oklahoma Health Sciences Center
    Wheeler Bio)

  • Allison J. Farrand

    (The University of Oklahoma Health Sciences Center
    Wheeler Bio)

  • Katia Flores

    (University of Chicago)

  • Craig J. Morton

    (University of Melbourne
    CSIRO Biomedical Manufacturing Program)

  • Michael W. Parker

    (University of Melbourne
    University of Melbourne
    St Vincent’s Institute of Medical Research)

  • Laurie E. Comstock

    (University of Chicago)

  • Rodney K. Tweten

    (The University of Oklahoma Health Sciences Center)

Abstract

Cholesterol-dependent cytolysins (CDCs) comprise a large family of pore-forming toxins produced by Gram-positive bacteria, which are used to attack eukaryotic cells. Here, we functionally characterize a family of 2-component CDC-like (CDCL) toxins produced by the Gram-negative Bacteroidota that form pores by a mechanism only described for the mammalian complement membrane attack complex (MAC). We further show that the Bacteroides CDCLs are not eukaryotic cell toxins like the CDCs, but instead bind to and are proteolytically activated on the surface of closely related species, resulting in pore formation and cell death. The CDCL-producing Bacteroides is protected from the effects of its own CDCL by the presence of a surface lipoprotein that blocks CDCL pore formation. These studies suggest a prevalent mode of bacterial antagonism by a family of two-component CDCLs that function like mammalian MAC and that are wide-spread in the gut microbiota of diverse human populations.

Suggested Citation

  • Hunter L. Abrahamsen & Tristan C. Sanford & Casie E. Collamore & Bronte A. Johnstone & Michael J. Coyne & Leonor García-Bayona & Michelle P. Christie & Jordan C. Evans & Allison J. Farrand & Katia Flo, 2024. "Distant relatives of a eukaryotic cell-specific toxin family evolved a complement-like mechanism to kill bacteria," Nature Communications, Nature, vol. 15(1), pages 1-15, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-49103-5
    DOI: 10.1038/s41467-024-49103-5
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    References listed on IDEAS

    as
    1. Marina Serna & Joanna L. Giles & B. Paul Morgan & Doryen Bubeck, 2016. "Structural basis of complement membrane attack complex formation," Nature Communications, Nature, vol. 7(1), pages 1-7, April.
    2. Emma C. Couves & Scott Gardner & Tomas B. Voisin & Jasmine K. Bickel & Phillip J. Stansfeld & Edward W. Tate & Doryen Bubeck, 2023. "Structural basis for membrane attack complex inhibition by CD59," Nature Communications, Nature, vol. 14(1), pages 1-13, December.
    3. Jordan C. Evans & Valentina Laclare McEneany & Michael J. Coyne & Elizabeth P. Caldwell & Madeline L. Sheahan & Salena S. Von & Emily M. Coyne & Rodney K. Tweten & Laurie E. Comstock, 2022. "A proteolytically activated antimicrobial toxin encoded on a mobile plasmid of Bacteroidales induces a protective response," Nature Communications, Nature, vol. 13(1), pages 1-13, December.
    Full references (including those not matched with items on IDEAS)

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