Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands

  1. Altaira D Dearborn
  2. Erin A Wall
  3. James L Kizziah
  4. Laura Klenow
  5. Laura K Parker
  6. Keith A Manning
  7. Michael S Spilman
  8. John M Spear
  9. Gail E Christie
  10. Terje Dokland  Is a corresponding author
  1. National Institutes of Health, United States
  2. Virginia Commonwealth University, United States
  3. University of Alabama at Birmingham, United States
  4. Direct Electron, LP, United States
  5. Florida State University, United States

Abstract

Staphylococcus aureus pathogenicity islands (SaPIs), such as SaPI1, exploit specific helper bacteriophages, like 80a, for their high frequency mobilization, a process termed 'molecular piracy'. SaPI1 redirects the helper's assembly pathway to form small capsids that can only accommodate the smaller SaPI1 genome, but not a complete phage genome. SaPI1 encodes two proteins, CpmA and CpmB, that are responsible for this size redirection. We have determined the structures of the 80a and SaPI1 procapsids to near-atomic resolution by cryo-electron microscopy, and show that CpmB competes with the 80a scaffolding protein (SP) for a binding site on the capsid protein (CP), and works by altering the angle between capsomers. We probed these interactions genetically and identified second-site suppressors of lethal mutations in SP. Our structures show, for the first time, the detailed interactions between SP and CP in a bacteriophage, providing unique insights into macromolecular assembly processes.

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Author details

  1. Altaira D Dearborn

    Protein Expression Laboratory, National Institute of Arthritis and Musculoskeletal and Skin Diseases, National Institutes of Health, Bethesda, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Erin A Wall

    Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. James L Kizziah

    Department of Microbiology, University of Alabama at Birmingham, Birmingham, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Laura Klenow

    Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Laura K Parker

    Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Keith A Manning

    Department of Microbiology, University of Alabama at Birmingham, Birmingham, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Michael S Spilman

    Direct Electron, LP, San Diego, United States
    Competing interests
    The authors declare that no competing interests exist.
  8. John M Spear

    Biological Science Imaging Resource, Florida State University, Tallahassee, United States
    Competing interests
    The authors declare that no competing interests exist.
  9. Gail E Christie

    Department of Microbiology and Immunology, Virginia Commonwealth University, Richmond, United States
    Competing interests
    The authors declare that no competing interests exist.
  10. Terje Dokland

    Department of Microbiology, University of Alabama at Birmingham, Birmingham, United States
    For correspondence
    dokland@uab.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-5655-4123

Funding

National Institutes of Health (R01 AI083255)

  • Terje Dokland

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Copyright

© 2017, Dearborn et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Altaira D Dearborn
  2. Erin A Wall
  3. James L Kizziah
  4. Laura Klenow
  5. Laura K Parker
  6. Keith A Manning
  7. Michael S Spilman
  8. John M Spear
  9. Gail E Christie
  10. Terje Dokland
(2017)
Competing scaffolding proteins determine capsid size during mobilization of Staphylococcus aureus pathogenicity islands
eLife 6:e30822.
https://doi.org/10.7554/eLife.30822

Share this article

https://doi.org/10.7554/eLife.30822

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