The giant staphylococcal protein Embp facilitates colonization of surfaces through Velcro-like attachment to fibrillated fibronectin

  1. Nasar Khan
  2. Hüsnü Aslan  Is a corresponding author
  3. Henning Büttner
  4. Holger Rohde
  5. Thaddeus Wayne Golbek
  6. Steven Joop Roeters
  7. Sander Woutersen
  8. Tobias Weidner
  9. Rikke Louise Meyer  Is a corresponding author
  1. Aarhus University, Denmark
  2. University Medical Centre Hamburg-Eppendorf, Germany
  3. University of Amsterdam, Netherlands

Abstract

Staphylococcus epidermidis causes some of the most hard-to-treat clinical infections by forming biofilms: Multicellular communities of bacteria encased in a protective matrix, supporting immune evasion and tolerance against antibiotics. Biofilms occur most commonly on medical implants, and a key event in implant colonization is the robust adherence to the surface, facilitated by interactions between bacterial surface proteins and host matrix components. S. epidermidis is equipped with a giant adhesive protein, Embp, which facilitates bacterial interactions with surface-deposited, but not soluble fibronectin. The structural basis behind this selective binding process has remained obscure. Using a suite of single-cell and single-molecule analysis techniques, we show that S. epidermidis is capable of such distinction because Embp binds specifically to fibrillated fibronectin on surfaces, while ignoring globular fibronectin in solution. S. epidermidis adherence is critically dependent on multi-valent interactions involving 50 fibronectin-binding repeats of Embp. This unusual, Velcro-like interaction proved critical for colonization of surfaces under high flow, making this newly identified attachment mechanism particularly relevant for colonization of intravascular devices, such as prosthetic heart valves or vascular grafts. Other biofilm-forming pathogens, such as Staphylococcus aureus, express homologs of Embp and likely deploy the same mechanism for surface colonization. Our results may open for a novel direction in efforts to combat devastating, biofilm-associated infections, as the development of implant materials that steer the conformation of adsorbed proteins is a much more manageable task than avoiding protein adsorption altogether.

Data availability

Figure 1: Source data file contains original image files. Figure 2: Data are as shown in the figures. Figure 3: Source data file contains data and graph. Figure 4 and 5: Source data file contains force spectroscopy curves and processing information. Figure 5: Source data file contains the data and graph.

Article and author information

Author details

  1. Nasar Khan

    Interdisciplinary Nanoscience Center, Aarhus University, Aarhus, Denmark
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-9196-9321
  2. Hüsnü Aslan

    Interdisciplinary Nanoscience Center, Aarhus University, Aarhus, Denmark
    For correspondence
    asl@dfm.dk
    Competing interests
    The authors declare that no competing interests exist.
  3. Henning Büttner

    Institute for Medical Microbiology, Virology and Hygiene, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-5086-4961
  4. Holger Rohde

    Institute for Medical Microbiology, Virology and Hygiene, University Medical Centre Hamburg-Eppendorf, Hamburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  5. Thaddeus Wayne Golbek

    Department of Chemistry, Aarhus University, Aarhus C, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  6. Steven Joop Roeters

    Department of Chemistry, Aarhus University, Aarhus C, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  7. Sander Woutersen

    Van 't Hoff Institute of Molecular Sciences, University of Amsterdam, Amsterdam, Netherlands
    Competing interests
    The authors declare that no competing interests exist.
  8. Tobias Weidner

    Department of Chemistry, Aarhus University, Aarhus C, Denmark
    Competing interests
    The authors declare that no competing interests exist.
  9. Rikke Louise Meyer

    Interdisciplinary Nanoscience Center, Aarhus University, Aarhus C, Denmark
    For correspondence
    rikke.meyer@inano.au.dk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6485-5134

Funding

Carlsbergfondet (CF16-0342)

  • Nasar Khan
  • Hüsnü Aslan

Lundbeckfonden (Postdoctoral fellowship)

  • Thaddeus Wayne Golbek
  • Steven Joop Roeters

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

Copyright

© 2022, Khan 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. Nasar Khan
  2. Hüsnü Aslan
  3. Henning Büttner
  4. Holger Rohde
  5. Thaddeus Wayne Golbek
  6. Steven Joop Roeters
  7. Sander Woutersen
  8. Tobias Weidner
  9. Rikke Louise Meyer
(2022)
The giant staphylococcal protein Embp facilitates colonization of surfaces through Velcro-like attachment to fibrillated fibronectin
eLife 11:e76164.
https://doi.org/10.7554/eLife.76164

Share this article

https://doi.org/10.7554/eLife.76164

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