Structural dynamics of RbmA governs plasticity of Vibrio cholerae biofilms

  1. Jiunn CN Fong
  2. Andrew Rogers
  3. Alicia K Michael
  4. Nicole C Parsley
  5. William-Cole Cornell
  6. Yu-Cheng Lin
  7. Praveen K Singh
  8. Raimo Hartmann
  9. Knut Drescher
  10. Evgeny Vinogradov
  11. Lars EP Dietrich
  12. Carrie L Partch  Is a corresponding author
  13. Fitnat H Yildiz  Is a corresponding author
  1. University of California, Santa Cruz, United States
  2. University of North Carolina Chapel Hill, United States
  3. Columbia University, United States
  4. Max Planck Institute for Terrestrial Microbiology, Germany
  5. National Research Council, Canada

Abstract

Biofilm formation is critical for the infection cycle of Vibrio cholerae. Vibrio exopolysaccharides (VPS) and the matrix proteins RbmA, Bap1 and RbmC are required for the development of biofilm architecture. We demonstrate that RbmA binds VPS directly and uses a binary structural switch within its first fibronectin type III (FnIII-1) domain to control RbmA structural dynamics and the formation of VPS-dependent higher-order structures. The structural switch in FnIII-1 regulates interactions in trans with the FnIII-2 domain, leading to open (monomeric) or closed (dimeric) interfaces. The ability of RbmA to switch between open and closed states is important for V. cholerae biofilm formation, as RbmA variants with switches that are locked in either of the two states lead to biofilms with altered architecture and structural integrity.

Article and author information

Author details

  1. Jiunn CN Fong

    Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  2. Andrew Rogers

    Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  3. Alicia K Michael

    Department of Chemistry and Biochemistry, University of California, Santa Cruz, Santa Cruz, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Nicole C Parsley

    Department of Chemistry, University of North Carolina Chapel Hill, Chapel Hill, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. William-Cole Cornell

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  6. Yu-Cheng Lin

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. Praveen K Singh

    Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  8. Raimo Hartmann

    Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  9. Knut Drescher

    Max Planck Institute for Terrestrial Microbiology, Marburg, Germany
    Competing interests
    The authors declare that no competing interests exist.
  10. Evgeny Vinogradov

    National Research Council, Ottawa, Canada
    Competing interests
    The authors declare that no competing interests exist.
  11. Lars EP Dietrich

    Department of Biological Sciences, Columbia University, New York, United States
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-2049-1137
  12. Carrie L Partch

    Department of Chemistry and Biochemistry, University of California, Santa Cruz, Santa Cruz, United States
    For correspondence
    cpartch@ucsc.edu
    Competing interests
    The authors declare that no competing interests exist.
  13. Fitnat H Yildiz

    Department of Microbiology and Environmental Toxicology, University of California, Santa Cruz, Santa Cruz, United States
    For correspondence
    fyildiz@ucsc.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6384-7167

Funding

National Institute of Allergy and Infectious Diseases (RO1AI055987)

  • Fitnat H Yildiz

National Institute of General Medical Sciences (GM107069)

  • Carrie L Partch

Human Frontier Science Program (CDA00084/2015-C)

  • Knut Drescher

National Institute of General Medical Sciences (CA189660)

  • Alicia K Michael

National Institute of Allergy and Infectious Diseases (R01 AI103369)

  • Lars EP Dietrich

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

Reviewing Editor

  1. Dianne K Newman, Howard Hughes Medical Institute, California Institute of Technology, United States

Version history

  1. Received: February 19, 2017
  2. Accepted: July 31, 2017
  3. Accepted Manuscript published: August 1, 2017 (version 1)
  4. Version of Record published: September 19, 2017 (version 2)

Copyright

© 2017, Fong 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. Jiunn CN Fong
  2. Andrew Rogers
  3. Alicia K Michael
  4. Nicole C Parsley
  5. William-Cole Cornell
  6. Yu-Cheng Lin
  7. Praveen K Singh
  8. Raimo Hartmann
  9. Knut Drescher
  10. Evgeny Vinogradov
  11. Lars EP Dietrich
  12. Carrie L Partch
  13. Fitnat H Yildiz
(2017)
Structural dynamics of RbmA governs plasticity of Vibrio cholerae biofilms
eLife 6:e26163.
https://doi.org/10.7554/eLife.26163

Share this article

https://doi.org/10.7554/eLife.26163

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