The dual role of amyloid β-sheet interaction sequences in the cell surface properties of FLO11-encoded flocculins in the yeast Saccharomyces cerevisiae

Abstract

Fungal adhesins (Als) or flocculins are family of cell surface proteins that mediate adhesion to diverse biotic and abiotic surfaces. A striking characteristic of Als proteins originally identified in the pathogenic Candida albicans is to form functional amyloids that mediate cis-interaction leading to the formation of adhesin nanodomains and trans- interaction between amyloid sequences of opposing cells. In this report, we show that flocculins encoded by FLO11 in Saccharomyces cerevisiae behave like adhesins in C. albicans. To do so, we show that the formation of nanodomains under an external physical force requires a threshold number of amyloid-forming sequences in the Flo11 protein. Then, using a genome editing approach, we constructed strains expressing variants of the Flo11 protein under the endogenous FLO11 promoter, leading to the demonstration that the loss of amyloid-forming sequences strongly reduces cell-cell interaction but has no effect on either plastic adherence or invasive growth in agar, both phenotypes being dependent on the N- and C-terminal ends of Flo11p. Finally, we show that the location of Flo11 is not altered either by the absence of amyloid-forming sequences or by the removal of the N- or C-terminus of the protein.

Data availability

The raw dataset has been deposited to Dryad and is accessible at https:/doi.org/10/10.5061/dryad.v41ns1rvvThe sequence of the FLO11 gene from the industrial strain used in this study has been deposited at NCBI under the provisional reference number Banklt246107 Seq1MW448340)

The following data sets were generated

Article and author information

Author details

  1. Clara Bouyx

    Toulouse Biotechnology Institute, INSA, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  2. Marion Schiavone

    Toulouse Biotechnology Institute, INSA, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  3. Marie-Ange Teste

    Toulouse Biotechnology Institute, INSA, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9173-9190
  4. Etienne Dague

    LAAS, CNRS, Toulouse, France
    Competing interests
    The authors declare that no competing interests exist.
  5. Nathalie Sieczkowski

    Lallemand, Lallemand SAS, Blagnac, France
    Competing interests
    The authors declare that no competing interests exist.
  6. Anne Julien

    Lallemand, Lallemand SAS, Blagnac, France
    Competing interests
    The authors declare that no competing interests exist.
  7. Jean Marie François

    Toulouse Biotechnology Institute, INSA, Toulouse, France
    For correspondence
    fran_jm@insa-toulouse.fr
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-9884-5535

Funding

Region Occitanie (n{degree sign}09003813)

  • Jean Marie François

Lallemand SAS (SAIC2016/048 and SAIC 2018/010)

  • Jean Marie François

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

Reviewing Editor

  1. Kevin J Verstrepen, VIB-KU Leuven Center for Microbiology, Belgium

Version history

  1. Received: March 19, 2021
  2. Accepted: August 29, 2021
  3. Accepted Manuscript published: September 1, 2021 (version 1)
  4. Version of Record published: September 22, 2021 (version 2)

Copyright

© 2021, Bouyx 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. Clara Bouyx
  2. Marion Schiavone
  3. Marie-Ange Teste
  4. Etienne Dague
  5. Nathalie Sieczkowski
  6. Anne Julien
  7. Jean Marie François
(2021)
The dual role of amyloid β-sheet interaction sequences in the cell surface properties of FLO11-encoded flocculins in the yeast Saccharomyces cerevisiae
eLife 10:e68592.
https://doi.org/10.7554/eLife.68592

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https://doi.org/10.7554/eLife.68592

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