Structure of the two-component S-layer of the archaeon Sulfolobus acidocaldarius

  1. Lavinia Gambelli
  2. Mathew McLaren
  3. Rebecca Conners
  4. Kelly Sanders
  5. Matthew C Gaines
  6. Lewis Clark
  7. Vicki AM Gold
  8. Daniel Kattnig
  9. Mateusz Sikora
  10. Cyril Hanus
  11. Michail N Isupov
  12. Bertram Daum  Is a corresponding author
  1. MRC Laboratory of Molecular Biology, United Kingdom
  2. University of Exeter, United Kingdom
  3. Max Planck Institute of Biophysics, Germany
  4. Inserm U894, University Paris-Descartes, France

Abstract

Surface layers (S-layers) are resilient two-dimensional protein lattices that encapsulate many bacteria and most archaea. In archaea, S-layers usually form the only structural component of the cell wall and thus act as the final frontier between the cell and its environment. Therefore, S-layers are crucial for supporting microbial life. Notwithstanding their importance, little is known about archaeal S-layers at the atomic level. Here, we combined single particle cryo electron microscopy (cryoEM), cryo electron tomography (cryoET) and Alphafold2 predictions to generate an atomic model of the two-component S-layer of Sulfolobus acidocaldarius. The outer component of this S-layer (SlaA) is a flexible, highly glycosylated, and stable protein. Together with the inner and membrane-bound component (SlaB), they assemble into a porous and interwoven lattice. We hypothesise that jackknife-like conformational changes, changes play important roles in S-layer assembly.

Data availability

The atomic coordinates of SlaA were deposited in the Protein Data Bank (https://www.rcsb.org/) with accession numbers PDB-7ZCX, PDDB-8AN3, and PDB-8AN3 for pH 4, 7 and 10, respectively. The electron density maps were deposited in the EM DataResource (https://www.emdataresource.org/) with accession numbers EMD-14635, EMD-15531 and EMD-15531 for pH 4, 7 and 10, respectively.Sub-tomogram averaging map of the S-layer has been deposited in the EMDB (EMD-18127) and models of the hexameric and trimeric pores in the Protein Databank under accession codes PDB-8QP0 and PDB-8QOX, respectivelyOther structural data used in this study are: H. volcanii csg (PDB ID: 7PTR, http://dx.doi.org/10.2210/pdb7ptr/pdb), and C. crescentus RsaA ((N-terminus PDB ID: 6T72, http://dx.doi.org/10.2210/pdb6t72/pdb, C-terminus PDB ID: 5N8P, http://dx.doi.org/10.2210/pdb5n8p/pdb).

Article and author information

Author details

  1. Lavinia Gambelli

    MRC Laboratory of Molecular Biology, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-2257-6364
  2. Mathew McLaren

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  3. Rebecca Conners

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  4. Kelly Sanders

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Matthew C Gaines

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  6. Lewis Clark

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0009-0003-9917-3912
  7. Vicki AM Gold

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6908-0745
  8. Daniel Kattnig

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  9. Mateusz Sikora

    Department of Theoretical Biophysics, Max Planck Institute of Biophysics, Frankfurt am Main, Germany
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1691-4045
  10. Cyril Hanus

    Institute of Psychiatry and Neurosciences of Paris, Inserm U894, University Paris-Descartes, Paris, France
    Competing interests
    The authors declare that no competing interests exist.
  11. Michail N Isupov

    Faculty of Health and Life Sci, University of Exeter, Exeter, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  12. Bertram Daum

    Living Systems Institute, University of Exeter, Exeter, United Kingdom
    For correspondence
    b.daum2@exeter.ac.uk
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3767-264X

Funding

European Research Council (803894)

  • Lavinia Gambelli
  • Mathew McLaren
  • Rebecca Conners
  • Kelly Sanders
  • Matthew C Gaines
  • Bertram Daum

Wellcome Trust (210363/Z/18/Z)

  • Rebecca Conners
  • Vicki AM Gold

Wellcome Trust (212439/Z/18/Z)

  • Bertram Daum

Agence Nationale de la Recherche (ANR-16-CE16-0009-01)

  • Cyril Hanus

Agence Nationale de la Recherche (ANR-21-CE16-0021-01)

  • Cyril Hanus

Leverhulme Trust (RPG-2020-261)

  • Daniel Kattnig

Biotechnology and Biological Sciences Research Council (BB/R008639/1)

  • Rebecca Conners

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

Reviewing Editor

  1. Han Remaut, VIB-VUB Center for Structural Biology, Belgium

Version history

  1. Received: November 1, 2022
  2. Accepted: January 19, 2024
  3. Accepted Manuscript published: January 22, 2024 (version 1)

Copyright

© 2024, Gambelli 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. Lavinia Gambelli
  2. Mathew McLaren
  3. Rebecca Conners
  4. Kelly Sanders
  5. Matthew C Gaines
  6. Lewis Clark
  7. Vicki AM Gold
  8. Daniel Kattnig
  9. Mateusz Sikora
  10. Cyril Hanus
  11. Michail N Isupov
  12. Bertram Daum
(2024)
Structure of the two-component S-layer of the archaeon Sulfolobus acidocaldarius
eLife 13:e84617.
https://doi.org/10.7554/eLife.84617

Share this article

https://doi.org/10.7554/eLife.84617

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