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PreprintCited by 35Advanced Electron Microscopy Techniques and ApplicationsBacterial Genetics and BiotechnologyBiochemical and Structural Characterization

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Interdigitated immunoglobulin arrays form the hyperstable surface layer of the extremophilic bacterium Deinococcus radiodurans

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von Kügelgen, Andriko, van Dorst, Sofie, Yamashita, Keitaro, Sexton, Danielle L., Tocheva, Elitza I., Murshudov, Garib, Alva, Vikram, Bharat, Tanmay A. M.·2022·Proceedings of the National Academy of Sciences
DOI 10.1101/2022.09.15.508085PMC PMC10120038

Preprint — published as 10.1073/pnas.2215808120 · Paper page

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Abstract

Deinococcus radiodurans is an atypical diderm bacterium with a remarkable ability to tolerate various environmental stresses, partly because of its complex cell envelope encapsulated within a hyperstable surface layer (S-layer). Despite decades of research into this cell envelope, atomic structural details of the S-layer have remained obscure. In this study, we report the electron cryomicroscopy structure of the D. radiodurans S-layer, showing how it is formed by the Hexagonally Packed Intermediate-layer (HPI) protein arranged in a planar hexagonal lattice. The HPI protein forms an array of immunoglobulin-like folds within the S-layer, with each monomer extending into the adjoining hexamer, leading to a highly interconnected, stable, sheet-like arrangement. Using electron cryotomography and subtomogram averaging from focused ion beam-milled D. radiodurans cells, we obtained a structure of the cellular S-layer, showing how this HPI S-layer coats native membranes on the surface of cells. Our S-layer structure from the diderm bacterium D. radiodurans shows similarities to immunoglobulin-like domain-containing S-layers from monoderm bacteria and archaea, highlighting shared traits in cell surface organization across different domains of life, with connotations on the evolution of immunoglobulin-based molecular recognition systems in eukaryotes.

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Metadata

Authors
von Kügelgen, A., van Dorst, S., Yamashita, K., Sexton, D. L., Tocheva, E. I., Murshudov, G., Alva, V., & Bharat, T. A. M.
Affiliations
  • MRC Laboratory of Molecular Biology (GB)
  • University of Oxford (GB)
  • University of British Columbia (CA)
  • Max Planck Institute for Biology (DE)
Corresponding author
Bharat, Tanmay A. M.
ORCID
Venue
Proceedings of the National Academy of Sciences
Publisher
openRxiv
Published
2022-09-15
Volume
120
Issue
16
Pages
e2215808120-e2215808120
ISSN
0027-8424 (ISSN-L)
DOI
10.1101/2022.09.15.508085
PMC
PMC10120038
OpenAlex
W4365136293
Cited by
35
References
1
Citations by year
2026: 6 · 2025: 9 · 2024: 13 · 2023: 7
FWCI
3.10
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • Proceedings of the National Academy of Sciences (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
Funders
  • European Molecular Biology Organization
  • UK Research and Innovation (MC_UP_1201/31)
  • Government of Canada (RGPIN 04345)
  • Leverhulme Trust
  • Human Frontier Science Program (RGY0074/2021)
  • Lister Institute of Preventive Medicine
  • Max-Planck-Gesellschaft
  • Natural Sciences and Engineering Research Council of Canada (546024, RGPIN 04345, 04345)
  • Medical Research Council (MC_UP_1201/31)
Topics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Structural Biology › Advanced Electron Microscopy Techniques and Applications
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Genetics › Bacterial Genetics and Biotechnology
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Biochemical and Structural Characterization
Keywords
Deinococcus radiodurans, surface layer, S-layer, immunoglobulin-like fold, cell envelope, cryo-electron tomography, subtomogram averaging, extremophiles, radioresistance (biology)
MeSH terms
Bacterial Proteins, Cell Membrane, Cell Wall, Immunoglobulins, Deinococcus

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