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PreprintCited by 18Advanced Electron Microscopy Techniques and ApplicationsBacterial Genetics and BiotechnologyEnzyme Structure and Function

The DOI matches its Crossref record; 1 of the 1 references it cites were found in a registry or an index.

Mapping the ultrastructural topology of the corynebacterial cell surface

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Isbilir, Buse, Yeates, Anna, Alva, Vikram, Bharat, Tanmay A.M.·2024·PLoS Biology
DOI 10.1101/2024.09.05.611374PMC PMC12021427

Preprint — published as 10.1371/journal.pbio.3003130 · Paper page

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Abstract

Corynebacterium glutamicum is a diderm bacterium extensively used in the industrial-scale production of amino acids. Corynebacteria belong to the bacterial family Mycobacteriaceae , which is characterized by a highly unusual cell envelope with an outer membrane consisting of mycolic acids. Despite the occurrence of this distinctive cell envelope in several bacterial pathogens, including Corynebacterium diphtheriae, Mycobacterium tuberculosis , and Mycobacterium leprae , its ultrastructural and molecular details remain elusive. To address this, we investigated the cell envelope of C. glutamicum using electron cryotomography and cryomicroscopy of focused ion beam-milled cells. Our high-resolution images allowed us to accurately map the different components of the cell envelope into the tomographic density. Our data reveal that C. glutamicum has a variable cell envelope, with the outermost layer comprising the surface (S-)layer, which decorates the mycomembrane in a patchy manner. We further isolated and resolved the structure of the S-layer at 3.1 Å resolution using single particle electron cryomicroscopy. Our structure shows that the S-layer of C. glutamicum is composed of a hexagonal array of the PS2 protein, which interacts directly with the mycomembrane via a coiled coil-containing anchoring segment. Bioinformatic analyses revealed that the PS2 S-layer is sparsely yet exclusively present within the Corynebacterium genus and absent in other genera of the Mycobacteriaceae family, suggesting distinct evolutionary pathways in the development of their cell envelopes. Our structural and cellular data collectively provide a high-resolution topography of the unusual C. glutamicum cell surface, features of which are shared by many pathogenic and microbiome-associated bacteria, as well as by several industrially significant bacterial species. This study, therefore, provides a strong experimental framework for understanding cell envelopes that contain mycolic acids.

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Metadata

Authors
Isbilir, B., Yeates, A., Alva, V., & Bharat, T. A. M.
Affiliations
  • MRC Laboratory of Molecular Biology (GB)
  • Max Planck Institute for Biology (DE)
Corresponding author
Bharat, Tanmay A.M.
ORCID
Venue
PLoS Biology
Publisher
openRxiv
Published
2024-09-05
Volume
23
Issue
4
Pages
e3003130-e3003130
ISSN
1544-9173 (ISSN-L)
DOI
10.1101/2024.09.05.611374
PMC
PMC12021427
OpenAlex
W4409474122
Cited by
18
References
1
Citations by year
2026: 8 · 2025: 10
FWCI
6.48
Type
journal article
Language
en
Open access
Licence
Locations
  • PLoS Biology (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • Europe PMC (PubMed Central) (publishedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • Apollo (University of Cambridge) (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • European Molecular Biology Organization
  • Human Frontier Science Program (RGY0074/2021)
  • Wellcome Trust (225317, 225317/Z/22/Z)
  • UK Research and Innovation (MC_UP_1201/31)
  • Leverhulme Trust
  • Lister Institute of Preventive Medicine
  • 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 › Structural Biology › Enzyme Structure and Function
Keywords
Corynebacterium glutamicum, mycomembrane, mycolic acids, S-layer, pS2 protein, cryo-electron tomography, Mycobacteriaceae
MeSH terms
Bacterial Proteins, Cell Membrane, Cell Wall, Mycolic Acids, Cryoelectron Microscopy, Corynebacterium glutamicum, Electron Microscope Tomography

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