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PreprintCited by 5Bacteriophages and microbial interactionsAdvanced Electron Microscopy Techniques and ApplicationsBacterial Genetics and Biotechnology

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A stargate mechanism of Microviridae genome delivery unveiled by cryogenic electron tomography

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Bardy, Pavol, MacDonald, Conor I.W., Kirchberger, Paul C., Jenkins, Huw T., Botka, Tibor, Byrom, Lewis, Alim, Nawshin T.B., Traore, Daouda A.K., König, Hannah C., Nicholas, Tristan R., Chechik, Maria, Hart, Samuel J., Turkenburg, Johan P., Blaza, James N., Beatty, J. Thomas, Fogg, Paul C.M., Antson, Alfred A.·2024·mBio
DOI 10.1101/2024.06.11.598214PMC PMC11980548

Preprint — published as 10.1128/mbio.03713-24 · Paper page

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Abstract

Single-stranded DNA bacteriophages of the Microviridae family are major components of the global virosphere. Microviruses are highly abundant in aquatic ecosystems and are prominent members of the mammalian gut microbiome, where their diversity has been linked to various chronic health disorders. Despite the clear importance of microviruses, little is known about the molecular mechanism of host infection. Here, we have characterized an exceptionally large microvirus, Ebor, and provide crucial insights into long-standing mechanistic questions. Cryogenic electron microscopy of Ebor revealed a capsid with trimeric protrusions that recognise lipopolysaccharides on the host surface. Cryogenic electron tomography of the host cell colonized with virus particles demonstrated that the virus initially attaches to the cell via five such protrusions, located at the corners of a single pentamer. This interaction triggers a stargate mechanism of capsid opening along the 5-fold symmetry axis, enabling delivery of the virus genome. Despite variations in specific virus-host interactions among different Microviridae family viruses, structural data indicate that the stargate mechanism of infection is universally employed by all members of the family. Startlingly, our data reveal a mechanistic link for the opening of relatively small capsids made out of a single jelly-roll fold with the structurally unrelated giant viruses.

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Metadata

Authors
Bardy, P., MacDonald, C. I. W., Kirchberger, P. C., Jenkins, H. T., Botka, T., Byrom, L., Alim, N. T. B., Traore, D. A. K., König, H. C., Nicholas, T. R., Chechik, M., Hart, S. J., Turkenburg, J. P., Blaza, J. N., Beatty, J. T., Fogg, P. C. M., & Antson, A. A.
Affiliations
  • University of York (GB)
  • Oklahoma State University (US)
  • Masaryk University (CZ)
  • University of British Columbia (CA)
Corresponding author
Antson, Alfred A.
ORCID
Venue
mBio
Publisher
openRxiv
Published
2024-06-11
Volume
16
Issue
4
Pages
e0371324-e0371324
ISSN
2150-7511 (ISSN-L)
DOI
10.1101/2024.06.11.598214
PMC
PMC11980548
OpenAlex
W4408618497
Cited by
5
References
1
Citations by year
2026: 4 · 2025: 1
FWCI
2.65
Type
journal article
Language
en
Open access
Licence
cc-by
Locations
  • mBio (publishedVersion, cc-by)
  • bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by)
  • PubMed Central (publishedVersion, cc-by)
  • PubMed (publishedVersion)
  • White Rose Research Online (University of Leeds, The University of Sheffield, University of York) (submittedVersion)
  • PubMed Central (submittedVersion, cc-by)
  • DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders
  • Wellcome Trust (206161, Z/17/Z, 109363, 224067/Z/21/Z, 206377, 206161/Z/17/Z, 109363/Z/15/A)
  • Yorkshire Forward (EP/K039660/1, EP/M028127/1)
  • European Commission (224067, LX22NPO5103)
  • Deutscher Akademischer Austauschdienst
  • Canadian Network for Research and Innovation in Machining Technology, Natural Sciences and Engineering Research Council of Canada (RGPIN 2018-03898)
  • University of Toronto
  • Mitacs
  • National Institutes of Health (5p20gm152333-02)
  • Natural Sciences and Engineering Research Council of Canada (rgpin-2018-03898)
  • Engineering and Physical Sciences Research Council (206161/Z/17/Z, EP/M028127/1, EP/K039660/1)
  • Biotechnology and Biological Sciences Research Council (BB/X018385/1)
  • National Institute of General Medical Sciences (1P20GM152333, U24GM129541, 1P20GM152333-01, 1P20GM152333-01:8040, P20 GM152333)
  • SLAC National Accelerator Laboratory
  • Common Fund
Topics
  • Life Sciences › Immunology and Microbiology › Virology › Bacteriophages and microbial interactions
  • 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
Keywords
Microviridae, Rhodobacter capsulatus, major capsid protein, lipopolysaccharide recognition, host cell attachment, lytic enzymes, gut virome

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