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Capsid structure of a fungal dsRNA megabirnavirus reveals its previously unidentified surface architecture
Uppsala University, Disciplinary Domain of Science and Technology, Biology, Department of Cell and Molecular Biology, Molecular biophysics.ORCID iD: 0000-0002-6445-2095
Okayama Univ, Inst Plant Sci & Resources, Kurashiki, Okayama, Japan.
Univ Tsukuba, Life Sci Ctr Survival Dynam, Tsukuba Adv Res Alliance, Tsukuba, Ibaraki, Japan..
Okayama Univ, Inst Plant Sci & Resources, Kurashiki, Okayama, Japan..ORCID iD: 0000-0003-0097-9856
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2023 (English)In: PLoS Pathogens, ISSN 1553-7366, E-ISSN 1553-7374, Vol. 19, no 2, article id e1011162Article in journal (Refereed) Published
Abstract [en]

Rosellinia necatrix megabirnavirus 1-W779 (RnMBV1) is a non-enveloped icosahedral double-stranded (ds)RNA virus that infects the ascomycete fungus Rosellinia necatrix, a causative agent that induces a lethal plant disease white root rot. Herein, we have first resolved the atomic structure of the RnMBV1 capsid at 3.2 Å resolution using cryo-electron microscopy (cryo-EM) single-particle analysis. Compared with other non-enveloped icosahedral dsRNA viruses, the RnMBV1 capsid protein structure exhibits an extra-long C-terminal arm and a surface protrusion domain. In addition, the previously unrecognized crown proteins are identified in a symmetry-expanded cryo-EM model and are present over the 3-fold axes. These exclusive structural features of the RnMBV1 capsid could have been acquired for playing essential roles in transmission and/or particle assembly of the megabirnaviruses. Our findings, therefore, will reinforce the understanding of how the structural and molecular machineries of the megabirnaviruses influence the virulence of the disease-related ascomycete fungus.

Author summary

A fungal plant soil-borne pathogen, Rosellinia necatrix, which can cause devastating disease white root rot in many highly valued fruit trees, is difficult to be controlled with conventional approaches such as fungicide applications. Rosellinia necatrix megabirnavirus 1-W779 (RnMBV1) is a dsRNA virus isolated from the R. necatrix field strain, W779, and this virus can be a viro-control candidate to confer hypovirulence in its host R. necatrix. To make use of RnMBV1 in the white root rot disease control, more molecular and structural investigations will offer us more insights. Here, we have performed cryo-electron microscopy (cryo-EM) single-particle analysis, to obtain the first atomic models of RnMBV1 particles. Based on the atomic structures, we found unique both surface and interior features. In addition, we found a previously unidentified protein on the viral surface. These aforementioned structural features might play important roles in the viral life cycles, and will encourage us to apply this fungal virus as a viro-control approach.

Place, publisher, year, edition, pages
Public Library of Science (PLoS), 2023. Vol. 19, no 2, article id e1011162
National Category
Structural Biology Microbiology
Identifiers
URN: urn:nbn:se:uu:diva-501867DOI: 10.1371/journal.ppat.1011162ISI: 000942039200002PubMedID: 36848381OAI: oai:DiVA.org:uu-501867DiVA, id: diva2:1757672
Funder
Swedish Research Council, 2018-03387Swedish Research Council Formas, 2018-00421The Royal Swedish Academy of Sciences, BS2018-0053Available from: 2023-05-17 Created: 2023-05-17 Last updated: 2024-02-14Bibliographically approved
In thesis
1. Structural Decorations in Viruses: Unraveling Acquired Functional Structures in Icosahedral RNA Virus Capsids
Open this publication in new window or tab >>Structural Decorations in Viruses: Unraveling Acquired Functional Structures in Icosahedral RNA Virus Capsids
2024 (English)Doctoral thesis, comprehensive summary (Other academic)
Abstract [en]

Viruses have a profound impact worldwide, posing challenges to animal welfare, agriculture, human health, and the ecosystem. This thesis examines the realm of non-enveloped icosahedral double-stranded (ds)RNA and single-stranded (ss)RNA viruses through three studies. In Paper I, we employed a reverse genetics approach to generate recombinant dsRNA totivirus-like viruses—which negatively impact fisheries and the economy—unraveling the intricate relationships between viral genes and life cycles. Our reverse genetic method has proven essential for generating infectious totivirus-like virus particles, allowing for a nuanced exploration of viral behaviors. Understanding these behaviors has the potential to help in developing effective virus control approaches. In Paper II, we elucidated the previously unknown capsid structure, uncovering the intriguing acquired features of a dsRNA megabirnavirus—Rosellinia necatrix megabirnavirus 1-W779 (RnMBV1)—through cryogenic electron microscopy single-particle analysis. RnMBV1, a fungal virus, has potential applications in controlling white root rot, a plant disease that causes substantial economic losses. Insights into this viral structural information can enhance our ability to leverage this fungal virus for economic and agricultural benefits. In Paper III, we obtained the capsid atomic models of a Marnaviridae ssRNA virus: Chaetoceros socialis forma radians RNA virus 1. Additionally, we generated a structure-based phylogeny using viral protein structures predicted by AlphaFold2; this was done to enhance our understanding of algal virus-host specificity. As harmful algal blooms (HABs) pose global threats to ecology and the economy, Chaetoceros algae have emerged as a contributing factor. Certain Marnaviridae viruses exhibit specific infection patterns in Chaetoceros, thereby influencing the occurrence and mitigation of HABs. Studies on Marnaviridae viruses collectively provide insights into the interactions between algal viruses and their hosts, paving the way for utilizing marine algal viruses to address HAB-related challenges. Together, our functional and structural analyses will contribute to a broader understanding of both dsRNA and ssRNA viruses, their behaviors, and their potential applications in addressing economic, agricultural, ecological, and healthcare issues.

Place, publisher, year, edition, pages
Uppsala: Acta Universitatis Upsaliensis, 2024. p. 69
Series
Digital Comprehensive Summaries of Uppsala Dissertations from the Faculty of Science and Technology, ISSN 1651-6214 ; 2364
Keywords
Viruses, RNA viruses, capsid, structure, cryo-EM
National Category
Structural Biology
Research subject
Molecular Life Sciences
Identifiers
urn:nbn:se:uu:diva-523070 (URN)978-91-513-2035-9 (ISBN)
Public defence
2024-04-09, room A1:111a, BMC, Husargatan 3, Uppsala, 13:15 (English)
Opponent
Supervisors
Available from: 2024-03-08 Created: 2024-02-13 Last updated: 2024-03-08Bibliographically approved

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Wang, HanOkamoto, Kenta

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