A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses
Abstract Marseilleviridae is a family of giant viruses, showing a characteristic internal membrane with extrusions underneath the icosahedral vertices. However, such large objects, with a maximum diameter of 250 nm are technically difficult to examine at sub-nanometre resolution by cryo-electron mic...
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| Format: | Article |
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Nature Portfolio
2022-12-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-022-24651-2 |
| _version_ | 1798005051996766208 |
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| author | Akane Chihara Raymond N. Burton-Smith Naoko Kajimura Kaoru Mitsuoka Kenta Okamoto Chihong Song Kazuyoshi Murata |
| author_facet | Akane Chihara Raymond N. Burton-Smith Naoko Kajimura Kaoru Mitsuoka Kenta Okamoto Chihong Song Kazuyoshi Murata |
| author_sort | Akane Chihara |
| collection | DOAJ |
| description | Abstract Marseilleviridae is a family of giant viruses, showing a characteristic internal membrane with extrusions underneath the icosahedral vertices. However, such large objects, with a maximum diameter of 250 nm are technically difficult to examine at sub-nanometre resolution by cryo-electron microscopy. Here, we tested the utility of 1 MV high-voltage cryo-EM (cryo-HVEM) for single particle structural analysis (SPA) of giant viruses using tokyovirus, a species of Marseilleviridae, and revealed the capsid structure at 7.7 Å resolution. The capsid enclosing the viral DNA consisted primarily of four layers: (1) major capsid proteins (MCPs) and penton proteins, (2) minor capsid proteins (mCPs), (3) scaffold protein components (ScPCs), and (4) internal membrane. The mCPs showed a novel capsid lattice consisting of eight protein components. ScPCs connecting the icosahedral vertices supported the formation of the membrane extrusions, and possibly act like tape measure proteins reported in other giant viruses. The density on top of the MCP trimer was suggested to include glycoproteins. This is the first attempt at cryo-HVEM SPA. We found the primary limitations to be the lack of automated data acquisition and software support for collection and processing and thus achievable resolution. However, the results pave the way for using cryo-HVEM for structural analysis of larger biological specimens. |
| first_indexed | 2024-04-11T12:33:06Z |
| format | Article |
| id | doaj.art-35198147665248e78414772613cdfc49 |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-04-11T12:33:06Z |
| publishDate | 2022-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-35198147665248e78414772613cdfc492022-12-22T04:23:41ZengNature PortfolioScientific Reports2045-23222022-12-0112111510.1038/s41598-022-24651-2A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant virusesAkane Chihara0Raymond N. Burton-Smith1Naoko Kajimura2Kaoru Mitsuoka3Kenta Okamoto4Chihong Song5Kazuyoshi Murata6Department of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI)Exploratory Research Center on Life and Living Systems (ExCELLS), National Institutes of Natural SciencesResearch Center for Ultra-High Voltage Electron Microscopy, Osaka UniversityResearch Center for Ultra-High Voltage Electron Microscopy, Osaka UniversityProgram in Molecular Biophysics, Department of Cell and Molecular Biology, Uppsala UniversityDepartment of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI)Department of Physiological Sciences, School of Life Science, The Graduate University for Advanced Studies (SOKENDAI)Abstract Marseilleviridae is a family of giant viruses, showing a characteristic internal membrane with extrusions underneath the icosahedral vertices. However, such large objects, with a maximum diameter of 250 nm are technically difficult to examine at sub-nanometre resolution by cryo-electron microscopy. Here, we tested the utility of 1 MV high-voltage cryo-EM (cryo-HVEM) for single particle structural analysis (SPA) of giant viruses using tokyovirus, a species of Marseilleviridae, and revealed the capsid structure at 7.7 Å resolution. The capsid enclosing the viral DNA consisted primarily of four layers: (1) major capsid proteins (MCPs) and penton proteins, (2) minor capsid proteins (mCPs), (3) scaffold protein components (ScPCs), and (4) internal membrane. The mCPs showed a novel capsid lattice consisting of eight protein components. ScPCs connecting the icosahedral vertices supported the formation of the membrane extrusions, and possibly act like tape measure proteins reported in other giant viruses. The density on top of the MCP trimer was suggested to include glycoproteins. This is the first attempt at cryo-HVEM SPA. We found the primary limitations to be the lack of automated data acquisition and software support for collection and processing and thus achievable resolution. However, the results pave the way for using cryo-HVEM for structural analysis of larger biological specimens.https://doi.org/10.1038/s41598-022-24651-2 |
| spellingShingle | Akane Chihara Raymond N. Burton-Smith Naoko Kajimura Kaoru Mitsuoka Kenta Okamoto Chihong Song Kazuyoshi Murata A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses Scientific Reports |
| title | A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses |
| title_full | A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses |
| title_fullStr | A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses |
| title_full_unstemmed | A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses |
| title_short | A novel capsid protein network allows the characteristic internal membrane structure of Marseilleviridae giant viruses |
| title_sort | novel capsid protein network allows the characteristic internal membrane structure of marseilleviridae giant viruses |
| url | https://doi.org/10.1038/s41598-022-24651-2 |
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