The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization.
Infecting a wide range of hosts, members of Reovirales (formerly Reoviridae) consist of a genome with different numbers of segmented double stranded RNAs (dsRNA) encapsulated by a proteinaceous shell and carry out genome replication and transcription inside the virion. Several cryo-electron microsco...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
| Published: |
Public Library of Science (PLoS)
2023-04-01
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| Series: | PLoS Pathogens |
| Online Access: | https://doi.org/10.1371/journal.ppat.1011341 |
| _version_ | 1797821962179837952 |
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| author | Qinfen Zhang Yuanzhu Gao Matthew L Baker Shanshan Liu Xudong Jia Haidong Xu Jianguo He Jason T Kaelber Shaoping Weng Wen Jiang |
| author_facet | Qinfen Zhang Yuanzhu Gao Matthew L Baker Shanshan Liu Xudong Jia Haidong Xu Jianguo He Jason T Kaelber Shaoping Weng Wen Jiang |
| author_sort | Qinfen Zhang |
| collection | DOAJ |
| description | Infecting a wide range of hosts, members of Reovirales (formerly Reoviridae) consist of a genome with different numbers of segmented double stranded RNAs (dsRNA) encapsulated by a proteinaceous shell and carry out genome replication and transcription inside the virion. Several cryo-electron microscopy (cryo-EM) structures of reoviruses with 9, 10 or 11 segmented dsRNA genomes have revealed insights into genome arrangement and transcription. However, the structure and genome arrangement of 12-segmented Reovirales members remain poorly understood. Using cryo-EM, we determined the structure of mud crab reovirus (MCRV), a 12-segmented dsRNA virus that is a putative member of Reovirales in the non-turreted Sedoreoviridae family, to near-atomic resolutions with icosahedral symmetry (3.1 Å) and without imposing icosahedral symmetry (3.4 Å). These structures revealed the organization of the major capsid proteins in two layers: an outer T = 13 layer consisting of VP12 trimers and unique VP11 clamps, and an inner T = 1 layer consisting of VP3 dimers. Additionally, ten RNA dependent RNA polymerases (RdRp) were well resolved just below the VP3 layer but were offset from the 5-fold axes and arranged with D5 symmetry, which has not previously been seen in other members of Reovirales. The N-termini of VP3 were shown to adopt four unique conformations; two of which anchor the RdRps, while the other two conformations are likely involved in genome organization and capsid stability. Taken together, these structures provide a new level of understanding for capsid stabilization and genome organization of segmented dsRNA viruses. |
| first_indexed | 2024-03-13T10:00:46Z |
| format | Article |
| id | doaj.art-01d0a9df04a54f14a6d1d6fc14f4820b |
| institution | Directory Open Access Journal |
| issn | 1553-7366 1553-7374 |
| language | English |
| last_indexed | 2024-03-13T10:00:46Z |
| publishDate | 2023-04-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Pathogens |
| spelling | doaj.art-01d0a9df04a54f14a6d1d6fc14f4820b2023-05-23T05:31:36ZengPublic Library of Science (PLoS)PLoS Pathogens1553-73661553-73742023-04-01194e101134110.1371/journal.ppat.1011341The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization.Qinfen ZhangYuanzhu GaoMatthew L BakerShanshan LiuXudong JiaHaidong XuJianguo HeJason T KaelberShaoping WengWen JiangInfecting a wide range of hosts, members of Reovirales (formerly Reoviridae) consist of a genome with different numbers of segmented double stranded RNAs (dsRNA) encapsulated by a proteinaceous shell and carry out genome replication and transcription inside the virion. Several cryo-electron microscopy (cryo-EM) structures of reoviruses with 9, 10 or 11 segmented dsRNA genomes have revealed insights into genome arrangement and transcription. However, the structure and genome arrangement of 12-segmented Reovirales members remain poorly understood. Using cryo-EM, we determined the structure of mud crab reovirus (MCRV), a 12-segmented dsRNA virus that is a putative member of Reovirales in the non-turreted Sedoreoviridae family, to near-atomic resolutions with icosahedral symmetry (3.1 Å) and without imposing icosahedral symmetry (3.4 Å). These structures revealed the organization of the major capsid proteins in two layers: an outer T = 13 layer consisting of VP12 trimers and unique VP11 clamps, and an inner T = 1 layer consisting of VP3 dimers. Additionally, ten RNA dependent RNA polymerases (RdRp) were well resolved just below the VP3 layer but were offset from the 5-fold axes and arranged with D5 symmetry, which has not previously been seen in other members of Reovirales. The N-termini of VP3 were shown to adopt four unique conformations; two of which anchor the RdRps, while the other two conformations are likely involved in genome organization and capsid stability. Taken together, these structures provide a new level of understanding for capsid stabilization and genome organization of segmented dsRNA viruses.https://doi.org/10.1371/journal.ppat.1011341 |
| spellingShingle | Qinfen Zhang Yuanzhu Gao Matthew L Baker Shanshan Liu Xudong Jia Haidong Xu Jianguo He Jason T Kaelber Shaoping Weng Wen Jiang The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization. PLoS Pathogens |
| title | The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization. |
| title_full | The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization. |
| title_fullStr | The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization. |
| title_full_unstemmed | The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization. |
| title_short | The structure of a 12-segmented dsRNA reovirus: New insights into capsid stabilization and organization. |
| title_sort | structure of a 12 segmented dsrna reovirus new insights into capsid stabilization and organization |
| url | https://doi.org/10.1371/journal.ppat.1011341 |
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