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Elucidation of the viral disassembly switch of tobacco mosaic virus

View ORCID ProfileFelix Weis, View ORCID ProfileMaximilian Beckers, View ORCID ProfileIris von der Hocht, View ORCID ProfileCarsten Sachse
doi: https://doi.org/10.1101/569178
Felix Weis
1European Molecular Biology Laboratory (EMBL), Structural and Computational Biology Unit, Meyerhofstraße 1, 69117 Heidelberg, Germany
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Maximilian Beckers
1European Molecular Biology Laboratory (EMBL), Structural and Computational Biology Unit, Meyerhofstraße 1, 69117 Heidelberg, Germany
2Candidate for Joint PhD degree from EMBL and Heidelberg University, Faculty of Biosciences
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Iris von der Hocht
3Ernst-Ruska Centre for Microscopy and Spectroscopy with Electrons (ER-C-3/Structural Biology), Forschungszentrum Jülich, 52425 Jülich, Germany
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Carsten Sachse
1European Molecular Biology Laboratory (EMBL), Structural and Computational Biology Unit, Meyerhofstraße 1, 69117 Heidelberg, Germany
3Ernst-Ruska Centre for Microscopy and Spectroscopy with Electrons (ER-C-3/Structural Biology), Forschungszentrum Jülich, 52425 Jülich, Germany
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  • For correspondence: c.sachse@fz-juelich.de
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Abstract

Stable capsid structures of viruses protect viral RNA while they also require controlled disassembly for releasing the viral genome in the host cell. A detailed understanding of viral disassembly processes and the involved structural switches is still lacking. Biochemically, this process has been extensively studied using the tobacco mosaic virus model system and carboxylate interactions have been proposed to play a critical part in this process. Here, we present two cryo-EM structures of the helical TMV assembly at 2.1 and 2.0 Å resolution in conditions of high Ca2+ concentration at low pH and in water. Based on our atomic models, we identified the conformational details of the disassembly switch mechanism: in high Ca2+/acidic pH environment the virion is stabilized between neighboring subunits through carboxyl groups E95 and E97 in close proximity to a Ca2+ binding site. Upon increase in pH and lower Ca2+ levels, mutual repulsion of the E95/E97 pair and Ca2+ removal destabilize the network of interactions at lower radius and release the switch of virus disassembly. Our TMV structures revealed the conformational details for one of the reference systems of viral assembly/disassembly and provide the mechanistic explanation of a plethora of experimental results that were acquired over decades.

Significance Statement Tobacco mosaic virus presents the text-book example of virus structure and RNA release from a viral capsid through disassembly. Despite the wealth of structural and biochemical data on the assembly/disassembly properties generated from more than 80 years of research, the atomic-resolution structural details of the proposed conformational changes have not been resolved to date. The here determined high-resolution cryo-EM structures reveal the conformational details of the molecular disassembly switch. When the virus enters the cell, carboxylate repulsion and loss of calcium-ion coordination destabilize the switch region and can trigger RNA release through virus disassembly. The two determined structural states resolve a long-standing question on environment-driven virus disassembly switches.

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The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted March 06, 2019.
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Elucidation of the viral disassembly switch of tobacco mosaic virus
Felix Weis, Maximilian Beckers, Iris von der Hocht, Carsten Sachse
bioRxiv 569178; doi: https://doi.org/10.1101/569178
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Elucidation of the viral disassembly switch of tobacco mosaic virus
Felix Weis, Maximilian Beckers, Iris von der Hocht, Carsten Sachse
bioRxiv 569178; doi: https://doi.org/10.1101/569178

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