Complex membrane remodeling during virion assembly of the 30,000 years-old Mollivirus sibericum
| العنوان: | Complex membrane remodeling during virion assembly of the 30,000 years-old Mollivirus sibericum |
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| المؤلفون: | A. Baskaran, Eugene Christo-Foroux, Chantal Abergel, Anastasia D. Gazi, Paul Walther, Esthel Pénard, Jacomine Krijnse-Locker, Emmanuelle R. J. Quemin, Simon Corroyer-Dulmont |
| المساهمون: | Institut Pasteur [Paris] (IP), Plateforme BioImagerie Ultrastructurale – Ultrastructural BioImaging Platform (UTechS UBI), Institut de Microbiologie de la Méditerranée (IMM), Aix Marseille Université (AMU)-Centre National de la Recherche Scientifique (CNRS), Universität Ulm - Ulm University [Ulm, Allemagne], Information génomique et structurale (IGS), The Ultrastructural Bio-Imaging Facility of the Institut Pasteur, Paris, France, directed by J. Krijnse-Locker, is a member of the national infrastructure France-BioImaging and supported by the French National Research Agency (ANR-10-INBS-04). The laboratory of C. Abergel is supported by the Fondation Bettencourt-Schueller (OTP51251) and by a DGA-MRIS scholarship (201760003). E. R. Quemin is currently funded by the Alexander von Humboldt Foundation (FRA 1200789 HFST-P)., We thank all the members of UBI, in particular, Martin Sachse for useful discussions, technical assistance, and critical readings of the manuscript. We also thank Elsa Garcin for useful discussions and critical editing of the manuscript., ANR-10-INBS-0004,France-BioImaging,Développment d'une infrastructure française distribuée coordonnée(2010), Institut Pasteur [Paris], Electron Microscopy (EM) Core Facility [Ulm], Universitätsklinikum Ulm - University Hospital of Ulm |
| المصدر: | Journal of Virology Journal of Virology, 2019, 93 (13), pp.e00388-19. ⟨10.1128/JVI.00388-19⟩ Journal of Virology, American Society for Microbiology, 2019, 93 (13), pp.e00388-19. ⟨10.1128/JVI.00388-19⟩ |
| بيانات النشر: | HAL CCSD, 2019. |
| سنة النشر: | 2019 |
| مصطلحات موضوعية: | Electron Microscope Tomography, viruses, Immunology, Mollivirus sibericum, Genome, Viral, Biology, Nucleocytoplasmic large DNA viruses, Virus Replication, Microbiology, 03 medical and health sciences, Capsid, Imaging, Three-Dimensional, Microscopy, Electron, Transmission, Virology, Viral factory, Giant Virus, 030304 developmental biology, 0303 health sciences, Mimivirus, Acanthamoeba castellanii, 030306 microbiology, Vesicle, Virus Assembly, DNA Viruses, Virion, Viral membrane, biology.organism_classification, Cell biology, Virus-Cell Interactions, Microscopy, Electron, Virion assembly, Insect Science, Giant Viruses, Host-Pathogen Interactions, [SDV.MP.VIR]Life Sciences [q-bio]/Microbiology and Parasitology/Virology, Viruses, Unclassified, Mimiviridae |
| الوصف: | Cellular membranes ensure functional compartmentalization by dynamic fusion-fission remodeling and are often targeted by viruses during entry, replication, assembly, and egress. Nucleocytoplasmic large DNA viruses (NCLDVs) can recruit host-derived open membrane precursors to form their inner viral membrane. Using complementary three-dimensional (3D)-electron microscopy techniques, including focused-ion beam scanning electron microscopy and electron tomography, we show that the giant Mollivirus sibericum utilizes the same strategy but also displays unique features. Indeed, assembly is specifically triggered by an open cisterna with a flat pole in its center and open curling ends that grow by recruitment of vesicles never reported for NCLDVs. These vesicles, abundant in the viral factory (VF), are initially closed but open once in close proximity to the open curling ends of the growing viral membrane. The flat pole appears to play a central role during the entire virus assembly process. While additional capsid layers are assembled from it, it also shapes the growing cisterna into immature crescent-like virions and is located opposite to the membrane elongation and closure sites, thereby providing virions with a polarity. In the VF, DNA-associated filaments are abundant, and DNA is packed within virions prior to particle closure. Altogether, our results highlight the complexity of the interaction between giant viruses and their host. Mollivirus assembly relies on the general strategy of vesicle recruitment, opening, and shaping by capsid layers similar to all NCLDVs studied until now. However, the specific features of its assembly suggest that the molecular mechanisms for cellular membrane remodeling and persistence are unique. IMPORTANCE Since the first giant virus Mimivirus was identified, other giant representatives are isolated regularly around the world and appear to be unique in several aspects. They belong to at least four viral families, and the ways they interact with their hosts remain poorly understood. We focused on Mollivirus sibericum, the sole representative of “Molliviridae,” which was isolated from a 30,000-year-old permafrost sample and exhibits spherical virions of complex composition. In particular, we show that (i) assembly is initiated by a unique structure containing a flat pole positioned at the center of an open cisterna, (ii) core packing involves another cisterna-like element seemingly pushing core proteins into particles being assembled, and (iii) specific filamentous structures contain the viral genome before packaging. Altogether, our findings increase our understanding of how complex giant viruses interact with their host and provide the foundation for future studies to elucidate the molecular mechanisms of Mollivirus assembly. |
| اللغة: | English |
| تدمد: | 0022-538X 1098-5514 |
| URL الوصول: | https://explore.openaire.eu/search/publication?articleId=doi_dedup___::a97af9fdbefd6f72135feae7c02b1d14 https://hal-amu.archives-ouvertes.fr/hal-02109276 |
| حقوق: | OPEN |
| رقم الأكسشن: | edsair.doi.dedup.....a97af9fdbefd6f72135feae7c02b1d14 |
| قاعدة البيانات: | OpenAIRE |
| تدمد: | 0022538X 10985514 |
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