Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>

ABSTRACT Similar to many eukaryotic viruses (and unlike bacteriophages), viruses infecting archaea are often encased in lipid-containing envelopes. However, the mechanisms of their morphogenesis and egress remain unexplored. Here, we used dual-axis electron tomography (ET) to characterize the morpho...

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Autores principales:	Emmanuelle R. J. Quemin, Petr Chlanda, Martin Sachse, Patrick Forterre, David Prangishvili, Mart Krupovic
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/5b221680de4c410a91a27fe7e1dd820e
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spelling	oai:doaj.org-article:5b221680de4c410a91a27fe7e1dd820e2021-11-15T15:50:16ZEukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>10.1128/mBio.01439-162150-7511https://doaj.org/article/5b221680de4c410a91a27fe7e1dd820e2016-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01439-16https://doaj.org/toc/2150-7511ABSTRACT Similar to many eukaryotic viruses (and unlike bacteriophages), viruses infecting archaea are often encased in lipid-containing envelopes. However, the mechanisms of their morphogenesis and egress remain unexplored. Here, we used dual-axis electron tomography (ET) to characterize the morphogenesis of Sulfolobus spindle-shaped virus 1 (SSV1), the prototype of the family Fuselloviridae and representative of the most abundant archaea-specific group of viruses. Our results show that SSV1 assembly and egress are concomitant and occur at the cellular cytoplasmic membrane via a process highly reminiscent of the budding of enveloped viruses that infect eukaryotes. The viral nucleoprotein complexes are extruded in the form of previously unknown rod-shaped intermediate structures which have an envelope continuous with the host membrane. Further maturation into characteristic spindle-shaped virions takes place while virions remain attached to the cell surface. Our data also revealed the formation of constricted ring-like structures which resemble the budding necks observed prior to the ESCRT machinery-mediated membrane scission during egress of various enveloped viruses of eukaryotes. Collectively, we provide evidence that archaeal spindle-shaped viruses contain a lipid envelope acquired upon budding of the viral nucleoprotein complex through the host cytoplasmic membrane. The proposed model bears a clear resemblance to the egress strategy employed by enveloped eukaryotic viruses and raises important questions as to how the archaeal single-layered membrane composed of tetraether lipids can undergo scission. IMPORTANCE The replication of enveloped viruses has been extensively studied in eukaryotes but has remained unexplored for enveloped viruses infecting Archaea. Here, we provide a sequential view on the assembly and egress of SSV1, a prototypic archaeal virus. The observed process is highly similar to the budding of eukaryotic enveloped viruses, including human immunodeficiency virus, influenza virus, and Ebola virus. The present study is the first to characterize such a phenomenon in archeal cells, showing that membrane budding is not an exclusive feature of eukaryotic viruses. Our results provide significant insights into the biogenesis and architecture of unique, spindle-shaped virions that infect archaea. Furthermore, our findings open doors for future inquiries into (i) the evolution of the virus budding process, (ii) mechanistic details of virus-mediated membrane scission in Archaea, and (iii) elucidation of virus- and host-encoded molecular players responsible for archaeal membrane and surface remodeling.Emmanuelle R. J. QueminPetr ChlandaMartin SachsePatrick ForterreDavid PrangishviliMart KrupovicAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 5 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Emmanuelle R. J. Quemin Petr Chlanda Martin Sachse Patrick Forterre David Prangishvili Mart Krupovic Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>
description	ABSTRACT Similar to many eukaryotic viruses (and unlike bacteriophages), viruses infecting archaea are often encased in lipid-containing envelopes. However, the mechanisms of their morphogenesis and egress remain unexplored. Here, we used dual-axis electron tomography (ET) to characterize the morphogenesis of Sulfolobus spindle-shaped virus 1 (SSV1), the prototype of the family Fuselloviridae and representative of the most abundant archaea-specific group of viruses. Our results show that SSV1 assembly and egress are concomitant and occur at the cellular cytoplasmic membrane via a process highly reminiscent of the budding of enveloped viruses that infect eukaryotes. The viral nucleoprotein complexes are extruded in the form of previously unknown rod-shaped intermediate structures which have an envelope continuous with the host membrane. Further maturation into characteristic spindle-shaped virions takes place while virions remain attached to the cell surface. Our data also revealed the formation of constricted ring-like structures which resemble the budding necks observed prior to the ESCRT machinery-mediated membrane scission during egress of various enveloped viruses of eukaryotes. Collectively, we provide evidence that archaeal spindle-shaped viruses contain a lipid envelope acquired upon budding of the viral nucleoprotein complex through the host cytoplasmic membrane. The proposed model bears a clear resemblance to the egress strategy employed by enveloped eukaryotic viruses and raises important questions as to how the archaeal single-layered membrane composed of tetraether lipids can undergo scission. IMPORTANCE The replication of enveloped viruses has been extensively studied in eukaryotes but has remained unexplored for enveloped viruses infecting Archaea. Here, we provide a sequential view on the assembly and egress of SSV1, a prototypic archaeal virus. The observed process is highly similar to the budding of eukaryotic enveloped viruses, including human immunodeficiency virus, influenza virus, and Ebola virus. The present study is the first to characterize such a phenomenon in archeal cells, showing that membrane budding is not an exclusive feature of eukaryotic viruses. Our results provide significant insights into the biogenesis and architecture of unique, spindle-shaped virions that infect archaea. Furthermore, our findings open doors for future inquiries into (i) the evolution of the virus budding process, (ii) mechanistic details of virus-mediated membrane scission in Archaea, and (iii) elucidation of virus- and host-encoded molecular players responsible for archaeal membrane and surface remodeling.
format	article
author	Emmanuelle R. J. Quemin Petr Chlanda Martin Sachse Patrick Forterre David Prangishvili Mart Krupovic
author_facet	Emmanuelle R. J. Quemin Petr Chlanda Martin Sachse Patrick Forterre David Prangishvili Mart Krupovic
author_sort	Emmanuelle R. J. Quemin
title	Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>
title_short	Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>
title_full	Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>
title_fullStr	Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>
title_full_unstemmed	Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>
title_sort	eukaryotic-like virus budding in <italic toggle="yes">archaea</italic>
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/5b221680de4c410a91a27fe7e1dd820e
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Eukaryotic-Like Virus Budding in <italic toggle="yes">Archaea</italic>

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