Model for a novel membrane envelope in a filamentous hyperthermophilic virus

Kasson, Peter M.; DiMaio, Frank; Xiong, Yong; Lucas-Staat, Soizick; Krupovìč, Mart; Schouten, Stefan; Prangishvili, David

doi:10.7554/elife.26268

Cited by 40 publications

(55 citation statements)

References 50 publications

Supporting

Mentioning

Contrasting

Order By: Relevance

“…Lipid analysis shows that the SEV1 envelope contains a similar but nonidentical set of the host membrane lipids. Differences in lipid distribution between virions and host cells are found in other archaeal viruses, i.e., STIV (47), SSV1 (36), and AFV1 (11). The lipid asymmetry probably results from a selective incorporation of lipids into the virion.…”

Section: Discussionmentioning

confidence: 96%

“…These include tailless icosahedral viruses of the families Turriviridae and Sphaerolipoviridae (6,7), filamentous viruses of the Tristromaviridae (8), and spindle-shaped viruses of the Fuselloviridae (9). Other archaeal viral genomes are not encased in a protein shell but instead are condensed by capsid proteins into various architectural forms, such as a cylinder (e.g., filamentous viruses of the order Ligamenvirales) (10,11), a sphere (e.g., spherical viruses of the Globuloviridae and Portogloboviridae) (12,13), a cone (e.g., bottle-shaped viruses of the Ampullaviridae) (14), and a coil (e.g., spiral coil-like viruses of the Spiraviridae) (15). Moreover, archaeal viruses are either enveloped or naked.…”

mentioning

confidence: 99%

See 1 more Smart Citation

Novel Sulfolobus Virus with an Exceptional Capsid Architecture

Wang

Guo

Feng

et al. 2018

J Virol

View full text Add to dashboard Cite

A novel archaeal virus, denoted ellipsoid virus 1 (SEV1), was isolated from an acidic hot spring in Costa Rica. The morphologically unique virion of SEV1 contains a protein capsid with 16 regularly spaced striations and an 11-nm-thick envelope. The capsid exhibits an unusual architecture in which the viral DNA, probably in the form of a nucleoprotein filament, wraps around the longitudinal axis of the virion in a plane to form a multilayered disk-like structure with a central hole, and 16 of these structures are stacked to generate a spool-like capsid. SEV1 harbors a linear double-stranded DNA genome of ∼23 kb, which encodes 38 predicted open reading frames (ORFs). Among the few ORFs with a putative function is a gene encoding a protein-primed DNA polymerase. Six-fold symmetrical virus-associated pyramids (VAPs) appear on the surface of the SEV1-infected cells, which are ruptured to allow the formation of a hexagonal opening and subsequent release of the progeny virus particles. Notably, the SEV1 virions acquire the lipid membrane in the cytoplasm of the host cell. The lipid composition of the viral envelope correlates with that of the cell membrane. These results suggest the use of a unique mechanism by SEV1 in membrane biogenesis. Investigation of archaeal viruses has greatly expanded our knowledge of the virosphere and its role in the evolution of life. Here we show that ellipsoid virus 1 (SEV1), an archaeal virus isolated from a hot spring in Costa Rica, exhibits a novel viral shape and an unusual capsid architecture. The SEV1 DNA wraps multiple times in a plane around the longitudinal axis of the virion to form a disk-like structure, and 16 of these structures are stacked to generate a spool-like capsid. The virus acquires its envelope intracellularly and exits the host cell by creating a hexagonal hole on the host cell surface. These results shed significant light on the diversity of viral morphogenesis.

show abstract

Section: Discussionmentioning

confidence: 96%

mentioning

confidence: 99%

Novel Sulfolobus Virus with an Exceptional Capsid Architecture

Wang

Guo

Feng

et al. 2018

J Virol

View full text Add to dashboard Cite

show abstract

“…Archaeal viruses display unique structures that are not encountered among bacterial or eukaryotic viruses, including spindle, two tailed, egg, bacilliform, spiral or even bottle-like shapes (Schleper et al 1992;Haring et al 2005;Häring et al 2005;Mochizuki et al 2010Mochizuki et al , 2011Mochizuki et al , 2012. In recent years, cryo-electron microscopy (cryoEM) has been employed to study the detailed threedimensional (3D) structure of a range of archaeal virions (Hong et al 2015;DiMaio et al 2015;Kasson et al 2017). The many unusual virion structures of archaeal viruses are a rich illustration of the diversity of solutions for the same purpose that can evolve in nature.…”

Section: Introductionmentioning

confidence: 99%

Structure and assembly mechanism of virus-associated pyramids

Quax

Daum

2017

Biophys Rev

View full text Add to dashboard Cite

Viruses have developed intricate molecular machines to infect, replicate within and escape from their host cells. Perhaps one of the most intriguing of these mechanisms is the pyramidal egress structure that has evolved in archaeal viruses, such as SIRV2 or STIV1. The structure and mechanism of these virus-associated pyramids (VAPs) has been studied by cryo-electron tomography and complementary biochemical techniques, revealing that VAPs are formed by multiple copies of a virus-encoded 10-kDa protein (PVAP) that integrate into the cell membrane and assemble into hollow, sevenfold symmetric pyramids. In this process, growing VAPs puncture the protective surface layer and ultimately open to release newly replicated viral particles into the surrounding medium. PVAP has the striking capability to spontaneously integrate and self-assemble into VAPs in biological membranes of the archaea, bacteria and eukaryotes. This renders the VAP a universal membrane remodelling system. In this review, we provide an overview of the VAP structure and assembly mechanism and discuss the possible use of VAPs in nanobiotechnology.

show abstract

“…Thermophilic virus capsids are amongst the strongest because they survive in an especially harsh environment. Previous studies of thermophilic viruses have focused on capsids of various shapes including icosahedral (Veesler et al, 2013), filamentous (Dimaio et al, 2015;Kasson et al, 2017;Liu et al, 2018), and lemon-shaped (Hochstein et al, 2018;Hong et al, 2015). However, for most of these viruses, close mesophilic homologs are not available, which makes it challenging to identify the structural mechanisms that underlie thermostability.…”

Section: Introductionmentioning

confidence: 99%

Principles for enhancing virus capsid capacity and stability from a thermophilic virus capsid structure

Stone¹,

Demo²,

Agnello³

et al. 2018

Preprint

View full text Add to dashboard Cite

The capsids of double-stranded DNA viruses protect the viral genome from the harsh extracellular environment, while maintaining stability against the high internal pressure of packaged DNA. To elucidate how capsids maintain stability in an extreme environment, we used cryoelectron microscopy to determine the capsid structure of the thermostable phage P74-26 to 2.8-Å resolution. We find the P74-26 capsid exhibits an overall architecture that is very similar to those of other tailed bacteriophages, allowing us to directly compare structures to derive the structural basis for enhanced stability. Our structure reveals 'lasso'-like interactions that appear to function like catch bonds. This architecture allows the capsid to expand during genome packaging, yet maintain structural stability. The P74-26 capsid has T=7 geometry despite being twice as large as mesophilic homologs. Capsid capacity is increased through a novel mechanism with a larger, flatter major capsid protein. Our results suggest that decreased icosahedral complexity (i.e. lower T number) leads to a more stable capsid assembly.

show abstract

Model for a novel membrane envelope in a filamentous hyperthermophilic virus

Cited by 40 publications

References 50 publications

Novel Sulfolobus Virus with an Exceptional Capsid Architecture

Novel Sulfolobus Virus with an Exceptional Capsid Architecture

Structure and assembly mechanism of virus-associated pyramids

Principles for enhancing virus capsid capacity and stability from a thermophilic virus capsid structure

Contact Info

Product

Resources

About