Virion Architecture Unifies Globally Distributed Pleolipoviruses Infecting Halophilic Archaea

Pietilä, Maija K.; Atanasova, Nina S.; Manole, Violeta; Liljeroos, Lassi; Butcher, Sarah J.; Oksanen, Hanna M.; Bamford, Dennis H.

doi:10.1128/jvi.06915-11

Cited by 79 publications

(188 citation statements)

References 66 publications

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“…1C). The buoyant density of the purified SSV1 virions in CsCl was estimated to be 1.29 g/ml, which is somewhat higher than that previ-ously reported for SSV1 (1.24 g/ml [32]) but similar to the buoyant density of membrane-containing pleolipoviruses (1.3 g/ml [62]). …”

Section: Aggregation Of Ssv1 Particles Is Modulated By Ionic and Hydrmentioning

confidence: 63%

Sulfolobus Spindle-Shaped Virus 1 Contains Glycosylated Capsid Proteins, a Cellular Chromatin Protein, and Host-Derived Lipids

Quemin

Pietilä

Oksanen

et al. 2015

J Virol

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Geothermal and hypersaline environments are rich in virus-like particles, among which spindle-shaped morphotypes dominate. Currently, viruses with spindle-or lemon-shaped virions are exclusive to Archaea and belong to two distinct viral families. The larger of the two families, the Fuselloviridae, comprises tail-less, spindle-shaped viruses, which infect hosts from phylogenetically distant archaeal lineages. Sulfolobus spindle-shaped virus 1 (SSV1) is the best known member of the family and was one of the first hyperthermophilic archaeal viruses to be isolated. SSV1 is an attractive model for understanding virus-host interactions in Archaea; however, the constituents and architecture of SSV1 particles remain only partially characterized. Here, we have conducted an extensive biochemical characterization of highly purified SSV1 virions and identified four virus-encoded structural proteins, VP1 to VP4, as well as one DNA-binding protein of cellular origin. The virion proteins VP1, VP3, and VP4 undergo posttranslational modification by glycosylation, seemingly at multiple sites. VP1 is also proteolytically processed. In addition to the viral DNA-binding protein VP2, we show that viral particles contain the Sulfolobus solfataricus chromatin protein Sso7d. Finally, we provide evidence indicating that SSV1 virions contain glycerol dibiphytanyl glycerol tetraether (GDGT) lipids, resolving a long-standing debate on the presence of lipids within SSV1 virions. A comparison of the contents of lipids isolated from the virus and its host cell suggests that GDGTs are acquired by the virus in a selective manner from the host cytoplasmic membrane, likely during progeny egress. Viruses infecting extremophilic archaea have evolved to withstand very high temperatures, low or high pH, or near-saturating salt concentrations (1-5). Remarkably, most of these viruses do not seem to be evolutionarily related to viruses of bacteria or eukaryotes and display a considerable diversity of unique virion morphotypes (3, 4). Indeed, 11 novel viral families have been established by the International Committee for the Taxonomy of Viruses (ICTV) for the classification of archaeal viruses, emphasizing the uniqueness of rod-shaped, spindle-shaped, dropletshaped, or even bottle-shaped particles that have never been observed among viruses infecting bacteria or eukaryotes (3). Functional studies proved to be highly challenging due to the lack of similarity between the protein sequences and structures of archaeal viruses and those from other viruses and cellular organisms (6-10). Among the morphotypes that are exclusively associated with archaea, spindle-shaped viruses are particularly widespread (11) and have been isolated from highly different environments, including deep-sea hydrothermal vents (12-14), hypersaline environments (15-18), anoxic freshwaters (19), cold Antarctic lakes (20), terrestrial hot springs (21-23), and acidic mines (24).Recently, we refined the evolutionary relationships among spindle-shaped viruses by assessing the morph...

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Section: Aggregation Of Ssv1 Particles Is Modulated By Ionic and Hydrmentioning

confidence: 63%

Sulfolobus Spindle-Shaped Virus 1 Contains Glycosylated Capsid Proteins, a Cellular Chromatin Protein, and Host-Derived Lipids

Quemin

Pietilä

Oksanen

et al. 2015

J Virol

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“…For a more detailed structural analysis, we used cryo-ET, a method of choice for 3D reconstruction of pleomorphic, membrane-containing particles (5,(18)(19)(20). In a total of 41 tomograms from three separate preparations of A2 virus collected from the cell culture supernatant, we analyzed 103 virions.…”

Section: Resultsmentioning

confidence: 99%

Architecture of respiratory syncytial virus revealed by electron cryotomography

Liljeroos

Krzyzaniak²,

Helenius³

et al. 2013

Proc. Natl. Acad. Sci. U.S.A.

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Human respiratory syncytial virus is a human pathogen that causes severe infection of the respiratory tract. Current information about the structure of the virus and its interaction with host cells is limited. We carried out an electron cryotomographic characterization of cell culture-grown human respiratory syncytial virus to determine the architecture of the virion. The particles ranged from 100 nm to 1,000 nm in diameter and were spherical, filamentous, or a combination of the two. The filamentous morphology correlated with the presence of a cylindrical matrix protein layer linked to the inner leaflet of the viral envelope and with local ordering of the glycoprotein spikes. Recombinant viruses with only the fusion protein in their envelope showed that these glycoproteins were predominantly in the postfusion conformation, but some were also in the prefusion form. The ribonucleocapsids were left-handed, randomly oriented, and curved inside the virions. In filamentous particles, they were often adjacent to an intermediate layer of protein assigned to M2-1 (an envelopeassociated protein known to mediate association of ribonucleocapsids with the matrix protein). Our results indicate important differences in structure between the Paramyxovirinae and Pneumovirinae subfamilies within the Paramyxoviridae, and provide fresh insights into host cell exit of a serious pathogen.cryo-ET | paramyxovirus | virus structure H uman respiratory syncytial virus (HRSV) causes severe disease, especially in children and the elderly (1, 2). In a study covering data from 2005, it was found that HRSV was responsible for 22% of acute lower respiratory infections worldwide and 66,000-199,000 deaths in children under the age of 5 y (2). Treatment is currently limited to purine analogs (Ribavirin) and passive immune-prophylaxis with humanized monoclonal antibodies (Palivizumab) (3).RSV belongs to the Paramyxoviridae, a large family of enveloped, negative-sense RNA viruses with many members from humans and animals. Together with human metapneumovirus, it constitutes the Pneumovirinae subfamily. Like other paramyxoviruses, it has a plasma-membrane-derived lipid envelope and a helical ribonucleocapsid (RNP) that contains a single viral RNA molecule associated with nucleoproteins (N), and an RNA-dependent RNA polymerase. The virion contains, in addition, a matrix protein (M) (4-7) and a transcription antiterminator, M2-1 (an envelopeassociated protein known to mediate association of RNPs with the M protein) (8-11). The lipid envelope contains two transmembrane glycoproteins: the fusion protein, F, and a glycoprotein, G, used for attachment to host cells. In addition, HRSV contains a small hydrophobic protein, SH, of unclear function and proteins of cellular origin, such as actin and chaperones (12). The RNP and F have been analyzed using 3D-EM and X-ray crystallography (13,14).HRSV particles are pleomorphic with both spherical and filamentous particles of different sizes (15). Early electron microscopy studies showed the presence of a helical p...

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“…[8][9][10][11][12][13][14][15][16][17][18] Seven of them form a recently described group of haloarchaeal pleomorphic viruses, HRPV-1, HRPV-2, HRPV-3, HRPV-6, HHPV-1, HGPV-1 and His2. 6,13,15,16,18,19 These viruses are distinctive due to their unusual morphotypes and diverse genomes despite their general relatedness. 6,15,16,18,19 Other sequenced haloarchaeal viruses are the spindle-shaped virus His1 and two icosahedral viruses SH1 and HHIV-2.…”

Section: Introductionmentioning

confidence: 99%