First Insights into the Entry Process of Hyperthermophilic Archaeal Viruses

Quemin, Emmanuelle R. J.; Lucas, Soizick; Daum, Bertram; Quax, Tessa E. F.; Kühlbrandt, Werner; Forterre, Patrick; Albers, Sonja‐Verena; Prangishvili, David; Krupovìč, Mart

doi:10.1128/jvi.02742-13

Cited by 68 publications

(85 citation statements)

References 53 publications

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“…A high-resolution cryoEM study of the SIRV2 virion showed that the genomic DNA is uniquely packaged in A-form (DiMaio et al 2015). The virions are not enveloped in a lipid membrane and possesses three tail fibres on each end of the capsid, which bind filamentous appendages on the cell surface of its host S. islandicus to aid the viral entry process (Quemin et al 2013;Quemin and Quax 2015). The turreted icosahedral particles of STIV1 enwrap a circular dsDNA genome (Rice et al 2004;Maaty et al 2006).…”

Section: Biological Function Of Vapsmentioning

confidence: 99%

Structure and assembly mechanism of virus-associated pyramids

Quax

Daum

2017

Biophys Rev

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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.

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Section: Biological Function Of Vapsmentioning

confidence: 99%

Structure and assembly mechanism of virus-associated pyramids

Quax

Daum

2017

Biophys Rev

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“…For conventional negative-stain TEM, samples were prepared as described previously (60). Briefly, 10 l of sample was adsorbed on grids for 1 min, air dried, and stained with 3% uranyl acetate, pH 4.5 (EuroMedex), for 1 min.…”

Section: Methodsmentioning

confidence: 99%

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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“…This morphological diversity suggests that the archaeal viruses may employ a variety of mechanisms to enter their hosts, but current insights into entry mechanisms are limited to an OppA transporter protein, Sso1273, possibly providing a receptor site for the Acidianus two-tailed virus (ATV) in Sulfolobus solfataricus P2 (4). And very recently, microscopic studies suggested that Sulfolobus islandicus rod-shaped virus 2 (SIRV2) enters the host cell by attaching and moving through a pilus-like filament; however, the nature of the structure and the identity of the involved proteins remain elusive (5).…”

mentioning

confidence: 99%

Unveiling Cell Surface and Type IV Secretion Proteins Responsible for Archaeal Rudivirus Entry

Deng

Bhoobalan-Chitty

et al. 2014

J Virol

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Sulfolobus mutants resistant to archaeal lytic virus Sulfolobus islandicus rod-shaped virus 2 (SIRV2) were isolated, and mutations were identified in two gene clusters, cluster sso3138 to sso3141 and cluster sso2386 and sso2387, encoding cell surface and type IV secretion proteins, respectively. The involvement of the mutations in the resistance was confirmed by genetic complementation. Blocking of virus entry into the mutants was demonstrated by the lack of early gene transcription, strongly supporting the idea of a role of the proteins in SIRV2 entry.T o date, relatively few archaeal viruses have been characterized, and most of those that have been characterized infect acidothermophilic members of the order Sulfolobales. Despite their limited number of around 50 species, they exhibit considerably greater morphological diversity than the more extensively characterized bacteriophages, about 95% of which show head-tail morphologies. Archaeal viruses, in contrast, exhibit fusiform shapes, often with one or two tails, bottle shapes, bearded-globular forms, and a wide variety of rod-like and filamentous morphotypes which often carry small terminal appendages (1-3). This morphological diversity suggests that the archaeal viruses may employ a variety of mechanisms to enter their hosts, but current insights into entry mechanisms are limited to an OppA transporter protein, Sso1273, possibly providing a receptor site for the Acidianus two-tailed virus (ATV) in Sulfolobus solfataricus P2 (4). And very recently, microscopic studies suggested that Sulfolobus islandicus rod-shaped virus 2 (SIRV2) enters the host cell by attaching and moving through a pilus-like filament; however, the nature of the structure and the identity of the involved proteins remain elusive (5).Sulfolobus solfataricus P2 is an acidothermophilic crenarchaeon that can host a wide range of archaeal viruses, many of which are propagated stably (1, 3, 6). Moreover, few of the viruses appear to induce cell lysis, possibly reflecting a need to minimize contact with the harsh hot acidic environment. However, recent studies have identified a few viruses that can enter a lytic phase, including the Sulfolobus turreted icosahedral virus (STIV), the two-tailed fusiform (ATV), and, more recently, the rudivirus SIRV2 (7-9).SIRV2 is classified in the family Rudiviridae together with other well-characterized viruses, including SIRV1 (10, 11), ARV1 (12) and SRV1, (13), all of which are rod shaped and lack an envelope, and their genomes consist of linear double-stranded DNA with covalently closed ends (10,14,15). In a recent microarray analysis of S. solfataricus infected with SIRV2, we demonstrated that the viral genes were activated at different times and that mainly stressresponse host genes and those implicated in vesicle formation were downregulated (16). The results also illustrated that SIRV2 infection at a multiplicity of infection (MOI) of 30 resulted in growth inhibition of S. solfataricus 5E6 (16). In the present experiment, the culture was infected at a lower...

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First Insights into the Entry Process of Hyperthermophilic Archaeal Viruses

Cited by 68 publications

References 53 publications

Structure and assembly mechanism of virus-associated pyramids

Structure and assembly mechanism of virus-associated pyramids

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

Unveiling Cell Surface and Type IV Secretion Proteins Responsible for Archaeal Rudivirus Entry

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