Atomic structure of the 75 MDa extremophile
            <i>Sulfolobus</i>
            turreted icosahedral virus determined by CryoEM and X-ray crystallography

Veesler, David; Ng, Thiam-Seng; Sendamarai, Anoop K.; Eilers, Brian J.; Lawrence, C. Martin; Lok, Shee-Mei; Young, Mark; Johnson, John E.; Fu, Chiyu

doi:10.1073/pnas.1300601110

Cited by 78 publications

(101 citation statements)

References 45 publications

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“…Viruses of the Turriviridae family resemble sphaerolipoviruses in overall virion organization but instead of the two capsid proteins employ one MCP with a double-jelly-roll (DJR) fold and one minor capsid protein with a single-jelly-roll fold (18). Similarly to sphaerolipoviruses, turriviruses encode A32-like genome-packaging ATPases.…”

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confidence: 99%

Bipartite Network Analysis of the Archaeal Virosphere: Evolutionary Connections between Viruses and Capsidless Mobile Elements

Iranzo

Koonin

Prangishvili

et al. 2016

J Virol

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Archaea and particularly hyperthermophilic crenarchaea are hosts to many unusual viruses with diverse virion shapes and distinct gene compositions. As is typical of viruses in general, there are no universal genes in the archaeal virosphere. Therefore, to obtain a comprehensive picture of the evolutionary relationships between viruses, network analysis methods are more productive than traditional phylogenetic approaches. Here we present a comprehensive comparative analysis of genomes and proteomes from all currently known taxonomically classified and unclassified, cultivated and uncultivated archaeal viruses. We constructed a bipartite network of archaeal viruses that includes two classes of nodes, the genomes and gene families that connect them. Dissection of this network using formal community detection methods reveals strong modularity, with 10 distinct modules and 3 putative supermodules. However, compared to similar previously analyzed networks of eukaryotic and bacterial viruses, the archaeal virus network is sparsely connected. With the exception of the tailed viruses related to bacteriophages of the order Caudovirales and the families Turriviridae and Sphaerolipoviridae that are linked to a distinct supermodule of eukaryotic and bacterial viruses, there are few connector genes shared by different archaeal virus modules. In contrast, most of these modules include, in addition to viruses, capsidless mobile elements, emphasizing tight evolutionary connections between the two types of entities in archaea. The relative contributions of distinct evolutionary origins, in particular from nonviral elements, and insufficient sampling to the sparsity of the archaeal virus network remain to be determined by further exploration of the archaeal virosphere. V iruses infecting archaea are among the most mysterious denizens of the virosphere. Archaeal viruses display a rich diversity of virion morphotypes and can be broadly divided into two categories: those that are structurally and genetically related to bacterial or eukaryotic viruses and those that are archaeon specific (1-4). The cosmopolitan fraction of archaeal viruses includes (i) head-tailed viruses of the order Caudovirales, with the 3 included families, Siphoviridae, Myoviridae, and Podoviridae; (ii) tailless icosahedral viruses of the families Sphaerolipoviridae and Turriviridae; and (iii) enveloped pleomorphic viruses of the family Pleolipoviridae. All of these viruses, except for those of the family Turriviridae, propagate in members of the archaeal phylum Euryarchaeota, whereas most of the archaeon-specific virus groups infect hyperthermophilic organisms of the phylum Crenarchaeota.The order Caudovirales contains three families, the Siphoviridae, Myoviridae, and Podoviridae, and includes both bacterial and archaeal viruses. Members of the Caudovirales feature icosahedral capsids and helical tails attached to one of the vertices of the capsid. These viruses have been largely isolated from hyperhalophilic archaea (order Halobacteriales), although one...

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confidence: 99%

Bipartite Network Analysis of the Archaeal Virosphere: Evolutionary Connections between Viruses and Capsidless Mobile Elements

Iranzo

Koonin

Prangishvili

et al. 2016

J Virol

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“…Furthermore, knowledge of the proteins residing at the VP17-surrounded pentagonal vertices was elusive. The 5-fold axes of some icosahedral viruses are occupied by penton proteins that exhibit a highly conserved single beta-barrel core fold (7,18,25,26). Among the 10 structural proteins identified in P23-77 virus particles, only three have been found to be associated with the capsid (3): the two MCPs, VP16 and VP17, and the 22-kDa minor capsid protein VP11.…”

Section: Importancementioning

confidence: 99%

The Minor Capsid Protein VP11 of Thermophilic Bacteriophage P23-77 Facilitates Virus Assembly by Using Lipid-Protein Interactions

Pawlowski

Moilanen

Rissanen

et al. 2015

J Virol

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Thermus thermophilus bacteriophage P23-77 is the type member of a new virus family of icosahedral, tailless, inner-membranecontaining double-stranded DNA (dsDNA) viruses infecting thermophilic bacteria and halophilic archaea. The viruses have a unique capsid architecture consisting of two major capsid proteins assembled in various building blocks. We analyzed the function of the minor capsid protein VP11, which is the third known capsid component in bacteriophage P23-77. Our findings show that VP11 is a dynamically elongated dimer with a predominantly ␣-helical secondary structure and high thermal stability. The high proportion of basic amino acids in the protein enables electrostatic interaction with negatively charged molecules, including nucleic acid and large unilamellar lipid vesicles (LUVs). The plausible biological function of VP11 is elucidated by demonstrating the interactions of VP11 with Thermus-derived LUVs and with the major capsid proteins by means of the dynamic-lightscattering technique. In particular, the major capsid protein VP17 was able to link VP11-complexed LUVs into larger particles, whereas the other P23-77 major capsid protein, VP16, was unable to link VP11-comlexed LUVs. Our results rule out a previously suggested penton function for VP11. Instead, the electrostatic membrane association of VP11 triggers the binding of the major capsid protein VP17, thus facilitating a controlled incorporation of the two different major protein species into the assembling capsid. IMPORTANCEThe study of thermophilic viruses with inner membranes provides valuable insights into the mechanisms used for stabilization and assembly of protein-lipid systems at high temperatures. Our results reveal a novel way by which an internal membrane and outer capsid shell are linked in a virus that uses two different major protein species for capsid assembly. We show that a positive protein charge is important in order to form electrostatic interactions with the lipid surface, thereby facilitating the incorporation of other capsid proteins on the membrane surface. This implies an alternative function for basic proteins present in the virions of other lipid-containing thermophilic viruses, whose proposed role in genome packaging is based on their capability to bind DNA. The unique minor capsid protein of bacteriophage P23-77 resembles in its characteristics the scaffolding proteins of tailed phages, though it constitutes a substantial part of the mature virion. V iruses from extremely hot environments need to develop special strategies to cope with high temperature. Hence, they provide a valuable source for the detection of novel enzymes for biotechnology and industrial processes. Their relative simple structure makes them an ideal model system for studying life at high temperatures. With respect to extreme thermophilic bacteria, the virus studied best on the structural level is P23-77, a strictly lytic phage infecting Thermus thermophilus ATCC 33923 (1, 2, 3). P23-77 is a representative of the novel Sphaerolipoviri...

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“…The exact evolutionary relationship between viruses infecting hosts from different domains of life is often enigmatic. In icosahedral archaeal viruses the major capsid protein has the double β-barrel fold (4,5), which also is found in the capsid proteins of many bacterial and eukaryotic viruses, pointing toward an evolutionary relationship among these viruses (6)(7)(8). In contrast, filamentous viruses infecting hosts from different cellular domains appear to be evolutionarily unrelated.…”

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confidence: 99%

A virus of hyperthermophilic archaea with a unique architecture among DNA viruses

Rensen

Mochizuki

Quemin

et al. 2016

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

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Viruses package their genetic material in diverse ways. Most known strategies include encapsulation of nucleic acids into spherical or filamentous virions with icosahedral or helical symmetry, respectively. Filamentous viruses with dsDNA genomes are currently associated exclusively with Archaea. Here, we describe a filamentous hyperthermophilic archaeal virus, Pyrobaculum filamentous virus 1 (PFV1), with a type of virion organization not previously observed in DNA viruses. The PFV1 virion, 400 ± 20 × 32 ± 3 nm, contains an envelope and an inner core consisting of two structural units: a rod-shaped helical nucleocapsid formed of two 14-kDa major virion proteins and a nucleocapsid-encompassing protein sheath composed of a single major virion protein of 18 kDa. The virion organization of PFV1 is superficially similar to that of negative-sense RNA viruses of the family Filoviridae, including Ebola virus and Marburg virus. The linear dsDNA of PFV1 carries 17,714 bp, including 60-bp-long terminal inverted repeats, and contains 39 predicted ORFs, most of which do not show similarities to sequences in public databases. PFV1 is a lytic virus that completely disrupts the host cell membrane at the end of the infection cycle.

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Atomic structure of the 75 MDa extremophile Sulfolobus turreted icosahedral virus determined by CryoEM and X-ray crystallography

Cited by 78 publications

References 45 publications

Bipartite Network Analysis of the Archaeal Virosphere: Evolutionary Connections between Viruses and Capsidless Mobile Elements

Bipartite Network Analysis of the Archaeal Virosphere: Evolutionary Connections between Viruses and Capsidless Mobile Elements

The Minor Capsid Protein VP11 of Thermophilic Bacteriophage P23-77 Facilitates Virus Assembly by Using Lipid-Protein Interactions

A virus of hyperthermophilic archaea with a unique architecture among DNA viruses

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