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

Rensen, Elena; Mochizuki, Tomohiro; Quemin, Emmanuelle R. J.; Schouten, Stefan; Krupovìč, Mart; Prangishvili, David

doi:10.1073/pnas.1518929113

Cited by 33 publications

(24 citation statements)

References 61 publications

(58 reference statements)

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“…Stained protein bands were excised, and digested "in gel" with trypsin. The digested peptides were analyzed at the Proteomics Platform of the Institut Pasteur by nano-LC-MS/MS using an Ultimate 3000 system (Dionex) as described previously (11). The peptide masses were searched against annotated SPV1 proteins using Andromeda (66) with MaxQuant software, version 1.3.0.5 (67).…”

Section: Discussionmentioning

confidence: 99%

“…has been identified for half a century, despite the isolation of thousands of new species (5), the variety of archaeal viral morphotypes continues to expand with the description of viruses from new environments and hosts (6)(7)(8)(9)(10)(11)(12)(13)(14)(15). There are reasons to believe that the known variety of archaeal viruses represents no more than the tip of an iceberg and that comprehensive information on them may shed light on the problems of origin and evolution of viruses and virus-host interactions (16)(17)(18)(19)(20)(21)(22)(23)(24)(25)(26)(27)(28).…”

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A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

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Encapsidation of genetic material into polyhedral particles is one of the most common structural solutions employed by viruses infecting hosts in all three domains of life. Here, we describe a new virus of hyperthermophilic archaea, Sulfolobus polyhedral virus 1 (SPV1), which condenses its circular double-stranded DNA genome in a manner not previously observed for other known viruses. The genome complexed with virion proteins is wound up sinusoidally into a spherical coil which is surrounded by an envelope and further encased by an outer polyhedral capsid apparently composed of the 20-kDa virion protein. Lipids selectively acquired from the pool of host lipids are integral constituents of the virion. None of the major virion proteins of SPV1 show similarity to structural proteins of known viruses. However, minor structural proteins, which are predicted to mediate host recognition, are shared with other hyperthermophilic archaeal viruses infecting members of the order Sulfolobales. The SPV1 genome consists of 20,222 bp and contains 45 open reading frames, only one-fifth of which could be functionally annotated.IMPORTANCE Viruses infecting hyperthermophilic archaea display a remarkable morphological diversity, often presenting architectural solutions not employed by known viruses of bacteria and eukaryotes. Here we present the isolation and characterization of Sulfolobus polyhedral virus 1, which condenses its genome into a unique spherical coil. Due to the original genomic and architectural features of SPV1, the virus should be considered a representative of a new viral family, "Portogloboviridae."KEYWORDS archaea, hyperthermophile, viral genome, virion structure O ne of the most unexpected results of recent studies on viral diversity is the unveiling of astounding morphological variety of DNA viruses in geothermal environments with temperatures exceeding 80°C (1). Hardly over two dozen viruses isolated from such environments, all parasitizing hyperthermophilic members of the domain Archaea, display diverse virion shapes, many of which have not been observed among viruses from the two other domains of life, Bacteria and Eukarya. Due to distinct genome compositions and peculiar morphological properties of these viruses, 11 new virus families were established by the International Committee on Taxonomy of Viruses (ICTV) for the classification of these viruses (1-4).The remarkable morphological diversity of hyperthermophilic archaeal viruses radically contrasts the limited structural diversity of double-stranded DNA (dsDNA) viruses of Bacteria, nearly all of which, with the exception of several pleomorphic species, have icosahedral particles, with or without helical tails (5). The existing picture seems to accurately reflect the actual differences between bacterial and archaeal viruses. The morphological landscape of bacterial viruses is formed by more than six thousand species, whereas that of hyperthermophilic archaeal viruses is formed by only a couple of dozen known species. Moreover, while no new morpho...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Liu

Ishino

et al. 2017

J Virol

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“…In recognition of this evolutionary relationship, the two families are unified within the order Ligamenvirales (28). Another family of enveloped filamentous viruses is the Tristromaviridae; these viruses do not share genes with other archaeal viruses and have a virion organization that is more complex than that of lipothrixviruses (29). The family Clavaviridae includes a single virus isolate with bacilliform virions.…”

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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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“…Cell pellets were collected from 2 ml enrichment cultures of sample J14 and J15 by centrifugation (12 000 r.p.m., 2 min, Eppendorf desktop centrifuge). DNA from cell fractions was isolated as described previously (Rensen et al ., ). The 16S rRNA gene libraries were prepared according to the 16S Metagenomic Sequencing Library Preparation protocol for the Illumina Miseq system (15044223 B).…”

Section: Methodsmentioning

confidence: 97%

“…S1). Nucleic acids were extracted from each CsCl fraction as described previously (Rensen et al ., ). Sequencing libraries were prepared from 50 ng input DNA of each fraction using the Illumina Nextera library preparation kit and sequenced on Illumina HiSeq 1500 (Illumina, San Diego, CA).…”

Section: Methodsmentioning

confidence: 97%

New archaeal viruses discovered by metagenomic analysis of viral communities in enrichment cultures

Liu

Brandt

Ishino

et al. 2019

Environmental Microbiology

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Summary Viruses infecting hyperthermophilic archaea of the phylum Crenarchaeota display enormous morphological and genetic diversity, and are classified into 12 families. Eight of these families include only one or two species, indicating sparse sampling of the crenarchaeal virus diversity. In an attempt to expand the crenarchaeal virome, we explored virus diversity in the acidic, hot spring Umi Jigoku in Beppu, Japan. Environmental samples were used to establish enrichment cultures under conditions favouring virus replication. The host diversity in the enrichment cultures was restricted to members of the order Sulfolobales. Metagenomic sequencing of the viral communities yielded seven complete or near‐complete double‐stranded DNA virus genomes. Six of these genomes could be attributed to polyhedral and filamentous viruses that were observed by electron microscopy in the enrichment cultures. Two icosahedral viruses represented species in the family Portogloboviridae. Among the filamentous viruses, two were identified as new species in the families Rudiviridae and Lipothrixviridae, whereas two other formed a group seemingly distinct from the known virus genera. No particle morphotype could be unequivocally assigned to the seventh viral genome, which apparently represents a new virus type. Our results suggest that filamentous viruses are globally distributed and are prevalent virus types in extreme geothermal environments.

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

Cited by 33 publications

References 61 publications

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

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

New archaeal viruses discovered by metagenomic analysis of viral communities in enrichment cultures

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