A Novel Type of Polyhedral Viruses Infecting Hyperthermophilic Archaea

Abstract

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...

Novel Sulfolobus Virus with an Exceptional Capsid Architecture

“…This unusual capsid architecture may represent a strategy for a virus to survive in a hot and acidic habitat. Interestingly, Sulfolobus polyhedral virus 1 (SPV1), a recently reported hot spring virus, appears to have a thread ball-like capsid bearing resemblance in DNA packaging to the capsid of SEV1 (13).…”

“…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.…”

A packing for A-form DNA in an icosahedral virus

“…The morphogenesis of the majority of these viruses involves formation of a nucleoprotein filament-from the genomic DNA and capsid proteinsand its condensation into bodies of different shapes. In case of the Sulfolobus polyhedral virus 1 (SPV1) from the family Portogloboviridae, such a nucleoprotein filament is condensed into the globular core, which is surrounded by a lipid envelope and further encased by an outer polyhedral capsid (3). The general design of the virion superficially resembles that of the icosahedral bacterial and archaeal viruses with an inner lipid envelope (families Tectiviridae, Corticoviridae, Sphaerolipoviridae, and Turriviridae), in which, however, DNA is present in the naked form (4)(5)(6)(7)(8)(9).…”

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

“…They share an overall 91.7% nucleotide sequence identity to each other. The former is identical to the genome of Sulfolobus polyhedral virus 1 (SPV1), which was previously isolated from the same enrichment culture and represents the first member of the proposed virus family Portogloboviridae (Liu et al ., ). The viral contig of 20 424 bp represents a member of the same family and is designated Sulfolobus polyhedral virus 2 (SPV2).…”

“…Following the new ICTV regulations, dsDNA viral genomes that have been assembled in the studies described here and elsewhere (Rosario et al ., ; Gudbergsdóttir et al ., ; Yutin et al ., ) can be officially classified as bona fide new viruses. Comparative genomics analysis of the viruses from the Umi Jigoku hot springs suggests that 4 of the 7 identified viruses should be assigned to known virus families: SBRV1 to the Rudiviridae (Prangishvili and Krupovic, ), SBFV3 to the Lipothrixviridae (Prangishvili and Krupovic, ) and SPV1 and SPV2 to the Portogloboviridae (Liu et al ., ). These taxonomic assignments are consistent with the presence, in the enrichment cultures, of virions typical in morphology and size for members of these families.…”