Viruses from extreme thermal environments

Rice, George; Stedman, Kenneth M.; Snyder, Jamie C.; Wiedenheft, Blake; Willits, Deborah A.; Brumfield, Susan K.; McDermott, Timothy R.; Young, Mark

doi:10.1073/pnas.231170198

Cited by 174 publications

(111 citation statements)

References 20 publications

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“…Enrichment cultures were established from a YNP acidic hot spring (pH 2.9-3.9, 72-92°C) in the Rabbit Creek thermal area (44°31.287ЈN, 110°48.647ЈW) within the Midway Geyser Basin, as described (4). A single-colony isolate of Sulfolobus solfataricus expressing a spherical virus-like particle was established by previously described methods (4).…”

Section: Methodsmentioning

confidence: 99%

“…Isolate YNPRC179 was inoculated into medium 88 (www.dsmz.de͞species͞gn301555.htm), and the culture supernatants were monitored for virus production by direct particle counts with a transmission electron microscope (TEM), as described (4). When virus titers reached maximum levels (typically 3 days), cells were removed by centrifugation (6,000 ϫ g for 10 min) and the supernatants filtered through Acrodisc PF 0.8͞0.2-m filters (Pall Gelman Laboratory, Ann Arbor, MI).…”

Section: Methodsmentioning

confidence: 99%

“…To date, of the Ϸ5,100 known viruses, only 36 have been isolated from Archaea [International Committee on Taxonomy of Viruses, www.ncbi.nlm.nih.gov͞ICTV (1)]. Viruses and viruslike particles have been isolated from high-temperature (Ն80°C) acidic pH (Ͻ3.0) terrestrial environments throughout the world (2)(3)(4). Typically, these environments are found in thermal features such as boiling hot springs, mud pots, fumaroles, and geysers, with a wide range of geochemical compositions (5,6).…”

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confidence: 99%

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The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life

Rice

Tang

Stedman

et al. 2004

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

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213

238

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Of the three domains of life (Eukarya, Bacteria, and Archaea), the least understood is Archaea and its associated viruses. Many Archaea are extremophiles, with species that are capable of growth at some of the highest temperatures and extremes of pH of all known organisms. Phylogenetic rRNA-encoding DNA analysis places many of the hyperthermophilic Archaea (species with an optimum growth >80°C) at the base of the universal tree of life, suggesting that thermophiles were among the first forms of life on earth. Very few viruses have been identified from Archaea as compared to Bacteria and Eukarya. We report here the structure of a hyperthermophilic virus isolated from an archaeal host found in hot springs in Yellowstone National Park. The sequence of the circular double-stranded DNA viral genome shows that it shares little similarity to other known genes in viruses or other organisms. By comparing the tertiary and quaternary structures of the coat protein of this virus with those of a bacterial and an animal virus, we find conformational relationships among all three, suggesting that some viruses may have a common ancestor that precedes the division into three domains of life >3 billion years ago.

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Section: Methodsmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

mentioning

confidence: 99%

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The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life

Rice

Tang

Stedman

et al. 2004

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

Self Cite

213

238

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“…Electron microscopy observations suggest that linear viruses dominate in high-temperature environments (12,33,35,42). Those which have been isolated and characterized to date infect members of the archaeal genera Sulfolobus, Acidianus, and Thermoproteus.…”

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confidence: 99%

Structure of the Acidianus Filamentous Virus 3 and Comparative Genomics of Related Archaeal Lipothrixviruses

Vestergaard

Aramayo

Basta

et al. 2008

J Virol

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Four novel filamentous viruses with double-stranded DNA genomes, namely, Acidianus filamentous virus 3 (AFV3), AFV6, AFV7, and AFV8, have been characterized from the hyperthermophilic archaeal genus Acidianus, and they are assigned to the Betalipothrixvirus genus of the family Lipothrixviridae. The structures of the approximately 2-m-long virions are similar, and one of them, AFV3, was studied in detail. It consists of a cylindrical envelope containing globular subunits arranged in a helical formation that is unique for any known double-stranded DNA virus. The envelope is 3.1 nm thick and encases an inner core with two parallel rows of protein subunits arranged like a zipper. Each end of the virion is tapered and carries three short filaments. Two major structural proteins were identified as being common to all betalipothrixviruses. The viral genomes were sequenced and analyzed, and they reveal a high level of conservation in both gene content and gene order over large regions, with this similarity extending partly to the earlier described betalipothrixvirus Sulfolobus islandicus filamentous virus. A few predicted gene products of each virus, in addition to the structural proteins, could be assigned specific functions, including a putative helicase involved in Holliday junction branch migration, a nuclease, a protein phosphatase, transcriptional regulators, and glycosyltransferases. The AFV7 genome appears to have undergone intergenomic recombination with a large section of an AFV2-like viral genome, apparently resulting in phenotypic changes, as revealed by the presence of AFV2-like termini in the AFV7 virions. Shared features of the genomes include (i) large inverted terminal repeats exhibiting conserved, regularly spaced direct repeats; (ii) a highly conserved operon encoding the two major structural proteins; (iii) multiple overlapping open reading frames, which may be indicative of gene recoding; (iv) putative 12-bp genetic elements; and (v) partial gene sequences corresponding closely to spacer sequences of chromosomal repeat clusters.

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“…These extreme environmental conditions favor not only the Archaea but also result in a relatively simplified microbial community structure. A number of viruses, exclusively archaeal, have been isolated out of these environments (Rice et al, 2001;Mochizuki et al, 2011;Pina et al, 2011;Prangishvili, 2013). These conditions offer a tractable system to study virus-host relationships, as well as viral and host community structure and stability.…”

Section: Introductionmentioning

confidence: 99%

Viral assemblage composition in Yellowstone acidic hot springs assessed by network analysis

et al. 2015

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Understanding of viral assemblage structure in natural environments remains a daunting task. Total viral assemblage sequencing (for example, viral metagenomics) provides a tractable approach. However, even with the availability of next-generation sequencing technology it is usually only possible to obtain a fragmented view of viral assemblages in natural ecosystems. In this study, we applied a network-based approach in combination with viral metagenomics to investigate viral assemblage structure in the high temperature, acidic hot springs of Yellowstone National Park, USA. Our results show that this approach can identify distinct viral groups and provide insights into the viral assemblage structure. We identified 110 viral groups in the hot springs environment, with each viral group likely representing a viral family at the sub-family taxonomic level. Most of these viral groups are previously unknown DNA viruses likely infecting archaeal hosts. Overall, this study demonstrates the utility of combining viral assemblage sequencing approaches with network analysis to gain insights into viral assemblage structure in natural ecosystems.

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Viruses from extreme thermal environments

Cited by 174 publications

References 20 publications

The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life

The structure of a thermophilic archaeal virus shows a double-stranded DNA viral capsid type that spans all domains of life

Structure of the Acidianus Filamentous Virus 3 and Comparative Genomics of Related Archaeal Lipothrixviruses

Viral assemblage composition in Yellowstone acidic hot springs assessed by network analysis

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