Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments

Rachel, Reinhard; Bettstetter, Marcus; Hedlund, Brian P.; Häring, Monika; Kessler, Alexandra; Stetter, Karl O.; Prangishvili, David

doi:10.1007/s00705-002-0895-2

Cited by 120 publications

(71 citation statements)

References 45 publications

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“…Viruses have been identified in all known extreme environments: hypersaline (Oren et al, 1997;Dyall-Smith et al, 2003;Pagaling et al, 2007;Sime-Ngando et al, 2010), alkaline lakes (Jiang et al, 2004), deserts (Prigent et al, 2005), polar regions (Maranger et al, 1994;Kepner et al, 1998;Borriss et al, 2003;Gowing, 2003), acid mine drainages (Kyle et al, 2008a), deep subsurface rocks (Bird et al, 2001;Kyle et al, 2008b), and in hydrothermal environments. The search for new viruses in the latter environment has been especially fruitful, following the pioneering work of Wolfram Zillig on the viruses of hyperthermophilic Archaea (Martin et al, 1984;Rice et al, 2001;Rachel et al, 2002). Many new viral families that infect hyperthermophilic Archaea in terrestrial and marine hot springs have been identified (Geslin et al, 2003b;Ortmann and Suttle, 2005;Geslin et al, 2005;Prangishvili et al, 2006a;Ortmann et al, 2006;Le Romancer et al, 2007).…”

Section: Introductionmentioning

confidence: 99%

Experimental fossilisation of viruses from extremophilic Archaea

et al. 2011

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Abstract. The role of viruses at different stages of the origin of life has recently been reconsidered. It appears that viruses may have accompanied the earliest forms of life, allowing the transition from an RNA to a DNA world and possibly being involved in the shaping of tree of life in the three domains that we know presently. In addition, a large variety of viruses has been recently identified in extreme environments, hosted by extremophilic microorganisms, in ecosystems considered as analogues to those of the early Earth. Traces of life on the early Earth were preserved by the precipitation of silica on the organic structures. We present the results of the first experimental fossilisation by silica of viruses from extremophilic Archaea (SIRV2 -Sulfolobus islandicus rod-shaped virus 2, TPV1 -Thermococcus prieurii virus 1, and PAV1 -Pyrococcus abyssi virus 1). Our results confirm that viruses can be fossilised, with silica precipitating on the different viral structures (proteins, envelope) over several months in a manner similar to that of other experimentally and naturally fossilised microorganisms. This study thus suggests that viral remains or traces could be preserved in the rock record although their identification may be challenging due to the small size of the viral particles.

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Section: Introductionmentioning

confidence: 99%

Experimental fossilisation of viruses from extremophilic Archaea

et al. 2011

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“…One group of ecosystems which has yielded exciting new results is geothermally heated hot aquatic environments. Screening for viruses in terrestrial hot springs with temperatures above 80°C in Iceland (20) and in Yellowstone National Park (13,15) has revealed numerous, different virus morphotypes, many of which have not been previously observed in nature. Several of the isolated viruses infect hyperthermophilic archaea from the Crenarchaeota kingdom, and they all have double-stranded DNA (dsDNA) genomes.…”

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Viral Diversity in Hot Springs of Pozzuoli, Italy, and Characterization of a Unique Archaeal Virus, Acidianus Bottle-Shaped Virus, from a New Family, the Ampullaviridae

Häring

Rachel

Peng

et al. 2005

J Virol

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Virus-like particles with five different morphotypes were observed in an enriched environmental sample from a hot, acidic spring (87 to 93°C, pH 1.5) in Pozzuoli, Italy. The morphotypes included rigid rods, flexible filaments, and novel, exceptional forms. Particles of each type were isolated, and they were shown to represent viable virions of five novel viruses which infect members of the hyperthermophilic archaeal genus Acidianus. One of these, named the Acidianus bottle-shaped virus, ABV, exhibits a previously unreported morphotype. The bottle-shaped virion carries an envelope which encases a funnel-shaped core. The pointed end of the virion is likely to be involved in adsorption and channeling of viral DNA into host cells. The broad end exhibits 20 (؎ 2) thin filaments which appear to be inserted into a disk, or ring, and are interconnected at their bases. These filaments are apparently not involved in adsorption. ABV virions contain six proteins in the size range 15 to 80 kDa and a 23.9-kb linear, double-stranded DNA genome. Virus replication does not cause lysis of host cells. On the basis of its unique morphotype and structure, we propose to assign ABV to a new viral family, the Ampullaviridae.Evidence supporting an extremely high abundance of viruses in the biosphere has stimulated a strong interest in determining the degree of viral diversity in different ecosystems (19). One group of ecosystems which has yielded exciting new results is geothermally heated hot aquatic environments. Screening for viruses in terrestrial hot springs with temperatures above 80°C in Iceland (20) and in Yellowstone National Park (13, 15) has revealed numerous, different virus morphotypes, many of which have not been previously observed in nature. Several of the isolated viruses infect hyperthermophilic archaea from the Crenarchaeota kingdom, and they all have double-stranded DNA (dsDNA) genomes. Moreover, on the basis of their exceptional morphological and genomic properties, five novel virus families have been established: the spindleshaped Fuselloviridae, the filamentous Lipothrixviridae, the rodshaped Rudiviridae, the droplet-shaped Guttaviridae (reviewed in references 12 and 21), and the spherical Globuloviridae (5).In order to confirm that hot aquatic environments constitute favorable habitats for viruses with unusual morphotypes, we examined viral diversity in a volcanic area near Naples, Italy, and the results reinforced previous observations. Virus-like particles with five different morphotypes were isolated from the environmental samples, and they were shown to be infectious virions. One of these novel viruses, the Acidianus bottleshaped virus (ABV), is described in detail. MATERIALS AND METHODS Enrichment cultures.A sample was taken from a water reservoir in the crater of the Solfatara volcano at Pozzuoli, Italy. Although the temperature of the lake was on average about 60°C, undercurrents close to the surface were hotter and generated steam. These undercurrents were caused by submerged hot springs, and a sample was...

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“…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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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.

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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Remarkable morphological diversity of viruses and virus-like particles in hot terrestrial environments

Cited by 120 publications

References 45 publications

Experimental fossilisation of viruses from extremophilic Archaea

Experimental fossilisation of viruses from extremophilic Archaea

Viral Diversity in Hot Springs of Pozzuoli, Italy, and Characterization of a Unique Archaeal Virus, Acidianus Bottle-Shaped Virus, from a New Family, the Ampullaviridae

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

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