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David Prangishvili and Mart Krupovic
A summary of this ICTV Report chapter has been published as an ICTV Virus Taxonomy Profile article in the Journal of General Virology, and should be cited when referencing this online chapter as follows:
Prangishvili, D., Krupovic, M., and ICTV Report Consortium, 2018, ICTV Virus Taxonomy Profile: Ampullaviridae, Journal of General Virology, 99: 288–289.
The family Ampullaviridae includes viruses with linear dsDNA genomes that replicate in hyperthermophilic archaea from the genus Acidianus. The virions have a unique champagne bottle-shaped morphology and consist of a nucleoprotein filament condensed into a cone-shaped core, which is encased by an envelope, with the base of the ‘bottle’ decorated with a ring of 20 filaments. Genome replication, presumably, is carried out by the virus-encoded protein-primed family B DNA polymerase. The bottle-shaped morphology is unprecedented among viruses of bacteria and eukaryotes and represents a group of archaea-specific virion morphotypes.
Table 1.Ampullaviridae. Characteristics of the family Ampullaviridae.
Acidianus bottle-shaped virus (EF432053), species Acidianus bottle-shaped virus, genus Ampullavirus
Bottle shaped; 230 nm long, 4–75 nm wide; the flat terminus is decorated with 20 nm-long filaments; envelope encases a cone-shaped nucleoprotein core
Linear, dsDNA (23,814 bp) with 590 bp terminal inverted repeats
Virus-encoded protein-primed family B DNA polymerase
Hyperthermophilic archaea from the genus Acidianus; non-lytic
Single genus with a single species; two related genomes have been obtained from metagenomics studies
The virion of Acidianus bottle shaped virus (ABV) is enveloped, resembles in its shape a bottle and has an overall length of about 230 nm and a width varying from about 75 nm, at the broad end, to 4 nm, at the pointed end (Figure 1.Ampullaviridae). The broad end of the virion exhibits 20 (±2) thin rigid filaments (20 nm long and 3 nm in width), which appear to be interconnected at their bases and regularly distributed around, and inserted into, a disc or ring. The 9 nm thick envelope encases a cone-shaped core formed by a torroidally supercoiled nucleoprotein filament, 7 nm in width. The bottle-shaped morphology is unprecedented among viruses of bacteria and eukaryotes and represents a group of archaea-specific virion morphotypes (Prangishvili et al., 2017).
ABV virion buoyant density in sucrose is about 1.3 g cm−3. The virions are fragile and partially disassembled after high speed ultracentrifugation as well as by prolonged storage. The pointed end of the virion, rather than the broad end, is likely to be involved in adsorption to the host cell surface (Häring et al., 2005).
ABV virions contain a single molecule of double-stranded (ds) DNA of 23,814 bp with 590 bp inverted terminal repeats. The GC content of the genome is 35% (Peng et al., 2007).
The ABV virion is enveloped but the exact lipid content of the viral envelope has not been characterized.
ABV virions carry six major proteins of 15–80 kDa (Häring et al., 2005).
The linear dsDNA genome of ABV is predicted to encode 57 proteins (Peng et al., 2007) (Figure 2.Ampullaviridae). Fifteen pairs of genes show small overlaps. Three genes contain putative internal start codons with ribosome-binding sites. The genome encodes a DNA polymerase, a putative glycosyltransferase, a thymidylate kinase, a Cas4-like endonuclease and two putative DNA-binding proteins with a winged helix-turn-helix and ribbon-helix-helix motifs, respectively. All these proteins are conserved in the two other, as yet unclassified, ampullavirus genomes (Acidianus bottle-shaped virus 2 , ABV2 and Acidianus bottle-shaped virus 3, ABV3) described in metagenomics studies (Figure 2.Ampullaviridae) (Gudbergsdóttir et al., 2016). Other predicted proteins have no known homologues. A potential 200 nt RNA transcript has predicted secondary structure highly similar to that of the prohead RNA of Bacillus phage phi29 and may be involved in genome packaging. The viral DNA polymerase is apparently responsible for genome replication. Its properties, predicted from sequence analysis, imply a protein-primed genome replication model (Peng et al., 2007).
Acidianus bottle-shaped virus was isolated from a hot acidic spring (87–93 °C, pH 1.5–2.0) in Pozzuoli, Italy. The host range is limited to autochthonous species of hyperthermophilic archaea from the genus Acidianus. ABV virions are released without apparent host cell lysis. Virus infection increases a generation time of the host from about 24 hours to about 48 hours. Release of particles is observed only in the stationary growth phase of the host culture (Häring et al., 2005).
Ampulla: From Latin ampulla, for “bottle”.
Related, unclassified, viruses have been identified by metagenomics studies of material from hot springs in Iceland, Italy and the USA (Figure 2.Ampullaviridae) (Gudbergsdóttir et al., 2016).
Most ampullavirus proteins have no known homologues. However, similar to many other hyperthermophilic archaeal viruses, ABV encodes a glycosyltransferase of the GT-B fold and a ribbon-helix-helix DNA binding protein (Krupovic et al., 2018). Protein-primed DNA polymerases homologous to that encoded by Acidianus bottle-shaped virus have also been described in members of the archaeal virus genera Gammapleolipovirus (family Pleolipoviridae) and Salterprovirus as well as in bacterial and eukaryotic viruses of the families Tectiviridae, Podoviridae (subfamily Picovirinae), Adenoviridae and Lavidaviridae (genus Mavirus) (Krupovic et al., 2018). Ampullaviruses, along with other archaeal viruses, may represent ancestral virus forms no longer observed amongst extant prokaryotic or eukaryotic viruses (Prangishvili 2015).
Since only one genus (Ampullavirus) is currently recognized in the family Ampullaviridae, the family description above corresponds to the genus description. For clarity, the additional information that can be found on the genus page is also presented below.
Acidianus bottle-shaped virus: genus of archaeal host Acidianus and shape of virion
Acidianus bottle-shaped virus 2
Acidianus bottle-shaped virus 3
Since only one genus is currently recognized, the genus description corresponds to the family description.
See discussion under family description.
David Prangishvili*Archaeal viruses Study Group ChairInstitut Pasteur Department of Microbiology 25, rue du Dr. Roux 75015 Paris, France Tel: +33 (0)144-38-9119E-mail: firstname.lastname@example.org
Mart Krupovic* Institut Pasteur Department of Microbiology 25, rue du Dr. Roux 75015 Paris, France Tel: +33(0)1-40-61-37 22 E-mail: email@example.com
* to whom correspondence should be addressed
The chapter in the Ninth ICTV Report, which served as the template for this chapter, was contributed by Prangishvili, D.
None currently associated with this report.
Gudbergsdóttir, S. R., Menzel, P., Krogh, A., Young, M. & Peng, X. (2016). Novel viral genomes identified from six metagenomes reveal wide distribution of archaeal viruses and high viral diversity in terrestrial hot springs. Environ Microbiol 18, 863-874. [PubMed]
Häring, M., Rachel, R., Peng, X., Garrett, R. A. & Prangishvili, D. (2005). 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. J Virol 79, 9904-9911. [PubMed]
Krupovic, M., Cvirkaite-Krupovic, V., Iranzo, J., Prangishvili, D. & Koonin, E. V. (2018). Viruses of archaea: Structural, functional, environmental and evolutionary genomics. Virus Res 244, 181-193. [PubMed]
Peng, X., Basta, T., Häring, M., Garrett, R. A. & Prangishvili, D. (2007). Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms. Virology 364, 237-243. [PubMed]
Prangishvili, D. (2015). Archaeal viruses: living fossils of the ancient virosphere? Ann N Y Acad Sci 1341, 35-40. [PubMed]
Prangishvili, D., Bamford, D. H., Forterre, P., Iranzo, J., Koonin, E. V. & Krupovic, M. (2017). The enigmatic archaeal virosphere. Nat Rev Microbiol 15, 724-739. [PubMed]
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