Family: Ampullaviridae
David Prangishvili and Mart Krupovic
The citation for this ICTV Report chapter is the summary published as Prangishvili et al., (2018):
ICTV Virus Taxonomy Profile: Ampullaviridae, Journal of General Virology, 99: 288–289.
Corresponding authors: David Prangishvili (david.prangishvili@pasteur.fr) and Mart Krupovic (mart.krupovic@pasteur.fr)
Edited by: Andrew M. Kropinski and Stuart G. Siddell
Posted: February 2018, updated June 2022
PDF: ICTV_Ampullaviridae.pdf (2018 version)
Summary
The family Ampullaviridae includes viruses with linear dsDNA genomes that replicate in hyperthermophilic archaea from the genus Acidianus (Table 1.Ampullaviridae). 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 members of the family Ampullaviridae.
| Characteristic | Description |
| Example | Acidianus bottle-shaped virus (EF432053), species Bottigliavirus ABV, genus Bottigliavirus |
| Virion | 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 |
| Genome | Linear, dsDNA (22–28 kbp) with terminal inverted repeats |
| Replication | Virus-encoded protein-primed family B DNA polymerase |
| Translation | Not characterised |
| Host range | Hyperthermophilic archaea from the genus Acidianus; non-lytic |
| Taxonomy | Single genus with three species |
Virion
Morphology
The virion of Acidianus bottle shaped virus (ABV), the only cultivated representative of the family, is enveloped and resembles in its shape a bottle with 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).
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| Figure 1. .Ampullaviridae. Negative-contrast electron micrographs of native (left) and partially degraded (right) virions of an isolate of Acidianus bottle-shaped virus. Schematic representation of the virion (bottom right). The scale bars represent 100 nm. (Modified with permission from (Häring et al., 2005)) |
Physicochemical and physical properties
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).
Nucleic acid
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 genomes of other members in the family are similarly sized: Acidianus bottle-shaped virus 2 (ABV2) and Acidianus bottle-shaped virus 3 (ABV3) genomes are 22 613 bp and 28 489 bp, respectively (Gudbergsdóttir et al., 2016).
Lipids
The ABV virion is enveloped but the exact lipid content of the viral envelope has not been characterized.
Proteins
ABV virions carry six major proteins of 15–80 kDa (Häring et al., 2005).
Genome organization and replication
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 genomes of ABV2 and ABV3, two other ampullaviruses 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).
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Biology
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).
Derivation of names
Ampullaviridae: from the Latin ampulla, meaning “bottle”
Bottigliavirus: from bottiglia, the Italian for bottle
Relationships within the family
The family includes three species. Whereas ABV was isolated, two other members, ABV2 and ABV3 have been identified by metagenomics studies of material from hot springs in Iceland, Italy and the USA (Figure 2. .Ampullaviridae) (Gudbergsdóttir et al., 2016). ABV2 is more closely related to ABV, with 75% nucleotide sequence identity over 80% of the genome length. By contrast, ABV3 is more divergent, showing little nucleotide sequence similarity to either ABV or ABV2 (only about 14% of the ABV3 genome can be aligned to that of ABV).
Relationships with other taxa
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), Nitmarvirus (family Thaspiviridae), Alphaovalivirus (family Ovaliviridae) and Salterprovirus (family Halspiviridae), 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).