Ampullaviridae

Chapter Contents

Citation

A summary of this ICTV online (10th) 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, (In Press).

Summary

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. 

Virion

Morphology

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., 2017:29123227RJOHTXPrangishvili et al., 2017, The enigmatic archaeal virosphere, Nat Rev Microbiol, 15, 12, 724-39}].

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., 2005:16014951RJOHTXHäring et al., 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, 15, 9904-11}])

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., 2005:16014951RJOHTXHäring et al., 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, 15, 9904-11}].

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., 2007:17412384RJOHTXPeng et al., 2007, Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms, Virology, 364, 1, 237-43}].

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., 2005:16014951RJOHTXHäring et al., 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, 15, 9904-11}].

Genome organization and replication

The linear dsDNA genome of ABV is predicted to encode 57 proteins [{Peng et al., 2007:17412384RJOHTXPeng et al., 2007, Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms, Virology, 364, 1, 237-43}] (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., 2016:26439881RJOHTXGudbergsdóttir et al., 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, 3, 863-74}]. 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., 2007:17412384RJOHTXPeng et al., 2007, Genome of the Acidianus bottle-shaped virus and insights into the replication and packaging mechanisms, Virology, 364, 1, 237-43}].

Figure 2.Ampullaviridae. Genome organisation of Acidianus bottle-shaped virus (ABV) and comparison with the related, unclassified viruses ABV2 and ABV3. The square indicates the position of the predicted non-coding RNA gene. Functionally annotated genes shared by the three viruses are highlighted with different colors. Abbreviations: DNAP, DNA polymerase; Cas4-like, Cas4-like nuclease; TK, thymidylate kinase; RHH, ribbon-helix-helix motif; GTase, glycosyltransferase; wHTH, winged helix-turn-helix motif.

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., 2005:16014951RJOHTXHäring et al., 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, 15, 9904-11}].

Derivation of names

Ampulla: From Latin ampulla, for “bottle”.

Phylogenetic relationships

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., 2016:26439881RJOHTXGudbergsdóttir et al., 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, 3, 863-74}].

Similarity 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., 2018:29175107RJOHTXKrupovic et al., 2018, Viruses of archaea: Structural, functional, environmental and evolutionary genomics, Virus Research, 244, 181-93}]. 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., 2018:29175107RJOHTXKrupovic et al., 2018, Viruses of archaea: Structural, functional, environmental and evolutionary genomics, Virus Research, 244, 181-93}]. Ampullaviruses, along with other archaeal viruses, may represent ancestral virus forms no longer observed amongst extant prokaryotic or eukaryotic viruses [{Prangishvili 2015:25716458RJOHTXPrangishvili 2015, Archaeal viruses: living fossils of the ancient virosphere?, Ann N Y Acad Sci, 1341, 35-40}].

 Genus: Ampullavirus

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.

Member Species

Virus names, the choice of exemplar isolates, and virus abbreviations, are not official ICTV designations.

Derivation of names

Acidianus bottle-shaped virus: genus of archaeal host Acidianus and shape of virion

Related, Unclassified Viruses

Virus names, the choice of exemplar isolates, and virus abbreviations, are not official ICTV designations.
Download GenBank/EMBL query for sequences listed in the table here.