Bicaudaviridae


Bicaudaviridae

Chapter Contents

Posted May 2018

Bicaudaviridae: The Family

Bicaudaviridae: Member Taxa

Bicaudaviridae: Supporting Information

  • Authors - Corresponding authors: David Prangishvili (david.prangishvili@pasteur.fr) and Mart Krupovic (krupovic@pasteur.fr)
  • References - Literature cited

Citation

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. ICTV Virus Taxonomy Profile: Bicaudaviridae. 2018. Journal of General Virology, 99: 864-865.

Summary

The family Bicaudaviridae includes viruses that infect hyperthermophilic archaea in the genus Acidianus. The circular double-stranded DNA genome of Acidianus two-tailed virus consists of 62,730 bp, and replication can be either lytic or lysogenic. The virions undergo unique extracellular morphogenesis. Virions are released from host cells as spindle-shaped particles, which subsequently develop long tails, one at each of the two pointed ends. The spindle-shaped morphology is unprecedented among viruses of bacteria and eukaryotes and represents a group of archaea-specific virion morphotypes.

Table 1.Bicaudaviridae. Characteristics of the family Bicaudaviridae.

Characteristic

Description

Typical member

Acidianus two-tailed virus (AJ888457), species Acidianus two-tailed virus, genus Bicaudavirus

Virion

Spindle-shaped upon release (120 x 80 nm), subsequently developing two tails each of up to 400 nm in length

Genome

Circular dsDNA of 62,730 bp

Replication

Lytic or lysogenic

Translation

Not known

Host range

Hyperthermophilic archaea from the genus Acidianus

Taxonomy

One genus including a single species

Virion

Morphology

Virions of Acidianus two-tailed virus (ATV) are released from host cells as spindle-shaped particles, about 120×80 nm, which subsequently develop two long tails, one at each of the two pointed ends (Table 1.Bicaudaviridae, Figure 1.Bicaudaviridae)  (Häring et al., 2005, Prangishvili et al., 2006). The tails are heterogeneous in length, reaching 400 nm. The tails have a tube-like structure with walls that are approximately 6 nm thick. The tube terminates with a narrow channel, which is 2 nm in width, and a terminal anchor-like structure formed by two furled filaments, each with a width of 4 nm.

Figure 1.Bicaudaviridae. Electron micrographs of different forms of Acidianus two-tailed virus. a, Virions in the infected cell culture at the late stage of tail development. b, extrusion of virions from an Acidianus convivator cell; c, virions in growing culture of infected A. convivator, two days post-infection; d, as for c, but purified by CsCl gradient centrifugation; e-h, as for d, but after incubation at 75°C for 2, 5, 6, and 7 days, respectively. Samples were negatively-stained with 3% uranyl acetate, except for b, which was platinum- shadowed. Bars: a-c, 0.5 µm; d-h, 0.1 µm (first published in (Häring et al., 2005)).

Physicochemical and physical properties

Extracellular morphological development of the virion takes place specifically at temperatures above 75 °C, close to that of the natural habitat, and does not require the presence of the host cells, an exogenous energy source or specific co-factors. The average volume of the tailless virion is about 1.4 nm3, and that of the two-tailed virion 6.2 nm3. However, the total surface areas for the two types of virions are similar, about 6×103 nm2. The mechanism of ATV tail development is unknown. The buoyant density of ATV virions in CsCl is about 1.3 g cm-3

Nucleic acid

Virions of ATV contain one molecule of circular dsDNA of 62,730 bp, with a GC content of 41.2%.

Proteins

Protein patterns of tailless and two-tailed virions are identical. The virions carry 11 major structural proteins (90, 80, 70, 60, 48, 45, 34, 22, 16, 14 and 12 kDa; Table 2.Bicaudaviridae), five of which are modified at their N-termini. Several of the larger proteins are rich in coiled-coil or low complexity sequence domains, or both. The 80 kDa protein appears to be modified in the two-tailed but not in the tail-less virions (Prangishvili et al., 2006). High resolution structures of 32 and 14 kDa proteins have been solved by X-ray crystallography (Felisberto-Rodrigues et al., 2012, Goulet et al., 2010) and both display unique folds that are not observed in proteins of other classified viruses (Krupovic et al., 2018). The structural protein encoded by ORF140 (Table 2.Bicaudaviridae) is a paralog of the major capsid protein encoded by ORF131. It has been shown that the product of ORF140 acts as a global transcription repressor, which forms a high-affinity complex with the host RNA polymerase by binding inside the DNA-binding channel. This interaction counteracts the formation of transcription pre-initiation complexes in vitro and represses transcription initiation as well as elongation (Sheppard et al., 2016). However, the role of ORF140 in transcription regulation in vivo, as well as in virion assembly and structure, remain to be investigated. ATV structural proteins encoded by ORF387, ORF653 and ORF800 as well as the non-structural protein containing the von Willebrand factor type A domain (encoded by ORF618) have been shown to interact with the MoxR-like AAA+ ATPase, which is also a structural virion component (Scheele et al., 2011). It has been suggested that the latter group of proteins may constitute a chaperone system for extracellular tail development.

Lipids

No lipids were obtained from ATV virions after treatment with chloroform/methanol (1:1, vol/vol).

Carbohydrates

Not known. Note that the virus encodes a putative glycosyltransferase.

Genome organization and replication 

The ATV genome encodes 72 predicted proteins and carries four putative transposable elements (Figure 2.Bicaudaviridae, Table 2.Bicaudaviridae). Forty-three genes are predicted to produce leader-less transcripts and 35 genes are organized in 12 putative operons. Several genes may have been produced by gene duplication. Besides structural virion proteins, the virus encodes several functionally diverse enzymes, including a putative integrase of the tyrosine recombinase superfamily, a glycosyltransferase, a ParB-like partitioning protein, a DNA repair photolyase, an acyltransferase and three distinct AAA+ ATPases. For two of the ATPases (ORF529 and ORF618), the activity has been demonstrated in vitro (Scheele et al., 2011, Erdmann et al., 2011).

Figure 2.Bicaudaviridae. Genome organization of Acidianus two-tailed virus showing location, sizes and transcriptional direction of the putative genes. Color-coded ORFs correspond to: red, virion proteins; black, transposable elements. ORFs shared with unclassified large spindle-shaped viruses are indicated with asterisks.

Table 2.Bicaudaviridae. Genome annotation of Acidianus two-tailed virus.

ORF

Protein
Accession Number

Gene product

Function

ORF54

YP_319832

gp01

ORF273

YP_319833

gp02

Structural protein (PDB id: 4art)

ORF79

YP_319834

gp03

ORF59a

YP_319835

gp04

ORF48

YP_319836

gp05

ORF117

YP_319837

gp06

Putative DNA-binding protein

ORF70

YP_319838

gp07

Transcription regulator, winged helix-turn-helix (wHTH) domain

ORF104a

YP_319839

gp08

ORF209

YP_319840

gp09

ORF409

YP_319841

gp10

TnpB protein associated with IS200/IS605 transposons

ORF82

YP_319842

gp11

ORF119

YP_319843

gp12

ORF58

YP_319844

gp13

ORF61

YP_319845

gp14

ORF127

YP_319846

gp15

ORF175

YP_319847

gp16

ORF80

YP_319848

gp17

ORF211

YP_319849

gp18

ORF98a

YP_319850

gp19

Transcription regulator, wHTH domain

ORF45

YP_319851

gp20

ORF240

YP_319852

gp21

ORF115

YP_319853

gp22

ORF167

YP_319854

gp23

ORF86

YP_319855

gp24

RNA-binding Lsm/Hfq-like protein

ORF111

YP_319856

gp25

ORF100

YP_319857

gp26

ORF59b

YP_319858

gp27

Transcription regulator, RHH domain

ORF189

YP_319859

gp28

Transcription regulator, C2H2-type zinc finger

ORF60

YP_319860

gp29

Transcription regulator, RHH domain

ORF161

YP_319861

gp30

ORF155

YP_319862

gp31

ORF187

YP_319863

gp32

Structural protein

ORF326a

YP_319864

gp33

Structural protein

ORF330

YP_319865

gp34

Acyltransferase, peptidoglycan/LPS O-acetylase

ORF220

YP_319866

gp35

ORF98b

YP_319867

gp36

Transcription regulator, C2H2-type zinc finger

ORF84

YP_319868

gp37

ORF81

YP_319869

gp38

ORF137

YP_319870

gp39

ORF457

YP_319871

gp40

TnpB protein associated with IS200/IS605 transposons

ORF193

YP_319872

gp41

ORF145

YP_319873

gp42

Structural protein, paralog of the major structural protein; transcriptional repressor

ORF383a

YP_319874

gp43

TnpB protein associated with IS200/IS605 transposons

ORF301

YP_319875

gp44

DNA repair photolyase, radical SAM superfamily

ORF161b

YP_319876

gp45

ORF38

YP_319877

gp46

ORF147

YP_319878

gp47

ORF800

YP_319879

gp48

Structural protein; tetratricopeptide repeat protein

ORF567

YP_319880

gp49

Structural protein

ORF1940

YP_319881

gp50

ORF134

YP_319882

gp51

ORF227

YP_319883

gp52

ORF529

YP_319884

gp53

AAA+ ATPase

ORF34

YP_319885

gp54

ORF286

YP_319886

gp55

DnaA-like AAA+ ATPase

ORF277

YP_319887

gp56

ORF653

YP_319888

gp57

Structural protein

ORF213

YP_319889

gp58

ORF104b

YP_319890

gp59

Structural protein

ORF710

YP_319891

gp60

ORF892

YP_319892

gp61

von Willebrand factor type A (vWA) domain

ORF131

YP_319893

gp62

Major structural protein (PDB id: 3faj)

ORF387

YP_319894

gp63

Structural protein

ORF362

YP_319895

gp64

ORF170

YP_319896

gp65

ORF618

YP_319897

gp66

Structural protein; MoxR-like AAA+ ATPase

ORF545

YP_319898

gp67

Glycosyltransferase, mannosyltransferase

ORF383b

YP_319899

gp68

TnpB protein associated with IS200/IS605 transposons

ORF192

YP_319900

gp69

ORF326b

YP_319901

gp70

ParB-like partitioning protein

ORF1334

YP_319902

gp71

ORF241

YP_319903

gp72

Integrase, tyrosine recombinase superfamily 

Antigenicity

Not known.

Biology

The 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. Infection leads either to viral replication and subsequent cell lysis or conversion of infected cell into a lysogen. The lysogenic cycle involves integration of the viral genome into the host chromosome, probably facilitated by a virus-encoded integrase. The lysogeny can be interrupted by stress factors, e.g. UV-irradiation or a decrease in temperature. The virus does not encode identifiable DNA and RNA polymerases and is likely to depend on the host machineries for genome replication and transcription.

Derivation of names

Bicauda: from Latin bi, “two”, and cauda, “tail”.

Phylogenetic relationships

Putative relatives, sharing a considerable fraction of genes with the bicaudavirus ATV (Figure 2.Bicaudaviridae) have been described, but remain unclassified. These include Acidianus tailed spindle virus (Hochstein et al., 2016), Sulfolobus tengchongensis spindle-shaped virus 1 (Xiang et al., 2005), Sulfolobus tengchongensis spindle-shaped virus 2 (Erdmann et al., 2014) as well as Sulfolobus monocaudaviruses 1 (Erdmann et al., 2013), 2, 3 and 4 (Gudbergsdóttir et al., 2016). Similar to ATV, Sulfolobus monocaudavirus 1 was reported to develop one or two tails extracellularly (Uldahl et al., 2016). By contrast, the other unclassified viruses contain a single long tail, which appears to develop intracellularly. In the future, these viruses are likely to be classified into new genera within the family Bicaudaviridae (Krupovic et al., 2014).

Similarity with other taxa 

Bicaudaviruses encode a conserved DnaA-like AAA+ ATPase, which is shared with members of the archaeal virus families Fuselloviridae (Iranzo et al., 2016) and Guttaviridae (Prangishvili et al., 2018), suggesting that the three groups of viruses might be evolutionarily related.

Related, Unclassified Viruses 

Virus name

Accession number

Virus abbreviation

Sulfolobus monocaudavirus 1

HG322870

SMV1

Sulfolobus monocaudavirus 2

KP238129

SMV2

Sulfolobus monocaudavirus 3

KP282677

SMV3

Sulfolobus monocaudavirus 4

KP282678

SMV4

Acidianus tailed spindle virus

KU645528

ATSV

Sulfolobus tengchongensis spindle-shaped virus 1

AJ783769

STSV1

Sulfolobus tengchongensis spindle-shaped virus 2

JQ287645

STSV2

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


Genus: Bicaudavirus


Since only one genus (Bicaudavirus) is currently recognized in the family Bicaudaviridae, 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

SpeciesVirus name(s)Exemplar isolateExemplar accession numberExemplar RefSeq numberAvailable sequenceOther isolatesOther isolate accession numbersVirus abbreviationIsolate abbreviation
Acidianus two-tailed virusAcidianus two-tailed virusAJ888457NC_007409Complete genomeATV

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

Derivation of names

Acidianus two-tailed virus: genus of archaeal host Acidianus and the distinguishing characteristic of the virion

Related, Unclassified Viruses

A closely related virus, Acidianus two-tailed virus 2, which shares 90% identity over 92% of the genome, is an unclassified virus within the genus Bicaudavirus.

Virus name

Accession number

Virus abbreviation

Acidianus two-tailed virus 2

KX607101

ATV2

Virus names and virus abbreviations are not official ICTV designations.