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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:
Bamford, D.H., Pietilä, M.K., Roine, E., Atanasova, N.S., Dienstbier, A., Oksanen, H.M., and ICTV Report Consortium, 2017, ICTV Virus Taxonomy Profile: Pleolipoviridae, Journal of General Virology, (In Press).
Members of family Pleolipoviridae (termed pleolipoviruses) are pseudo-spherical and pleomorphic archaeal viruses with a membrane vesicle enclosing different types of DNA genomes of approximately 7 to 16 kilonucleotides or kbp. Typically, virions contain a single type of spike protein at the envelope and a single type of internal membrane protein embedded in the envelope. All viruses infect extremely halophilic archaea in the class Halobacteria (phylum Euryarchaeota). Pleolipoviruses have a narrow host range and a persistent, non-lytic life cycle.
Table 1.Pleolipoviridae. Characteristics of the family Pleolipoviridae.
Halorubrum pleomorphic virus 1 (FJ685651), species Halorubrum virus HRPV1, genus Alphapleolipovirus
Enveloped, pseudo-spherical and pleomorphic, virions (diameters 40 – 70 nm), typically with a single type of spike protein at the envelope and a single type of internal membrane protein species embedded in the envelope
Circular ssDNA, circular dsDNA or linear dsDNA, approximately 7 – 16 kilonucleotides or kbp
Possibly rolling circle replication for circular genomes; protein primed replication for linear genomes
Prokaryotic translation using viral mRNA and host ribosomes
Archaea, euryarchaeal Halorubrum, Haloarcula or Halogeometricum strains
Three genera Alphapleolipovirus, Betapleolipovirus and Gammapleolipovirus
Virions consist of a genome surrounded by a pleomorphic membrane vesicle of 40 - 70 nm in diameter with irregularly distributed spike structures (Pietilä et al., 2009, Pietilä et al., 2012) (Figure 1.Pleolipoviridae). Virions lack a capsid or a nucleocapsid structure. There are two to four types of major structural protein forming the spikes or associating with the membrane as internal membrane proteins. The spikes are formed of one or two types of membrane-anchored protein species. The spike protein is anchored to the lipid membrane with a C-terminal transmembrane domain domain (Pietilä et al., 2010, Senčilo et al., 2012). The internal membrane proteins (either one or two types) are located in the inner side of the membrane vesicle.
Figure 1.Pleolipoviridae. Morphology of pleolipoviral virions. (A) Electron micrograph of negatively stained Halorubrum pleomorphic virus 1 (HPRV-1) particles. Scale bar, 50 nm. (B) Schematic presentation of the pleolipovirus virion.
Virions are typically very stable at high ionic strengths (e.g. above 2.5 M NaCl) and are inactivated in the absence of NaCl with some exceptions. Virion buoyant densities in CsCl are from 1.26 to 1.34 g cm-3. Infectivity is sensitive to detergents and the organic solvent chloroform. Virions are stable at temperatures below 60 °C.
Members of family Pleolipoviridae have different types of DNA genomes (Senčilo et al., 2012, Roine et al., 2010). Genomes are circular single-stranded DNA of approximately 7.0-10.7 kilonucleotides, circular double-stranded DNA of approximately 8.1-9.7 kbp, or linear double-stranded DNA of approximately 16 kbp (Figure 2.Pleolipoviridae). The genomes of pleolipoviruses share little similarity with each other at the nucleotide sequence level. Members of Alphapleolipovirus have either single-stranded or double-stranded circular DNA genomes. Genomes of members of the genus Betapleolipovirus are circular double-stranded DNA molecules with single-stranded discontinuities, and the linear genome of the only member of the genus Gammapleolipovirus contains inverted terminal repeat sequences and terminal proteins attached to the genome ends.
Figure 2.Pleolipoviridae. A linear representation of pleolipovirus genomes. All genomes are circular except the His2 genome, which is a linear molecule. The genomes are either single-stranded (Haloarcula hispanica pleomorphic virus 2 (HHPV-2), Halorubrum pleomorphic virus 6 (HRPV-6), Halorubrum pleomorphic virus 2 (HRPV-2) and Halorubrum pleomorphic virus 1 (HRPV-1) or double-stranded DNA molecules (Haloarcula hispanica pleomorphic virus 1 (HHPV-1), Halorubrum pleomorphic virus 3 (HRPV-3), Halogeometricum pleomorphic virus 1 (HGPV-1) and His2 virus (His2)), although the HRPV-3 and HGPV-1 genomes have stretches of ssDNA. The directionality of the genes/ORFs is indicated by arrows. The identities (%) between the amino acid sequences of pairs of predicted (or identified) gene products are indicated. Based on the genome organization and the relatedness of the VP3-like proteins (homologous with HRPV-1 VP3 protein), the members of the Pleolipoviridae can be divided into three genera, which are indicated on the left. Modified from (Pietilä et al., 2016) with permission of Springer.
The genomes have from 8 to 35 predicted open reading frames (ORFs), of which 2-4 have been shown to code for structural proteins and the rest have unknown functions or predicted function based on sequence similarity. Virions contain one or two types of internal membrane protein, with several predicted transmembrane regions, and one or two types of spike protein, which are processed during maturation. The non-structural proteins of the members of the genus Alphapleolipovirus include putative rolling circle replication initiation proteins (RCR Reps) and members of the genus Gammapleolipovirus encode a putative type B DNA polymerase (Pietilä et al., 2009, Roine et al., 2010, Bath et al., 2006, Senčilo et al., 2012).
The lipids are derived from host cell membranes. Viral lipid species composition is similar to that of the host archaeon. Lipids form the sole outer layer of the virion with virus-specific spike and internal membrane proteins. Details of the lipid species composition are given in the corresponding sections of the genera.
Virions can contain carbohydrates in the form of glycolipids. The spike protein of Halorubrum pleomorphic virus 1 (HRPV-1) is N-glycosylated (Kandiba et al., 2012).
The genes encoding the two major structural proteins and a putative NTPase belong to a cluster of five genes/ORFs (genes 3, 4 and 8; ORFs 6 and 7 of Halorubrum pleomorphic virus 1) that are collinear and conserved among members of the family Pleolipoviridae (Figure 2.Pleolipoviridae; (Senčilo et al., 2012). Pleolipoviruses have non-lytic life cycles. Although there is no direct evidence for the entry mechanism, it has been proposed that the entry of pleolipoviral genomes occurs by membrane fusion of the viral envelope with the host cell cytoplasmic membrane (Pietilä et al., 2009). Viruses are predicted to employ different genome replication strategies, including rolling circle replication (RCR; circular genomes) and protein-primed replication carried out by family B-type polymerase (linear genomes), although direct experimental evidence is missing (Pietilä et al., 2009, Roine et al., 2010, Bath et al., 2006). Viruses exit the cells continuously starting 3-4 hours post infection (Pietilä et al., 2012, Senčilo et al., 2012). During the infection cycle, host growth can be slightly retarded, although the infected cells are consuming oxygen as much as the non-infected ones (Pietilä et al., 2009, Pietilä et al., 2012, Roine et al., 2010, Senčilo et al., 2012). The non-lytic life cycle is also evidenced by the hazy appearance of the plaques the viruses form on the host lawn. The characteristics of the life cycle and the presence of lipid envelope in the virions suggest that pleolipoviruses exit host cells using budding.
The current members of family Pleolipoviridae have a narrow host range. They infect only their original isolation hosts, all of which belong to the class Halobacteria. Pleolipoviruses display a wide geographical distribution and originate from hypersaline environments such as solar salterns and hypersaline lakes in Europe, Asia and Australia (Pietilä et al., 2012, Bath et al., 2006, Atanasova et al., 2012, Li et al., 2014)
The following criteria are used to differentiate genera in the family:
Pleo: from Greek pleo, “many”.
Lipo: from Greek lipos, “lipid”.
Members of family Pleolipoviridae share a similar structural protein pattern, genome synteny, and some sequence similarity. On the basis of amino acid sequence identity, the internal membrane protein (protein VP3 of Halorubrum pleomorphic virus 1 (HRPV-1)) is the most conserved among the members of family Pleolipoviridae. Phylogenetic analysis based on the amino acid sequences of VP3-like proteins divides the pleolipoviruses into three groups, which are consistent with the division of the viruses into the three genera (Senčilo et al., 2012, Pietilä et al., 2016).
Members of the family Pleolipoviridae form a distinct group of viruses. Their structural proteins share no significant amino acid similarity with the structural proteins of any other virus. Acholeplasma virus L2 (APVL2, family Plasmaviridae) infecting the bacterium Acholeplasma laidlawii displays similar virion morphology (quasi-spherical, pleomorphic) as that of pleolipoviruses. In both cases, the virion envelope is composed of host-derived lipids that are acquired unselectively (Al-Shammari and Smith 1981, Dybvig et al., 1985, Maniloff et al., 1994). The APVL2 genome is a circular double-stranded DNA molecule (~12 kbp) as the genomes of some viruses belonging to the genus Alphapleolipovirus (Pietilä et al., 2009, Senčilo et al., 2012). Nevertheless, the genome sequence of APVL2 shares no identity with pleolipoviral sequences at the nucleotide sequence level. On the basis of virion morphology and structural protein patterns, it has been hypothesized that HRPV-1 could be related to mycoplasmavirus L172 which infects Acholeplasma laidlawii and contains a circular single-stranded DNA genome (Pietilä et al., 2009, Dybvig et al., 1985). Currently, there is no genome sequence data available for mycoplasmavirus L172 and it has not been officially classified to any taxon.
Halorubrum pleomorphic virus 7
Halorubrum pleomorphic virus 8
Haloarcula pleomorphic virus 2
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