Comparative genomic analysis of the family Iridoviridae: re-annotating and defining the core set of iridovirus genes

Eaton, Heather E.; Metcalf, Julie; Penny, Emily; Tcherepanov, Vasily; Upton, Chris; Brunetti, Craig R.

doi:10.1186/1743-422x-4-11

Cited by 167 publications

(95 citation statements)

References 30 publications

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“…The elevated frequency of genomic rearrangements among them appears to be a common feature of other vertebrate iridoviruses (23,35) and is different from the extensive conservation of a central genome core in the related double-stranded DNA (dsDNA) Poxviridae family, which is probably related to their different replicative mechanisms. This result, together with the elevated branch length observed among the three LCDV viruses in our phylogenetic analyses, might reflect that the lymphocystiviruses have evolved over an extended time period in heterogeneous host species and locations.…”

Section: Discussionmentioning

confidence: 87%

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Concurrence of Iridovirus, Polyomavirus, and a Unique Member of a New Group of Fish Papillomaviruses in Lymphocystis Disease-Affected Gilthead Sea Bream

López-Bueno

Mavian

Labella

et al. 2016

J Virol

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Lymphocystis disease is a geographically widespread disease affecting more than 150 different species of marine and freshwater fish. The disease, provoked by the iridovirus lymphocystis disease virus (LCDV), is characterized by the appearance of papillomalike lesions on the skin of affected animals that usually self-resolve over time. Development of the disease is usually associated with several environmental factors and, more frequently, with stress conditions provoked by the intensive culture conditions present in fish farms. In gilthead sea bream (Sparus aurata), an economically important cultured fish species in the Mediterranean area, a distinct LCDV has been identified but not yet completely characterized. We have used direct sequencing of the virome of lymphocystis lesions from affected S. aurata fish to obtain the complete genome of a new LCDV-Sa species that is the largest vertebrate iridovirus sequenced to date. Importantly, this approach allowed us to assemble the full-length circular genome sequence of two previously unknown viruses belonging to the papillomaviruses and polyomaviruses, termed Sparus aurata papillomavirus 1 (SaPV1) and Sparus aurata polyomavirus 1 (SaPyV1), respectively. Epidemiological surveys showed that lymphocystis disease was frequently associated with the concurrent appearance of one or both of the new viruses. SaPV1 has unique characteristics, such as an intron within the L1 gene, and as the first member of the Papillomaviridae family described in fish, provides evidence for a more ancient origin of this family than previously thought. IMPORTANCELymphocystis disease affects marine and freshwater fish species worldwide. It is characterized by the appearance of papillomalike lesions on the skin that contain heavily enlarged cells (lymphocysts). The causative agent is the lymphocystis disease virus (LCDV), a large icosahedral virus of the family Iridoviridae. In the Mediterranean area, the gilthead sea bream (Sparus aurata), an important farmed fish, is frequently affected. Using next-generation sequencing, we have identified within S. aurata lymphocystis lesions the concurrent presence of an additional LCDV species (LCDV-Sa) as well as two novel viruses. These are members of polyomavirus and papillomavirus families, and here we report them to be frequently associated with the presence of lymphocysts in affected fish. Because papillomaviruses have not been described in fish before, these findings support a more ancient origin of this virus family than previously thought and evolutionary implications are discussed. L ymphocystis is a widely distributed disease affecting over 150 different marine and freshwater fish species (1). It was initially described during the 19th century and is characterized by the appearance of papillomalike lesions on the skin and fins, which develop over prolonged periods of time ranging from weeks to months. Occasionally, lesions on internal organs have been described, but the condition is rarely life-threatening and the outgrowths usually self-r...

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Section: Discussionmentioning

confidence: 87%

“…The LCDV-Sa genome contains 183 putative ORFs, including orthologues of all 26 conserved iridovirus core genes (23). To assess the phylogenetic position of LCDV-Sa, we used the concatenated sequence of proteins encoded by the 26 core genes to calculate maximum-likelihood trees, including representatives of all groups of vertebrate iridoviruses.…”

Section: Resultsmentioning

confidence: 99%

Concurrence of Iridovirus, Polyomavirus, and a Unique Member of a New Group of Fish Papillomaviruses in Lymphocystis Disease-Affected Gilthead Sea Bream

López-Bueno

Mavian

Labella

et al. 2016

J Virol

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“…To date, 12 genome sequences of iridoviruses including at least one from each genus have been completely sequenced and analysed [2,[4][5][6][7][8][9][10][11][12][13][14]. These analyses show that iridoviruses encode a number of cellular protein homologues that may be mostly involved in nucleic acid metabolism, such as ribonucleotide reductase (RR), thymidylate synthase (TS), deoxyuridine triphosphatase (DUT), and purine nucleoside phosphorylase (PNP) [15]. The presence of the cellular homologue genes may be of significant advantage for iridoviruses that independently replicate in the cytoplasm of the host cell [16].…”

Section: Introductionmentioning

confidence: 99%

“…It has been reported that viral TKs are responsible for virus-efficient replication in some specific cell type, virus virulence, pathogenesis and reactivation from latency [20,28]. As for the iridoviruses, TK is conserved within the genome sequences of all the sequenced members in the family Iridoviridae and belongs to the core genes of iridoviruses [15]. Furthermore, TK activity has also been shown in Bohle iridovirus [23].…”

Section: Introductionmentioning

confidence: 99%

Rana grylio virus thymidine kinase gene: an early gene of iridovirus encoding for a cytoplasmic protein

et al. 2009

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The presence of thymidine kinase (TK) is a feature of many large DNA viruses. Here, a TK gene homologue was cloned and characterized from Rana grylio virus (RGV), a member of family Iridoviridae. RGV TK encodes a protein of 195 aa with a predicted molecular mass of 22.1 kDa. Homologues of the protein were present in all the currently sequenced iridoviruses, and phylogenetic analysis showed that it was much close to cellular TK type 2 (TK2), deoxycytidine kinase (dCK) and deoxyguanosine kinase (dGK). Subsequently, Western blotting revealed TK expression increased with time from 6 h postinfection in RGV-infected cells. Using drug inhibition analysis by protein synthesis inhibitor (cycloheximide) and DNA replication inhibitor (cytosine arabinofuranoside), RGV TK was classified as the early expression gene during in vitro infection. Subcellular localization by TK-GFP fusion protein expression and immunofluorescence staining showed RGV TK was an exclusively cytoplasmic protein in fish cells. Collectively, current data indicate that RGV TK was an early gene of iridovirus which encoded a cytoplasmic protein in fish cells.

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“…To date, the genomes of twelve iridoviruses, including FV3, have been completely sequenced [8,9], and 26 core genes have been predicted to exist in all iridoviruses [10]. One of these is a gene belonging to ERV1 (essential for respiration and viability) family.…”

Section: Introductionmentioning

confidence: 99%

Cloning, expression and subcellular distribution of a Rana grylio virus late gene encoding ERV1 homologue

2008

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An essential for respiration and viability (ERV1) homologue, 88R, was cloned and characterized from Rana grylio virus (RGV). Database searches found its homologues in all sequenced iridoviruses, and sequence alignment revealed a highly conserved motif shared by all ERV1 family proteins: Cys-X-X-Cys. RT-PCR and western blot analysis revealed that 88R begins to transcribe and translate at 6 h postinfection (p.i.) and remains detectable at 48 h p.i. during RGV infection course. Furthermore, using drug inhibition analysis by a de novo protein synthesis inhibitor and a viral DNA replication inhibitor, RGV 88R was classified as a late (L) viral gene during the in vitro infection. 88R-EGFP fusion protein was observed in both the cytoplasm and nucleus of pEGFP-N3-88R transfected EPC cells. Although result of immunofluorescence is similar, 88R protein was not detected in viromatrix. Moreover, function of RGV 88R on virus replication were evaluated by RNAi assay. Nevertheless, effect of knockdown of RGV 88R expression on virus replication was not detected in cultured fish cell lines. Collectively, current data indicate that RGV 88R was a late gene of iridovirus encoding protein that distributed both the cytoplasm and nucleus.

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Comparative genomic analysis of the family Iridoviridae: re-annotating and defining the core set of iridovirus genes

Cited by 167 publications

References 30 publications

Concurrence of Iridovirus, Polyomavirus, and a Unique Member of a New Group of Fish Papillomaviruses in Lymphocystis Disease-Affected Gilthead Sea Bream

Concurrence of Iridovirus, Polyomavirus, and a Unique Member of a New Group of Fish Papillomaviruses in Lymphocystis Disease-Affected Gilthead Sea Bream

Rana grylio virus thymidine kinase gene: an early gene of iridovirus encoding for a cytoplasmic protein

Cloning, expression and subcellular distribution of a Rana grylio virus late gene encoding ERV1 homologue

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