Virus taxonomy: classification and nomenclature of viruses

Comparative analysis of the protein sequences encoded in the genomes of three families of large DNA viruses that replicate, completely or partly, in the cytoplasm of eukaryotic cells (poxviruses, asfarviruses, and iridoviruses) and phycodnaviruses that replicate in the nucleus reveals 9 genes that are shared by all of these viruses and 22 more genes that are present in at least three of the four compared viral families. Although orthologous proteins from different viral families typically show weak sequence similarity, because of which some of them have not been identified previously, at least five of the conserved genes appear to be synapomorphies (shared derived characters) that unite these four viral families, to the exclusion of all other known viruses and cellular life forms. Cladistic analysis with the genes shared by at least two viral families as evolutionary characters supports the monophyly of poxviruses, asfarviruses, iridoviruses, and phycodnaviruses. The results of genome comparison allow a tentative reconstruction of the ancestral viral genome and suggest that the common ancestor of all of these viral families was a nucleocytoplasmic virus with an icosahedral capsid, which encoded complex systems for DNA replication and transcription, a redox protein involved in disulfide bond formation in virion membrane proteins, and probably inhibitors of apoptosis. The conservation of the disulfide-oxidoreductase, a major capsid protein, and two virion membrane proteins indicates that the odd-shaped virions of poxviruses have evolved from the more common icosahedral virion seen in asfarviruses, iridoviruses, and phycodnaviruses.

Common Origin of Four Diverse Families of Large Eukaryotic DNA Viruses

Publisher Summary This chapter focuses on the advances in iridovirus research over the past decade. It summarizes salient features of the iridovirus research studies, and discusses their importance to future work. As knowledge of iridovirus biology increases, so does the understanding of the taxonomic structure of the family. A new genus (Megalocytivirus) has recently been created to accommodate a number of viruses isolated from diseased fish in Southeast Asia, and an established one (Chloriridovirus) is about to be validated following the sequencing of the genome of the mosquito pathogen IIV-3. Genomic sequencing projects have clarified evolutionary relationships between iridoviruses and other families of large, nucleocytoplasmic DNA viruses. Iridoviruses appear situated at the center of a clade of DNA viruses that include the poxviruses, phycodnaviruses,ASFV, ascoviruses, and possibly a new giant virus of amoebae (mimivirus). Not all iridovirus infections result in mortal disease. The recognition that many iridovirus infections are chronic, especially among insects, should stimulate studies on the importance of such illnesses on host fitness. Sublethal effects have been demonstrated in infected insects, and theoretical studies suggest such effects have a major influence on the dynamics of host populations. However, the consequences of chronic disease on the demography (fecundity, fertility, death rate, etc.) of infected amphibian and fish populations are notable by their absence. The ability to detect iridovirus infections has advanced markedly with the adoption of highly sensitive loop-mediated isothermal amplification and multiplex polymerase chain reaction techniques for rapid diagnosis of infected individuals.

A decade of advances in iridovirus research.

Although possessing novel replicative and structural features, the family Iridoviridae has not been as extensively studied as other families of large, DNA-containing viruses (e.g., poxviridae and herpesviridae). This oversight most likely reflects the inability of iridoviruses to infect mammals and birds, and their heretofore low pathogenicity among cold-blooded animals and invertebrates. In fact, the original frog virus isolates (e.g., frog viruses 1-3) would likely have been considered orphan viruses since they were isolated from apparently healthy frogs. However, recent disease outbreaks among commercially and recreationally important fish, cultured and wild frogs, and endangered salamanders has challenged this benign view and have implicated several members of the genus Ranavirus as pathogens. This review explores three facets of ranavirus biology. In the first the salient features of ranavirus replication are summarized using frog virus 3 as a model. Secondly, criteria for characterizing new ranavirus isolates, based on biochemical (viral protein profiles, DNA restriction fragment length polymorphisms, and nucleotide sequence analysis), ecological (host range, tissue tropism), and clinical considerations, are detailed. Lastly, the principal agents of ranavirus-mediated disease and immune responses to these viruses are discussed. In light of the above, it is clear that ranaviruses are no longer orphan viruses, and that they have a significant impact on diverse populations of ectothermic animals.

Ranaviruses (family Iridoviridae): emerging cold-blooded killers

Ostreid herpesvirus 1 (OsHV-1) is the only member of the Herpesviridae that has an invertebrate host and is associated with sporadic mortality in the Pacific oyster (Crassostrea gigas) and other bivalve species. Cryo-electron microscopy of purified capsids revealed the distinctive T=16 icosahedral structure characteristic of herpesviruses, although the preparations examined lacked pentons. The gross genome organization of OsHV-1 was similar to that of certain mammalian herpesviruses (including herpes simplex virus and human cytomegalovirus), consisting of two invertible unique regions (UL, 167·8 kbp; US, 3·4 kbp) each flanked by inverted repeats (TRL/IRL, 7·6 kbp; TRS/IRS, 9·8 kbp), with an additional unique sequence (X, 1·5 kbp) between IRL and IRS. Of the 124 unique genes predicted from the 207 439 bp genome sequence, 38 were members of 12 families of related genes and encoded products related to helicases, inhibitors of apoptosis, deoxyuridine triphosphatase and RING-finger proteins, in addition to membrane-associated proteins. Eight genes in three of the families appeared to be fragmented. Other genes that did not belong to the families were predicted to encode DNA polymerase, the two subunits of ribonucleotide reductase, a helicase, a primase, the ATPase subunit of terminase, a RecB-like protein, additional RING-like proteins, an ion channel and several other membrane-associated proteins. Sequence comparisons showed that OsHV-1 is at best tenuously related to the two classes of vertebrate herpesviruses (those associated with mammals, birds and reptiles, and those associated with bony fish and amphibians). OsHV-1 thus represents a third major class of the herpesviruses.

Kristin Müller

Papers

Analysis of the first complete DNA sequence of an invertebrate iridovirus: coding strategy of the genome of Chilo iridescent virus.