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Diversity of Large DNA Viruses of Invertebrates ⇑ Trevor Williams A, Max Bergoin B, Monique M

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Diversity of Large DNA Viruses of Invertebrates ⇑ Trevor Williams A, Max Bergoin B, Monique M Journal of Invertebrate Pathology 147 (2017) 4–22 Contents lists available at ScienceDirect Journal of Invertebrate Pathology journal homepage: www.elsevier.com/locate/jip Diversity of large DNA viruses of invertebrates ⇑ Trevor Williams a, Max Bergoin b, Monique M. van Oers c, a Instituto de Ecología AC, Xalapa, Veracruz 91070, Mexico b Laboratoire de Pathologie Comparée, Faculté des Sciences, Université Montpellier, Place Eugène Bataillon, 34095 Montpellier, France c Laboratory of Virology, Wageningen University, Droevendaalsesteeg 1, 6708 PB Wageningen, The Netherlands article info abstract Article history: In this review we provide an overview of the diversity of large DNA viruses known to be pathogenic for Received 22 June 2016 invertebrates. We present their taxonomical classification and describe the evolutionary relationships Revised 3 August 2016 among various groups of invertebrate-infecting viruses. We also indicate the relationships of the Accepted 4 August 2016 invertebrate viruses to viruses infecting mammals or other vertebrates. The shared characteristics of Available online 31 August 2016 the viruses within the various families are described, including the structure of the virus particle, genome properties, and gene expression strategies. Finally, we explain the transmission and mode of infection of Keywords: the most important viruses in these families and indicate, which orders of invertebrates are susceptible to Entomopoxvirus these pathogens. Iridovirus Ó Ascovirus 2016 Elsevier Inc. All rights reserved. Nudivirus Hytrosavirus Filamentous viruses of hymenopterans Mollusk-infecting herpesviruses 1. Introduction in the cytoplasm. This group comprises viruses in the families Poxviridae (subfamily Entomopoxvirinae) and Iridoviridae. The Invertebrate DNA viruses span several virus families, some of viruses in the family Ascoviridae are also discussed as part of which also include members that infect vertebrates, whereas other this group as their replication starts in the nucleus, which families are restricted to invertebrates. In this review we provide later degrades. All these viruses are discussed as one group an overview of the large DNA viruses known to be pathogenic for as they share evolutionary relationships and are placed invertebrate species. We define viruses as ‘‘large” when they have together in the proposed order Megavirales (Colson et al., a particle length or diameter over 100 nm. It is important to note 2013), that also contains viruses that infect protists (Mimiviri- that arthropods, in particular insects, mites and ticks, may also dae) or the symbiotic algae of such protists (Phycodnaviridae). serve as vectors for viruses that cause diseases in vertebrates and (b) Enveloped viruses with rod-shaped nucleocapsids and a large plants. Therefore, plant- and vertebrate-infecting viruses may also circular dsDNA genome that replicate and assemble in the replicate in blood-feeding and plant-sucking arthropods. Most of nucleus of infected cells. This group comprises viruses in the these vector-borne viruses are RNA viruses and will not be consid- families Baculoviridae, Nudiviridae, Hytrosaviridae and ered further. Exceptions include the DNA viruses in the genus Bego- Nimaviridae. We will also consider two not yet classified movirus (family Geminiviridae), which are transmitted by whiteflies dsDNA viruses of Hymenoptera, Leptopilina boulardi and infect a variety of plant species, but have a mutualistic rather filamentous virus and Apis mellifera filamentous virus in this than pathogenic relationship with their insect vector. group. The large DNA viruses that are pathogenic to invertebrates can (c) Viruses with icosahedral capsids surrounded by an envelope be divided in three main groups that share several characteristics and containing linear dsDNA. This group is formed by within each group (see also Fig. 1 and Supplementary Table S1): viruses in the family Malacoherpesviridae in the order Herpesvirales that infect ostreid and haliotid mollusks. (a) Eukaryotic nucleo-cytoplasmic large DNA viruses (NCLDVs) with a double stranded (ds) linear or circular genome that In the sections below we describe the general properties of the complete all or part of their replication and capsid assembly three known groups with large, autonomously replicating DNA viruses of invertebrates from a taxonomical perspective. For this, we have referred to the most recent Taxonomy Release from the ⇑ Corresponding author. International Committee on Taxonomy of Viruses (ICTV, 2015). We E-mail address: [email protected] (M.M. van Oers). http://dx.doi.org/10.1016/j.jip.2016.08.001 0022-2011/Ó 2016 Elsevier Inc. All rights reserved. T. Williams et al. / Journal of Invertebrate Pathology 147 (2017) 4–22 5 Fig. 1. Large invertebrate DNA virus diversity. Virus particle morphology is indicated per group. For the family Baculoviridae budded viruses (BV) (a) as well as occluded viruses (ODV) of GVs/SNPVs (b) and MNPVs (c) are depicted. The size of the occlusion body (OB, in gray) is not to scale (courtesy of Eugene Ryabov). will describe the evolutionary relationships between the viruses in insects. They share significant morphological and molecular similar- these groups and, where appropriate, their relationships to ities with their vertebrate counterparts, the chordopoxviruses vertebrate-infecting viruses. We will also examine how some of (ChPVs). The brick-shaped or ovoid mature EV virions the large DNA viruses of invertebrates relate to endogenous viral ele- (Figs. 1 and 2A) consist of three major components: an outer lipopro- ments in the genomes of parasitic wasps that provide these wasps tein envelope, one or two lateral bodies and a centrally positioned with the ability to produce polydnaviruses or virus-like particles. electron dense core containing the genome. The size of EV particles For detailed descriptions of the biological properties and how all varies from 250 to 400 nm in length and 150–250 nm in width. Their these viruses may relate to the food chain, we refer to the respective envelope is ornamented with globular prominent structures giving papers elsewhere in this special issue of the Journal of Invertebrate the particles a mulberry-like appearance. The lateral bodies occupy Pathology. For an overview of the small DNA viruses in inverte- the space between the envelope and the central core, which consists brates, including viruses belonging to the subfamily Densovirinae of a thick coat containing a folded cable-like structure surrounding in the family Parvoviridae, to the families Bidnaviridae and Circoviri- the viral DNA (Bergoin and Dales, 1971; Granados and Roberts, dae we refer to the respective manuscript by Tijssen et al. (this issue). 1970). Three morphotypes of EVs are observed that differ in the shape of the core (Granados, 1981). EVs infecting coleopterans exhi- 2. Nucleo-cytoplasmic large DNA viruses bit a kidney-shaped unilaterally concave core and a single lateral body located in its concavity (morphotype A). Those infecting lepi- 2.1. Entomopoxviruses dopterans and orthopterans possess a cylindrical core flanked by two discrete lateral bodies (morphotype B). EVs infecting dipterans 2.1.1. General characteristics possess a biconcave core flanked by two symmetrically positioned Entomopoxviruses (EVs) represent a homogeneous group of lateral bodies (morphotype C) resembling the typical dumbbell- large cytoplasmic dsDNA viruses that infect different orders of shaped core of vertebrate poxviruses. 6 T. Williams et al. / Journal of Invertebrate Pathology 147 (2017) 4–22 1964; Roberts and Granados, 1968; Vago and Bergoin, 1968). These inclusions consist of a proteinaceous crystalline lattice in which mature virions are occluded in a manner similar to the virions of baculoviruses and cypoviruses. Spheroids allow the virus to retain its infectivity in the environment, sometimes for months, between host generations. The major component of spheroids is a 110– 115 kDa cysteine-rich protein termed spheroidin (Hall and Moyer, 1991, 1993; Sanz et al., 1994). Bipyramidal-shaped inclu- sions, 1–10 lm in length, named spindles, are frequently observed in EV infections. They are devoid of virions and consist of a crystal of a 36–44 kDa cysteine-rich protein termed fusolin that shares significant homology with the GP37 baculovirus glycoprotein (Dall et al., 1993; Gauthier et al., 1995; Gross et al., 1993). In lepi- dopteran EVs spindles may be occluded along with virions in the spheroid matrix (Arif and Kurstak, 1991; Bird, 1974). 2.1.2. Host range and taxonomy EVs have been isolated from 40 different species of insects, mostly from the orders Lepidoptera, Coleoptera, Orthoptera, and Diptera (Arif and Kurstak, 1991; Granados, 1981), but also from Blattoidea (Radek and Fabel, 2000) and Hymenoptera (Lawrence, 2002). The host spectrum of EVs seems to be restricted to species of the same or closely related genera as that of the host from which they were isolated (Levin et al., 1993; Takatsuka et al., 2010). EVs are named after the host species from which they were isolated. For example, the EVs isolated from Melolontha melolontha is named Melolontha melolontha entomopoxvirus (MMEV). All EVs are clas- sified in the subfamily Entomopoxvirinae of the family Poxviridae (Skinner et al., 2011). They are assigned to three genera based on the shape of virion core and the insect order from which they were isolated: Alphaentomopoxvirus that infect Coleoptera, Betaento- mopoxvirus that infect Lepidoptera and Orthoptera and Gammaen- tomopoxvirus
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