A Unique Nodavirus with Novel Features: Mosinovirus Expresses Two Subgenomic RNAs, a Capsid Gene of Unknown Origin, and a Suppressor of the Antiviral RNA Interference Pathway

Abstract

Insects are a reservoir for many known and novel viruses. We discovered an unknown virus, tentatively named mosinovirus (MoNV), in mosquitoes from a tropical rainforest region in Côte d'Ivoire. The MoNV genome consists of two segments of positive-sense RNA of 2,972 nucleotides (nt) (RNA 1) and 1,801 nt (RNA 2). Its putative RNA-dependent RNA polymerase shares 43% amino acid identity with its closest relative, that of the Pariacoto virus (family Nodaviridae). Unexpectedly, for the putative capsid protein, maximal pairwise identity of 16% to Lake Sinai virus 2, an unclassified virus with a nonsegmented RNA genome, was found. Moreover, MoNV virions are nonenveloped and about 50 nm in diameter, larger than any of the known nodaviruses. Mature MoNV virions contain capsid proteins of ϳ56 kDa, which do not seem to be cleaved from a longer precursor. Northern blot analyses revealed that MoNV expresses two subgenomic RNAs of 580 nt (RNA 3) and 292 nt (RNA 4). RNA 4 encodes a viral suppressor of RNA interference (RNAi) that shares its mechanism with the B2 RNAi suppressor protein of other nodaviruses despite lacking recognizable similarity to these proteins. MoNV B2 binds long double-stranded RNA (dsRNA) and, accordingly, inhibits Dicer-2-mediated processing of dsRNA into small interfering RNAs (siRNAs). Phylogenetic analyses indicate that MoNV is a novel member of the family Nodaviridae that acquired its capsid gene via reassortment from an unknown, distantly related virus beyond the family level. IMPORTANCEThe identification of novel viruses provides important information about virus evolution and diversity. Here, we describe an unknown unique nodavirus in mosquitoes, named mosinovirus (MoNV). MoNV was classified as a nodavirus based on its genome organization and on phylogenetic analyses of the RNA-dependent RNA polymerase. Notably, its capsid gene was acquired from an unknown virus with a distant relationship to nodaviruses. Another remarkable feature of MoNV is that, unlike other nodaviruses, it expresses two subgenomic RNAs (sgRNAs). One of the sgRNAs expresses a protein that counteracts antiviral defense of its mosquito host, whereas the function of the other sgRNA remains unknown. Our results show that complete genome segments can be exchanged beyond the species level and suggest that insects harbor a large repertoire of exceptional viruses.

Genome sequence heterogeneity of Lake Sinai Virus found in honey bees and Orf1/RdRP-based polymorphisms in a single host

“…They have a different genome organization, leading to the proposition of the genus Sinaivirus for the LSVs and Chroparavirus for AACV and CBPV (Kuchibhatla et al, 2014). The capsid protein from Mosinovirus (MoNV) is also related to the LSVs, although this virus is taxonomically placed within the Nodavirirdae based on its RdRP protein (Schuster et al, 2014).…”

Viral gut metagenomics of sympatric wild and domestic canids, and monitoring of viruses: Insights from an endangered wolf population

“…Alphanodaviruses have been mostly isolated from insects, opposing to betanodaviruses which infect fish and are responsible for viral nervous necrosis in several species (Bailey & Scott, ; Shetty, Maiti, Shivakumar Santhosh, Venugopal, & Karunasagar, ). We tentatively named the virus caninovirus (Canine nodavirus), as previously done for Mosinovirus virus (mosquito nodavirus; Schuster et al., ; 2I). The capsid of caninovirus shares its highest similarity with the Pariacoto virus (63.3% aa), which was isolated from a southern armyworm in Peru (Figure j).…”

Comparative genome analysis reveals a distinct influence of nucleotide composition on virus–host species‐specific interaction of prawn‐infecting nodavirus

“…The nucleotide composition at non‐synonymous and synonymous codon positions of RdRp and capsid of the nodavirus was analysed and compared in order to comprehend the properties and fundamental characteristic of the nodavirus genome. Due to the extreme divergence between RdRp and capsid of the mosinovirus (MoNV) that was reported recently (Domingo, Sheldon, & Perales, ; Schuster et al, ), the two RNA segments of the nodavirus were analysed separately in detail in the current analysis that is different from the previous studies (He & Teng, ; Kapoor, Simmonds, Lipkin, Zaidi, & Delwart, ; Schuster et al, ; Tyagi, Kumar, & Singh, ). The phylogenetic data classified MoNV as a novel member of alphanodavirus based on similar RdRp gene properties.…”

“…The phylogenetic data classified MoNV as a novel member of alphanodavirus based on similar RdRp gene properties. Owing to the theory of viral quasispecies evolution, MoNV is most likely acquired its unique capsid gene via reassortment from an unknown virus beyond the family level (Domingo et al, ; Schuster et al, ). A further study on the nodavirus genome organization should, therefore, be carried out.…”