Background:The Asian bush mosquitoAedes japonicusis rapidly invading North America and Europe. Due to its potential to transmit multiple pathogenic arthropod-borne (arbo)viruses including Zika virus, West Nile virus and chikungunya virus, it is important to understand the biology of this vector mosquito in more detail. In addition to arboviruses, mosquitoes can also carry insect-specific viruses that receive increasing attention due to their potential effects on host physiology and arbovirus transmission. In this study, we characterized the collection of viruses, referred to as the virome, circulating inAe. japonicuspopulations in the Netherlands and France.Results:Applying a small RNA-based metagenomic approach toAe. japonicus, we uncovered a distinct group of viruses present in samples from both the Netherlands and France. These included one known virus,Ae. japonicus narnavirus 1(AejapNV1), and three new virus species that we namedAe. japonicus totivirus 1(AejapTV1),Ae. japonicus anphevirus 1(AejapAV1) andAe. japonicus bunyavirus 1(AejapBV1). We also discovered sequences that were presumably derived from two additional novel viruses:Ae. japonicus bunyavirus 2(AejapBV2) andAe. japonicus rhabdovirus 1(AejapRV1). All six viruses induced strong RNA interference responses, including the production of 21 nucleotide sized small interfering RNAs, a signature of active replication in the host. Notably, AejapBV1 and AejapBV2 belong to different viral families, however, no RNA-dependent RNA polymerase sequence has been found for AejapBV2. Intriguingly, our small RNA-based approach identified a ~1 kb long ambigrammatic RNA that is associated with AejapNV1 as a secondary segment but showed no similarity to any sequence in public databases. We confirmed the presence of AejapNV1 primary and secondary segments, AejapTV1, AejapAV1 and AejapBV1 by reverse-transcriptase PCR in wild-caughtAe. japonicusmosquitoes. AejapNV1 and AejapTV1 were found at high prevalence (87-100%) in adult females, adult males and larvae.Conclusions:Using a small RNA-based, sequence-independent metagenomic strategy, we uncovered a conserved and prevalent virome amongAe. japonicusmosquito populations. The high prevalence of AejapNV1 and AejapTV1 across all tested mosquito life stages suggests that these viruses are intimately associated withAe. japonicusand may affect different aspects of the physiology of this vector mosquito.
Usutu virus (USUV) is a mosquito-borne flavivirus of African origin. Over the past decades, USUV has spread through Europe causing mass die-offs among multiple bird species. The natural transmission cycle of USUV involves Culex spp. mosquitoes as vectors and birds as amplifying hosts. Next to birds and mosquitoes, USUV has also been isolated from multiple mammalian species, including humans, which are considered dead-end hosts. USUV isolates are phylogenetically classified into an African and European branch, subdivided into eight genetic lineages (Africa 1, 2, and 3 and Europe 1, 2, 3, 4, and 5 lineages). Currently, multiple African and European lineages are co-circulating in Europe. Despite increased knowledge of the epidemiology and pathogenicity of the different lineages, the effects of co-infection and transmission efficacy of the co-circulating USUV strains remain unclear. In this study, we report a comparative study between two USUV isolates as follows: a Dutch isolate (USUV-NL, Africa lineage 3) and an Italian isolate (USUV-IT, Europe lineage 2). Upon co-infection, USUV-NL was consistently outcompeted by USUV-IT in mosquito, mammalian, and avian cell lines. In mosquito cells, the fitness advantage of USUV-IT was most prominently observed in comparison to the mammalian or avian cell lines. When Culex pipiens mosquitoes were orally infected with the different isolates, no overall differences in vector competence for USUV-IT and USUV-NL were observed. However, during the in vivo co-infection assay, it was observed that USUV-NL infectivity and transmission were negatively affected by USUV-IT but not vice versa.
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