Abstract

BackgroundArthropod-borne viruses (arboviruses) transmitted by mosquito vectors cause many important emerging or resurging infectious diseases in humans including dengue, chikungunya and Zika. Understanding the co-evolutionary processes among viruses and vectors is essential for the development of novel transmission-blocking strategies. Episomal viral DNA fragments are produced from arboviral RNA upon infection of mosquito cells and adults. Additionally, sequences from insect-specific viruses and arboviruses have been found integrated into mosquito genomes.ResultsWe used a bioinformatic approach to analyse the presence, abundance, distribution, and transcriptional activity of integrations from 425 non-retroviral viruses, including 133 arboviruses, across the presently available 22 mosquito genome sequences. Large differences in abundance and types of viral integrations were observed in mosquito species from the same region. Viral integrations are unexpectedly abundant in the arboviral vector species Aedes aegypti and Ae. albopictus, in which they are approximately ~10-fold more abundant than in other mosquito species analysed. Additionally, viral integrations are enriched in piRNA clusters of both the Ae. aegypti and Ae. albopictus genomes and, accordingly, they express piRNAs, but not siRNAs.ConclusionsDifferences in the number of viral integrations in the genomes of mosquito species from the same geographic area support the conclusion that integrations of viral sequences is not dependent on viral exposure, but that lineage-specific interactions exist. Viral integrations are abundant in Ae. aegypti and Ae. albopictus, and represent a thus far underappreciated component of their genomes. Additionally, the genome locations of viral integrations and their production of piRNAs indicate a functional link between viral integrations and the piRNA pathway. These results greatly expand the breadth and complexity of small RNA-mediated regulation and suggest a role for viral integrations in antiviral defense in these two mosquito species.

Highlights

  • Arthropod-borne viruses transmitted by mosquito vectors cause many important emerging or resurging infectious diseases in humans including dengue, chikungunya and Zika

  • Anopheline species had a maximum of seven NIRVSloci, one NIRVS-locus was found in Cx. quinquefasciatus, NIRVS were detected in Ae. aegypti, and 72 were found in Ae. albopictus

  • Even if further studies are essential to clarify the effect of NIRVSderived PIWI-interacting RNA (piRNA) on mosquito immunity, our study clearly demonstrates that Ae. aegypti and Ae. albopictus have a high number of NIRVS in their genome, which confers heritable immune signals

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Summary

Introduction

Arthropod-borne viruses (arboviruses) transmitted by mosquito vectors cause many important emerging or resurging infectious diseases in humans including dengue, chikungunya and Zika. Mosquitoes of the Aedes and Culex genera within the Culicinae subfamily are the primary vectors of RNA viruses These viruses include taxa with different RNA genomic structures and replication strategies, but all are non-retroviral viruses [3]. Within the Aedes genus, Aedes aegypti and Aedes albopictus are the main arboviral vectors due to their broad geographic distribution, adaptation to breed in human habitats, and the wide number of viral species from different genera that they can vector [4, 5] These two mosquito species are able to efficiently transmit arboviruses of the genera Flavivirus (e.g. dengue [DENV], Zika [ZKV], Usutu, Japanese encephalitis and yellow fever virus), Alphavirus (e.g. chikungunya virus [CHIKV]), viruses of the Venezuelan equine encephalitis [VEE] and eastern equine encephalitis [EEE] complexes), Orthobunyavirus (e.G. Potosi, Cache Valley and La Crosse virus [LACV]), Phlebovirus (e.g. Rift Valley fever virus [RVFV])

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