Endogenous viral elements are widespread in arthropod genomes and commonly give rise to piRNAs

Abstract

Arthropod genomes contain sequences derived from integrations of DNA and non-retroviral RNA viruses. These sequences, known as endogenous viral elements (EVEs), have been acquired over the course of evolution and have been proposed to serve as a record of past viral infection. Recent evidence indicates that EVEs can function as templates for the biogenesis of PIWI-interacting RNAs (piRNAs) in some mosquito species and cell lines, raising the possibility that EVEs may function as a source of immunological memory in these organisms. However, whether EVEs are capable of acting as templates for piRNA production in other arthropod species is unknown. Here we used publically available genome assemblies and small RNA sequencing datasets to characterize the repertoire and function of EVEs across 48 arthropod genomes. We found that EVEs are widespread in arthropod genomes and primarily correspond to unclassified ssRNA viruses and viruses belonging to the Rhabdoviridae and Parvoviridae families. Additionally, EVEs were enriched in piRNA clusters in a majority of species and we found that production of primary piRNAs from EVEs is common, particularly for EVEs located within piRNA clusters. While we found evidence suggesting that piRNAs mapping to a number of EVEs are produced via the ping-pong cycle, potentially pointing towards a role for EVE-derived piRNAs during viral infection, limited nucleotide identity between currently described viruses and EVEs identified here likely limits the extent to which this process plays a role during infection with known viruses.

Genome-wide profiling of piRNAs in the whitefly Bemisia tabaci reveals cluster distribution and association with begomovirus transmission

“…Recent studies have demonstrated the adaptive antiviral immunity in the mosquito A . aegyti [43] as well as many of other arthropods [44] suggesting likely involvement of piRNAs in facilitating TYLCV transmission by the vector whitefly B . tabaci .…”

The dual lifestyle of genome‐integrating virophages in protists

“…In principle, viruses of any Baltimore class can eventually become part of a host genome, although at highly different frequencies. [44][45][46][47][48] Retroviral elements are the most abundant class of endogenous viruses in vertebrates because of the mandatory genome integration step of their replication cycles. 49,50 The retroviral RNA is delivered to the cytoplasm, reverse-transcribed, and the dsDNA genome migrates into the nucleus via nuclear pores or during cell division.…”

“…Mavirus joins an illustrious list of endogenous virus elements (EVEs) found in eukaryotic genomes. In principle, viruses of any Baltimore class can eventually become part of a host genome, although at highly different frequencies …”

Novel insights into endogenous RNA viral elements in Ixodes scapularis and other arbovirus vector genomes

“…Additionally, large-scale sequence analysis has shown that many of these NIRVS cluster within piRNA producing genomic regions and produce primary piRNAs (Whitfield et al. 2017; Ter Horst et al 2018). This suggests that NIRVS have a functional role, perhaps involving the piRNA pathway.…”