A novel insect-infecting virga/nege-like virus group and its pervasive endogenization into insect genomes

Abstract

Insects are the host and vector of diverse viruses including those that infect vertebrates, plants, and fungi. Recent wide-scale transcriptomic analyses have uncovered the existence of a number of novel insect viruses belonging to an alphavirus-like superfamily (virgavirus/negevirus-related lineage). In this study, through an in silico search using publicly available insect transcriptomic data, we found numerous virus-like sequences related to insect virga/nege-like viruses. Phylogenetic analysis showed that these novel viruses and related virus-like sequences fill the major phylogenetic gaps between insect and plant virga/negevirus lineages. Interestingly, one of the phylogenetic clades represents a unique insect-infecting virus group. Its members encode putative coat proteins which contained a conserved domain similar to that usually found in the coat protein of plant viruses in the family Virgaviridae. Furthermore, we discovered endogenous viral elements (EVEs) related to virga/nege-like viruses in the insect genomes, which enhances our understanding on their evolution. Database searches using the sequence of one member from this group revealed the presence of EVEs in a wide range of insect species, suggesting that there has been prevalent infection by this virus group since ancient times. Besides, we present detailed EVE integration profiles of this virus group in some species of the Bombus genus of bee families. A large variation in EVE patterns among Bombus species suggested that while some integration events occurred after the species divergence, others occurred before it. Our analyses support the view that insect and plant virga/nege-related viruses might share common virus origin(s).

Endogenous Viral Elements Are Widespread in Arthropod Genomes and Commonly Give Rise to PIWI-Interacting RNAs

“…Previous studies have revealed the presence of EVEs related to plant-infecting viruses within arthropod genomes (14,35,36). Interestingly, many of these EVEs correspond to viral families known to contain viruses that are transmitted by insect vectors but that do not replicate within insects.…”

“…While we cannot draw conclusions regarding the origin of these EVEs related to plant viruses based on the present data, others have suggested that the phylogenetic position of such EVEs firmly within the known genetic diversity of plant viruses, as well as the fact that some plant virus-related EVEs encode putative proteins homologous to the movement proteins of plant viruses, indicates that they are derived from bona fide plant viruses rather than undocumented insect viruses (36). Yet others argue for the existence of ancient and undocumented viral families occupying phylogenetic gaps between insect-and plant-infecting viruses and that EVEs related to plant-infecting viruses may in fact be derived from novel families of insect-infecting viruses (35).…”

Virome Analysis of Aphid Populations That Infest the Barley Field: The Discovery of Two Novel Groups of Nege/Kita-Like Viruses and Other Novel RNA Viruses

“…Recently, the presence of several nege/kita-like viruses and related virus-like sequences, has been reported from invertebrate meta-transcriptome analyses or surveys of insect transcriptomic datasets (Shi et al, 2016a;Kondo et al, 2019). To further explore the presence of unknown nege/kitavirus-like sequences, we conducted tBlastN searches against publicly available TSA datasets using BARV-1 and BARV-2 sequences as queries.…”

“…Members of these two proposed genera, together with two proposed taxa of arthropod-restrictive viruses, "Nelorpivirus" and "Sandewavirus, " which all have non-segmented genomes, could be classified into a novel viral family or be assigned to the family Kitaviridae. However, it is to too early to establish a family for these viruses or to assign them into the Kitaviridae, because there is no reliable statistical support for these lineages within the currently available phylogenetic trees (Kallies et al, 2014;Nunes et al, 2017;Kondo et al, 2019;Ramos-González et al, 2020; Figure 3). The result of molecular phylogenetics indicate that the two major lineages of kitaviruses (cile/higreviruses and bulunerviruses) are not monophyletic, which all have two or multi-segmented RNA genomes and separately encode their replicase (RdRp) and SP24 family protein on the different segments (Locali-Fabris et al, 2006;Melzer et al, 2013;Hao et al, 2018), suggesting that genome segmentation possibly occurred independently during the evolution of kitaviruses.…”

“…(class Arachnida) (Tassi et al, 2017;Freitas-Astua et al, 2018). Recently, a meta-transcriptomic approach on invertebrates expanded the diversity of nege-and nege-like viruses infecting or associated with mosquitos and flies (Webster et al, 2015(Webster et al, , 2016Shi et al, 2017;Medd et al, 2018;Sadeghi et al, 2018;Pettersson et al, 2019) and other invertebrates (Shi et al, 2016a;Debat, 2017;Feng et al, 2017;Nunes et al, 2017;Schoonvaere et al, 2018;Kondo et al, 2019). Nevertheless, there is still very limited information about the relationships between negeviruses and kitaviruses and also the evolutionary history of these two virus groups.…”