Ancient origin of Jingchuvirales derived glycoproteins integrated in arthropod genomes

Abstract

Endogenous virus elements (EVEs) are viral-derived sequences integrated into their host genomes. EVEs of the Jingchuvirales order were detected in a wide range of insect genomes covering several distantly related families. Moreover, Jingchuvirales -derived glycoproteins were recently associated by our group with the origin of a putative new retrovirus based on a glycoprotein captured by a mosquito retrotransposon. But, except for mosquitoes, there is a lack of a more detailed understanding of the endogenization mechanism, timing, and frequency per Jingchuvirales viral lineages. Here we screened Jingchuvirales glycoprotein-derived EVEs (Jg-EVEs) in eukaryotic genomes. We found six distinct endogenization events of Jg-EVEs, that belong to two out of five known Jingchuvirales families ( Chuviridae and Natareviridae ). For seven arthropod families bearing Jg-EVEs there is no register of bona fide circulating chuvirus infection. Hence, our results show that Jingchuvirales viruses infected or still infect these host families. Although we found abundant evidence of LTR-Gypsy retrotransposons fragments associated with the glycoprotein in Hymenoptera and other insect orders, our results show that the widespread distribution of Jingchuvirales glycoproteins in extant Arhtropods is a result of multiple ancient endogenization events and that these virus fossils are being vertically inherited in Arthropods genomes for millions of years.

EEfinder, a tool for identification of bacterial and viral endogenized elements in eukaryotic genomes

“…In the final step, EEfinder extracts the flanks of each element, with the length adjustable by the user ( Figure 1-VI) . These flanks can be utilized in further analyses, such as gene orthology, transposon searches, or host gene identification 17,21 .…”

Endogenous Viral Elements in Ixodid Tick Genomes

“…The order Jingchuvirales was characterized in 2015 and elevated in 2018 as a sister order to Mononegavirales that contains viruses (most of which are placed in the family Chuviridae) broadly dispersed throughout multiple arthropod orders [64,65]. (Chuviral-like endogenous viral elements have been identified throughout an equally broad array of 15 arthropod families and one nematode, with enrichment of glycoprotein genes in select insect lineages associated with retrotransposons that facilitated their capture and amplification [66], indicating that these viruses have had long-standing and ancient associations with invertebrates.) Our analysis identified six well-supported and independent lineages of Chuviridae EVEs within tick genomes: (1) a glycoprotein-encoding element with homology to Blacklegged tick chuvirus-2 (genus Nigecruvirus) in all three Ixodes species studied; (2) a lineage of elements with top hits to ORF3 (otherwise reported as a nucleoprotein, N gene) of the previous Nigecruvirus contained in the same Ixodes species; (3) a lineage comprising ORF3/hypothetical protein-encoding elements with top hits to members of genus Mivirus in all three Ixodes species, sister to a single Morsuvirus-like element detected in I. persulcatus; (4) a glycoprotein-encoding element from the three Ixodes species with homology to the latter Mivirus strains; (5) a nucleoprotein-encoding element with top hits to various Mivirus strains present in all three Rhipicephalus species examined + D. silvarum and H. longicornis; and ( 6) an RNA-dependent RNA polymerase-encoding element with top hits to various Mivirus strains detected in H. longicornis and I. ricinus (Figure 10A-F, respectively).…”