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.

摘要：内源病毒元件（Endogenous Virus Elements, EVEs）是整合至宿主基因组内的病毒衍生序列。京楚病毒目（Jingchuvirales）的内源病毒元件已在多个亲缘关系较远的昆虫类群基因组中被检测到。此外，我们团队近期基于某蚊类逆转录转座子（retrotransposon）捕获的糖蛋白（glycoprotein）序列，证实京楚病毒目来源的糖蛋白与一种潜在新型逆转录病毒的起源存在关联。不过，除蚊类外，目前学界对京楚病毒目各病毒谱系的内源化机制、发生时序与发生频率仍缺乏深入认知。为此，本研究对真核生物基因组中的京楚病毒目糖蛋白衍生内源病毒元件（Jg-EVEs）进行了系统筛选。本研究共检测到6次独立的Jg-EVEs内源化事件，这些事件分属于目前已报道的5个京楚病毒目科中的2个：楚病毒科（Chuviridae）与纳塔病毒科（Natareviridae）。其中，7个携带Jg-EVEs的节肢动物类群，此前并无其感染真正循环性楚病毒的记录。据此可知，京楚病毒目病毒曾感染或仍可感染这些宿主类群。尽管我们在膜翅目及其他昆虫类群中发现了大量与糖蛋白相关的长末端重复序列-吉普赛逆转录转座子（LTR-Gypsy retrotransposons）片段，但本研究结果表明，京楚病毒目糖蛋白在现存节肢动物中的广泛分布，源于多次古老的内源化事件，且这些病毒"化石"已在节肢动物基因组中垂直传递了数百万年。