Abstract

Tissue samples from Australian carpet pythons (Morelia spilota) with neurological disease were screened for viruses using next-generation sequencing. Coding complete genomes of two bornaviruses were identified with the gene order 3’-N-X-P-G-M-L, representing a transposition of the G and M genes compared to other bornaviruses and most mononegaviruses. Use of these viruses to search available vertebrate genomes enabled recognition of further endogenous bornavirus-like elements (EBLs) in diverse placental mammals, including humans. Codivergence patterns and shared integration sites revealed an ancestral laurasiatherian EBLG integration (77 million years ago [MYA]) and a previously identified afrotherian EBLG integration (83 MYA). The novel python bornaviruses clustered more closely with these EBLs than with other exogenous bornaviruses, suggesting that these viruses diverged from previously known bornaviruses prior to the end-Cretaceous (K-Pg) extinction, 66 MYA. It is possible that EBLs protected mammals from ancient bornaviral disease, providing a selective advantage in the recovery from the K-Pg extinction. A degenerate PCR primer set was developed to detect a highly conserved region of the bornaviral polymerase gene. It was used to detect 15 more genetically distinct bornaviruses from Australian pythons that represent a group that is likely to contain a number of novel species.

Highlights

  • Bornaviruses are enveloped viruses with single stranded, negative sense, non-segmented, RNA genomes classified to the family Bornaviridae in the order Mononegavirales [1]

  • The prototypic bornavirus, Borna disease virus, was first detected in horses and sheep [8] but since a number of animal hosts have been found to be susceptible to bornavirus infection including rabbits, guinea pigs, macaques, chickens, quail, parrots, canaries, geese, ducks and swans [3, 4, 9,10,11,12,13,14]

  • We investigated whether the jungle carpet python virus (JCPV)–and southwest carpet python virus (SWCPV)–like EBLs were the result of a single integration event into an ancestral mammalian genome or the result of multiple independent integrations

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Summary

Introduction

Bornaviruses are enveloped viruses with single stranded, negative sense, non-segmented, RNA genomes classified to the family Bornaviridae in the order Mononegavirales [1]. The prototypic bornavirus, Borna disease virus (originally BDV, BoDV-1), was first detected in horses and sheep [8] but since a number of animal hosts have been found to be susceptible to bornavirus infection including rabbits, guinea pigs, macaques, chickens, quail, parrots, canaries, geese, ducks and swans [3, 4, 9,10,11,12,13,14]. It was thought that only “warm-blooded” animals (birds and mammals) were susceptible to bornavirus infection [7, 15]. Recent studies have shown that bornaviruses can infect non-avian reptiles. In 2014, a coding complete genome of a bornavirus was recovered from banked frozen tissue from a wild-caught Loveridge’s garter snake (Elapsoidea loveridgei), but no clinical or other data was associated with this sequence [19]. The host specificity, association with disease, zoonotic potential, and prevalence of these reptile bornaviruses is totally unknown

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