Identification of a reptile lyssavirus in Anolis allogus provided novel insights into lyssavirus evolution

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ORIGINAL PAPER

Identification of a reptile lyssavirus in Anolis allogus provided novel insights into lyssavirus evolution Masayuki Horie1,2   · Hiroshi Akashi3 · Masakado Kawata4 · Keizo Tomonaga2,5,6 Received: 19 September 2020 / Accepted: 21 October 2020 © Springer Science+Business Media, LLC, part of Springer Nature 2020

Abstract Lyssaviruses (genus Lyssavirus) are negative-strand RNA viruses belonging to the family Rhabdoviridae. Although a lyssalike virus (frog lyssa-like virus 1 [FLLV-1]), which is distantly related to lyssaviruses, was recently identified in frogs, a large phylogenetic gap exists between those viruses, and thus the evolution of lyssaviruses is unclear. In this study, we detected a lyssa-like virus from publicly available RNA-seq data obtained using the brain and skin of Anolis allogus (Spanish flag anole), which was designated anole lyssa-like virus 1 (ALLV-1), and determined its complete coding sequence. Via mapping analysis, we demonstrated that ALLV-1 was actively replicating in the original brain and skin samples. Phylogenetic analyses revealed that ALLV-1 is more closely related to lyssaviruses than FLLV-1. Overall, the topology of the tree is compatible with that of hosts, suggesting the long-term co-divergence of lyssa-like and lyssaviruses and vertebrates. The ψ region, which is a long 3′ untranslated region of unknown origin present in the G mRNA of lyssaviruses (approximately 400–700 nucleotides), is also present in the genome of ALLV-1, but it is much shorter (approximately 180 nucleotides) than those of lyssaviruses. Interestingly, FLLV-1 lacks the ψ region, suggesting that the ψ region was acquired after the divergence of the FLLV-1 and ALLV-1/lyssavirus lineages. To the best of our knowledge, this is the first report to identify a lyssa-like virus in reptiles, and thus, our findings provide novel insights into the evolution of lyssaviruses. Keywords Lyssavirus · Anolis allogus · Metaviromics

Introduction Edited by Zhen F. Fu. Electronic supplementary material  The online version of this article (https​://doi.org/10.1007/s1126​2-020-01803​-y) contains supplementary material, which is available to authorized users. * Masayuki Horie horie.masayuki.3m@kyoto‑u.ac.jp 1



Hakubi Center for Advanced Research, Kyoto University, Kyoto, Japan

2



Department of Virology, Institute for Frontier Life and Medical Sciences, Kyoto University, Kyoto, Japan

3

Faculty of Industrial Science and Technology, Tokyo University of Science, Tokyo, Japan

4

Graduate School of Life Sciences, Tohoku University, Sendai, Japan

5

Department of Mammalian Regulatory Network, Graduate School of Biostudies, Kyoto University, Kyoto, Japan

6

Department of Molecular Virology, Graduate School of Medicine, Kyoto University, Kyoto, Japan



Lyssaviruses (genus Lyssavirus) are negative-strand RNA viruses belonging to the family Rhabdoviridae of the order Mononegavirales [1]. Currently, this genus contains 17 species. Lyssaviruses are circulating in many mammalian species [1, 2], and many of these viruses