Endogenous Bornavirus-like Elements in Bats: Evolutionary Insights from the Conserved Riboviral L-Gene in Microbats and Its Antisense Transcription in Myotis daubentonii

Author:

Ritsch Muriel12ORCID,Eulenfeld Tom123ORCID,Lamkiewicz Kevin12ORCID,Schoen Andreas4ORCID,Weber Friedemann4ORCID,Hölzer Martin25ORCID,Marz Manja1267ORCID

Affiliation:

1. RNA Bioinformatics and High-Throughput Analysis, Friedrich Schiller University Jena, 07743 Jena, Germany

2. European Virus Bioinformatics Center, 07743 Jena, Germany

3. Cluster of Excellence Balance of the Microverse, Friedrich Schiller University Jena, 07743 Jena, Germany

4. Institute for Virology, FB10-Veterinary Medicine, Justus Liebig University, 35392 Gießen, Germany

5. Genome Competence Center (MF1), Robert Koch Institute, 13353 Berlin, Germany

6. German Centre for Integrative Biodiversity Research (iDiv) Halle-Jena-Leipzig, 04103 Leipzig, Germany

7. Fritz Lipmann Institute-Leibniz Institute on Aging, 07745 Jena, Germany

Abstract

Bats are ecologically diverse vertebrates characterized by their ability to host a wide range of viruses without apparent illness and the presence of numerous endogenous viral elements (EVEs). EVEs are well preserved, expressed, and may affect host biology and immunity, but their role in bat immune system evolution remains unclear. Among EVEs, endogenous bornavirus-like elements (EBLs) are bornavirus sequences integrated into animal genomes. Here, we identified a novel EBL in the microbat Myotis daubentonii, EBLL-Cultervirus.10-MyoDau (short name is CV.10-MyoDau) that shows protein-level conservation with the L-protein of a Cultervirus (Wuhan sharpbelly bornavirus). Surprisingly, we discovered a transcript on the antisense strand comprising three exons, which we named AMCR-MyoDau. The active transcription in Myotis daubentonii tissues of AMCR-MyoDau, confirmed by RNA-Seq analysis and RT-PCR, highlights its potential role during viral infections. Using comparative genomics comprising 63 bat genomes, we demonstrate nucleotide-level conservation of CV.10-MyoDau and AMCR-MyoDau across various bat species and its detection in 22 Yangochiropera and 12 Yinpterochiroptera species. To the best of our knowledge, this marks the first occurrence of a conserved EVE shared among diverse bat species, which is accompanied by a conserved antisense transcript. This highlights the need for future research to explore the role of EVEs in shaping the evolution of bat immunity.

Funder

TMWWDG grant

Deutsche Forschungsgemeinschaft

European Union’s Horizon 2020 research and innovation program

Carl Zeiss Stiftung

Publisher

MDPI AG

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