Diversification of mammalian deltaviruses by host shifting

Bergner, L. M. , Orton, R. J. , Broos, A. , Tello, C., Becker, D. J., Carrera, J. E., Patel, A. H. , Biek, R. and Streicker, D. G. (2021) Diversification of mammalian deltaviruses by host shifting. Proceedings of the National Academy of Sciences of the United States of America, 118(3), e201990711. (doi: 10.1073/pnas.2019907118) (PMID:33397804) (PMCID:PMC7826387)

Abstract

Hepatitis delta virus (HDV) is an unusual RNA agent that replicates using host machinery but exploits hepatitis B virus (HBV) to mobilize its spread within and between hosts. In doing so, HDV enhances the virulence of HBV. How this seemingly improbable hyperparasitic lifestyle emerged is unknown, but it underpins the likelihood that HDV and related deltaviruses may alter other host–virus interactions. Here, we show that deltaviruses diversify by transmitting between mammalian species. Among 96,695 RNA sequence datasets, deltaviruses infected bats, rodents, and an artiodactyl from the Americas but were absent from geographically overrepresented Old World representatives of each mammalian order, suggesting a relatively recent diversification within the Americas. Consistent with diversification by host shifting, both bat and rodent-infecting deltaviruses were paraphyletic, and coevolutionary modeling rejected cospeciation with mammalian hosts. In addition, a 2-y field study showed common vampire bats in Peru were infected by two divergent deltaviruses, indicating multiple introductions to a single host species. One vampire bat-associated deltavirus was detected in the saliva of up to 35% of individuals, formed phylogeographically compartmentalized clades, and infected a sympatric bat, illustrating horizontal transmission within and between species on ecological timescales. Consistent absence of HBV-like viruses in two deltavirus-infected bat species indicated acquisitions of novel viral associations during the divergence of bat and human-infecting deltaviruses. Our analyses support an American zoonotic origin of HDV and reveal prospects for future cross-species emergence of deltaviruses. Given their peculiar life history, deltavirus host shifts will have different constraints and disease outcomes compared to ordinary animal pathogens.

• Item Type: Articles
• Status: Published
• Refereed: Yes
• Glasgow Author(s) Enlighten ID: Orton, Dr Richard and Biek, Professor Roman and Broos, Ms Alice and Streicker, Professor Daniel and Bergner, Dr Laura and Patel, Professor Arvind
• Authors: Bergner, L. M., Orton, R. J., Broos, A., Tello, C., Becker, D. J., Carrera, J. E., Patel, A. H., Biek, R., and Streicker, D. G.
• College/School: College of Medical Veterinary and Life Sciences > School of Infection & Immunity; College of Medical Veterinary and Life Sciences > School of Infection & Immunity > Centre for Virus Research; College of Medical Veterinary and Life Sciences > School of Biodiversity, One Health & Veterinary Medicine
• Journal Name: Proceedings of the National Academy of Sciences of the United States of America
• Publisher: National Academy of Sciences
• ISSN: 0027-8424
• ISSN (Online): 1091-6490
• Published Online: 04 January 2021
• Copyright Holders: Copyright © 2021 Bergner et al.
• First Published: First published in Proceedings of the National Academy of Sciences of the United States of America 118(3):e2019907118
• Publisher Policy: Reproduced in accordance with the publisher copyright policy

Project Code	Award No	Project Name	Principal Investigator	Funder's Name	Funder Ref	Lead Dept
169793		Managing viral emergence at the interface of bats and livestock	Daniel Streicker	Wellcome Trust (WELLCOTR)	102507/Z/13/ZR	Institute of Biodiversity, Animal Health and Comparative Medicine
		Viral Genomics and Bioinformatics	Andrew Davison	Medical Research Council (MRC)	MC_UU_12014/12	III-MRC-GU Centre for Virus Research