Endogenous Viral Elements in Shrew Genomes Provide Insights into Pestivirus Ancient History

Author:

Li Yiqiao1ORCID,Bletsa Magda1ORCID,Zisi Zafeiro1,Boonen Ine1,Gryseels Sophie12,Kafetzopoulou Liana13,Webster Joanne P4,Catalano Stefano4,Pybus Oliver G4ORCID,Van de Perre Frederik2,Li Haotian5,Li Yaoyao5,Li Yuchun5,Abramov Alexei6,Lymberakis Petros7ORCID,Lemey Philippe1ORCID,Lequime Sébastian18ORCID

Affiliation:

1. Department of Microbiology, Immunology and Transplantation, Rega Institute , KU Leuven, 3000 Leuven , Belgium

2. Belgium Evolutionary Ecology Group, University of Antwerp , 2610 Wilrijk , Belgium

3. Virology Department, Belgium Bernhard Nocht Institute for Tropical Medicine , 20359 Hamburg , Germany

4. Department of Pathobiology and Population Science, Royal Veterinary College, University of London , Herts, AL9 7TA , UK

5. Marine College, Shandong University (Weihai) , 264209 Weihai , China

6. Laboratory of Theriology, Zoological Institute of the Russian Academy of Sciences , 190121 Saint Petersburg , Russia

7. Natural History Museum of Crete , Iraklio 712 02 , Greece

8. Cluster of Microbial Ecology, Groningen Institute for Evolutionary Life Sciences, University of Groningen , 9747 AG Groningen , the Netherlands

Abstract

Abstract As viral genomic imprints in host genomes, endogenous viral elements (EVEs) shed light on the deep evolutionary history of viruses, ancestral host ranges, and ancient viral–host interactions. In addition, they may provide crucial information for calibrating viral evolutionary timescales. In this study, we conducted a comprehensive in silico screening of a large data set of available mammalian genomes for EVEs deriving from members of the viral family Flaviviridae, an important group of viruses including well-known human pathogens, such as Zika, dengue, or hepatitis C viruses. We identified two novel pestivirus-like EVEs in the reference genome of the Indochinese shrew (Crocidura indochinensis). Homologs of these novel EVEs were subsequently detected in vivo by molecular detection and sequencing in 27 shrew species, including 26 species representing a wide distribution within the Crocidurinae subfamily and one in the Soricinae subfamily on different continents. Based on this wide distribution, we estimate that the integration event occurred before the last common ancestor of the subfamily, about 10.8 million years ago, attesting to an ancient origin of pestiviruses and Flaviviridae in general. Moreover, we provide the first description of Flaviviridae-derived EVEs in mammals even though the family encompasses numerous mammal-infecting members. This also suggests that shrews were past and perhaps also current natural reservoirs of pestiviruses. Taken together, our results expand the current known Pestivirus host range and provide novel insight into the ancient evolutionary history of pestiviruses and the Flaviviridae family in general.

Funder

European Union’s Horizon 2020

Research Foundation – Flanders

Ministry of Science and Higher Education of the Russian Federation

National Natural Science Foundation of China

Research Foundation– Flanders

UK Research and Innovation

Emerging Livestock Systems

Publisher

Oxford University Press (OUP)

Subject

Genetics,Molecular Biology,Ecology, Evolution, Behavior and Systematics

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