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Cell Host Microbe. 2017 Sep 13;22(3):387-399.e6. doi: 10.1016/j.chom.2017.07.019. Epub 2017 Aug 31.

Deciphering the Origin and Evolution of Hepatitis B Viruses by Means of a Family of Non-enveloped Fish Viruses.

Author information

1
Institute for Medical Informatics and Biometry, Technische Universität Dresden, 01307 Dresden, Germany.
2
University of Heidelberg, Department of Infectious Diseases, Molecular Virology, 69120 Heidelberg, Germany. Electronic address: stefan.seitz@med.uni-heidelberg.de.
3
Structural and Computational Biology Unit, European Molecular Biology Laboratory, 69117 Heidelberg, Germany.
4
Department of Evolutionary Biology, Evolutionary Biology Centre (EBC), Uppsala University, 75236 Uppsala, Sweden.
5
Department of Internal Medicine 2/Molecular Biology, University Hospital Freiburg, 79106 Freiburg, Germany.
6
Department of Psychiatry and the Behavioral Sciences, Keck School of Medicine, University of Southern California, Los Angeles, CA 90033, USA.
7
University of Heidelberg, Department of Infectious Diseases, Molecular Virology, 69120 Heidelberg, Germany.
8
Zoological Institute, University of Basel, 4051 Basel, Switzerland.
9
Institute for Medical Informatics and Biometry, Technische Universität Dresden, 01307 Dresden, Germany; Institute for Bioinformatics, University Medicine Greifswald, 17487 Greifswald, Germany.
10
University of Heidelberg, Department of Infectious Diseases, Molecular Virology, 69120 Heidelberg, Germany; Division of Virus-Associated Carcinogenesis, German Cancer Research Center (DKFZ), 69120 Heidelberg, Germany.

Abstract

Hepatitis B viruses (HBVs), which are enveloped viruses with reverse-transcribed DNA genomes, constitute the family Hepadnaviridae. An outstanding feature of HBVs is their streamlined genome organization with extensive gene overlap. Remarkably, the ∼1,100 bp open reading frame (ORF) encoding the envelope proteins is fully nested within the ORF of the viral replicase P. Here, we report the discovery of a diversified family of fish viruses, designated nackednaviruses, which lack the envelope protein gene, but otherwise exhibit key characteristics of HBVs including genome replication via protein-primed reverse-transcription and utilization of structurally related capsids. Phylogenetic reconstruction indicates that these two virus families separated more than 400 million years ago before the rise of tetrapods. We show that HBVs are of ancient origin, descending from non-enveloped progenitors in fishes. Their envelope protein gene emerged de novo, leading to a major transition in viral lifestyle, followed by co-evolution with their hosts over geologic eras.

KEYWORDS:

hepadnaviruses; hepatitis B virus; overlapping open reading frames; viral gene evolution; virus discovery; virus origins; virus-host long-term co-evolution

PMID:
28867387
PMCID:
PMC5604429
DOI:
10.1016/j.chom.2017.07.019
[Indexed for MEDLINE]
Free PMC Article

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