A Novel Orthohepadnavirus Identified in a Dead Maxwell’s Duiker (Philantomba maxwellii) in Taï National Park, Côte d’Ivoire

New technologies enable viral discovery in a diversity of hosts, providing insights into viral evolution. We used one such approach, the virome capture sequencing for vertebrate viruses (VirCapSeq-VERT) platform, on 21 samples originating from six dead Maxwell’s duikers (Philantomba maxwellii) from Taï National Park, Côte d’Ivoire. We detected the presence of an orthohepadnavirus in one animal and characterized its 3128 bp genome. The highest viral copy numbers were detected in the spleen, followed by the lung, blood, and liver, with the lowest copy numbers in the kidney and heart; the virus was not detected in the jejunum. Viral copy numbers in the blood were in the range known from humans with active chronic infections leading to liver histolytic damage, suggesting this virus could be pathogenic in duikers, though many orthohepadnaviruses appear to be apathogenic in other hosts, precluding a formal test of this hypothesis. The virus was not detected in 29 other dead duiker samples from the Côte d’Ivoire and Central African Republic, suggesting either a spillover event or a low prevalence in these populations. Phylogenetic analysis placed the virus as a divergent member of the mammalian clade of orthohepadnaviruses, though its relationship to other orthohepadnaviruses remains uncertain. This represents the first orthohepadnavirus described in an artiodactyl. We have tentatively named this new member of the genus Orthohepadnavirus (family Hepadnaviridae), Taï Forest hepadnavirus. Further studies are needed to determine whether it, or some close relatives, are present in a broader range of artiodactyls, including livestock.

[1]  J. R. Rebello Pinho,et al.  A novel hepatitis B virus species discovered in capuchin monkeys sheds new light on the evolution of primate hepadnaviruses. , 2018, Journal of hepatology.

[2]  M. Shi,et al.  A Novel Hepadnavirus Identified in an Immunocompromised Domestic Cat in Australia , 2018, Viruses.

[3]  M. Suchard,et al.  Posterior Summarization in Bayesian Phylogenetics Using Tracer 1.7 , 2018, Systematic biology.

[4]  Daniel L. Ayres,et al.  Bayesian phylogenetic and phylodynamic data integration using BEAST 1.10 , 2018, Virus evolution.

[5]  E. Holmes,et al.  Extensive diversity and evolution of hepadnaviruses in bats in China , 2017, Virology.

[6]  L. Kaderali,et al.  Deciphering the Origin and Evolution of Hepatitis B Viruses by Means of a Family of Non-enveloped Fish Viruses , 2017, Cell host & microbe.

[7]  R. Wittig,et al.  Low antibody prevalence against Bacillus cereus biovar anthracis in Taï National Park, Côte d'Ivoire, indicates high rate of lethal infections in wildlife , 2017, PLoS neglected tropical diseases.

[8]  Kevin E. Langergraber,et al.  Persistent anthrax as a major driver of wildlife mortality in a tropical rainforest , 2017, Nature.

[9]  O. Gascuel,et al.  SMS: Smart Model Selection in PhyML , 2017, Molecular biology and evolution.

[10]  Yan Zhu,et al.  Detection and genome characterization of four novel bat hepadnaviruses and a hepevirus in China , 2017, Virology Journal.

[11]  K. Grützmacher,et al.  Codetection of Respiratory Syncytial Virus in Habituated Wild Western Lowland Gorillas and Humans During a Respiratory Disease Outbreak , 2016, EcoHealth.

[12]  E. Holmes,et al.  Distinct Viral Lineages from Fish and Amphibians Reveal the Complex Evolutionary History of Hepadnaviruses , 2016, Journal of Virology.

[13]  J. Drexler,et al.  Bat hepadnaviruses and the origins of primate hepatitis B viruses. , 2016, Current opinion in virology.

[14]  Andrew Rambaut,et al.  Exploring the temporal structure of heterochronous sequences using TempEst (formerly Path-O-Gen) , 2016, Virus evolution.

[15]  W. Lipkin,et al.  Virome Capture Sequencing Enables Sensitive Viral Diagnosis and Comprehensive Virome Analysis , 2015, mBio.

[16]  B. He,et al.  Identification of a novel orthohepadnavirus in pomona roundleaf bats in China , 2014, Archives of Virology.

[17]  C. Boesch,et al.  The ecology of primate retroviruses - an assessment of 12 years of retroviral studies in the Taï national park area, Côte d׳Ivoire. , 2014, Virology.

[18]  Björn Usadel,et al.  Trimmomatic: a flexible trimmer for Illumina sequence data , 2014, Bioinform..

[19]  M. Tschapka,et al.  Bats carry pathogenic hepadnaviruses antigenically related to hepatitis B virus and capable of infecting human hepatocytes , 2013, Proceedings of the National Academy of Sciences.

[20]  Wei Qiu,et al.  Hepatitis Virus in Long-Fingered Bats, Myanmar , 2013, Emerging infectious diseases.

[21]  Heng Li Aligning sequence reads, clone sequences and assembly contigs with BWA-MEM , 2013, 1303.3997.

[22]  K. Katoh,et al.  MAFFT Multiple Sequence Alignment Software Version 7: Improvements in Performance and Usability , 2013, Molecular biology and evolution.

[23]  Sergey I. Nikolenko,et al.  SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing , 2012, J. Comput. Biol..

[24]  Shane S. Sturrock,et al.  Geneious Basic: An integrated and extendable desktop software platform for the organization and analysis of sequence data , 2012, Bioinform..

[25]  A. Nitsche,et al.  Multicolour, multiplex real-time PCR assay for the detection of human-pathogenic poxviruses. , 2010, Molecular and cellular probes.

[26]  O. Gascuel,et al.  SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. , 2010, Molecular biology and evolution.

[27]  A. Rambaut,et al.  BEAST: Bayesian evolutionary analysis by sampling trees , 2007, BMC Evolutionary Biology.

[28]  W. Karesh,et al.  Wild Animal Mortality Monitoring and Human Ebola Outbreaks, Gabon and Republic of Congo, 2001–2003 , 2005, Emerging infectious diseases.

[29]  P. Formenty,et al.  Multiple Ebola Virus Transmission Events and Rapid Decline of Central African Wildlife , 2004, Science.

[30]  E. Holmes,et al.  Geographic and species association of hepatitis B virus genotypes in non-human primates. , 2003, Virology.

[31]  F. Rousseau,et al.  Serum HBV DNA as a marker of efficacy during therapy for chronic HBV infection: Analysis and review of the literature , 2003, Hepatology.

[32]  W. Gerlich,et al.  Universal primers for real-time amplification of DNA from all known Orthohepadnavirus species. , 2003, Journal of clinical virology : the official publication of the Pan American Society for Clinical Virology.

[33]  F. Hufert,et al.  Molecular Epidemiology of Hepatitis B Virus Variants in Nonhuman Primates , 2000, Journal of Virology.

[34]  P. D. Hodgson,et al.  Posttranscriptional Inhibition of Class I Major Histocompatibility Complex Presentation on Hepatocytes and Lymphoid Cells in Chronic Woodchuck Hepatitis Virus Infection , 2000, Journal of Virology.

[35]  A. Prince,et al.  Full-genome sequence analyses of hepatitis B virus (HBV) strains recovered from chimpanzees infected in the wild: implications for an origin of HBV. , 2000, Virology.

[36]  R. Rico-Hesse,et al.  Isolation of a hepadnavirus from the woolly monkey, a New World primate. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[37]  M. Buendia,et al.  A new hepadnavirus endemic in arctic ground squirrels in Alaska , 1996, Journal of virology.

[38]  C. Boesch,et al.  Isolation and partial characterisation of a new strain of Ebola virus , 1995, The Lancet.

[39]  B. Tennant,et al.  Lymphoid cells in the spleens of woodchuck hepatitis virus-infected woodchucks are a site of active viral replication , 1987, Journal of virology.

[40]  H. Varmus,et al.  Nucleotide sequence of an infectious molecularly cloned genome of ground squirrel hepatitis virus , 1984, Journal of virology.

[41]  P. Marion,et al.  A virus in Beechey ground squirrels that is related to hepatitis B virus of humans. , 1980, Proceedings of the National Academy of Sciences of the United States of America.

[42]  J. Summers,et al.  A virus similar to human hepatitis B virus associated with hepatitis and hepatoma in woodchucks. , 1978, Proceedings of the National Academy of Sciences of the United States of America.

[43]  S. Locarnini,et al.  Origins and Evolution of Hepatitis B Virus and Hepatitis D Virus. , 2016, Cold Spring Harbor perspectives in medicine.