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Virus discovery reveals frequent infection by diverse novel members of the Flaviviridae in wild lemurs

  • Marta Canuti
  • Cathy V. Williams
  • Selena M. Sagan
  • Bas B. Oude Munnink
  • Sashi Gadi
  • Joost T. P. Verhoeven
  • Paul Kellam
  • Matthew Cotten
  • Andrew S. Lang
  • Randall E. Junge
  • John M. Cullen
  • Lia van der Hoek
Original Article

Abstract

Lemurs are highly endangered mammals inhabiting the forests of Madagascar. In this study, we performed virus discovery on serum samples collected from 84 wild lemurs and identified viral sequence fragments from 4 novel viruses within the family Flaviviridae, including members of the genera Hepacivirus and Pegivirus. The sifaka hepacivirus (SifHV, two genotypes) and pegivirus (SifPgV, two genotypes) were discovered in the diademed sifaka (Propithecus diadema), while other pegiviral fragments were detected in samples from the indri (Indri indri, IndPgV) and the weasel sportive lemur (Lepilemur mustelinus, LepPgV). Although data are preliminary, each viral species appeared host species-specific and frequent infection was detected (18 of 84 individuals were positive for at least one virus). The complete coding sequence and partial 5’ and 3’ untranslated regions (UTRs) were obtained for SifHV and its genomic organization was consistent with that of other hepaciviruses, with one unique polyprotein and highly structured UTRs. Phylogenetic analyses showed the SifHV belonged to a clade that includes several viral species identified in rodents from Asia and North America, while SifPgV and IndPgV were more closely related to pegiviral species A and C, that include viruses found in humans as well as New- and Old-World monkeys. Our results support the current proposed model of virus-host co-divergence with frequent occurrence of cross-species transmission for these genera and highlight how the discovery of more members of the Flaviviridae can help clarify the ecology and evolutionary history of these viruses. Furthermore, this knowledge is important for conservation and captive management of lemurs.

Notes

Acknowledgements

This study was supported by funding from the European Community’s Seventh Framework Programme (FP7/2007–2013) under the project EMPERIE, EC Grant agreement number 223498.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

Sampling was conducted in accordance with all applicable rules and regulations for conducting research on wildlife in Madagascar and research permits were issued by the Secretariat General, Direction Generale des Foret (permit numbers: 215/07, 149/08, 161/08, 018/09, 098/09, 197/13).

Supplementary material

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Supplementary material 1 (PDF 1628 kb)

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Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2018

Authors and Affiliations

  1. 1.Department of BiologyMemorial University of NewfoundlandSt. John’sCanada
  2. 2.Duke Lemur CenterDuke UniversityDurhamUSA
  3. 3.Department of Microbiology and ImmunologyMcGill UniversityMontréalCanada
  4. 4.Department of BiochemistryMcGill UniversityMontréalCanada
  5. 5.Laboratory of Experimental Virology, Department of Medical MicrobiologyAcademic Medical Center of the University of AmsterdamAmsterdamNetherlands
  6. 6.Department of Population Health and Pathobiology, College of Veterinary MedicineNorth Carolina State UniversityRaleighUSA
  7. 7.The Wellcome Trust Sanger Institute, Wellcome Genome CampusCambridgeUK
  8. 8.Department of Animal HealthColumbus Zoo and AquariumPowellUSA
  9. 9.Department of ViroscienceErasmus MCRotterdamThe Netherlands
  10. 10.Division of Infectious Diseases, Department of MedicineImperial College LondonLondonUK

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