Virus discovery reveals frequent infection by diverse novel members of the Flaviviridae in wild lemurs
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.
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.
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).
- 4.Schwitzer C, Mittermeier RA, Rylands AB, et al (2017) Primates in peril: the world’s 25 most endangered primates, 2016–2018. In: IUCN SSC Primate Specialist Group PSG International Primatological Society IPS and Conservation International CI Bristol Zoological Society, Arlington, VAGoogle Scholar
- 12.Hartlage AS, Cullen JM, Kapoor A (2016) The strange, expanding world of animal hepaciviruses. Annu Rev Virol 3:53–75. https://doi.org/10.1146/annurev-virology-100114-055104 Google Scholar
- 34.SignalP 4.0: discriminating signal peptides from transmembrane regions | Nat Methods. https://www.nature.com/articles/nmeth.1701. Accessed 16 Jun 2018
- 35.Gupta R, Jung E, Brunak S (2004) Prediction of N-glycosylation sites in human proteins. http://www.cbs.dtu.dk/services/NetNGlyc/abstract.php. Accessed 18 Jun 2018
- 36.Chenna R, Sugawara H, Koike T et al (2003) Multiple sequence alignment with the Clustal series of programs. Nucleic Acids Res 31:3497–3500Google Scholar
- 41.Nei M, Gojobori T (1986) Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. Mol Biol Evol 3:418–426Google Scholar
- 46.Felsenstein J (1981) Evolutionary trees from DNA sequences: a maximum likelihood approach. J Mol Evol 17:368–376Google Scholar
- 47.Dean AG, Sullivan KM, Soe MM (2014) OpenEpi: Open Source Epidemiologic Statistics for Public HealthGoogle Scholar
- 50.Honda M, Brown EA, Lemon SM (1996) Stability of a stem-loop involving the initiator AUG controls the efficiency of internal initiation of translation on hepatitis C virus RNA. RNA 2:955–968Google Scholar
- 67.Gommery D, Ramanivosoa B, Faure M et al (2011) Les plus anciennes traces d’activités anthropiques de Madagascar sur des ossements d’hippopotames subfossiles d’Anjohibe (Province de Mahajanga). Oldest evidence of human activities in Madagascar on subfossil hippopotamus bones from Anjohibe (Mahajanga Province). Comptes Rendus Palevol 10:271–278. https://doi.org/10.1016/j.crpv.2011.01.006 Google Scholar
- 68.A refined chronology of prehistoric Madagascar and the demise of the megafauna—ScienceDirect. https://www.sciencedirect.com/science/article/pii/S0277379110002246. Accessed 2 Aug 2018
- 71.Tamura K, Nei M (1993) Estimation of the number of nucleotide substitutions in the control region of mitochondrial DNA in humans and chimpanzees. Mol Biol Evol 10:512–526Google Scholar
- 72.Tamura K (1992) Estimation of the number of nucleotide substitutions when there are strong transition-transversion and G + C-content biases. Mol Biol Evol 9:678–687Google Scholar