Discovery of Jogalong virus, a novel hepacivirus identified in a Culex annulirostris (Skuse) mosquito from the Kimberley region of Western Australia

Autoři: Simon H. Williams aff001;  Avram Levy aff003;  Rachel A. Yates aff001;  Nilusha Somaweera aff004;  Peter J. Neville aff004;  Jay Nicholson aff004;  Michael D. A. Lindsay aff004;  John S. Mackenzie aff003;  Komal Jain aff001;  Allison Imrie aff002;  David W. Smith aff002;  W. Ian Lipkin aff001
Působiště autorů: Center for Infection and Immunity, Mailman School of Public Health of Columbia University, New York, New York, United States of America aff001;  Faculty of Health and Medical Sciences, University of Western Australia, Nedlands, Western Australia, Australia aff002;  PathWest Laboratory Medicine WA, Nedlands, Western Australia, Australia aff003;  Environmental Health Directorate, Public and Aboriginal Health Division, Department of Health, Western Australia, Perth, Western Australia, Australia aff004;  Faculty of Health Sciences, Curtin University, Perth, Western Australia, Australia aff005
Vyšlo v časopise: PLoS ONE 15(1)
Kategorie: Research Article


The discovery of hepaciviruses in non-human hosts has accelerated following the advancement of high-throughput sequencing technology. Hepaciviruses have now been described in reptiles, fish, birds, and an extensive array of mammals. Using metagenomic sequencing on pooled samples of field-collected Culex annulirostris mosquitoes, we discovered a divergent hepacivirus-like sequence, named Jogalong virus, from the Kimberley region in northern Western Australia. Using PCR, we screened the same 300 individual mosquitoes and found just a single positive sample (1/300, 0.33%). Phylogenetic analysis of the hepacivirus NS5B protein places Jogalong virus within the genus Hepacivirus but on a distinct and deeply rooted monophyletic branch shared with duck hepacivirus, suggesting a notably different evolutionary history. Vertebrate barcoding PCR targeting two mitochondrial genes, cytochrome c oxidase subunit I and cytochrome b, indicated that the Jogalong virus-positive mosquito had recently fed on the tawny frogmouth (Podargus strigoides), although it is currently unknown whether this bird species contributes to the natural ecology of this virus.

Klíčová slova:

Birds – Blood – Ducks – Hepacivirus – Mosquitoes – Phylogenetic analysis – Polymerase chain reaction – Sequence assembly tools


1. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis. 2005;5(9):558–67. doi: 10.1016/S1473-3099(05)70216-4 16122679

2. Firth C, Bhat M, Firth MA, Williams SH, Frye MJ, Simmonds P, et al. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. MBio. 2014;5(5):e01933–14. doi: 10.1128/mBio.01933-14 25316698

3. Kapoor A, Simmonds P, Scheel TK, Hjelle B, Cullen JM, Burbelo PD, et al. Identification of rodent homologs of hepatitis C virus and pegiviruses. MBio. 2013;4(2):e00216–13. doi: 10.1128/mBio.00216-13 23572554

4. Drexler JF, Corman VM, Muller MA, Lukashev AN, Gmyl A, Coutard B, et al. Evidence for novel hepaciviruses in rodents. PLoS Pathog. 2013;9(6):e1003438. doi: 10.1371/journal.ppat.1003438 23818848

5. Wu Z, Lu L, Du J, Yang L, Ren X, Liu B, et al. Comparative analysis of rodent and small mammal viromes to better understand the wildlife origin of emerging infectious diseases. Microbiome. 2018;6(1):178. doi: 10.1186/s40168-018-0554-9 30285857

6. de Souza WM, Fumagalli MJ, Sabino-Santos G Jr., Motta Maia FG, Modha S, Teixeira Nunes MR, et al. A Novel Hepacivirus in Wild Rodents from South America. Viruses. 2019;11(3):297. doi: 10.3390/v11030297 30909631

7. Baechlein C, Fischer N, Grundhoff A, Alawi M, Indenbirken D, Postel A, et al. Identification of a Novel Hepacivirus in Domestic Cattle from Germany. J Virol. 2015;89(14):7007–15. doi: 10.1128/JVI.00534-15 25926652

8. Corman VM, Grundhoff A, Baechlein C, Fischer N, Gmyl A, Wollny R, et al. Highly divergent hepaciviruses from African cattle. J Virol. 2015;89(11):5876–82. doi: 10.1128/JVI.00393-15 25787289

9. Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA, Mishra N, et al. Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol. 2012;86(11):6171–8. doi: 10.1128/JVI.00250-12 22491452

10. Lauck M, Sibley SD, Lara J, Purdy MA, Khudyakov Y, Hyeroba D, et al. A novel hepacivirus with an unusually long and intrinsically disordered NS5A protein in a wild Old World primate. J Virol. 2013;87(16):8971–81. doi: 10.1128/JVI.00888-13 23740998

11. Canuti M, Williams CV, Sagan SM, Oude Munnink BB, Gadi S, Verhoeven JTP, et al. Virus discovery reveals frequent infection by diverse novel members of the Flaviviridae in wild lemurs. Arch Virol. 2019;164(2):509–22. doi: 10.1007/s00705-018-4099-9 30460488

12. Quan PL, Firth C, Conte JM, Williams SH, Zambrana-Torrelio CM, Anthony SJ, et al. Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci U S A. 2013;110(20):8194–9. doi: 10.1073/pnas.1303037110 23610427

13. Harvey E, Rose K, Eden JS, Lo N, Abeyasuriya T, Shi M, et al. Extensive Diversity of RNA Viruses in Australian Ticks. J Virol. 2019;93(3). doi: 10.1128/JVI.01358-18 30404810

14. Shi M, Lin XD, Chen X, Tian JH, Chen LJ, Li K, et al. The evolutionary history of vertebrate RNA viruses. Nature. 2018;556(7700):197–202. doi: 10.1038/s41586-018-0012-7 29618816

15. Shi M, Lin XD, Vasilakis N, Tian JH, Li CX, Chen LJ, et al. Divergent Viruses Discovered in Arthropods and Vertebrates Revise the Evolutionary History of the Flaviviridae and Related Viruses. J Virol. 2015;90(2):659–69. doi: 10.1128/JVI.02036-15 26491167

16. Chu L, Jin M, Feng C, Wang X, Zhang D. A highly divergent hepacivirus-like flavivirus in domestic ducks. J Gen Virol. 2019; July 8. doi: 10.1099/jgv.0.001298 31282853

17. Rohe D, Fall RP. A miniature battery powered CO2 baited light trap for mosquito borne encephalitis surveillance. Bulletin of the Society of Vector Ecology. 1979;4:24–7.

18. Broom AK, Lindsay MD, Johansen CA, Wright AE, Mackenzie JS. Two possible mechanisms for survival and initiation of Murray Valley encephalitis virus activity in the Kimberley region of Western Australia. Am J Trop Med Hyg. 1995;53(1):95–9. 7625542

19. Liehne PF. An atlas of the mosquitoes of Western Australia. Health Department of Western Australia. Perth, Western Australia. 1991.

20. Madeley CF, Lennette DA, Halonen P. Specimen collection and transport. In: Lennette EH, Halonen P, Murphy FA, editors. Laboratory diagnosis of infectious diseases: principles and practice. 2. New York, NY: Springer-Verlag; 1988. p. 7.

21. Chidlow G, Harnett G, Williams S, Levy A, Speers D, Smith DW. Duplex real-time reverse transcriptase PCR assays for rapid detection and identification of pandemic (H1N1) 2009 and seasonal influenza A/H1, A/H3, and B viruses. J Clin Microbiol. 2010;48(3):862–6. doi: 10.1128/JCM.01435-09 20071557

22. Schmieder R, Edwards R. Quality control and preprocessing of metagenomic datasets. Bioinformatics. 2011;27(6):863–4. doi: 10.1093/bioinformatics/btr026 21278185

23. Langmead B, Salzberg SL. Fast gapped-read alignment with Bowtie 2. Nat Methods. 2012;9(4):357–9. doi: 10.1038/nmeth.1923 22388286

24. Li D, Luo R, Liu CM, Leung CM, Ting HF, Sadakane K, et al. MEGAHIT v1.0: A fast and scalable metagenome assembler driven by advanced methodologies and community practices. Methods. 2016;102:3–11. doi: 10.1016/j.ymeth.2016.02.020 27012178

25. Almagro Armenteros JJ, Tsirigos KD, Sonderby CK, Petersen TN, Winther O, Brunak S, et al. SignalP 5.0 improves signal peptide predictions using deep neural networks. Nat Biotechnol. 2019;37:420–3. doi: 10.1038/s41587-019-0036-z 30778233

26. Kearse M, Moir R, Wilson A, Stones-Havas S, Cheung M, Sturrock S, et al. Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics. 2012;28(12):1647–9. doi: 10.1093/bioinformatics/bts199 22543367

27. Tamura K, Stecher G, Peterson D, Filipski A, Kumar S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol Biol Evol. 2013;30(12):2725–9. doi: 10.1093/molbev/mst197 24132122

28. Le SQ, Gascuel O. An improved general amino acid replacement matrix. Mol Biol Evol. 2008;25(7):1307–20. doi: 10.1093/molbev/msn067 18367465

29. Townzen JS, Brower AV, Judd DD. Identification of mosquito bloodmeals using mitochondrial cytochrome oxidase subunit I and cytochrome b gene sequences. Med Vet Entomol. 2008;22(4):386–93. doi: 10.1111/j.1365-2915.2008.00760.x 19120966

30. Government of Western Australia. Medical Entomology: 2017/2018 surveillance program annual report Perth, Western Australia: Department of Health; 2018

31. Reeves LE, Gillett-Kaufman JL, Kawahara AY, Kaufman PE. Barcoding blood meals: New vertebrate-specific primer sets for assigning taxonomic identities to host DNA from mosquito blood meals. PLoS Negl Trop Dis. 2018;12(8):e0006767. doi: 10.1371/journal.pntd.0006767 30161128

32. Calvignac S, Konecny L, Malard F, Douady CJ. Preventing the pollution of mitochondrial datasets with nuclear mitochondrial paralogs (numts). Mitochondrion. 2011;11(2):246–54. doi: 10.1016/j.mito.2010.10.004 21047564

33. Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, et al. Redefining the invertebrate RNA virosphere. Nature. 2016;540:539–43. doi: 10.1038/nature20167 27880757

34. Serventy DL. Feeding methods of Podargus. Emu. 1936;36(2):74–90.

35. Stephenson EB, Murphy AK, Jansen CC, Peel AJ, McCallum H. Interpreting mosquito feeding patterns in Australia through an ecological lens: an analysis of blood meal studies. Parasit Vectors. 2019;12(1):156. doi: 10.1186/s13071-019-3405-z 30944025

36. Hartlage AS, Cullen JM, Kapoor A. The Strange, Expanding World of Animal Hepaciviruses. Annu Rev Virol. 2016;3(1):53–75. doi: 10.1146/annurev-virology-100114-055104 27741408

Článek vyšel v časopise


2020 Číslo 1
Nejčtenější tento týden