Enhanced arbovirus surveillance with deep sequencing: Identification of novel rhabdoviruses and bunyaviruses in Australian mosquitoes

Virology

Volumn 448, Issue , 2014, Pages 146-158

  Coffey, Lark L ^a,b   Page, Brady L ^a,b   Greninger, Alexander L ^b   Herring, Belinda L ^c   Russell, Richard C ^d,e   Doggett, Stephen L ^e   Haniotis, John ^e   Wang, Chunlin ^f   Deng, Xutao ^a,b   Delwart, Eric L ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c GRIFFITH UNIVERSITY   (Australia)

^d UNIVERSITY OF SYDNEY   (Australia)

^e WESTMEAD HOSPITAL   (Australia)

^f STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Arbovirus surveillance; Australia; Bunyavirus; Deep sequencing; Mosquito; Novel virus; Reovirus; Rhabdovirus; Virus discovery

Indexed keywords

PROTEOME;

ARBOVIRUS; ARTICLE; BEAUMONT VIRUS; BLINDNESS; BUNYAVIRUS; CELL CULTURE; CYTOPATHOGENIC EFFECT; DEEP SEQUENCING; DIMARHABDOVIRUS; GENE SEQUENCE; GENETIC STRAIN; INOCULATION; KANGAROO; LIAO NING VIRUS; MAMMAL CELL; METAGENOMICS; MOSQUITO; MURRUMBRIDGEE VIRUS; NONHUMAN; NORTH CREEK VIRUS; NUCLEOTIDE SEQUENCE; ORBIVIRUS; ORTHOBUNYAVIRUS; PRIORITY JOURNAL; REOVIRUS; RHABDOVIRUS; SALT ASH VIRUS; STRETCH LAGOON VIRUS; UNINDEXED SEQUENCE; VIRUS GENOME; VIRUS IDENTIFICATION; VIRUS STRAIN; WALLAL VIRUS; WARREGO VIRUS;

EID: 84886425546     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.09.026     Document Type: Article

References (63)

1. Animal Health Australia, 2010. 2009-2010 Report National Arbovirus Monitoring Program.
2. Attoui H., Mohd Jaafar F., Belhouchet M., Tao S., Chen B., Liang G., Tesh R.B., de Micco P., de Lamballerie X. Liao ning virus, a new Chinese seadornavirus that replicates in transformed and embryonic mammalian cells. Journal of General Virology 2006, 87:199-208.
3. Azuolas J.K., Wishart E., Bibby S., Ainsworth C. Isolation of Ross River virus from mosquitoes and from horses with signs of musculo-skeletal disease. Australian Veterinary Journal 2003, 81:344-347.
4. Belaganahalli M.N., Maan S., Maan N.S., Tesh R., Attoui H., Mertens P.P. Umatilla virus genome sequencing and phylogenetic analysis: identification of stretch lagoon orbivirus as a new member of the Umatilla virus species. PLoS One 2011, 6:e23605.
5. Bishop-Lilly K.A., Turell M.J., Willner K.M., Butani A., Nolan N.M., Lentz S.M., Akmal A., Mateczun A., Brahmbhatt T.N., Sozhamannan S., Whitehouse C.A., Read T.D. Arbovirus detection in insect vectors by rapid, high-throughput pyrosequencing. PLoS Neglected Tropical Diseases 2010, 4:e878.
6. Blacksell S.D., Lunt R.A., White J.R. Rapid identification of Australian bunyavirus isolates belonging to the Simbu serogroup using indirect ELISA formats. Journal of Virological Methods 1997, 66:123-133.
7. Boughton C.R., Hawkes R.A., Naim H.M. Arbovirus infection in humans in NSW: seroprevalence and pathogenicity of certain Australian bunyaviruses. Australian and New Zealand Journal of Medicine 1990, 20:51-55.
8. Brown S.E., Gorman B.M., Tesh R.B., Knudson D.L. Coltiviruses isolated from mosquitoes collected in Indonesia. Virology 1993, 196:363-367.
9. Chen B., Tao S. Arbovirus survey in China in recent ten years. Chinese Medical Journal (England) 1996, 109:13-15.
10. Chowdhary R., Street C., Travassos da Rosa A., Nunes M.R., Tee K.K., Hutchison S.K., Vasconcelos P.F., Tesh R.B., Lipkin W.I., Briese T. Genetic characterization of the Wyeomyia group of orthobunyaviruses and their phylogenetic relationships. Journal of General Virology 2012, 93:1023-1034.
11. Clements A.N. Osmotic and ionic regulation. The Biology of Mosquitoes 2000, vol. 1:125. CABI Publishing, New York.
12. Cooper R.D., Frances S.P., Waterson D.G., Piper R.G., Sweeney A.W. Distribution of anopheline mosquitoes in northern Australia. Journal of the American Mosquito Control Association 1996, 12:656-663.
13. Cowled C., Palacios G., Melville L., Weir R., Walsh S., Davis S., Gubala A., Lipkin W.I., Briese T., Boyle D. Genetic and epidemiological characterization of Stretch Lagoon orbivirus, a novel orbivirus isolated from Culex and Aedes mosquitoes in northern Australia. Journal of General Virology 2009, 90:1433-1439.
14. Foley D.H., Wilkerson R.C., Cooper R.D., Volovsek M.E., Bryan J.H. A molecular phylogeny of Anopheles annulipes (Diptera: Culicidae) sensu lato: the most species-rich anopheline complex. Molecular Phylogenetics and Evolution 2007, 43:283-297.
15. Grard G., Fair J.N., Lee D., Slikas E., Steffen I., Muyembe J.J., Sittler T., Veeraraghavan N., Ruby J.G., Wang C., Makuwa M., Mulembakani P., Tesh R.B., Mazet J., Rimoin A.W., Taylor T., Schneider B.S., Simmons G., Delwart E., Wolfe N.D., Chiu C.Y., Leroy E.M. A novel rhabdovirus associated with acute hemorrhagic fever in central Africa. PLoS Pathogens 2012, 8:e1002924.
16. Hall-Mendelin S., Allcock R., Kresoje N., van den Hurk A.F., Warrilow D. Detection of arboviruses and other micro-organisms in experimentally infected mosquitoes using massively parallel sequencing. PLoS One 2013, 8:e58026.
17. Harley D., Sleigh A., Ritchie S. Ross River virus transmission, infection, and disease: a cross-disciplinary review. Clinical Microbiology Reviews 2001, 14:909-932.
18. Hooper P. Kangaroo blindness and some other new viral diseases in Australia. Australian Veterinary Journal 1999, 77:514-515.
19. Hooper P.T., Lunt R.A., Gould A.R., Hyatt A.D., Russell G.M., Kattenbelt J.A., Blacksell S.D., Reddacliff L.A., Kirkland P.D., Davis R.J., Durham P.J., Bishop A.L., Waddington J. Epidemic of blindness in kangaroos-evidence of a viral aetiology. Australian Veterinary Journal 1999, 77:529-536.
20. Jansen C.C., Prow N.A., Webb C.E., Hall R.A., Pyke A.T., Harrower B.J., Pritchard I.L., Zborowski P., Ritchie S.A., Russell R.C., Van Den Hurk A.F. Arboviruses isolated from mosquitoes collected from urban and peri-urban areas of eastern Australia. Journal of the American Mosquito Control Association 2009, 25:272-278.
21. Johansen C.A., Nisbet D.J., Zborowski P., van den Hurk A.F., Ritchie S.A., Mackenzie J.S. Flavivirus isolations from mosquitoes collected from western Cape York Peninsula, Australia, 1999-2000. Journal of the American Mosquito Control Association 2003, 19:392-396.
22. Johansen C.A., Nisbet D.J., Foley P.N., Van Den Hurk A.F., Hall R.A., Mackenzie J.S., Ritchie S.A. Flavivirus isolations from mosquitoes collected from Saibai Island in the Torres Strait, Australia, during an incursion of Japanese encephalitis virus. Medical and Veterinary Entomology 2004, 18:281-287.
23. Junglen S., Drosten C. Virus discovery and recent insights into virus diversity in arthropods. Current Opinion in Microbiology 2013, 16:507-513.
24. Kay B.H., Boyd A.M., Ryan P.A., Hall R.A. Mosquito feeding patterns and natural infection of vertebrates with Ross River and Barmah Forest viruses in Brisbane, Australia. American Journal of Tropical Medicine and Hygiene 2007, 76:417-423.
25. Knope, K., Whelan, P., Smith, D., Nicholson, J., Moran, R., Doggett, S., Sly, A., Hobby, M., Wright, P. 2013. Arboviral Diseases and Malaria in Australia, 2010-11: Annual Report of the National Arbovirus and Malaria Advisory Committee. Commun Dis Intell Q Rep 37:E1-E20.
26. Kuzmin I.V., Novella I.S., Dietzgen R.G., Padhi A., Rupprecht C.E. The rhabdoviruses: biodiversity, phylogenetics, and evolution. Infection, Genetics and Evolution 2009, 9:541-553.
27. Li Q. First isolation of eight strains of new orbivirus (Banna) from patients with innominate fever in Xinjiang. Endemic Diseases Bulletin 1992, 7:77-82.
28. Li W.J., Wang J.L., Li M.H., Fu S.H., Wang H.Y., Wang Z.Y., Jiang S.Y., Wang X.W., Guo P., Zhao S.C., Shi Y., Lu N.N., Nasci R.S., Tang Q., Liang G.D. Mosquitoes and mosquito-borne arboviruses in the Qinghai-Tibet Plateau-focused on the Qinghai area, China. American Journal of Tropical Medicine and Hygiene 2010, 82:705-711.
29. Liting S., Chen B., Chou Z. Isolation and identification of new members of coltivirus from mosquitoes collected in China. Zhonghua Shi Yan He Lin Chuang Bing Du Xue Za Zhi 1995, 9:7-10.
30. Liu H., Li M.H., Zhai Y.G., Meng W.S., Sun X.H., Cao Y.X., Fu S.H., Wang H.Y., Xu L.H., Tang Q., Liang G.D. Banna virus, China, 1987-2007. Emerging Infectious Diseases 2010, 16:514-517.
31. Lu Z., Liu H., Fu S., Lu X., Dong Q., Zhang S., Tong S., Li M., Li W., Tang Q., Liang G. Liao ning virus in China. Virology Journal 2011, 8:282.
32. Lv X., Mohd Jaafar F., Sun X., Belhouchet M., Fu S., Zhang S., Tong S.X., Lv Z., Mertens P.P., Liang G., Attoui H. Isolates of Liao ning virus from wild-caught mosquitoes in the Xinjiang province of China in 2005. PLoS One 2012, 7:e37732.
33. Ma M., Huang Y., Gong Z., Zhuang L., Li C., Yang H., Tong Y., Liu W., Cao W. Discovery of DNA viruses in wild-caught mosquitoes using small RNA high throughput sequencing. PLoS One 2011, 6:e24758.
34. Mertens P., Maan S., Samuel A., Attoui H. Orbiviruses, Reoviridae. Virus taxonomy: either report of the international committee on taxonomy of viruses 2005, 466-483. Elsevier Academic Press, London. C. Fauquet, M. Mayo, J. Maniloff, U. Desselberger, L. Ball (Eds.).
35. Monath T.P., Cropp C.B., Frazier C.L., Murphy F.A., Whitfield S.G. Viruses isolated from reptiles: identification of three new members of the family Rhabdoviridae. Archives of Virology 1979, 60:1-12.
36. Mores C.N., Turell M.J., Dyer J., Rossi C.A. Phylogenetic relationships among orthobunyaviruses isolated from mosquitoes captured in Peru. Vector Borne and Zoonotic Diseases 2009, 9:25-32.
37. Murray M.D., Kirkland P.D. Bluetongue and Douglas virus activity in New South Wales in 1989: further evidence for long-distance dispersal of the biting midge Culicoides brevitarsis. Australian Veterinary Journal 1995, 72:56-57.
38. Nabeshima T., Thi Nga P., Guillermo P., Parquet Mdel C., Yu F., Thanh Thuy N., Minh Trang B., Tran Hien N., Sinh Nam V., Inoue S., Hasebe F., Morita K. Isolation and molecular characterization of Banna virus from mosquitoes, Vietnam. Emerging Infectious Diseases 2008, 14:1276-1279.
39. Ng T.F., Willner D.L., Lim Y.W., Schmieder R., Chau B., Nilsson C., Anthony S., Ruan Y., Rohwer F., Breitbart M. Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS One 2011, 6:e20579.
40. Powers A.M., Logue C.H. Changing patterns of chikungunya virus: re-emergence of a zoonotic arbovirus. Journal of General Virology 2007, 88:2363-2377.
41. Quan P.L., Junglen S., Tashmukhamedova A., Conlan S., Hutchison S.K., Kurth A., Ellerbrok H., Egholm M., Briese T., Leendertz F.H., Lipkin W.I. Moussa virus: a new member of the Rhabdoviridae family isolated from Culex decens mosquitoes in Cote d'Ivoire. Virus Research 2010, 147:17-24.
42. Quan P.L., Williams D.T., Johansen C.A., Jain K., Petrosov A., Diviney S.M., Tashmukhamedova A., Hutchison S.K., Tesh R.B., Mackenzie J.S., Briese T., Lipkin W.I. Genetic characterization of K13965, a strain of Oak Vale virus from Western Australia. Virus Research 2011, 160:206-213.
43. Reddacliff L., Kirkland P., Philbey A., Davis R., Vogelnest L., Hulst F., Blyde D., Deykin A., Smith J., Hooper P., Gould A., Hyatt A. Experimental reproduction of viral chorioretinitis in kangaroos. Australian Veterinary Journal 1999, 77:522-528.
44. Ruby J.G., Bellare P., Derisi J.L. PRICE: software for the targeted assembly of components of (Meta) genomic sequence data. G3 (Bethesda) 2013, 3:865-880.
45. Russell R.C. A Colour Photo Atlas of Mosquitoes of Southeastern Australia 1996, Department of Medical Entomology, Westmead, New South Wales.
46. Russell R.C., Cloonan M.J., Wells P.J., Vale T.G. Mosquito (Diptera: Culicidae) and arbovirus activity on the south coast of New South Wales, Australia, in 1985-1988. Journal of Medical Entomology 1991, 28:796-804.
47. Russell R.C., Doggett S.L., Clancy J., Haniotis J., Patsouris K., Hueston L., Marchetti M., Dwyer D.E. Arbovirus and vector surveillance in NSW, 1997-2000. Arbovirus Research in Australia 2001, 8:304-313.
48. Savji N., Palacios G., Travassos da Rosa A., Hutchison S., Celone C., Hui J., Briese T., Calisher C.H., Tesh R.B., Lipkin W.I. Genomic and phylogenetic characterization of Leanyer virus, a novel orthobunyavirus isolated in northern Australia. Journal of General Virology 2011, 92:1676-1687.
49. Simmons C.P., Farrar J.J., van Vinh Chau N., Wills B. Dengue. New England Journal of Medicine 2012, 366:1423-1432.
50. St George T.D., Standfast H.A., Cybinski D.H., Filippich C., Carley J.G. Peaton virus: a new Simbu group arbovirus isolated from cattle and Culicoides brevitarsis in Australia. Australian Journal of Biological Sciences 1980, 33:235-243.
51. Standfast H.A., Dyce A.L., George T.D., Muller M.J., Doherty R.L., Carley J.G., Filippich C. Isolation of arboviruses from insects collected at Beatrice Hill, Northern Territory of Australia, 1974-1976. Australian Journal of Biological Sciences 1984, 37:351-366.
52. Suthar M.S., Diamond M.S., Gale M. West Nile virus infection and immunity. Nature Reviews Microbiology 2013, 11:115-128.
53. Swei A., Russell B.J., Naccache S.N., Kabre B., Veeraraghavan N., Pilgard M.A., Johnson B.J., Chiu C.Y. The genome sequence of Lone Star virus, a highly divergent bunyavirus found in the Amblyomma americanum tick. PLoS One 2013, 8:e62083.
54. Tallis G., Ng S., Azuolas J. A sero-prevalence study for 'wallal-type' virus infection among park workers. Australian and New Zealand Journal of Public Health 1998, 22:515.
55. Tamura K., Peterson D., Peterson N., Stecher G., Nei M., Kumar S. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Molecular Biology and Evolution 2011, 28:2731-2739.
56. Tao S.J., Chen B.Q. Studies of coltivirus in China. Chinese Medical Journal (England) 2005, 118:581-586.
57. Thompson J.D., Higgins D.G., Gibson T.J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 1994, 22:4673-4680.
58. Van Den Hurk A.F., Montgomery B.L., Northill J.A., Smith I.L., Zborowski P., Ritchie S.A., Mackenzie J.S., Smith G.A. Short report: the first isolation of Japanese encephalitis virus from mosquitoes collected from mainland Australia. American Journal of Tropical Medicine and Hygiene 2006, 75:21-25.
59. Vasilakis N., Widen S., Travassos da Rosa A.P., Wood T.G., Walker P.J., Holmes E.C., Tesh R.B. Malpais spring virus is a new species in the genus vesiculovirus. Virology Journal 2013, 10:69.
60. Victoria J.G., Kapoor A., Li L., Blinkova O., Slikas B., Wang C., Naeem A., Zaidi S., Delwart E. Metagenomic analyses of viruses in stool samples from children with acute flaccid paralysis. Journal of Virology 2009, 83:4642-4651.
61. Walter C.T., Barr J.N. Recent advances in the molecular and cellular biology of bunyaviruses. Journal ofGeneral Virology 2011, 92:2467-2484.
62. Xu P., Wang Y., Zuo J., Lin J., Xu P. Isolation of orbiviruses from sera of patients with unknown fever and encephalitis collected from Yunnan Province. Chinese Journal of Virology 1990, 6:27-33.
63. Yu X.J., Liang M.F., Zhang S.Y., Liu Y., Li J.D., Sun Y.L., Zhang L., Zhang Q.F., Popov V.L., Li C., Qu J., Li Q., Zhang Y.P., Hai R., Wu W., Wang Q., Zhan F.X., Wang X.J., Kan B., Wang S.W., Wan K.L., Jing H.Q., Lu J.X., Yin W.W., Zhou H., Guan X.H., Liu J.F., Bi Z.Q., Liu G.H., Ren J., Wang H., Zhao Z., Song J.D., He J.R., Wan T., Zhang J.S., Fu X.P., Sun L.N., Dong X.P., Feng Z.J., Yang W.Z., Hong T., Zhang Y., Walker D.H., Wang Y., Li D.X. Fever with thrombocytopenia associated with a novel bunyavirus in China. The New England Journal of Medicine 2011, 364:1523-1532.