Characterization of viral communities of biting midges and identification of novel thogotovirus species and rhabdovirus genus

Viruses

Volumn 8, Issue 3, 2016, Pages

  Temmam, Sarah ^a   Monteil Bouchard, Sonia ^a   Robert, Catherine ^a   Baudoin, Jean Pierre ^a   Sambou, Masse ^a   Aubadie Ladrix, Maxence ^a   Labas, Noémie ^a   Raoult, Didier ^a,b   Mediannikov, Oleg ^a   Desnues, Christelle ^a  

^a AIX MARSEILLE UNIVERSITÉ   (France)

^b TIMONE HOSPITAL   (France)

Author keywords

Biting midges; Epizooties; Rhabdovirus; Thogotovirus; Viral metagenomics; Zoonoses

Indexed keywords

ARTICLE; BIOINFORMATICS; CERATOPOGONIDAE; COMMUNITY DYNAMICS; DISEASE TRANSMISSION; METAGENOMICS; MOLECULAR BIOLOGY; NEXT GENERATION SEQUENCING; NONHUMAN; ORGANISM COMMUNITY; PHYLOGENY; QUANTITATIVE ANALYSIS; RHABDOVIRIDAE; RNA ANALYSIS; SEQUENCE ANALYSIS; SPECIES DIVERSITY; THOGOTOVIRUS; TRANSMISSION ELECTRON MICROSCOPY; VIRAL COMMUNITY; ANIMAL; BIOTA; CLASSIFICATION; DISEASE CARRIER; HIGH THROUGHPUT SEQUENCING; ISOLATION AND PURIFICATION; RNA VIRUS; SENEGAL; VIROLOGY;

ANIMALS; BIOTA; CERATOPOGONIDAE; DISEASE VECTORS; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; RNA VIRUSES; SENEGAL;

EID: 84960477453     PISSN: None     EISSN: 19994915     Source Type: Journal    
DOI: 10.3390/v8030077     Document Type: Article

References (62)

1. Woolhouse, M.; Scott, F.; Hudson, Z.; Howey, R.; Chase-Topping, M. Human viruses: discovery and emergence. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2012, 367, 2864-2871. [CrossRef] [PubMed]
2. Cutler, S.J.; Fooks, A.R.; van der Poel, W.H. Public health threat of new, reemerging, and neglected zoonoses in the industrialized world. Emerg. Infect. Dis. 2010, 16, 1-7. [CrossRef] [PubMed]
3. Temmam, S.; Davoust, B.; Berenger, J.M.; Raoult, D.; Desnues, C. Viral metagenomics on animals as a tool for the detection of zoonoses prior to human infection? Int. J. Mol. Sci. 2014, 15, 10377-10397. [CrossRef] [PubMed]
4. 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.; Sozhammannan, S.; et al. Arbovirus detection in insect vectors by rapid, high-throughput pyrosequencing. PLoS Negl. Trop. Dis. 2010, 4. [CrossRef] [PubMed]
5. Dinsdale, E.A.; Edwards, R.A.; Hall, D.; Angly, F.; Breitbart, M.; Brulc, J.M.; Furlan, M.; Desnues, C.; Haynes, M.; Li, L.; et al. Functional metagenomic profiling of nine biomes. Nature 2008, 452, 629-632. [CrossRef] [PubMed]
6. Chandler, J.A.; Thongsripong, P.; Green, A.; Kittayapong, P.; Wilcox, B.A.; Schroth, G.P.; Kapan, D.D.; Bennett, S.N. Metagenomic shotgun sequencing of a Bunyavirus in wild-caught Aedes aegypti from Thailand informs the evolutionary and genomic history of the Phleboviruses. Virology 2014, 464-465, 312-319. [CrossRef] [PubMed]
7. Chandler, J.A.; Liu, R.M.; Bennett, S.N. RNA shotgun llinoisics sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front. Microbiol. 2015, 6. [CrossRef] [PubMed]
8. 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. [CrossRef] [PubMed]
9. Tokarz, R.; Williams, S.H.; Sameroff, S.; Sanchez Leon, M.; Jain, K.; Lipkin, W.I. Virome analysis of Amblyomma americanum, Dermacentor variabilis, and Ixodes scapularis ticks reveals novel highly divergent vertebrate and invertebrate viruses. J. Virol. 2014, 88, 11480-11492. [CrossRef] [PubMed]
10. Xia, H.; Hu, C.; Zhang, D.; Tang, S.; Zhang, Z.; Kou, Z.; Fan, Z.; Bente, D.; Zeng, C.; Li, T. Metagenomic profile of the viral communities in Rhipicephalus spp. Ticks from Yunnan, China. PLoS ONE 2015, 10. [CrossRef] [PubMed]
11. Borkent, A.World Species of Biting Midges (Diptera: Ceratopogonidae). 2014. Available online: http://wwx. inhs.illinois.edu/files/9913/9144/3328/CeratopogonidaeCatalog.pdf (accessed on 20 October 2015).
12. Borkent, A. The Subgeneric Classification of Species of Culicoides-Thoughts and a Warning. 2014. Available online: http://wwx.inhs.illinois.edu/files/9613/9136/7590/CulicoidesSubgenera.pdf (accessed on 20 October 2015).
13. Bassene, H.; Sambou, M.; Fenollar, F.; Clarke, S.; Djiba, S.; Mourembou, G.; LY, A.B.; Raoult, D.; Mediannikov, O. High prevalence of Mansonella perstans filariasis in rural Senegal. Am. J. Trop. Med. Hyg. 2015, 93, 601-606. [CrossRef] [PubMed]
14. Agbolade, O.M.; Akinboye, D.O.; Olateju, T.M.; Ayanbiyi, O.A.; Kuloyo, O.O.; Fenuga, O.O. Biting of anthropophilic Culicoides fulvithorax (Diptera: Ceratopogonidae), a vector of Mansonella perstans in Nigeria. Korean J. Parasitol 2006, 44, 67-72. [CrossRef]
15. Mellor, P.S.; Boorman, J.; Baylis, M. Culicoides biting midges: Their role as arbovirus vectors. Annu. Rev. Entomol. 2000, 45, 307-340. [CrossRef] [PubMed]
16. Tesh, R.B. The emerging epidemiology of Venezuelan hemorrhagic fever and Oropouche fever in tropical South America. Ann. N. Y. Acad. Sci. 1994, 740, 129-137. [CrossRef] [PubMed]
17. Temmam, S.; Monteil-Bouchard, S.; Robert, C.; Pascalis, H.; Michelle, C.; Jardot, P.; Charrel, R.; Raoult, D.; Desnues, C. Host-Associated Metagenomics: A Guide to Generating Infectious RNA Viromes. PLoS ONE 2015, 10. [CrossRef] [PubMed]
18. Froussard, P. A random-PCR method (rPCR) to construct whole cDNA library from low amounts of RNA. Nucleic Acids Res. 1992, 20, 2900. [CrossRef] [PubMed]
19. Metavir server. Available online: http://metavir-meb.univ-bpclermont.fr (accessed on 20 October 2015).
20. MG-RAST server. Available online: http://metagenomics.anl.gov/ (accessed on 20 October 2015).
21. Meyer, F.; Paarmann, D.; D'Souza, M.; Olson, R.; Glass, E.M.; Kubal, M.; Paczian, T.; Rodriguez, A.; Stevens, R.;Wilke, A.; et al. The metagenomics RAST server-a public resource for the automatic phylogenetic and functional analysis of metagenomes. BMC Bioinformatics 2008, 9. [CrossRef] [PubMed]
22. Edgar, R.C. MUSCLE: A multiple sequence alignment method with reduced time and space complexity. BMC Bioinform. 2004, 5. [CrossRef] [PubMed]
23. Tamura, K.; Stecher, G.; Peterson, D.; Filipski, A.; Kumar, S. MEGA6: Molecular Evolutionary Genetics Analysis version 6.0. Mol. Biol. Evol. 2013, 30, 2725-2729. [CrossRef] [PubMed]
24. Ronquist, F.; Huelsenbeck, J.P. MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 2003, 19, 1572-1574. [CrossRef] [PubMed]
25. Sime-Ngando, T.; Mignot, J.P.; Amblard, C.; Bourdier, G.; Desvilettes, C.; Quiblier-Lloberas, C. Characterization of planktonic virus-like particles in a French mountain lake: methodological aspects and preliminary results. Annal. Limnol. 1996, 32, 259-263. [CrossRef]
26. Coffey, L.L.; Page, B.L.; Greninger, A.L.; Herring, B.L.; Russell, R.C.; Doggett, S.L.; Haniotis, J.; Wang, C.; Deng, X.; Delwart, E.L. Enhanced arbovirus surveillance with deep sequencing: Identification of novel rhabdoviruses and bunyaviruses in Australian mosquitoes. Virology 2014, 448, 146-158. [CrossRef] [PubMed]
27. Walker, P.J.; Firth, C.; Widen, S.G.; Blasdell, K.R.; Guzman, H.; Wood, T.G.; Paradkar, P.N.; Holmes, E.C.; Tesh, R.B.; Vasilakis, N. Evolution of genome size and complexity in the Rhabdoviridae. PLoS Pathog. 2015, 11. [CrossRef] [PubMed]
28. Kuwata, R.; Isawa, H.; Hoshino, K.; Tsuda, Y.; Yanase, T.; Sasaki, T.; Kobayashi, M.; Sawabe, K. RNA splicing in a new rhabdovirus from Culex mosquitoes. J. Virol. 2011, 85, 6185-6196. [CrossRef] [PubMed]
29. Qin, X.C.; Shi, M.; Tian, J.H.; Lin, X.D.; Gao, D.Y.; He, J.R.; Wang, J.B.; Li, C.X.; Kang, Y.J.; Yu, B.; et al. A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors. Proc. Natl. Acad. Sci. USA 2014, 111, 6744-6749. [CrossRef] [PubMed]
30. Maruyama, S.R.; Castro-Jorge, L.A.; Ribeiro, J.M.; Gardinassi, L.G.; Garcia, G.R.; Brandão, L.G.; Rodrigues, A.R.; Okada, M.I.; Abrão, E.P.; Ferreira, B.R.; et al. Characterisation of divergent flavivirus NS3 and NS5 protein sequences detected in Rhipicephalus microplus ticks from Brazil. Mem. Inst. Oswaldo Cruz 2014, 109, 38-50. [CrossRef] [PubMed]
31. Fort, P.; Albertini, A.; Van-Hua, A.; Berthomieu, A.; Roche, S.; Delsuc, F.; Pasteur, N.; Capy, P.; Gaudin, Y.; Weill, M. Fossil rhabdoviral sequences integrated into arthropod genomes: ontogeny, evolution, and potential functionality. Mol. Biol. Evol. 2012, 29, 381-390. [CrossRef] [PubMed]
32. Katzourakis, A.; Gifford, R.J. Endogenous viral elements in animal genomes. PLoS Genet. 2010, 6. [CrossRef] [PubMed]
33. Carpenter, S.; Groschup, M.H.; Garros, C.; Felippe-Bauer, M.L.; Purse, B.V. Culicoides biting midges, arboviruses and public health in Europe. Antiviral Res. 2013, 100, 102-113. [CrossRef] [PubMed]
34. Kedmi, M.; Van Straten, M.; Ezra, E.; Galon, N.; Klement, E. Assessment of the productivity effects associated with epizootic hemorrhagic disease in dairy herds. J. Dairy Sci. 2010, 93, 2486-2495. [CrossRef] [PubMed]
35. Nusinovici, S.; Souty, C.; Seegers, H.; Beaudeau, F.; Fourichon, C. Decrease in milk yield associated with exposure to bluetongue virus serotype 8 in cattle herds. J. Dairy Sci. 2013, 96, 877-888. [CrossRef] [PubMed]
36. Sambou, M.; Aubadie-Ladrix, M.; Fenollar, F.; Fall, B.; Bassene, H.; Almeras, L.; Sambe-Ba, B.; Perrot, N.; Chatellier, S.; Faye, N.; et al. Comparison of matrix-assisted laser desorption ionization-time of flight mass spectrometry and molecular biology techniques for identification of Culicoides (Diptera: Ceratopogonidae) biting midges in Senegal. J. Clin. Microbiol. 2015, 53, 410-418. [CrossRef] [PubMed]
37. Diouf, N.D.; Etter, E.; Lo, M.M.; Akakpo, A.J. Outbreaks of African horse sickness in Senegal, and methods of control of the 2007 epidemic. Vet. Rec. 2013, 172. [CrossRef] [PubMed]
38. Lefèvre, P.C.; Calvez, D. La fièvre catarrhale du mouton (bluetongue) en Afrique Intertropicale: influence des facteurs écologiques sur la prévalence de l'infection. Rev. Elev. Med. Vét. Pays Trop. 1986, 39, 263-268. [PubMed]
39. Diarra, M.; Fall, M.; Fall, A.G.; Diop, A.; Seck, M.T.; Garros, C.; Balenghien, T.; Allène, X. Seasonal dynamics of Culicoides (Diptera: Ceratopogonidae) biting midges, potential vectors of African horse sickness and bluetongue viruses in the Niayes area of Senegal. Parasit. Vectors. 2014, 7, 147. [CrossRef] [PubMed]
40. Daszak, P. Can we predict future trends in disease emergence? Chapter 5: Infectious disease emergence: Past, present and Future. In Microbial Evolution and Co-Adaptation, A Tribute to the Life and Scientific Legacies of Joshua Lederberg: Workshop Summary; National Academies Press: Washington, DC, USA, 2009.
41. Karabatsos, N. International Catalogue of Arboviruses, Including Certain Other Viruses of Vertebrates, 3rd ed.; American Society of Tropical Medicine and Hygiene for The Subcommittee on Information Exchange of the American Committee on Arthropod-borne Viruses: San Antonio, TX, USA, 1985.
42. Frese, M.; Weeber, M.; Weber, F.; Speth, V.; Haller, O. Mx1 sensitivity: Batken virus is an orthomyxovirus closely related to Dhori virus. J. Gen. Virol. 1997, 78, 2453-2458. [CrossRef] [PubMed]
43. Hubálek, Z.; Rudolf, I.; Nowotny, N. Arboviruses pathogenic for domestic and wild animals. Adv. Virus Res. 2014, 89, 201-275. [PubMed]
44. Hubálek, Z.; Rudolf, I. Tick-borne viruses in Europe. Parasitol. Res. 2012, 111, 9-36. [CrossRef] [PubMed]
45. Filipe, A.R.; Calischer, C.H.; Lazuick, J. Antibodies to Congo-Crimean haemorrhagic fever, Dhori, Thogoto and Bhanja viruses in southern Portugal. Acta Virol. 1985, 29, 324-328. [PubMed]
46. Ogen-Odoi, A.; Miller, B.R.; Happ, C.M.; Maupin, G.O.; Burkot, T.R. Isolation of thogoto virus (Orthomyxoviridae) from the banded mongoose, Mongos mungo (Herpestidae), in Uganda. Am. J. Trop. Med. Hyg. 1999, 60, 439-440. [PubMed]
47. Da Silva, E.V.; Da Rosa, A.P.; Nunes, M.R.; Diniz, J.A.; Tesh, R.B.; Cruz, A.C.; Tesh, C.M.; Vasconcelos, P.F. Araguari virus, a new member of the family Orthomyxoviridae: serologic, ultrastructural, and molecular characterization. Am. J. Trop. Med. Hyg. 2005, 73, 1050-1058. [PubMed]
48. Lutomiah, J.; Musila, L.; Makio, A.; Ochieng, C.; Koka, H.; Chepkorir, E.; Mutisya, J.; Mulwar, F.; Khamadi, S.; Miller, B.R.; et al. Ticks and tick-borne viruses from livestock hosts in arid and semiarid regions of the eastern and northeastern parts of Kenya. J. Med. Entomol. 2014, 51, 269-277. [CrossRef] [PubMed]
49. Briese, T.; Chowdhary, R.; Travassos da Rosa, A.; Hutchison, S.K.; Popov, V.; Street, C.; Tesh, R.B.; Lipkin,W.I. Upolu virus and Aransas Bay virus, two presumptive bunyaviruses, are novel members of the family Orthomyxoviridae. J. Virol. 2014, 88, 5298-5309. [CrossRef] [PubMed]
50. Moore, D.L.; Causey, O.R.; Carey, D.E.; Reddy, S.; Cooke, A.R.; Akinkugbe, F.M.; David-West, T.S.; Kemp, G.E. Arthropod-borne viral infections of man in Nigeria, 1964-1970. Ann. Trop. Med. Parasitol. 1975, 69, 49-64. [PubMed]
51. Butenko, A.M.; Leshchinskaia, E.V.; Semashko, I.V.; Donets, M.A.; Mart'ianova, L.I. Dhori virus-A causative agent of human disease. 5 cases of laboratory infection. Vopr. Virusol. 1987, 32, 724-729. [PubMed]
52. Kosoy, O.I.; Lambert, A.J.; Hawkinson, D.J.; Pastula, D.M.; Goldsmith, C.S.; Hunt, D.C.; Staples, J.E. Novel thogotovirus associated with febrile illness and death, United States, 2014. Emerg. Infect. Dis. 2015, 21, 760-764. [CrossRef] [PubMed]
53. Vasilakis, N.; Tesh, R.B. Insect-specific viruses and their potential impact on arbovirus transmission. Curr. Opin. Virol. 2014, 15, 69-74. [CrossRef] [PubMed]
54. Li, C.X.; Shi, M.; Tian, J.H.; Lin, X.D.; Kang, Y.J.; Chen, L.J.; Qin, X.C.; Xu, J.; Holmes, E.C.; Zhang, Y.Z. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. Elife 2015, 4. [CrossRef] [PubMed]
55. Cui, J.; Holmes, E.C. Endogenous RNA viruses of plants in insect genomes. Virology 2012, 427, 77-79. [CrossRef] [PubMed]
56. Ballinger, M.J.; Bruenn, J.A.; Hay, J.; Czechowski, D.; Taylor, D.J. Discovery and evolution of bunyavirids in arctic phantom midges and ancient bunyavirid-like sequences in insect genomes. J. Virol. 2014, 88, 8783-8794. [CrossRef] [PubMed]
57. Feschotte, C.; Gilbert, C. Endogenous viruses: insights into viral evolution and impact on host biology. Nat. Rev. Genet. 2012, 13, 283-296. [CrossRef] [PubMed]
58. Liu, H.; Fu, Y.; Xie, J.; Cheng, J.; Ghabrial, S.A.; Li, G.; Peng, Y.; Yi, X.; Jiang, D.Widespread endogenization of densoviruses and parvoviruses in animal and human genomes. J. Virol. 2011, 85, 9863-9876. [CrossRef] [PubMed]
59. Boller, K.; Schönfeld, K.; Lischer, S.; Fisher, N.; Hoffmann, A.; Kurth, R.; Tönjes, R.R. Human endogenous retrovirus HERV-K113 is capable of producing intact viral particles. J. Gen. Virol. 2008, 89, 567-572. [CrossRef] [PubMed]
60. Bézier, A.; Louis, F.; Jancek, S.; Periquet, G.; Thézé, J.; Gyapay, G.; Musset, K.; Lesobre, J.; Lenoble, P.; Dupuy, C.; et al. Functional endogenous viral elements in the genome of the parasitoid wasp Cotesia congregata: insights into the evolutionary dynamics of bracoviruses. Philos. Trans. R. Soc. Lond. B Biol. Sci. 2013, 368. [CrossRef] [PubMed]
61. Rosario, K.; Capobianco, H.; Ng, T.F.; Breitbart, M.; Polston, J.E. RNA viral metagenome of whiteflies leads to the discovery and characterization of a whitefly-transmitted carlavirus in North America. PLoS ONE 2014, 9. [CrossRef] [PubMed]
62. Sparks, M.E.; Gundersen-Rindal, R.E. The Lymantria dispar IPLB-Ld652Y cell line transcriptome comprises diverse virus-associated transcripts. Viruses 2011, 3, 2339-2350. [CrossRef] [PubMed]