West African Anopheles gambiae mosquitoes harbor a taxonomically diverse virome including new insect-specific flaviviruses, mononegaviruses, and totiviruses

Virology

Volumn 498, Issue , 2016, Pages 288-299

  Fauver, Joseph R ^a   Grubaugh, Nathan D ^a   Krajacich, Benjamin J ^a   Weger Lucarelli, James ^a   Lakin, Steven M ^a   Fakoli, Lawrence S ^b   Bolay, Fatorma K ^b   Diclaro, Joseph W ^c   Dabiré, Kounbobr Roch ^d   Foy, Brian D ^a   Brackney, Doug E ^a,e   Ebel, Gregory D ^a   Stenglein, Mark D ^a  

^a Veterinary Dentistry and Oral Surgery   (United States)

^b Liberian Institute for Biomedical Research   (Liberia)

^c US Naval Medical Research Unit No 3 Egypt   (Egypt)

^d Institut de Recherche en Sciences de la Santé   (Burkina Faso)

^e Northeast Regional Center for Excellence in Vector Borne Diseases   (United States)

Author keywords

Anopheles gambiae; Arthropod viruses; Bioinformatics; Flavivirus; Metagenomics; Mononegavirus; Pathogen discovery; Surveillance; Totivirus; Virome; Virus discovery

Indexed keywords

ADULT; ANOPHELES; ANOPHELES FUNESTUS; ANOPHELES GAMBIAE; ANOPHELES RUFIPES; ARTICLE; BURKINA FASO; CONTROLLED STUDY; FLAVIVIRUS; GENE SEQUENCE; LIBERIA; METAGENOMICS; MONONEGAVIRALES; NONHUMAN; PRIORITY JOURNAL; SENEGAL; TOTIVIRUS; VIRUS GENOME; VIRUS IDENTIFICATION; AMINO ACID SEQUENCE; ANIMAL; BIODIVERSITY; CLASSIFICATION; GENETICS; INSECT VECTOR; INSECT VIRUS; METAGENOME; MICROFLORA; OPEN READING FRAME; PHYLOGENY; RNA VIRUS; VIROLOGY; VIRUS GENE;

AMINO ACID SEQUENCE; ANIMALS; ANOPHELES GAMBIAE; BIODIVERSITY; BURKINA FASO; FLAVIVIRUS; GENES, VIRAL; GENOME, VIRAL; INSECT VECTORS; INSECT VIRUSES; LIBERIA; METAGENOME; METAGENOMICS; MICROBIOTA; OPEN READING FRAMES; PHYLOGENY; RNA VIRUSES; SENEGAL; TOTIVIRUS;

EID: 84987981859     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2016.07.031     Document Type: Article

References (99)

1. Alout, H., Krajacich, B.J., Meyers, J.I., Grubaugh, N.D., Brackney, D.E., Kobylinski, K.C., Diclaro, J.W. 2nd, Bolay, F.K., Fakoli, L.S., Diabate, A., Dabire, R.K., Bougma, R.W., Foy, B.D., Evaluation of ivermectin mass drug administration for malaria transmission control across different West African environments. Malar. J., 13, 2014, 417.
2. Altschul, S.F., Gish, W., Miller, W., Myers, E.W., Lipman, D.J., Basic local alignment search tool. J. Mol. Biol. 215 (1990), 403–410.
3. Altschul, S.F., Madden, T.L., Schaffer, A.A., Zhang, J., Zhang, Z., Miller, W., Lipman, D.J., Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res. 25 (1997), 3389–3402.
4. Attoui, H., Mohd Jaafar, F., Belhouchet, M., Biagini, P., Cantaloube, J.-F., de Micco, P., de Lamballerie, X., Expansion of family Reoviridae to include nine-segmented dsRNA viruses: Isolation and characterization of a new virus designated aedes pseudoscutellaris reovirus assigned to a proposed genus (Dinovernavirus). Virology 343 (2005), 212–223.
5. Auguste, A.J., Carrington, C.V., Forrester, N.L., Popov, V.L., Guzman, H., Widen, S.G., Wood, T.G., Weaver, S.C., Tesh, R.B., Characterization of a novel Negevirus and a novel Bunyavirus isolated from Culex (Culex) declarator mosquitoes in Trinidad. J. Gen. Virol. 95 (2014), 481–485.
6. Auguste, A.J., Kaelber, J.T., Fokam, E.B., Guzman, H., Carrington, C.V., Erasmus, J.H., Kamgang, B., Popov, V.L., Jakana, J., Liu, X., Wood, T.G., Widen, S.G., Vasilakis, N., Tesh, R.B., Chiu, W., Weaver, S.C., A newly isolated reovirus has the simplest genomic and structural organization of any reovirus. J. Virol. 89 (2015), 676–687.
7. Bankevich, A., Nurk, S., Antipov, D., Gurevich, A.A., Dvorkin, M., Kulikov, A.S., Lesin, V.M., Nikolenko, S.I., Pham, S., Prjibelski, A.D., Pyshkin, A.V., Sirotkin, A.V., Vyahhi, N., Tesler, G., Alekseyev, M.A., Pevzner, P.A., SPAdes: a new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol.: J. Comput. Mol. Cell Biol. 19 (2012), 455–477.
8. Blitvich, B.J., Firth, A.E., Insect-specific flaviviruses: a systematic review of their discovery, host range, mode of transmission, superinfection exclusion potential and genomic organization. Viruses 7 (2015), 1927–1959.
9. Boissière, A., Tchioffo, M.T., Bachar, D., Abate, L., Marie, A., Nsango, S.E., Shahbazkia, H.R., Awono-Ambene, P.H., Levashina, E.A., Christen, R., Morlais, I., Midgut microbiota of the malaria mosquito vector Anopheles gambiae and interactions with Plasmodium falciparum Infection. PLoS Pathog., 8, 2012, e1002742.
10. Bolger, A.M., Lohse, M., Usadel, B., Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinforma. (Oxf., Engl.) 30 (2014), 2114–2120.
11. Bolling, B., Weaver, S., Tesh, R., Vasilakis, N., Insect-specific virus discovery: significance for the arbovirus community. Viruses, 7, 2015, 2851.
12. Bolling, B.G., Olea-Popelka, F.J., Eisen, L., Moore, C.G., Blair, C.D., Transmission dynamics of an insect-specific flavivirus in a naturally infected Culex pipiens laboratory colony and effects of co-infection on vector competence for West Nile virus. Virology 427 (2012), 90–97.
13. Buck, M., Nilsson, L.K., Brunius, C., Dabire, R.K., Hopkins, R., Terenius, O., Bacterial associations reveal spatial population dynamics in Anopheles gambiae mosquitoes. Sci. Rep., 6, 2016, 22806.
14. Carissimo, G., Eiglmeier, K., Reveillaud, J., Holm, I., Diallo, M., Diallo, D., Vantaux, A., Kim, S., Ménard, D., Siv, S., Belda, E., Bischoff, E., Antoniewski, C., Vernick, K.D., Identification and characterization of two novel RNA viruses from anopheles gambiae species complex mosquitoes. PloS One, 11, 2016, e0153881.
15. Chandler, J.A., Liu, R.M., Bennett, S.N., RNA shotgun metagenomic sequencing of northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front. Microbiol., 6, 2015, 185.
16. 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 464–465 (2014), 312–319.
17. Cirimotich, C.M., Dong, Y., Clayton, A.M., Sandiford, S.L., Souza-Neto, J.A., Mulenga, M., Dimopoulos, G., Natural microbe-mediated refractoriness to Plasmodium infection in Anopheles gambiae. Science 332 (2011), 855–858.
18. Cook, P.E., McGraw, E.A., Wolbachia pipientis: an expanding bag of tricks to explore for disease control. Trends Parasitol. 26 (2010), 373–375.
19. Cook, S., Bennett, S.N., Holmes, E.C., De Chesse, R., Moureau, G., de Lamballerie, X., Isolation of a new strain of the flavivirus cell fusing agent virus in a natural mosquito population from Puerto Rico. J. Gen. Virol. 87 (2006), 735–748.
20. Cook, S., Chung, B.Y., Bass, D., Moureau, G., Tang, S., McAlister, E., Culverwell, C.L., Glucksman, E., Wang, H., Brown, T.D., Gould, E.A., Harbach, R.E., de Lamballerie, X., Firth, A.E., Novel virus discovery and genome reconstruction from field RNA samples reveals highly divergent viruses in dipteran hosts. PloS One, 8, 2013, e80720.
21. Cook, S., Moureau, G., Kitchen, A., Gould, E.A., de Lamballerie, X., Holmes, E.C., Harbach, R.E., Molecular evolution of the insect-specific flaviviruses. J. Gen. Virol. 93 (2012), 223–234.
22. Crochu, S., Cook, S., Attoui, H., Charrel, R.N., De Chesse, R., Belhouchet, M., Lemasson, J.J., de Micco, P., de Lamballerie, X., Sequences of flavivirus-related RNA viruses persist in DNA form integrated in the genome of Aedes spp. mosquitoes. J. Gen. Virol. 85 (2004), 1971–1980.
23. Dantas, M.D., Cavalcante, G.H., Oliveira, R.A., Lanza, D.C., New insights about ORF1 coding regions support the proposition of a new genus comprising arthropod viruses in the family Totiviridae. Virus Res. 211 (2016), 159–164.
24. Dong, Y., Manfredini, F., Dimopoulos, G., Implication of the mosquito midgut microbiota in the defense against malaria parasites. PLoS Pathog., 5, 2009, e1000423.
25. Fauver, J.R., Pecher, L., Schurich, J.A., Bolling, B.G., Calhoon, M., Grubaugh, N.D., Burkhalter, K.L., Eisen, L., Andre, B.G., Nasci, R.S., LeBailly, A., Ebel, G.D., Moore, C.G., Temporal and spatial variability of entomological risk indices for west nile virus infection in Northern Colorado: 2006–2013. J. Med. Entomol., 2015.
26. Firth, A.E., Blitvich, B.J., Wills, N.M., Miller, C.L., Atkins, J.F., Evidence for ribosomal frameshifting and a novel overlapping gene in the genomes of insect-specific flaviviruses. Virology 399 (2010), 153–166.
27. Gendrin, M., Rodgers, F.H., Yerbanga, R.S., Ouedraogo, J.B., Basanez, M.G., Cohuet, A., Christophides, G.K., Antibiotics in ingested human blood affect the mosquito microbiota and capacity to transmit malaria. Nat. Commun., 6, 2015, 5921.
28. Grubaugh, N.D., Massey, A., Shives, K.D., Stenglein, M.D., Ebel, G.D., Beckham, J.D., West nile virus population structure, injury, and interferon-stimulated gene expression in the brain from a fatal case of encephalitis. Open Forum Infect. Dis., 3, 2016, ofv182.
29. Grubaugh, N.D., Sharma, S., Krajacich, B.J., Fakoli Iii, L.S., Bolay, F.K., Diclaro Ii, J.W., Johnson, W.E., Ebel, G.D., Foy, B.D., Brackney, D.E., Xenosurveillance: a novel mosquito-based approach for examining the human-pathogen landscape. PLoS Negl. Trop. Dis., 9, 2015, e0003628.
30. Hermanns, K., Zirkel, F., Kurth, A., Drosten, C., Junglen, S., Cimodo virus belongs to a novel lineage of reoviruses isolated from African mosquitoes. J. Gen. Virol. 95 (2014), 905–909.
31. Holt, R.A., Subramanian, G.M., Halpern, A., Sutton, G.G., Charlab, R., Nusskern, D.R., Wincker, P., Clark, A.G., Ribeiro, J.M., Wides, R., Salzberg, S.L., Loftus, B., Yandell, M., Majoros, W.H., Rusch, D.B., Lai, Z., Kraft, C.L., Abril, J.F., Anthouard, V., Arensburger, P., Atkinson, P.W., Baden, H., de Berardinis, V., Baldwin, D., Benes, V., Biedler, J., Blass, C., Bolanos, R., Boscus, D., Barnstead, M., Cai, S., Center, A., Chaturverdi, K., Christophides, G.K., Chrystal, M.A., Clamp, M., Cravchik, A., Curwen, V., Dana, A., Delcher, A., Dew, I., Evans, C.A., Flanigan, M., Grundschober-Freimoser, A., Friedli, L., Gu, Z., Guan, P., Guigo, R., Hillenmeyer, M.E., Hladun, S.L., Hogan, J.R., Hong, Y.S., Hoover, J., Jaillon, O., Ke, Z., Kodira, C., Kokoza, E., Koutsos, A., Letunic, I., Levitsky, A., Liang, Y., Lin, J.J., Lobo, N.F., Lopez, J.R., Malek, J.A., McIntosh, T.C., Meister, S., Miller, J., Mobarry, C., Mongin, E., Murphy, S.D., O'Brochta, D.A., Pfannkoch, C., Qi, R., Regier, M.A., Remington, K., Shao, H., Sharakhova, M.V., Sitter, C.D., Shetty, J., Smith, T.J., Strong, R., Sun, J., Thomasova, D., Ton, L.Q., Topalis, P., Tu, Z., Unger, M.F., Walenz, B., Wang, A., Wang, J., Wang, M., Wang, X., Woodford, K.J., Wortman, J.R., Wu, M., Yao, A., Zdobnov, E.M., Zhang, H., Zhao, Q., Zhao, S., Zhu, S.C., Zhimulev, I., Coluzzi, M., della Torre, A., Roth, C.W., Louis, C., Kalush, F., Mural, R.J., Myers, E.W., Adams, M.D., Smith, H.O., Broder, S., Gardner, M.J., Fraser, C.M., Birney, E., Bork, P., Brey, P.T., Venter, J.C., Weissenbach, J., Kafatos, F.C., Collins, F.H., Hoffman, S.L., The genome sequence of the malaria mosquito Anopheles gambiae. Science 298 (2002), 129–149.
32. Hoshino, K., Isawa, H., Tsuda, Y., Yano, K., Sasaki, T., Yuda, M., Takasaki, T., Kobayashi, M., Sawabe, K., Genetic characterization of a new insect flavivirus isolated from Culex pipiens mosquito in Japan. Virology 359 (2007), 405–414.
33. Huang, Y., Mi, Z., Zhuang, L., Ma, M., An, X., Liu, W., Cao, W., Tong, Y., Presence of entomobirnaviruses in Chinese mosquitoes in the absence of Dengue virus co-infection. J. Gen. Virol. 94 (2013), 663–667.
34. Hughes, G.L., Rivero, A., Rasgon, J.L., Wolbachia can enhance plasmodium infection in mosquitoes: implications for malaria control?. PLoS Pathog., 10, 2014, e1004182.
35. Isawa, H., Kuwata, R., Hoshino, K., Tsuda, Y., Sakai, K., Watanabe, S., Nishimura, M., Satho, T., Kataoka, M., Nagata, N., Hasegawa, H., Bando, H., Yano, K., Sasaki, T., Kobayashi, M., Mizutani, T., Sawabe, K., Identification and molecular characterization of a new non segmented double-stranded RNA virus isolated from Culex mosquitoes in Japan. Virus Res. 155 (2011), 147–155.
36. Junglen, S., Drosten, C., Virus discovery and recent insights into virus diversity in arthropods. Curr. Opin. Microbiol. 16 (2013), 507–513.
37. Kallies, R., Kopp, A., Zirkel, F., Estrada, A., Gillespie, T.R., Drosten, C., Junglen, S., Genetic characterization of goutanap virus, a novel virus related to negeviruses, cileviruses and higreviruses. Viruses 6 (2014), 4346–4357.
38. Katoh, K., Standley, D.M., MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30 (2013), 772–780.
39. Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., Thierer, T., Ashton, B., Meintjes, P., Drummond, A., Geneious Basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformation 28 (2012), 1647–1649.
40. Kenney, J.L., Solberg, O.D., Langevin, S.A., Brault, A.C., Characterization of a novel insect-specific flavivirus from Brazil: potential for inhibition of infection of arthropod cells with medically important flaviviruses. J. Gen. Virol. 95 (2014), 2796–2808.
41. Kent, R.J., Crabtree, M.B., Miller, B.R., Transmission of West Nile virus by Culex quinquefasciatus say infected with Culex Flavivirus Izabal. PLoS Negl. Trop. Dis., 4, 2010, e671.
42. Koyama, S., Urayama, S., Ohmatsu, T., Sassa, Y., Sakai, C., Takata, M., Hayashi, S., Nagai, M., Furuya, T., Moriyama, H., Satoh, T., Ono, S., Mizutani, T., Identification, characterization and full-length sequence analysis of a novel dsRNA virus isolated from the arboreal ant Camponotus yamaokai. J. Gen. Virol. 96 (2015), 1930–1937.
43. Krajacich, B.J., Slade, J.R., Mulligan, R.F., LaBrecque, B., Alout, H., Grubaugh, N.D., Meyers, J.I., Fakoli, L.S. 3rd, Bolay, F.K., Brackney, D.E., Burton, T.A., Seaman, J.A., Diclaro, J.W. 2nd, Dabire, R.K., Foy, B.D., Sampling host-seeking anthropophilic mosquito vectors in west Africa: comparisons of an active human-baited tent-trap against gold standard methods. Am. J. Trop. Med. Hyg. 92 (2015), 415–421.
44. Krishna, S.S., Majumdar, I., Grishin, N.V., Structural classification of zinc fingers: survey and summary. Nucleic Acids Res. 31 (2003), 532–550.
45. Kuhn, J.H., Bekal, S., Caì, Y., Clawson, A.N., Domier, L.L., Herrel, M., Jahrling, P.B., Kondo, H., Lambert, K.N., Mihindukulasuriya, K.A., Nowotny, N., Radoshitzky, S.R., Schneider, U., Staeheli, P., Suzuki, N., Tesh, R.B., Wang, D., Wang, L.-F., Dietzgen, R.G., Nyamiviridae: proposal for a new family in the order Mononegavirales. Arch. Virol., 158, 2013, 10.1007/s00705-00013-01674-y.
46. Kuhn, J.H., Durrwald, R., Bao, Y., Briese, T., Carbone, K., Clawson, A.N., deRisi, J.L., Garten, W., Jahrling, P.B., Kolodziejek, J., Rubbenstroth, D., Schwemmle, M., Stenglein, M., Tomonaga, K., Weissenbock, H., Nowotny, N., Taxonomic reorganization of the family Bornaviridae. Arch. Virol. 160 (2015), 621–632.
47. Kuno, G., Chang, G.J., Tsuchiya, K.R., Karabatsos, N., Cropp, C.B., Phylogeny of the genus Flavivirus. J. Virol. 72 (1998), 73–83.
48. 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. 85 (2011), 6185–6196.
49. Kuwata, R., Satho, T., Isawa, H., Yen, N.T., Phong, T.V., Nga, P.T., Kurashige, T., Hiramatsu, Y., Fukumitsu, Y., Hoshino, K., Sasaki, T., Kobayashi, M., Mizutani, T., Sawabe, K., Characterization of Dak Nong virus, an insect nidovirus isolated from Culex mosquitoes in Vietnam. Arch. Virol. 158 (2013), 2273–2284.
50. Ladner, J.T., Beitzel, B., Chain, P.S., Davenport, M.G., Donaldson, E.F., Frieman, M., Kugelman, J.R., Kuhn, J.H., O'Rear, J., Sabeti, P.C., Wentworth, D.E., Wiley, M.R., Yu, G.Y., Sozhamannan, S., Bradburne, C., Palacios, G., Standards for sequencing viral genomes in the era of high-throughput sequencing. mBio, 5, 2014 e01360-01314.
51. Lanciotti, R.S., Ludwig, M.L., Rwaguma, E.B., Lutwama, J.J., Kram, T.M., Karabatsos, N., Cropp, B.C., Miller, B.R., Emergence of Epidemic O'nyong-nyong fever in Uganda after a 35-Year absence: genetic characterization of the virus. Virology 252 (1998), 258–268.
52. Langmead, B., Salzberg, S.L., Fast gapped-read alignment with Bowtie 2. Nat. Methods 9 (2012), 357–359.
53. Lee, J.S., Grubaugh, N.D., Kondig, J.P., Turell, M.J., Kim, H.C., Klein, T.A., O'Guinn, M.L., Isolation and genomic characterization of Chaoyang virus strain ROK144 from Aedes vexans nipponii from the Republic of Korea. Virology 435 (2013), 220–224.
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.
55. Li, W., Godzik, A., Cd-hit: a fast program for clustering and comparing large sets of protein or nucleotide sequences. Bioinformation 22 (2006), 1658–1659.
56. Lutwama, J.J., Kayondo, J., Savage, H.M., Burkot, T.R., Miller, B.R., Epidemic O'Nyong-Nyong fever in southcentral Uganda, 1996–1997: entomologic studies in Bbaale village, Rakai District. Am. J. Trop. Med. Hyg. 61 (1999), 158–162.
57. Marklewitz, M., Gloza-Rausch, F., Kurth, A., Kummerer, B.M., Drosten, C., Junglen, S., First isolation of an Entomobirnavirus from free-living insects. J. Gen. Virol. 93 (2012), 2431–2435.
58. Marklewitz, M., Handrick, S., Grasse, W., Kurth, A., Lukashev, A., Drosten, C., Ellerbrok, H., Leendertz, F.H., Pauli, G., Junglen, S., Gouleako virus isolated from West African mosquitoes constitutes a proposed novel genus in the family Bunyaviridae. J. Virol. 85 (2011), 9227–9234.
59. Marklewitz, M., Zirkel, F., Rwego, I.B., Heidemann, H., Trippner, P., Kurth, A., Kallies, R., Briese, T., Lipkin, W.I., Drosten, C., Gillespie, T.R., Junglen, S., Discovery of a unique novel clade of mosquito-associated bunyaviruses. J. Virol. 87 (2013), 12850–12865.
60. Martinez, J., Lepetit, D., Ravallec, M., Fleury, F., Varaldi, J., Additional heritable virus in the parasitic wasp Leptopilina boulardi: prevalence, transmission and phenotypic effects. J. Gen. Virol. 97 (2016), 523–535.
61. Mihindukulasuriya, K.A., Nguyen, N.L., Wu, G., Huang, H.V., da Rosa, A.P., Popov, V.L., Tesh, R.B., Wang, D., Nyamanini and midway viruses define a novel taxon of RNA viruses in the order Mononegavirales. J. Virol. 83 (2009), 5109–5116.
62. Misencik, M.J., Grubaugh, N.D., Andreadis, T.G., Ebel, G.D., Armstrong, P.M., Isolation of a novel insect-specific flavivirus from culiseta melanura in the Northeastern United States. Vector Borne Zoonotic Dis. 16 (2016), 181–190.
63. Nabeshima, T., Inoue, S., Okamoto, K., Posadas-Herrera, G., Yu, F., Uchida, L., Ichinose, A., Sakaguchi, M., Sunahara, T., Buerano, C.C., Tadena, F.P., Orbita, I.B., Natividad, F.F., Morita, K., Tanay virus, a new species of virus isolated from mosquitoes in the Philippines. J. Gen. Virol. 95 (2014), 1390–1395.
64. Nasar, F., Palacios, G., Gorchakov, R.V., Guzman, H., Da Rosa, A.P., Savji, N., Popov, V.L., Sherman, M.B., Lipkin, W.I., Tesh, R.B., Weaver, S.C., Eilat virus, a unique alphavirus with host range restricted to insects by RNA replication. Proc. Natl. Acad. Sci. USA 109 (2012), 14622–14627.
65. Newman, C.M., Cerutti, F., Anderson, T.K., Hamer, G.L., Walker, E.D., Kitron, U.D., Ruiz, M.O., Brawn, J.D., Goldberg, T.L., Culex flavivirus and West Nile virus mosquito co infection and positive ecological association in Chicago. U. S. Vector Borne Zoonotic Dis. 11 (2011), 1099–1105.
66. Nga, P.T., Parquet, Md.C., Lauber, C., Parida, M., Nabeshima, T., Yu, F., Thuy, N.T., Inoue, S., Ito, T., Okamoto, K., Ichinose, A., Snijder, E.J., Morita, K., Gorbalenya, A.E., Discovery of the first insect nidovirus, a missing evolutionary link in the emergence of the largest RNA virus genomes. PLoS Pathog., 7, 2011, e1002215.
67. Poulos, B.T., Tang, K.F., Pantoja, C.R., Bonami, J.R., Lightner, D.V., Purification and characterization of infectious myonecrosis virus of penaeid shrimp. J. Gen. Virol. 87 (2006), 987–996.
68. Pybus, O.G., Rambaut, A., Holmes, E.C., Harvey, P.H., New inferences from tree shape: numbers of missing taxa and population growth rates. Syst. Biol. 51 (2002), 881–888.
69. 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 Res. 147 (2010), 17–24.
70. Ren, X., Hoiczyk, E., Rasgon, J.L., Viral paratransgenesis in the malaria vector Anopheles gambiae. PLoS Pathog., 4, 2008, e1000135.
71. Ronquist, F., Huelsenbeck, J.P., MrBayes 3: bayesian phylogenetic inference under mixed models. Bioinformation 19 (2003), 1572–1574.
72. Schuster, S., Zirkel, F., Kurth, A., van Cleef, K.W., Drosten, C., van Rij, R.P., Junglen, S., A unique nodavirus with novel features: mosinovirus expresses two subgenomic RNAs, a capsid gene of unknown origin, and a suppressor of the antiviral RNA interference pathway. J. Virol. 88 (2014), 13447–13459.
73. Soding, J., Biegert, A., Lupas, A.N., The HHpred interactive server for protein homology detection and structure prediction. Nucleic Acids Res. 33 (2005), W244–W248.
74. Spear, A., Sisterson, M.S., Yokomi, R., Stenger, D.C., Plant-feeding insects harbor double-stranded RNA viruses encoding a novel proline-alanine rich protein and a polymerase distantly related to that of fungal viruses. Virology 404 (2010), 304–311.
75. Suh, E., Mercer, D.R., Fu, Y., Dobson, S.L., Pathogenicity of life-shortening Wolbachia in Aedes albopictus after transfer from Drosophila melanogaster. Appl. Environ. Microbiol. 75 (2009), 7783–7788.
76. Suzuki, Y., Niu, G., Hughes, G.L., Rasgon, J.L., A viral over-expression system for the major malaria mosquito Anopheles gambiae. Sci. Rep., 4, 2014, 5127.
77. Talavera, G., Castresana, J., Improvement of phylogenies after removing divergent and ambiguously aligned blocks from protein sequence alignments. Syst. Biol. 56 (2007), 564–577.
78. 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. 88 (2014), 11480–11492.
79. Tyler, S., Bolling, B.G., Blair, C.D., Brault, A.C., Pabbaraju, K., Armijos, M.V., Clark, D.C., Calisher, C.H., Drebot, M.A., Distribution and phylogenetic comparisons of a novel mosquito flavivirus sequence present in Culex tarsalis Mosquitoes from western Canada with viruses isolated in California and Colorado. Am. J. Trop. Med. Hyg. 85 (2011), 162–168.
80. Van Regenmortel, M.H.V., Fauquet, C.M., Bishop, D.H.L., Carstens, E.B., Estes, M.K., Lemon, S.M., Maniloff, J., Mayo, M.A., McGeoch, D.J., Pringle, C.R., Wickner, R.B., 2000b. Order Mononegavirales, Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses Academic Press, pp. 525–530.
81. Van Regenmortel, M.H.V., Fauquet, C.M., Bishop, D.H.L., Carstens, E.B., Estes, M.K., Lemon, S.M., Maniloff, J., Mayo, M.A., McGeoch, D.J., Pringle, C.R., Wickner, R.B., 2000b. Order Mononegavirales, Virus Taxonomy. Seventh Report of the International Committee on Taxonomy of Viruses Academic Press, pp. 525–530.
82. Vancini, R., Paredes, A., Ribeiro, M., Blackburn, K., Ferreira, D., Kononchik, J.P. Jr., Hernandez, R., Brown, D., Espirito Santo virus: a new birnavirus that replicates in insect cells. J. Virol. 86 (2012), 2390–2399.
83. Vasilakis, N., Castro-Llanos, F., Widen, S.G., Aguilar, P.V., Guzman, H., Guevara, C., Fernandez, R., Auguste, A.J., Wood, T.G., Popov, V., Mundal, K., Ghedin, E., Kochel, T.J., Holmes, E.C., Walker, P.J., Tesh, R.B., Arboretum and Puerto Almendras viruses: two novel rhabdoviruses isolated from mosquitoes in Peru. J. Gen. Virol. 95 (2014), 787–792.
84. Vasilakis, N., Forrester, N.L., Palacios, G., Nasar, F., Savji, N., Rossi, S.L., Guzman, H., Wood, T.G., Popov, V., Gorchakov, R., González, A.V., Haddow, A.D., Watts, D.M., da Rosa, A.P.A.T., Weaver, S.C., Lipkin, W.I., Tesh, R.B., Negevirus: a proposed new taxon of insect-specific viruses with wide geographic distribution. J. Virol. 87 (2013), 2475–2488.
85. Vasilakis, N., Guzman, H., Firth, C., Forrester, N.L., Widen, S.G., Wood, T.G., Rossi, S.L., Ghedin, E., Popov, V., Blasdell, K.R., Walker, P.J., Tesh, R.B., Mesoniviruses are mosquito-specific viruses with extensive geographic distribution and host range. Virol. J., 11, 2014, 97.
86. Vasilakis, N., Tesh, R.B., Insect-specific viruses and their potential impact on arbovirus transmission. Curr. Opin. Virol. 15 (2015), 69–74.
87. Wang, L., Lv, X., Zhai, Y., Fu, S., Wang, D., Rayner, S., Tang, Q., Liang, G., Genomic characterization of a novel virus of the family Tymoviridae isolated from mosquitoes. PloS One, 7, 2012, e39845.
88. Warrilow, D., Watterson, D., Hall, R.A., Davis, S.S., Weir, R., Kurucz, N., Whelan, P., Allcock, R., Hall-Mendelin, S., O'Brien, C.A., Hobson-Peters, J., A new species of mesonivirus from the Northern Territory, Australia. PloS One, 9, 2014, e91103.
89. Weiss, B., Aksoy, S., Microbiome influences on insect host vector competence. Trends Parasitol. 27 (2011), 514–522.
90. World Health Organization, 2015. World Malaria Report.
91. World Health Organization, 2016. Lymphatic filariasis Epidemiology.
92. Wu, Q., Luo, Y., Lu, R., Lau, N., Lai, E.C., Li, W.X., Ding, S.W., Virus discovery by deep sequencing and assembly of virus-derived small silencing RNAs. Proc. Natl. Acad. Sci. USA 107 (2010), 1606–1611.
93. Wu, T.D., Nacu, S., Fast and SNP-tolerant detection of complex variants and splicing in short reads. Bioinformation 26 (2010), 873–881.
94. Yamao, T., Eshita, Y., Kihara, Y., Satho, T., Kuroda, M., Sekizuka, T., Nishimura, M., Sakai, K., Watanabe, S., Akashi, H., Rongsriyam, Y., Komalamisra, N., Srisawat, R., Miyata, T., Sakata, A., Hosokawa, M., Nakashima, M., Kashige, N., Miake, F., Fukushi, S., Nakauchi, M., Saijo, M., Kurane, I., Morikawa, S., Mizutani, T., Novel virus discovery in field-collected mosquito larvae using an improved system for rapid determination of viral RNA sequences (RDV ver4.0). Arch. Virol. 154 (2009), 153–158.
95. Zabalou, S., Riegler, M., Theodorakopoulou, M., Stauffer, C., Savakis, C., Bourtzis, K., Wolbachia-induced cytoplasmic incompatibility as a means for insect pest population control. Proc. Natl. Acad. Sci. USA 101 (2004), 15042–15045.
96. Zhai, Y., Attoui, H., Mohd Jaafar, F., Wang, H.Q., Cao, Y.X., Fan, S.P., Sun, Y.X., Liu, L.D., Mertens, P.P., Meng, W.S., Wang, D., Liang, G., Isolation and full-length sequence analysis of Armigeres subalbatus totivirus, the first totivirus isolate from mosquitoes representing a proposed novel genus (Artivirus) of the family Totiviridae. J. Gen. Virol. 91 (2010), 2836–2845.
97. Zhao, Y., Tang, H., Ye, Y., RAPSearch2: a fast and memory-efficient protein similarity search tool for next-generation sequencing data. Bioinformation 28 (2012), 125–126.
98. Zirkel, F., Kurth, A., Quan, P.L., Briese, T., Ellerbrok, H., Pauli, G., Leendertz, F.H., Lipkin, W.I., Ziebuhr, J., Drosten, C., Junglen, S., An insect nidovirus emerging from a primary tropical rainforest. mBio, 2, 2011 e00077-00011.
99. Zirkel, F., Roth, H., Kurth, A., Drosten, C., Ziebuhr, J., Junglen, S., Identification and characterization of genetically divergent members of the newly established family Mesoniviridae. J. Virol. 87 (2013), 6346–6358.