Advertisement

Virologica Sinica

, Volume 33, Issue 1, pp 59–66 | Cite as

Comparative Metagenomic Profiling of Viromes Associated with Four Common Mosquito Species in China

  • Han Xia
  • Yujuan Wang
  • Chenyan Shi
  • Evans Atoni
  • Lu Zhao
  • Zhiming Yuan
Research Article

Abstract

Vast viruses are thought to be associated with mosquitoes. Anopheles sinensis, Armigeres subalbatus, Culex quinquefasciatus, and Culex tritaeniorhynchus are very common mosquito species in China, and whether the virome structure in each species is species-specific has not been evaluated. In this study, a total of 2222 mosquitoes were collected from the same geographic location, and RNAs were sequenced using the Illumina Miseq platform. After querying to the Refseq database, a total of 3,435,781, 2,223,509, 5,727,523, and 6,387,867 paired-end reads were classified under viral sequences from An. sinensis, Ar. subalbatus, Cx. quinquefasciatus, and Cx. tritaeniorhynchus, respectively, with the highest prevalence of virus-associated reads being observed in Cx. quinquefasciatus. The metagenomic comparison analysis showed that the virus-related reads were distributed across 26 virus families, together with an unclassified group of viruses. Anelloviridae, Circoviridae, Genomoviridae, Iridoviridae, Mesoniviridae, Microviridae, Myoviridae, Parvoviridae, Phenuiviridae, and Podoviridae were the top ten significantly different viral families among the four species. Further analysis reveals that the virome is species-specific in four mosquito samples, and several viral sequences which maybe belong to novel viruses are discovered for the first time in those mosquitoes. This investigation provides a basis for a comprehensive knowledge on the mosquito virome status in China.

Keywords

Mosquito Comparative metagenomics Virome China 

Notes

Acknowledgements

We thank the Hubei Provincial Center for Disease Control and Prevention for assistance in mosquito sampling within the Hubei Province. This work was supported by the Ministry of Science and Technology of China (Science and Technology Basic Work Program 2013FY113500).

Author Contributions

HX and ZY designed the experiments. YW, and LZ, carried out the experiments. HX, YW, CS, and AE analyzed the data. HX, YW and ZY wrote the paper. HX and CS checked and finalized the manuscript. All authors read and approved the final manuscript.

Compliance with Ethics Standards

Conflict of interest

The authors declare that they have no conflict of interest.

Animal and Human Rights Statement

This article does not contain any studies with human or animal subjects performed by any of the authors.

Supplementary material

12250_2018_15_MOESM1_ESM.xlsx (11 kb)
Supplementary Table S1 Metacomp analysis result (XLSX 10 kb)

References

  1. Bolling B, Weaver S, Tesh R, Vasilakis N (2015) Insect-specific virus discovery: significance for the arbovirus community. Viruses 7:4911–4928.  https://doi.org/10.3390/v7092851 CrossRefPubMedPubMedCentralGoogle Scholar
  2. Brinkmann A, Nitsche A, Kohl C (2016) Viral metagenomics on blood-feeding arthropods as a tool for human disease surveillance. Int J Mol Sci.  https://doi.org/10.3390/ijms17101743 PubMedPubMedCentralGoogle Scholar
  3. Chandler JA, Liu RM, Bennett SN (2015) RNA shotgun metagenomic sequencing of Northern California (USA) mosquitoes uncovers viruses, bacteria, and fungi. Front Microbiol 6:185.  https://doi.org/10.3389/fmicb.2015.00185 CrossRefPubMedPubMedCentralGoogle Scholar
  4. Chen WJ, Dong CF, Chiou LY, Chuang WL (2000) Potential role of Armigeres subalbatus (Diptera: Culicidae) in the transmission of Japanese encephalitis virus in the absence of rice culture on Liu-chiu islet, Taiwan. J Med Entomol 37:108–113.  https://doi.org/10.1603/0022-2585-37.1.108 CrossRefPubMedGoogle Scholar
  5. Conway MJ, Colpitts TM, Fikrig E (2014) Role of the vector in arbovirus transmission. Annu Rev Virol 1:71–88.  https://doi.org/10.1146/annurev-virology-031413-085513 CrossRefPubMedGoogle Scholar
  6. Farajollahi A, Fonseca DM, Kramer LD, Marm Kilpatrick A (2011) “Bird biting” mosquitoes and human disease: a review of the role of Culex pipiens complex mosquitoes in epidemiology. Infect Genet Evol 11:1577–1585.  https://doi.org/10.1016/j.meegid.2011.08.013 CrossRefPubMedPubMedCentralGoogle Scholar
  7. Frey KG, Biser T, Hamilton T, Santos CJ, Pimentel G, Mokashi VP, Bishop-Lilly KA (2016) Bioinformatic characterization of mosquito viromes within the Eastern United States and Puerto Rico: discovery of novel viruses. Evol Bioinform 12:1–12.  https://doi.org/10.4137/EBO.S38518 CrossRefGoogle Scholar
  8. Lauber C, Ziebuhr J, Junglen S, Drosten C, Zirkel F, Nga PT, Morita K, Snijder EJ, Gorbalenya AE (2012) Mesoniviridae: a proposed new family in the order Nidovirales formed by a single species of mosquito-borne viruses. Arch Virol 157:1623–1628.  https://doi.org/10.1007/s00705-012-1295-x CrossRefPubMedPubMedCentralGoogle Scholar
  9. Li W, Cao Y, Fu S, Wang J, Li M, Jiang S, Wang X, Xing S, Feng L, Wang Z, Shi Y, Zhao S, Wang H, Wang Z, Liang G (2014) Tahyna virus infection, a neglected arboviral disease in the Qinghai-Tibet Plateau of China. Vector Borne Zoonotic Dis 14:353–357.  https://doi.org/10.1089/vbz.2013.1351 CrossRefPubMedPubMedCentralGoogle Scholar
  10. Liu H, Li MH, Zhai YG, Meng WS, Sun XH, Cao YX, Fu SH, Wang HY, Xu LH, Tang Q, Liang GD (2010) Banna virus, China, 1987–2007. Emerg Infect Dis 16:514–517.  https://doi.org/10.3201/eid1603.091160 CrossRefPubMedPubMedCentralGoogle Scholar
  11. Liu H, Lu HJ, Liu ZJ, Jing J, Ren JQ, Liu YY, Lu F, Jin NY (2013) Japanese encephalitis virus in mosquitoes and swine in Yunnan province, China 2009–2010. Vector Borne Zoonotic Dis 13:41–49.  https://doi.org/10.1089/vbz.2012.1016 CrossRefPubMedPubMedCentralGoogle Scholar
  12. Menzel P, Ng KL, Krogh A (2016) Fast and sensitive taxonomic classification for metagenomics with Kaiju. Nat Commun 7:11257.  https://doi.org/10.1038/ncomms11257 CrossRefPubMedPubMedCentralGoogle Scholar
  13. Ng TFF, Willner DL, Lim YW, Schmieder R, Chau B, Nilsson C, Anthony S, Ruan Y, Rohwer F, Breitbart M (2011) Broad surveys of DNA viral diversity obtained through viral metagenomics of mosquitoes. PLoS ONE 6:e20579.  https://doi.org/10.1371/journal.pone.0020579 CrossRefPubMedPubMedCentralGoogle Scholar
  14. Nga PT, de Parquet MC, Lauber C, Parida M, Nabeshima T, Yu F, Thuy NT, Inoue S, Ito T, Okamoto K, Ichinose A, Snijder EJ, Morita K, Gorbalenya AE (2011) Discovery of the first insect nidovirus, a missing evolutionary link in the emergence of the largest RNA virus genomes. PLoS Pathog 7:e1002215.  https://doi.org/10.1371/journal.ppat.1002215 CrossRefPubMedPubMedCentralGoogle Scholar
  15. Rajavel AR (1992) Larval habitat of Armigeres subalbatus (COQ) and its characteristics in Pondicherry. Southeast Asian J Trop Med Public Health 23:470–473PubMedGoogle Scholar
  16. Samy AM, Elaagip AH, Kenawy MA, Ayres CFJ, Peterson AT, Soliman DE (2016) Climate change influences on the global potential distribution of the mosquito Culex quinquefasciatus, vector of West Nile virus and lymphatic filariasis. PLoS ONE 11:e0163863.  https://doi.org/10.1371/journal.pone.0163863 CrossRefPubMedPubMedCentralGoogle Scholar
  17. Self LS, Shin HK, Kim KH, Lee KW, Chow CY, Hong HK (1973) Ecological studies on Culex tritaeniorhynchus as a vector of Japanese encephalitis. Bull World Health Organ 49:41–47PubMedPubMedCentralGoogle Scholar
  18. Shi C, Liu Y, Hu X, Xiong J, Zhang B, Yuan Z (2015) A metagenomic survey of viral abundance and diversity in mosquitoes from Hubei province. PLoS ONE 10:e0129845.  https://doi.org/10.1371/journal.pone.0129845 CrossRefPubMedPubMedCentralGoogle Scholar
  19. Shi M, Lin XD, Tian JH, Chen LJ, Chen X, Li CX, Qin XC, Li J, Cao JP, Eden JS, Buchmann J, Wang W, Xu J, Holmes EC, Zhang YZ (2016) Redefining the invertebrate RNA virosphere. Nature 540:539–543CrossRefGoogle Scholar
  20. Tang Y, Diao Y, Chen H, Ou Q, Liu X, Gao X, Yu C, Wang L (2013) Isolation and genetic characterization of a tembusu virus strain isolated from mosquitoes in shandong, China. Transbound Emerg Dis 62:209–216.  https://doi.org/10.1111/tbed.12111 CrossRefPubMedGoogle Scholar
  21. Wang Y, Xia H, Zhang B, Liu X, Yuan Z (2017) Isolation and characterization of a novel mesonivirus from Culex mosquitoes in China. Virus Res 240:130–139.  https://doi.org/10.1016/j.virusres.2017.08.001 CrossRefPubMedGoogle Scholar
  22. Xia H, Hu C, Zhang D, Tang S, Zhang Z, Kou Z, Fan Z, Bente D, Zeng C, Li T (2015) Metagenomic profile of the viral communities in Rhipicephalus spp. ticks from Yunnan, China. PLoS ONE 10:e0121609.  https://doi.org/10.1371/journal.pone.0121609 CrossRefPubMedPubMedCentralGoogle Scholar
  23. Xu P, Wang Y, Zuo J, Lin J, Xu P (1990) New orbiviruses isolated from patients with unknown fever and encephalitis in Yunnan province. Chin J Virol 6:27–33Google Scholar
  24. Zhai P, Yang L, Guo X, Wang Z, Guo J, Wang X, Zhu H (2017) MetaComp: comprehensive analysis software for comparative meta-omics including comparative metagenomics. BMC Bioinformatics 18:434.  https://doi.org/10.1186/s12859-017-1849-8 CrossRefPubMedPubMedCentralGoogle Scholar
  25. Zhang HL (1990) The natural infection rate of mosquitoes by Japanese encephalitis B virus in Yunnan province. Zhonghua Yu Fang Yi Xue Za Zhi 24:265–267 (in Chinese) PubMedGoogle Scholar
  26. Zheng Y, Cao Y, Fu S, Cheng J, Zhao J, Dai P, Kong X, Liang G (2015) Isolation and identification of mosquito-borne arboviruses in Yuncheng city, Shanxi province, 2012. Zhonghua Liu Xing Bing Xue Za Zhi 36:368–373 (in Chinese) PubMedGoogle Scholar
  27. Zhu G, Xia H, Zhou H, Li J, Lu F, Liu Y, Cao J, Gao Q, Sattabongkot J (2013) Susceptibility of Anopheles sinensis to Plasmodium vivax in malarial outbreak areas of central China. Parasit Vectors 6:176.  https://doi.org/10.1186/1756-3305-6-176 CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Wuhan Institute of Virology, CAS and Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  1. 1.Key Laboratory of Special Pathogens and Biosafety, Wuhan Institute of VirologyChinese Academy of SciencesWuhanChina
  2. 2.University of Chinese Academy of SciencesBeijingChina
  3. 3.Department of Microbiology and Immunology, Laboratory of Viral Metagenomics, Rega Institute for Medical Research LeuvenKU Leuven - University of LeuvenLouvainBelgium

Personalised recommendations