Abstract
Mosquito transmitted viruses are responsible for an increasing burden of human disease. Despite this, little is known about the diversity and ecology of viruses within individual mosquito hosts. Here, using a meta-transcriptomic approach, we determined the viromes of 2,438 individual mosquitoes (81 species), spanning ~4,000 km along latitudes and longitudes in China. From these data we identified 393 viral species associated with mosquitoes, including 7 (putative) species of arthropod-borne viruses (that is, arboviruses). We identified potential mosquito species and geographic hotspots of viral diversity and arbovirus occurrence, and demonstrated that the composition of individual mosquito viromes was strongly associated with host phylogeny. Our data revealed a large number of viruses shared among mosquito species or genera, enhancing our understanding of the host specificity of insect-associated viruses. We also detected multiple virus species that were widespread throughout the country, perhaps reflecting long-distance mosquito dispersal. Together, these results greatly expand the known mosquito virome, linked viral diversity at the scale of individual insects to that at a country-wide scale, and offered unique insights into the biogeography and diversity of viruses in insect vectors.
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Data availability
The meta-transcriptomic sequencing reads (non-host, non-rRNA reads) generated in this study have been deposited in the CNSA (CNGB Sequence Archive) of CNGBdb (China National GeneBank database, https://db.cngb.org/cnsa/; project accession: CNP0004669). The assembled viral genome sequences have been deposited in the CNGBdb with the accession codes N_AAACQU010000000-N_AAADML010000000 (Supplementary Data 2). The sample metadata and other materials required to reproduce our computational and statistical results are provided in the GitHub repository along with code and scripts (https://github.com/Augustpan/MosquitoVirome).
Code availability
Code and scripts are provided in a GitHub repository (https://github.com/Augustpan/MosquitoVirome).
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Acknowledgements
This study was funded by grants from the National Key R&D Program of China (2021YFC2300900), National Natural Science Foundation of China (32270160), Shenzhen Science and Technology Program (JCYJ20210324124414040) and open project of BGI-Shenzhen Shenzhen 518000, China (BGIRSZ20210001). M.S. was supported by Shenzhen Science and Technology Program (KQTD20200820145822023), Guangdong Province ‘Pearl River Talent Plan’ Innovation, Entrepreneurship Team Project (2019ZT08Y464) and the Fund of Shenzhen Key Laboratory (ZDSYS20220606100803007). E.C.H. was supported by an NHMRC (Australia) Investigator Award (GNT2017197). We gratefully acknowledge colleagues at BGI-Shenzhen and China National Genebank (CNGB) for RNA extraction, library construction and sequencing.
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Contributions
Conceptualization: D. Wa., Junh. L., W.-C.W. and M.S.; methodology: Y.-F.P., H.Z., Q.-Y.G., D. Wa., Junh. L., W.-C.W. and M.S.; sample collection and processing: Q.-Y.G., G.-Y.L., G.-Y.X., S.-J.L., Ji. W., X. Ho., C.-H.Y., J.-X.C., Y.-Q.L., M.-W.P., S.-Q.M., J.-B.K., X.-X.C., X. Hu., Ju. W., C., Y.-H.W., J.-B.W., T.A. and W.-C.W.; data analysis: Y.-F.P., H.Z., Q.-Y.G., P.-B.S., D. Wa., Junh. L., W.-C.W. and M.S.; writing—original draft: Y.-F.P.; writing—review and editing: H.Z., Q.-Y.G., P.-B.S., J.-H.T., Y.F., K.L., W.-H.Y., D. Wu., G.T., B.Z., Z.R., S.P., G.-Y.L., S.-J.L., G.-Y.X., Ji. W., X. Ho., M.-W.P., J.-B.K., X.-X.C., C.-H.Y., S.-Q.M., Y.-Q.L., J.-X.C., Ju. W., C., Y.-H.W., J.-B.W., T.A., X. Hu., J.-S.E., Jun. L., D.G., G.L., X.J., E.C.H., B.L., D. Wa., Junh. L., W.-C.W. and M.S; funding acquisition: D. Wa., Junh. L., W.-C.W. and M.S.; resources (sampling): J.-H.T., Y.F., K.L., W.-H.Y., D. Wu., G.T., B.Z. and W.-C.W.; resources (computational): D. Wa., Junh. L. and M.S.; supervision: B.L., D. Wa., Junh. L., W.-C.W. and M.S.
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Extended data
Extended Data Fig. 1 Phylogenetic diversity of the 564 viruses determined in this study and the identification of mosquito-associated viruses.
The phylogenetic trees were estimated using hallmark proteins of respective viral taxa. Trees of RNA viruses were estimated at the ‘super clade’ level, while those of DNA virus were constructed at family level. The hallmark proteins utilized were the RNA-directed RNA replicase (RdRp) for all RNA viruses, Rep protein for the Circoviridae, NS1 protein for the Parvoviridae, and DNA polymerase for other DNA viruses. The number of mosquito-associated species and the total viral species is shown below the superclade names (number of mosquito-associated species / number of total species). Viral families were indicated with vertical lines and abbreviated family names (the suffixes ‘-viridae’ were omitted) on the right side of each tree.
Supplementary information
Supplementary Information
Supplementary Figs. 1–16 and Tables 1–14.
Supplementary Data 1 and 2
Supplementary Data 1. Sample and library metadata. Supplementary Data 2. Virus metadata.
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Pan, YF., Zhao, H., Gou, QY. et al. Metagenomic analysis of individual mosquito viromes reveals the geographical patterns and drivers of viral diversity. Nat Ecol Evol (2024). https://doi.org/10.1038/s41559-024-02365-0
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DOI: https://doi.org/10.1038/s41559-024-02365-0