Abstract
Invertebrate species are a natural reservoir of viral genetic diversity, and invertebrate pests are widely distributed in crop fields. However, information on viruses infecting invertebrate pests of crops is limited. In this report, we describe the deep metatranscriptomic sequencing of 88 invertebrate samples covering all major invertebrate pests in rice fields. We identified 296 new RNA viruses and 13 known RNA viruses. These viruses clustered within 31 families, with many highly divergent viruses constituting potentially new families and genera. Of the identified viruses, 13 RNA viruses clustered within the Fiersviridae family of bacteriophages, and 48 RNA viruses clustered within families and genera of mycoviruses. We detected known rice viruses in novel invertebrate hosts at high abundances. Furthermore, some novel RNA viruses have genome structures closely matching to known plant viruses and clustered within genera of several plant virus species. Forty-five potential insect pathogenic RNA viruses were detected in invertebrate species. Our analysis revealed that host taxonomy plays a major role and geographical location plays an important role in structuring viral diversity. Cross-species transmission of RNA viruses was detected between invertebrate hosts. Newly identified viral genomes showed extensive variation for invertebrate viral families or genera. Together, the large-scale metatranscriptomic analysis greatly expands our understanding of RNA viruses in rice invertebrate species, the results provide valuable information for developing efficient strategies to manage insect pests and virus-mediated crop diseases.
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All viral genome sequences described in this study were deposited in the GenBank database under accession numbers (MZ209608-MZ210057). Raw sequence data reads are available at the Sequence Read Archive (SRA) of the National Center for Biotechnology Information Sequence SRA database under BioProject accession number (PRJNA629998).
References
Aiewsakun, P., and Simmonds, P. (2018). The genomic underpinnings of eukaryotic virus taxonomy: creating a sequence-based framework for family-level virus classification. Microbiome 6, 38.
Antipov, D., Raiko, M., Lapidus, A., and Pevzner, P.A. (2020). Metaviral SPAdes: assembly of viruses from metagenomic data. Bioinformatics 36, 4126–4129.
Biedermann, P.H.W., and Vega, F.E. (2020). Ecology and evolution of insect-fungus mutualisms. Annu Rev Entomol 65, 431–455.
Bondy-Denomy, J., Qian, J., Westra, E.R., Buckling, A., Guttman, D.S., Davidson, A.R., and Maxwell, K.L. (2016). Prophages mediate defense against phage infection through diverse mechanisms. ISME J 10, 2854–2866.
Bonilla-Rosso, G., Steiner, T., Wichmann, F., Bexkens, E., and Engel, P. (2020). Honey bees harbor a diverse gut virome engaging in nested strain-level interactions with the microbiota. Proc Natl Acad Sci USA 117, 7355–7362.
Bonning, B.C., and Miller, W.A. (2010). Dicistroviruses. Annu Rev Entomol 55, 129–150.
Capella-Gutiérrez, S., Silla-Martínez, J.M., and Gabaldón, T. (2009). trimAl: a tool for automated alignment trimming in large-scale phylogenetic analyses. Bioinformatics 25, 1972–1973.
Chao, S., Wang, H., Zhang, S., Chen, G., Mao, C., Hu, Y., Yu, F., Wang, S., Lv, L., Chen, L., et al. (2022). Novel RNA viruses discovered in weeds in rice fields. Viruses 14, 2489.
Chen, Y., Li, X., Song, J., Yang, D., Liu, W., Chen, H., Wu, B., and Qian, P. (2019). Isolation and characterization of a novel temperate bacteriophage from gut-associated Escherichia within black soldier fly larvae (Hermetia illucens L. [Diptera: Stratiomyidae]). Arch Virol 164, 2277–2284.
Csardi, G., and Nepusz, T. (2006). The igraph software package for complex network research. Inter J Complex Syst 1695, 1–9.
Darriba, D., Taboada, G.L., Doallo, R., and Posada, D. (2011). ProtTest 3: fast selection of best-fit models of protein evolution. Bioinformatics 27, 1164–1165.
Dedrick, R.M., Jacobs-Sera, D., Bustamante, C.A.G., Garlena, R.A., Mavrich, T.N., Pope, W.H., Reyes, J.C.C., Russell, D.A., Adair, T., Alvey, R., et al. (2017). Prophage-mediated defence against viral attack and viral counter-defence. Nat Microbiol 2, 16251.
Dillon, R.J., and Dillon, V.M. (2004). The gut bacteria of insects: nonpathogenic interactions. Annu Rev Entomol 49, 71–92.
Dolja, V.V., Krupovic, M., and Koonin, E.V. (2020). Deep roots and splendid boughs of the global plant virome. Annu Rev Phytopathol 58, 23–53.
Dudas, G., and Obbard, D.J. (2015). Are arthropods at the heart of virus evolution? eLife 4, e06837.
Fenn, K., and Blaxter, M. (2006). Wolbachia genomes: revealing the biology of parasitism and mutualism. Trends Parasitol 22, 60–65.
Guo, J., Xu, C., Wu, D., Zhao, Y., Qiu, Y., Wang, X., Ouyang, Y., Cai, B., Liu, X., Jing, S., et al. (2018). Bph6 encodes an exocyst-localized protein and confers broad resistance to planthoppers in rice. Nat Genet 50, 297–306.
Guo, Y.Y. (2015). Crop Diseases and Insect Pests in China (in Chinese). Beijing: China Agriculture Press.
Haas, B.J., Papanicolaou, A., Yassour, M., Grabherr, M., Blood, P.D., Bowden, J., Couger, M.B., Eccles, D., Li, B., Lieber, M., et al. (2013). De novo transcript sequence reconstruction from RNA-seq using the Trinity platform for reference generation and analysis. Nat Protoc 8, 1494–1512.
Haelewaters, D., Blackwell, M., and Pfister, D.H. (2021). Laboulbeniomycetes: intimate fungal associates of arthropods. Annu Rev Entomol 66, 257–276.
Hajek, A.E., and St. Leger, R.J. (1994). Interactions between fungal pathogens and insect hosts. Annu Rev Entomol 39, 293–322.
Hedges, L.M., Brownlie, J.C., O’Neill, S.L., and Johnson, K.N. (2008). Wolbachia and virus protection in insects. Science 322, 702.
Hibino, H. (1996). Biology and epidemiology of rice viruses. Annu Rev Phytopathol 34, 249–274.
Holland, J., Spindler, K., Horodyski, F., Grabau, E., Nichol, S., and Vandepol, S. (1982). Rapid evolution of RNA genomes. Science 215, 1577–1585.
Horiuchi, H., Moriyama, H., and Fukuhara, T. (2003). Inheritance of Oryza sativa endornavirus in F1 and F2 hybrids between japonica and indica rice. Genes Genet Syst 78, 229–234.
Huelsenbeck, J.P., and Ronquist, F. (2001). MRBAYES: Bayesian inference of phylogenetic trees. Bioinformatics 17, 754–755.
Jałoszyński, P., Matsumura, Y., and Beutel, R.G. (2015). Evolution of a giant intromittent organ in Scydmaeninae (Coleoptera: Staphylinidae): Functional morphology of the male postabdomen in Mastigini. Arthropod Struct Dev 44, 77–98.
Jing, T.Z., Qi, F.H., and Wang, Z.Y. (2020). Most dominant roles of insect gut bacteria: digestion, detoxification, or essential nutrient provision? Microbiome 8, 38.
Jover, L.F., Cortez, M.H., and Weitz, J.S. (2013). Mechanisms of multi-strain coexistence in host-phage systems with nested infection networks. J Theor Biol 332, 65–77.
Katoh, K., and Standley, D.M. (2013). MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol Biol Evol 30, 772–780.
Kim, H., and Lee, J.H. (2008). Phenology simulation model of Scotinophara lurida (Hemiptera: Pentatomidae). Environ Entomol 37, 660–669.
Kittayapong, P., Jamnongluk, W., Thipaksorn, A., Milne, J.R., and Sindhusake, C. (2003). Wolbachia infection complexity among insects in the tropical rice-field community. Mol Ecol 12, 1049–1060.
Kucuk, R.A. (2020). Gut bacteria in the Holometabola: a review of obligate and facultative symbionts. J Insect Sci 20, 22.
Langmead, B., and Salzberg, S.L. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359.
Lefkowitz, E.J., Dempsey, D.M., Hendrickson, R.C., Orton, R.J., Siddell, S.G., and Smith, D.B. (2018). Virus taxonomy: the database of the International Committee on Taxonomy of Viruses (ICTV). Nucleic Acids Res 46, D708–D717.
Li, B., and Dewey, C.N. (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinf 12, 323.
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., and Zhang, Y.Z. (2015). Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4, e05378.
Li, H., Young, S.E., Poulsen, M., and Currie, C.R. (2021). Symbiont-mediated digestion of plant biomass in fungus-farming insects. Annu Rev Entomol 66, 297–316.
Li, N., Li, C., Hu, T., Li, J., Zhou, H., Ji, J., Wu, J., Kang, W., Holmes, E.C., Shi, W., et al. (2023). Nationwide genomic surveillance reveals the prevalence and evolution of honeybee viruses in China. Microbiome 11, 6.
Liu, W., Hajano, J.U.D., and Wang, X. (2018). New insights on the transmission mechanism of tenuiviruses by their vector insects. Curr Opin Virol 33, 13–17.
Liu, X.D., and Guo, H.F. (2019). Importance of endosymbionts Wolbachia and Rickettsia in insect resistance development. Curr Opin Insect Sci 33, 84–90.
Liu, Y., Wu, H., Chen, H., Liu, Y., He, J., Kang, H., Sun, Z., Pan, G., Wang, Q., Hu, J., et al. (2015). A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat Biotechnol 33, 301–305.
López-Bueno, A., Tamames, J., Velázquez, D., Moya, A., Quesada, A., and Alcami, A. (2009). High diversity of the viral community from an Antarctic lake. Science 326, 858–861.
Ma, Y., Marais, A., Lefebvre, M., Theil, S., Svanella-Dumas, L., Faure, C., and Candresse, T. (2019). Phytovirome analysis of wild plant populations: comparison of double-stranded RNA and virion-associated nucleic acid metagenomic approaches. J Virol 94, e01462–19.
Moriyama, H., Horiuchi, H., Koga, R., and Fukuhara, T. (1999). Molecular characterization of two endogenous double-stranded RNAs in rice and their inheritance by interspecific hybrids. J Biol Chem 274, 6882–6888.
Nakashima, N., Sasaki, J., and Toriyama, S. (1999). Determining the nucleotide sequence and capsid-coding region of Himetobi P virus: a member of a novel group of RNA viruses that infect insects. Arch Virol 144, 2051–2058.
Nguyen, L.T., Schmidt, H.A., von Haeseler, A., and Minh, B.Q. (2015). IQ-TREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32, 268–274.
Ni, X.B., Cui, X.M., Liu, J.Y., Ye, R.Z., Wu, Y.Q., Jiang, J.F., Sun, Y., Wang, Q., Shum, M.H.H., Chang, Q.C., et al. (2023). Metavirome of 31 tick species provides a compendium of 1,801 RNA virus genomes. Nat Microbiol 8, 162–173.
Ortiz-Urquiza, A., and Keyhani, N.O. (2016). Molecular genetics of beauveria bassiana infection of insects. Adv Genet 94, 165–249.
Pathak, M.D., and Khan, Z.R. (1994). Insect Pests of Rice. Manila: International Rice Research Institute.
Penadés, J.R., Chen, J., Quiles-Puchalt, N., Carpena, N., and Novick, R.P. (2015). Bacteriophage-mediated spread of bacterial virulence genes. Curr Opin Microbiol 23, 171–178.
Petersen, L.M., Bautista, E.J., Nguyen, H., Hanson, B.M., Chen, L., Lek, S.H., Sodergren, E., and Weinstock, G.M. (2017). Community characteristics of the gut microbiomes of competitive cyclists. Microbiome 5, 98.
Qin, P., Lu, H., Du, H., Wang, H., Chen, W., Chen, Z., He, Q., Ou, S., Zhang, H., Li, X., et al. (2021). Pan-genome analysis of 33 genetically diverse rice accessions reveals hidden genomic variations. Cell 184, 3542–3558.e16.
R Core Team. (2020). R: A language and environment for statistical computing. R Foundation for Statistical Computing. Vienna.
Robinson, J.T., Thorvaldsdóttir, H., Winckler, W., Guttman, M., Lander, E.S., Getz, G., and Mesirov, J.P. (2011). Integrative genomics viewer. Nat Biotechnol 29, 24–26.
Rosa, C., Lachance, M., Silva, J., Teixeira, A., Marini, M., Antonini, Y., and Martins, R. (2003). Yeast communities associated with stingless bees. FEMS Yeast Res 4, 271–275.
Ryabov, E.V. (2017). Invertebrate RNA virus diversity from a taxonomic point of view. J Invertebr Pathol 147, 37–50.
Salmond, G.P.C., and Fineran, P.C. (2015). A century of the phage: past, present and future. Nat Rev Microbiol 13, 777–786.
Shepard, B.M., Barrion, A.T., and Litsinger, J.A. (1995). Rice-feeding Insects of Tropical Asia. Manila: International Rice Research Institute.
Shi, M., Lin, X.D., Tian, J.H., Chen, L.J., Chen, X., Li, C.X., Qin, X.C., Li, J., Cao, J.P., Eden, J.S., et al. (2016). Redefining the invertebrate RNA virosphere. Nature 540, 539–543.
Shi, M., Neville, P., Nicholson, J., Eden, J.S., Imrie, A., and Holmes, E.C. (2017). Highresolution metatranscriptomics reveals the ecological dynamics of mosquito-associated RNA viruses in Western Australia. J Virol 91, e00680–17.
Sinkins, S.P. (2004). Wolbachia and cytoplasmic incompatibility in mosquitoes. Insect Biochem Mol Biol 34, 723–729.
Steinhauer, D.A., and Holland, J.J. (1987). Rapid evolution of RNA viruses. Annu Rev Microbiol 41, 409–431.
Stouthamer, R., Breeuwer, J.A.J., and Hurst, G.D.D. (1999). Wolbachia Pipientis: microbial manipulator of arthropod reproduction. Annu Rev Microbiol 53, 71–102.
Teixeira, L., Ferreira, A., and Ashburner, M. (2008). The bacterial symbiont Wolbachia induces resistance to RNA viral infections in Drosophila melanogaster. PLoS Biol 6, e2.
Wang, W., Mauleon, R., Hu, Z., Chebotarov, D., Tai, S., Wu, Z., Li, M., Zheng, T., Fuentes, R.R., Zhang, F., et al. (2018). Genomic variation in 3,010 diverse accessions of Asian cultivated rice. Nature 557, 43–49.
Webster, C.L., Waldron, F.M., Robertson, S., Crowson, D., Ferrari, G., Quintana, J.F., Brouqui, J.M., Bayne, E.H., Longdon, B., Buck, A.H., et al. (2015). The discovery, distribution, and evolution of viruses associated with Drosophila melanogaster. PLoS Biol 13, e1002210.
Wei, T., and Li, Y. (2016). Rice reoviruses in insect vectors. Annu Rev Phytopathol 54, 99–120.
Werren, J.H., Baldo, L., and Clark, M.E. (2008). Wolbachia: master manipulators of invertebrate biology. Nat Rev Microbiol 6, 741–751.
Wolf, Y.I., Kazlauskas, D., Iranzo, J., Lucia-Sanz, A., Kuhn, J.H., Krupovic, M., Dolja, V.V., and Koonin, E.V. (2018). Origins and evolution of the global RNA virome. mBio 9, e02329–18.
Wu, Z., Lu, L., Du, J., Yang, L., Ren, X., Liu, B., Jiang, J., Yang, J., Dong, J., Sun, L., et al. (2018). Comparative analysis of rodent and small mammal viromes to better understand the wildlife origin of emerging infectious diseases. Microbiome 6, 178.
Xie, J., and Jiang, D. (2014). New insights into mycoviruses and exploration for the biological control of crop fungal diseases. Annu Rev Phytopathol 52, 45–68.
Xu, H.J., Xue, J., Lu, B., Zhang, X.C., Zhuo, J.C., He, S.F., Ma, X.F., Jiang, Y.Q., Fan, H. W., Xu, J.Y., et al. (2015). Two insulin receptors determine alternative wing morphs in planthoppers. Nature 519, 464–467.
Yuan, H., Xu, P., Xiao, Y., Yang, L., Yang, X., and Wu, K. (2020). Infection of cotton bollworm by Helicoverpa armigera iflavirus decreases larval fitness. J Invertebr Pathol 173, 107384.
Zhang, S., Zhu, Z., Sun, S., Chen, Q., Deng, F., and Yang, K. (2015). Genome sequencing and analysis of a granulovirus isolated from the Asiatic rice leafroller, Cnaphalocrocis medinalis. Virol Sin 30, 417–424.
Zhang, Y.Y., Chen, Y., Wei, X., and Cui, J. (2022). Viromes in marine ecosystems reveal remarkable invertebrate RNA virus diversity. Sci China Life Sci 65, 426–437.
Zhang, Y.Z., Shi, M., and Holmes, E.C. (2018). Using metagenomics to characterize an expanding virosphere. Cell 172, 1168–1172.
Zhou, G., Xu, D., Xu, D., and Zhang, M. (2013). Southern rice black-streaked dwarf virus: a white-backed planthopper-transmitted fijivirus threatening rice production in Asia. Front Microbiol 4.
Acknowledgement
This work was supported by the National Natural Science Foundation of China (31972983, 32072487), the Key Technology R&D Program of Zhejiang Province (2021C02006), the Central Public-interest Scientific Institution Basal Research Fund (CPSIBRF-CNRRI-202115). We would like to thank D. Streicker for the prediction of viral hosts, we also thanks P. Krell and B. Meng for fruitful discussions and comments on the manuscript.
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Wang, H., Chao, S., Yan, Q. et al. Genetic diversity of RNA viruses infecting invertebrate pests of rice. Sci. China Life Sci. 67, 175–187 (2024). https://doi.org/10.1007/s11427-023-2398-y
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DOI: https://doi.org/10.1007/s11427-023-2398-y