Abstract
Little is known about ocean viromes and the ecological drivers of the evolution of aquatic RNA viruses. This study employed a meta-transcriptomic approach to characterize the viromes of 58 marine invertebrate species across three seas. This revealed the presence of 315 newly identified RNA viruses in nine viral families or orders (Durnavirales, Totiviridae, Bunyavirales, Hantaviridae, Picornavirales, Flaviviridae, Hepelivirales, Solemoviridae, and Tombusviridae), with most of them being sufficiently divergent to the already documented viruses. Notably, this study revealed three marine invertebrate hantaviruses that are rooted to vertebrate hantaviruses, further supporting that hantaviruses may have a marine origin. We have also found evidence for possible host sharing and switch events during virus evolution. Overall, we have revealed the hidden diversity of marine invertebrate RNA viruses.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Altschul, S.F., Gish, W., Miller, W., Myers, E.W., and Lipman, D.J. (1990). Basic local alignment search tool. J Mol Biol 215, 403–410.
Buchfink, B., Xie, C., and Huson, D.H. (2015). Fast and sensitive protein alignment using DIAMOND. Nat Methods 12, 59–60.
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.
Chang, W.S., Eden, J.S., Hall, J., Shi, M., Rose, K., and Holmes, E.C. (2020a). Metatranscriptomic analysis of virus diversity in urban wild birds with paretic disease. J Virol 94.
Chang, W.S., Li, C.X., Hall, J., Eden, J.S., Hyndman, T.H., Holmes, E.C., and Rose, K. (2020b). Meta-transcriptomic discovery of a divergent circovirus and a chaphamaparvovirus in captive reptiles with proliferative respiratory syndrome. Viruses 12, 1073.
Dorrington, R.A., Jiwaji, M., Awando, J.A., and Bruyn, M.M. (2020). Advances in tetravirus research: new insight into the infectious virus lifecycle and an expanding host range. Curr Issues Mol Biol 34, 145–162.
Folmer, O., Black, M., Hoeh, W., Lutz, R., and Vrijenhoek, R. (1994). DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol Mar Biol Biotechnol 3, 294–299.
Geoghegan, J.L., and Holmes, E.C. (2017). Predicting virus emergence amid evolutionary noise. Open Biol 7, 170189.
Guajardo-Leiva, S., Chnaiderman, J., Gaggero, A., and Díez, B. (2020). Metagenomic Insights into the sewage RNA virosphere of a large city. Viruses 12, 1050.
Gulino, K., Rahman, J., Badri, M., Morton, J., Bonneau, R., and Ghedin, E. (2020). Initial mapping of the New York City wastewater virome. mSystems 5.
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.
Harder, T.C., Buda, S., Hengel, H., Beer, M., and Mettenleiter, T.C. (2016). Poultry food products—a source of avian influenza virus transmission to humans? Clin Microbiol Infect 22, 141–146.
Iturriza-Gomara, M., and O’Brien, S.J. (2016). Foodborne viral infections. Curr Opin Infect Dis 29, 495–501.
Junglen, S., and Drosten, C. (2013). Virus discovery and recent insights into virus diversity in arthropods. Curr Opin Microbiol 16, 507–513.
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.
Koonin, E.V., Senkevich, T.G., and Dolja, V.V. (2006). The ancient Virus World and evolution of cells. Biol Direct 1, 29.
Kumar, S., Stecher, G., Li, M., Knyaz, C., and Tamura, K. (2018). MEGA X: molecular evolutionary genetics analysis across computing platforms. Mol Biol Evol 35, 1547–1549.
Laenen, L., Vergote, V., Calisher, C.H., Klempa, B., Klingström, J., Kuhn, J.H., and Maes, P. (2019). Hantaviridae: Current classification and future perspectives. Viruses 11, 788.
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 negativesense RNA viruses. eLife 4, e05378.
Linder, P., and Jankowsky, E. (2011). From unwinding to clamping—the DEAD box RNA helicase family. Nat Rev Mol Cell Biol 12, 505–516.
Lopez, J.V., Kamel, B., Medina, M., Collins, T., and Baums, I.B. (2019). Multiple facets of marine invertebrate conservation genomics. Annu Rev Anim Biosci 7, 473–497.
Lu, S., Wang, J., Chitsaz, F., Derbyshire, M.K., Geer, R.C., Gonzales, N.R., Gwadz, M., Hurwitz, D.I., Marchler, G.H., Song, J.S., et al. (2020). CDD/SPARCLE: the conserved domain database in 2020. Nucleic Acids Res 48, D265–D268.
Magbanua, F.O., Natividad, K.T., Migo, V.P., Alfafara, C.G., de la Peña, F. O., Miranda, R.O., Albaladejo, J.D., Nadala Jr, E., Loh, P.C., and Mahilum-Tapay, L. (2000). White spot syndrome virus (WSSV) in cultured Penaeus monodon in the Philippines. Dis Aquat Org 42, 77–82.
Mahar, J.E., Shi, M., Hall, R.N., Strive, T., and Holmes, E.C. (2020). Comparative analysis of RNA virome composition in rabbits and associated ectoparasites. J Virol 94.
Marklewitz, M., Zirkel, F., Kurth, A., Drosten, C., and Junglen, S. (2015). Evolutionary and phenotypic analysis of live virus isolates suggests arthropod origin of a pathogenic RNA virus family. Proc Natl Acad Sci USA 112, 7536–7541.
Metzger, M.J., Paynter, A.N., Siddall, M.E., and Goff, S.P. (2018). Horizontal transfer of retrotransposons between bivalves and other aquatic species of multiple phyla. Proc Natl Acad Sci USA 115, E4227–E4235.
Middelboe, M., and Brussaard, C.P.D. (2017). Marine viruses: key players in marine ecosystems. Viruses 9, 302.
Moon, K., Jeon, J.H., Kang, I., Park, K.S., Lee, K., Cha, C.J., Lee, S.H., and Cho, J.C. (2020). Freshwater viral metagenome reveals novel and functional phage-borne antibiotic resistance genes. Microbiome 8, 75.
Nguyen, L.T., Schmidt, H.A., von Haeseler, A., and Minh, B.Q. (2015). IQTREE: a fast and effective stochastic algorithm for estimating maximum-likelihood phylogenies. Mol Biol Evol 32, 268–274.
Pettersson, J.H.O., Ellström, P., Ling, J., Nilsson, I., Bergström, S., González-Acuña, D., Olsen, B., and Holmes, E.C. (2020). Circumpolar diversification of the Ixodes uriae tick virome. PLoS Pathog 16, e1008759.
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. (2014). A tick-borne segmented RNA virus contains genome segments derived from unsegmented viral ancestors. Proc Natl Acad Sci USA 111, 6744–6749.
Rosani, U., Shapiro, M., Venier, P., and Allam, B. (2019). A needle in a haystack: tracing bivalve-associated viruses in high-throughput transcriptomic data. Viruses 11, 205.
Roux, S., Brum, J.R., Dutilh, B.E., Sunagawa, S., Duhaime, M.B., Loy, A., Poulos, B.T., Solonenko, N., Lara, E., Poulain, J., et al. (2016). Ecogenomics and potential biogeochemical impacts of globally abundant ocean viruses. Nature 537, 689–693.
Salazar, G., Paoli, L., Alberti, A., Huerta-Cepas, J., Ruscheweyh, H.J., Cuenca, M., Field, C.M., Coelho, L.P., Cruaud, C., Engelen, S., et al. (2019). Gene expression changes and community turnover differentially shape the global ocean metatranscriptome. Cell 179, 1068–1083.e21.
Shannon, P., Markiel, A., Ozier, O., Baliga, N.S., Wang, J.T., Ramage, D., Amin, N., Schwikowski, B., and Ideker, T. (2003). Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13, 2498–2504.
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., Lin, X.D., Chen, X., Tian, J.H., Chen, L.J., Li, K., Wang, W., Eden, J.S., Shen, J.J., Liu, L., et al. (2018a). The evolutionary history of vertebrate RNA viruses. Nature 556, 197–202.
Shi, M., Zhang, Y.Z., and Holmes, E.C. (2018b). Meta-transcriptomics and the evolutionary biology of RNA viruses. Virus Res 243, 83–90.
Simmonds, P., Adams, M.J., Benkő, M., Breitbart, M., Brister, J.R., Carstens, E.B., Davison, A.J., Delwart, E., Gorbalenya, A.E., Harrach, B., et al. (2017). Virus taxonomy in the age of metagenomics. Nat Rev Microbiol 15, 161–168.
Thakur, P.C., Corsin, F., Turnbull, J.F., Shankar, K.M., Hao, N.V., Padiyar, P.A., Madhusudhan, M., Morgan, K.L., and Mohan, C.V. (2002). Estimation of prevalence of white spot syndrome virus (WSSV) by polymerase chain reaction in Penaeus monodon postlarvae at time of stocking in shrimp farms of Karnataka, India: a population-based study. Dis Aquat Org 49, 235–243.
Vainio, E.J., Chiba, S., Ghabrial, S.A., Maiss, E., Roossinck, M., Sabanadzovic, S., Suzuki, N., Xie, J., Nibert, M., and ICTV Report Consortium, (2018). ICTV virus taxonomy profile: Partitiviridae. J General Virol 99, 17–18.
Vlok, M., Gibbs, A.J., and Suttle, C.A. (2019). Metagenomes of a freshwater charavirus from British Columbia provide a window into ancient lineages of viruses. Viruses 11, 299.
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.
Wille, M., Shi, M., Klaassen, M., Hurt, A.C., and Holmes, E.C. (2019). Virome heterogeneity and connectivity in waterfowl and shorebird communities. ISME J 13, 2603–2616.
Wille, M., Harvey, E., Shi, M., Gonzalez-Acuña, D., Holmes, E.C., and Hurt, A.C. (2020). Sustained RNA virome diversity in Antarctic penguins and their ticks. ISME J 14, 1768–1782.
Wu, H., Pang, R., Cheng, T., Xue, L., Zeng, H., Lei, T., Chen, M., Wu, S., Ding, Y., Zhang, J., et al. (2020). Abundant and diverse RNA viruses in insects revealed by RNA-seq analysis: ecological and evolutionary implications. mSystems 5.
Zhang, Y.Z., Shi, M., and Holmes, E.C. (2018). Using metagenomics to characterize an expanding virosphere. Cell 172, 1168–1172.
Zhang, Y.Z., Chen, Y.M., Wang, W., Qin, X.C., and Holmes, E.C. (2019). Expanding the RNA virosphere by unbiased metagenomics. Annu Rev Virol 6, 119–139.
Zhang, Z., Qin, F., Chen, F., Chu, X., Luo, H., Zhang, R., Du, S., Tian, Z., and Zhao, Y. (2021). Culturing novel and abundant pelagiphages in the ocean. Environ Microbiol 23, 1145–1161.
Acknowledgements
This work was supported by the National Natural Science Foundation of China (31970176), Collaborative Research Grant (KLMVI-OP-202002) of CAS Key Laboratory of Molecular Virology & Immunology, Institut Pasteur of Shanghai, Chinese Academy of Sciences, Guangdong Provincial Key Laboratory of Fishery Ecology and Environment (FEEL-2019-6), and CAS Pioneer Hundred Talents Program.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Compliance and ethics The author(s) declare that they have no conflict of interest.
Supplementary Materials for
Rights and permissions
About this article
Cite this article
Zhang, YY., Chen, Y., Wei, X. et al. Viromes in marine ecosystems reveal remarkable invertebrate RNA virus diversity. Sci. China Life Sci. 65, 426–437 (2022). https://doi.org/10.1007/s11427-020-1936-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11427-020-1936-2