Skip to main content
SpringerLink
Log in

Diversity and connectedness of brine shrimp viruses in global hypersaline ecosystems

  • Research Paper
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Brine shrimp (Artemia) has existed on Earth for 400 million years and has major ecological importance in hypersaline ecosystems. As a crucial live food in aquaculture, brine shrimp cysts have become one of the most important aquatic products traded worldwide. However, our understanding of the biodiversity, prevalence and global connectedness of viruses in brine shrimp is still very limited. A total of 143 batches of brine shrimp (belonging to seven species) cysts were collected from six continents including 21 countries and more than 100 geographic locations worldwide during 1977–2019. In total, 55 novel RNA viruses were identified, which could be assigned to 18 different viral families and related clades. Eleven viruses were dsRNA viruses, 16 were +ssRNA viruses, and 28 were–ssRNA viruses. Phylogenetic analyses of the RNA-directed RNA polymerase (RdRp) showed that brine shrimp viruses were often grouped with viruses isolated from other invertebrates and fungi. Remarkably, most brine shrimp viruses were related to those from different hosts that might feed on brine shrimp or share the same ecological niche. A notable case was the novel brine shrimp noda-like virus 3, which shared 79.25% (RdRp) and 63.88% (capsid proteins) amino acid identity with covert mortality nodavirus (CMNV) that may cause losses in aquaculture. In addition, both virome composition and phylogenetic analyses revealed global connectedness in certain brine shrimp viruses, particularly among Asia and Northern America. This highlights the incredible species diversity of viruses in these ancient species and provides essential data for the prevalence of RNA viruses in the global aquaculture industry. More broadly, these findings provide novel insights into the previously unrecognized RNA virosphere in hypersaline ecosystems worldwide and demonstrate that human activity might have driven the global connectedness of brine shrimp viruses.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Abatzopoulos, T.J., Beardmore, J.A., Clegg, J.S., and Sorgeloos, P. (2002). Artemia: Basic and Applied Biology. Dordrecht: Springer.

    Book  Google Scholar 

  • Barata, C., Hontoria, F., and Amat, F. (1995). Life history, resting egg formation, and hatching may explain the temporal-geographical distribution of Artemia strains in the Mediterranean basin. Hydrobiologia 298, 295–305.

    Article  Google Scholar 

  • Bolger, A.M., Lohse, M., and Usadel, B. (2014). Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics 30, 2114–2120.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brock, T.D. (1976). Halophilic-blue-green algae. Arch Microbiol 107, 109–111.

    Article  CAS  PubMed  Google Scholar 

  • Camacho, C., Coulouris, G., Avagyan, V., Ma, N., Papadopoulos, J., Bealer, K., and Madden, T.L. (2009). BLAST+: architecture and applications. BMC Bioinformatics 10, 421.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Chen, Y.M., Sadiq, S., Tian, J.H., Chen, X., Lin, X.D., Shen, J.J., Chen, H., Hao, Z.Y., Wille, M., Zhou, Z.C., et al. (2022). RNA viromes from terrestrial sites across China expand environmental viral diversity. Nat Microbiol 7, 1312–1323.

    Article  CAS  PubMed  Google Scholar 

  • Dattilo, A.M., Bracchini, L., Carlini, L., Loiselle, S., and Rossi, C. (2005). Estimate of the effects of ultraviolet radiation on the mortality of Artemia franciscana in naupliar and adult stages. Int J Biometeorol 49, 388–395.

    Article  PubMed  Google Scholar 

  • Dong, X., Hu, T., Liu, Q., Li, C., Sun, Y., Wang, Y., Shi, W., Zhao, Q., and Huang, J. (2020). A novel hepe-Like virus from farmed giant freshwater prawn Macrobrachium rosenbergii. Viruses 12, 323.

    Article  PubMed  PubMed Central  Google Scholar 

  • Emerson, J.B., Thomas, B.C., Andrade, K., Allen, E.E., Heidelberg, K.B., and Banfield, J. F. (2012). Dynamic viral populations in hypersaline systems as revealed by metagenomic assembly. Appl Environ Microbiol 78, 6309–6320.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gajardo, G.M., and Beardmore, J.A. (2012). The brine shrimp Artemia: adapted to critical life conditions. Front Physio 3, 185.

    Article  Google Scholar 

  • Grabherr, M.G., Haas, B.J., Yassour, M., Levin, J.Z., Thompson, D.A., Amit, I., Adiconis, X., Fan, L., Raychowdhury, R., Zeng, Q., et al. (2011). Full-length transcriptome assembly from RNA-Seq data without a reference genome. Nat Biotechnol 29, 644–652.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gregory, A.C., Zayed, A.A., Conceição-Neto, N., Temperton, B., Bolduc, B., Alberti, A., Ardyna, M., Arkhipova, K., Carmichael, M., Cruaud, C., et al. (2019). Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123.e14.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Harvey, E., and Holmes, E.C. (2022). Diversity and evolution of the animal virome. Nat Rev Microbiol 20, 321–334.

    Article  CAS  PubMed  Google Scholar 

  • He, W.T., Hou, X., Zhao, J., Sun, J., He, H., Si, W., Wang, J., Jiang, Z., Yan, Z., Xing, G., et al. (2022). Virome characterization of game animals in China reveals a spectrum of emerging pathogens. Cell 185, 1117–1129.e8.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hoa, N.V., and Sorgeloos, P. (2020). Brine shrimp Artemia as a direct human food. World Aquac 51, 24–25.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kearse, M., Moir, R., Wilson, A., Stones-Havas, S., Cheung, M., Sturrock, S., Buxton, S., Cooper, A., Markowitz, S., Duran, C., et al. (2012). Geneious basic: an integrated and extendable desktop software platform for the organization and analysis of sequence data. Bioinformatics 28, 1647–1649.

    Article  PubMed  PubMed Central  Google Scholar 

  • Langmead, B., and Salzberg, S.L. (2012). Fast gapped-read alignment with Bowtie 2. Nat Methods 9, 357–359.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Lavens, P., and Sorgeloos, P. (1996). Manual on the Production and Use of Live Food for Aquaculture. Rome: FAO.

    Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Saccò, M., White, N.E., Harrod, C., Salazar, G., Aguilar, P., Cubillos, C.F., Meredith, K., Baxter, B.K., Oren, A., Anufriieva, E., et al. (2021). Salt to conserve: a review on the ecology and preservation of hypersaline ecosystems. Biol Rev 96, 2828–2850.

    Article  PubMed  Google Scholar 

  • Santos, F., Yarza, P., Parro, V., Briones, C., and Antón, J. (2010). The metavirome of a hypersaline environment. Environ Microbiol 12, 2965–2976.

    Article  CAS  PubMed  Google Scholar 

  • Savage, A., and Knott, B. (1998). Artemia parthenogenetica in Lake Hayward, Western Australia. II. Feeding biology in a shallow, seasonally stratified, hypersaline lake. Int J Salt Lake Res 7, 13–24.

    Article  Google Scholar 

  • Seck, E.H., Dufour, J.C., Raoult, D., and Lagier, J.C. (2018). Halophilic & halotolerant prokaryotes in humans. Future Microbiol 13, 799–812.

    Article  CAS  PubMed  Google Scholar 

  • Shadrin, N., Yakovenko, V., and Anufriieva, E. (2019). Suppression of Artemia spp. (Crustacea, Anostraca) populations by predators in the Crimean hypersaline lakes: A review of the evidence. Internat Rev Hydrobiol 104, 5–13.

    Article  Google Scholar 

  • Shi, C., Beller, L., Deboutte, W., Yinda, K.C., Delang, L., Vega-Rúa, A., Failloux, A.B., and Matthijnssens, J. (2019). Stable distinct core eukaryotic viromes in different mosquito species from Guadeloupe, using single mosquito viral metagenomics. Microbiome 7, 121.

    Article  PubMed  PubMed Central  Google Scholar 

  • 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. (2018). The evolutionary history of vertebrate RNA viruses. Nature 556, 197–202.

    Article  CAS  PubMed  Google Scholar 

  • 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.

    Article  CAS  PubMed  Google Scholar 

  • Silva, S.M., Lavander, H.D., Luna, M.M., Silva, A.O., Gálvez, A.O., and Coimbra, M.R. (2015). Artemia franciscana as a vector for infectious myonecrosis virus (IMNV) to Litopenaeus vannamei juvenile. J Invertebr Pathol 126, 1–5.

    Article  PubMed  Google Scholar 

  • Sorgeloos, P., Dhert, P., and Candreva, P. (2001). Use of the brine shrimp, Artemia spp., in marine fish larviculture. Aquaculture 200, 147–159.

    Article  Google Scholar 

  • Sorgeloos, P., Lavens, P., Léger, P., Tackaert, W., and Versichele, D. (1986). Manual for the Culture and Use of Brine Shrimp Artemia in Aquaculture. Ghent: State University of Ghent, Artemia Reference Center.

    Google Scholar 

  • Sudhakaran, R., Yoganandhan, K., Ishaq Ahmed, V.P., and Sahul Hameed, A.S. (2006). Artemia as a possible vector for Macrobrachium rosenbergii nodavirus (MrNV) and extra small virus transmission (XSV) to Macrobrachium rosenbergii post-larvae. Dis Aquat Org 70, 161–166.

    Article  CAS  Google Scholar 

  • Triantaphyllidis, G., Abatzopoulos, T., and Sorgeloos, P. (1998). Review of the biogeography of the genus Artemia (Crustacea, Anostraca). J Biogeogr 25, 213–226.

    Article  Google Scholar 

  • Van Stappen, G., Sui, L., Hoa, V.N., Tamtin, M., Nyonje, B., Medeiros Rocha, R., Sorgeloos, P., and Gajardo, G. (2020). Review on integrated production of the brine shrimp Artemia in solar salt ponds. Rev Aquacult 12, 1054–1071.

    Article  Google Scholar 

  • Ventosa, A., de la Haba, R.R., Sánchez-Porro, C., and Papke, R.T. (2015). Microbialdiversity of hypersaline environments: a metagenomic approach. Curr Opin Microbiol 25, 80–87.

    Article  CAS  PubMed  Google Scholar 

  • Wang, C., Liu, S., Li, X., Hao, J., Tang, K.F.J., and Zhang, Q. (2019). Infection of covert mortality nodavirus in Japanese flounder reveals host jump of the emerging alphanodavirus. J Gen Virol 100, 166–175.

    Article  CAS  PubMed  Google Scholar 

  • Wang, C., Liu, S., Tang, K.F.J., and Zhang, Q. (2021). Natural infection of covert mortality nodavirus affects Zebrafish (Danio rerio). J Fish Dis 44, 1315–1324.

    Article  CAS  PubMed  Google Scholar 

  • Wang, Y.T., Shi, C.Y., Sui, L.Y., Ye, S.G., Dong, X., and Huang, J. (2020). Research progress on the risk of Artemia acting as a kind of live feed to spread shrimp pathogens (in Chinese). China Anim Health Inspect 37, 61–67.

    Google Scholar 

  • 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.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu, T., Liu, S., Li, X., and Zhang, Q. (2020). Genomic characterization of covert mortality nodavirus from farming shrimp: evidence for a new species within the family Nodaviridae. Virus Res 286, 198092.

    Article  CAS  PubMed  Google Scholar 

  • Yao, L., Wang, C., Wang, W., Li, Y., Liu, S., Kong, J., and Zhang, Q. (2022). Cases report of covert mortality nodavirus infection in indoor farming Penaeus vannamei. Aquac Rep 25, 101238.

    Article  Google Scholar 

  • Zhang, B., Guo, J.C., Shang, Z.H., and Yu, X. (1993). The inoculation of A. franciscana in Bohai Bay saltworks, China (in Chinese). J Salt Chem Ind 22, 7–9.

    Google Scholar 

  • Zhang, Q., Liu, Q., Liu, S., Yang, H., Liu, S., Zhu, L., Yang, B., Jin, J., Ding, L., Wang, X., et al. (2014). A new nodavirus is associated with covert mortality disease of shrimp. J Gen Virol 95, 2700–2709.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Q., Xu, T., Wan, X., Liu, S., Wang, X., Li, X., Dong, X., Yang, B., and Huang, J. (2017). Prevalence and distribution of covert mortality nodavirus (CMNV) in cultured crustacean. Virus Res 233, 113–119.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, Q.Y., Tao, J.J., Gui, L., Zhou, G.Z., Ruan, H.M., Li, Z.Q., and Gui, J.F. (2007). Isolation and characterization of Scophthalmus maximus rhabdovirus. Dis Aquat Org 74, 95–105.

    Article  CAS  Google Scholar 

  • 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.

    Article  PubMed  Google Scholar 

  • Zhang, Y.Z., Shi, M., and Holmes, E.C. (2018). Using metagenomics to characterize an expanding virosphere. Cell 172, 1168–1172.

    Article  CAS  PubMed  Google Scholar 

  • Zuo, J.J., Xu, Q., Deng, Y.G., Liang, X.J., Han, X.K., and Sui, L.Y. (2022). Comparative study of Artemia taxonomic and evolution using three DNA barcodes (in Chinese). J Tianjin Univ Sci Technol 37, 28–36.

    Google Scholar 

Download references

Acknowledgement

This work was supported by the National Key Research and Development Program of China (2018YFD0900501), Central Public-interest Scientific Institution Basal Research Fund, YSFRI, CAFS (20603022022005), Shinan District Science and Technology Foundation (Qingdao) (2022-2-027-ZH), Central Public-interest Scientific Institution Basal Research Fund, CAFS (2020TD39), China Agriculture Research System (CARS-48). C.L. was supported by the Youth Innovation Team of Shandong Higher Education Institution (2021KJ064) and the National Natural Science Foundation of China (32200004). W.S. was supported by the Academic Promotion Programme of Shandong First Medical University (2019QL006). E.C.H. was funded by a National Medical Health and Research Council (Australia) Investigator Grant (GNT2017197). We thank Chengyin Shi, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Science, for his guidance in the study.

Author information

Author notes

  1. Contributed equally to this work

Authors and Affiliations

  1. State Key Laboratory of Mariculture Biobreeding and Sustainable Goods, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences; Laboratory for Marine Fisheries Science and Food Production Processes, Laoshan Laboratory; Key Laboratory of Maricultural Organism Disease Control, Ministry of Agriculture and Rural Affairs; Qingdao Key Laboratory of Mariculture Epidemiology and Biosecurity, Qingdao, 266071, China

    Xuan Dong, Yiting Wang, Fan Zhang, Fanzeng Meng, Guohao Wang, Jiahao Qin & Jie Huang

  2. Shandong Provincial Hospital Affiliated to Shandong First Medical University, Jinan, 250021, China

    Cixiu Li & Tao Hu

  3. Key Laboratory of Emerging Infectious Diseases in Universities of Shandong, Shandong First Medical University & Shandong Academy of Medical Sciences, Taian, 271000, China

    Cixiu Li, Tao Hu & Weifeng Shi

  4. Dalian Ocean University, Dalian, 116023, China

    Yiting Wang

  5. Asian Regional Artemia Reference Center, Tianjin University of Science & Technology, Tianjin, 300457, China

    Meirong Gao, Xuekai Han & Liying Sui

  6. Ghent University, Ghent, 9000, Belgium

    Hans Nauwynck & Patrick Sorgeloos

  7. Sydney Institute for Infectious Diseases, School of Medical Sciences, The University of Sydney, Sydney, 2006, Australia

    Edward C. Holmes

  8. Network of Aquaculture Centres in Asia-Pacific, Bangkok, 10900, Thailand

    Jie Huang

  9. School of Public Health, Shandong First Medical University & Shandong Academy of Medical Sciences, Jinan, 250117, China

    Weifeng Shi

Authors
  1. Xuan Dong
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Cixiu Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Yiting Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Tao Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Fan Zhang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Fanzeng Meng
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Meirong Gao
    View author publications

    You can also search for this author in PubMed Google Scholar

  8. Xuekai Han
    View author publications

    You can also search for this author in PubMed Google Scholar

  9. Guohao Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  10. Jiahao Qin
    View author publications

    You can also search for this author in PubMed Google Scholar

  11. Hans Nauwynck
    View author publications

    You can also search for this author in PubMed Google Scholar

  12. Edward C. Holmes
    View author publications

    You can also search for this author in PubMed Google Scholar

  13. Patrick Sorgeloos
    View author publications

    You can also search for this author in PubMed Google Scholar

  14. Liying Sui
    View author publications

    You can also search for this author in PubMed Google Scholar

  15. Jie Huang
    View author publications

    You can also search for this author in PubMed Google Scholar

  16. Weifeng Shi
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding authors

Correspondence to Patrick Sorgeloos, Liying Sui, Jie Huang or Weifeng Shi.

Ethics declarations

The author(s) declare that they have no conflict of interest.

Electronic supplementary material

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Dong, X., Li, C., Wang, Y. et al. Diversity and connectedness of brine shrimp viruses in global hypersaline ecosystems. Sci. China Life Sci. 67, 188–203 (2024). https://doi.org/10.1007/s11427-022-2366-8

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-022-2366-8

Keywords

Search

Navigation