Elimination of Decapod iridovirus 1 (DIV1) infection at high water temperature: a new environmental control strategy

Yue Wang1, Linxin Dai1, Zuluan Liang1, Naijie Hu1, Danqing Hou1, Yinhuan Zhou1, Chengbo Sun1,2,3
1College of Fisheries, Guangdong Ocean University, Zhanjiang, China
2Guangdong Provincial Key Laboratory of Pathogenic Biology and Epidemiology for Aquatic Economic Animals, Zhanjiang, China
3Guangdong Provincial Laboratory of Southern Marine Science and Engineering, Zhanjiang, China

Tóm tắt

Decapod iridovirus 1 (DIV1) poses a major challenge to sustainable shrimp farming and poses a serious hazard to aquaculture industry. This study investigated the complex interaction between DIV1 infection and water temperature, focusing on the effect of high temperature on DIV1 infection due to Penaeus monodon. Using models of latent and acute infection, the study revealed the response of P. monodon to DIV1 under different conditions. In the experimental set-up, the effect of high water temperature (34 ± 1 °C) compared with room temperature (26 ± 1 °C) was investigated. DIV1 replication was significantly inhibited in the high-temperature group (H), resulting in complete viral elimination within 15 days. DIV1 did not resurface even after return to room temperature (26 ± 1 °C), indicating sustained antiviral effects. Compared with the room temperature (26 ± 1 °C) group (N), the H group showed a 100% reduction in the incidence of latent and acute infection. Exposure to high water temperature directly impaired the viability of DIV1, enhancing the immune system of P. monodon, and expediting metabolic processes for efficient DIV1 clearance. The study highlights the significant inhibitory effects of high water temperature (34 ± 1 °C) on DIV1 infection in P. monodon, resulting in viral eradication. This discovery offers a potential strategy for mitigating DIV1 infections in shrimp aquaculture, prompting further investigation into underlying mechanisms. Optimising parameters and protocols for high-temperature treatment is crucial for viral control. Exploring the broader implications of the findings on other viral infections in crustacean aquaculture could provide valuable insights for comprehensive disease prevention and control.

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Tài liệu tham khảo

Abdel-Latif HMR, Yilmaz E, Dawood MAO, Ringø E, Ahmadifar E, Yilmaz S. Shrimp vibriosis and possible control measures using probiotics, postbiotics, prebiotics, and synbiotics: A review. Aquaculture. 2022;551:737951. https://doi.org/10.1016/j.aquaculture.2022.737951. Abdelrahman HA, Abebe A, Boyd CE. Influence of variation in water temperature on survival, growth and yield of Pacific white shrimp Litopenaeus vannamei in inland ponds for low-salinity culture. Aquacult Res. 2019;50(2):658–72. https://doi.org/10.1111/are.13943. Baker TS, Yan X, Olson NH, Van Etten JL, Bergoin M, Rossmann MG. Structure and assembly of large lipid-containing dsDNA viruses. Nature structural & molecular biology. 2000;7(2):101–3. https://doi.org/10.1038/72360. Chen X. Susceptible Host Survey of Decapod Iridescent Virus 1 (DIV1). Shanghai Ocean University; 2019. https://doi.org/10.27314/d.cnki.gsscu.2019.000033. (in Chinese with English abstract). Chen X, Qiu L, Wang H, Zou P, Dong X, Li F, Huang J. Susceptibility of Exopalaemon carinicauda to the Infection with Shrimp Hemocyte Iridescent Virus (SHIV 20141215), a Strain of Decapod Iridescent Virus 1 (DIV1). Viruses. 2019;11(4). https://doi.org/10.3390/v11040387. Chinchar VG. Ranaviruses (family Iridoviridae): emerging cold-blooded killers. Arch Virol. 2002;147(3):447–70. https://doi.org/10.1007/s007050200000. Chinchar VG, Yu KH, Jancovich JK. The molecular biology of frog virus 3 and other iridoviruses infecting cold-blooded vertebrates. Viruses. 2011;3(10):1959–85. https://doi.org/10.3390/v3101959. Du H, Dai W, Han X, Li W, Xu Y, Xu Z. Effect of low water temperature on viral replication of white spot syndrome virus in Procambarus clarkii. Aquaculture. 2008;277(3):149–51. https://doi.org/10.1016/j.aquaculture.2008.03.003. Du H, Li W, Xu Z, Kil Z. Effect of hyperthermia on the replication of white spot syndrome virus (WSSV) in Procambarus clarkii. Dis Aquat Organ. 2006;71(2):175. https://doi.org/10.3354/dao071175. Duan Y, Wang Y, Huang J, Li H, Dong H, Zhang J. Toxic effects of cadmium and lead exposure on intestinal histology, oxidative stress response, and microbial community of Pacific white shrimp Litopenaeus vannamei. Mar Pollut Bull. 2021;167:112220. https://doi.org/10.1016/j.marpolbul.2021.112220. Granja CB, Vidal OM, Parra G, Salazar M. Hyperthermia reduces viral load of white spot syndrome virus in Penaeus vannamei. Dis Aquat Organ. 2006;68(2):175. https://doi.org/10.3354/dao068175. Guo X, Qiu L, Gao W, Wang G, Chen X, Huang J. Radical thermal therapy against infection with decapod iridescent virus 1 (DIV1). Aquaculture. 2022;561:738636. https://doi.org/10.1016/j.aquaculture.2022.738636. He Z, Chen X, Zhao J, Hou D, Fu Z, Zhong Y, Sun C. Establishment of infection mode and Penaeus monodon hemocytes transcriptomics analysis under decapod iridescent virus 1 (DIV1) challenge. Aquaculture. 2021;542:736816. https://doi.org/10.1016/j.aquaculture.2021.736816. He Z, Zhong Y, Hou D, Hu X, Fu Z, Liu L, Sun C. Integrated Analysis of mRNA-Seq and MiRNA-Seq Reveals the Molecular Mechanism of the Intestinal Immune Response in Marsupenaeus japonicus Under Decapod Iridescent Virus 1 Infection. Front Immunol. 2022;12:807093. https://doi.org/10.3389/fimmu.2021.807093. He Z, Zhong Y, Liao M, Dai L, Wang Y, Zhang S, Sun C. Integrated analysis of intestinal microbiota and metabolomic reveals that decapod iridescent virus 1 (DIV1) infection induces secondary bacterial infection and metabolic reprogramming in Marsupenaeus japonicus. Front Immunol. 2022;13:982717. https://doi.org/10.3389/fimmu.2022.982717. Hicks CC, Cohen PJ, Graham NAJ, Nash KL, Allison EH, D’Lima C, Macneil MA. Harnessing global fisheries to tackle micronutrient deficiencies. Nature (London). 2019;574(7776):95–8. https://doi.org/10.1038/s41586-019-1592-6. Jihongwu ZCZ. Principal Component Analysis on Trace Elements of Shrimp. J Guangdong Ocean Univ. 2010;30(1):72–5. https://doi.org/10.3969/j.issn.1673-9159.2010.01.014. Jiravanichpaisal P, Söderhäll K, Söderhäll I. Effect of water temperature on the immune response and infectivity pattern of white spot syndrome virus (WSSV) in freshwater crayfish. Fish Shellfish Immunol. 2004;17(3):265–75. https://doi.org/10.1016/j.fsi.2004.03.010. Liao M, Liao X, Long X, Zhao J, He Z, Zhang J, Sun C. Host-microbiota interactions and responses of Metapenaeus ensis infected with decapod iridescent virus 1. Front Microbiol. 2022;13:1097931. https://doi.org/10.3389/fmicb.2022.1097931. Liao X, Wang C, Wang B, Qin H, Hu S, Zhao J, Zhang S. Research into the hemocyte immune response of Fenneropenaeus merguiensis under decapod iridescent virus 1 (DIV1) challenge using transcriptome analysis. Fish Shellfish Immunol. 2020;104:8–17. https://doi.org/10.1016/j.fsi.2020.05.053. Luo S. Effect of water temperature on the infection of White spotsyndrome virus (WSSV) in Procambarus clarkii. Third Institute of Oceanography State Oceanic Administration; 2010. https://kns.cnki.net/kcms/detail/detail.aspx?FileName=2010263188.nh&DbName=CMFD2011. (in Chinese with English abstract). Marschang RE. Viruses infecting reptiles. Viruses. 2011;3(11):2087–126. https://doi.org/10.3390/v3112087. Matthews RE. Third report of the International Committee on Taxonomy of Viruses. Classification and nomenclature of viruses. Intervirology. 1979;12(3–5):129–296. https://doi.org/10.1159/000149081. Montgomery-Brock D, Tacon AGJ, Poulos B, Lightner D. Reduced replication of infectious hypodermal and hematopoietic necrosis virus (IHHNV) in Litopenaeus vannamei held in warm water. Aquaculture. 2007;265(1):41–8. https://doi.org/10.1016/j.aquaculture.2007.01.025. Pan L, Jin C. A review on hemocyanins of crustacean. J Fish China. 2008;32:484–91.https://kns.cnki.net/kcms/detail/detail.aspx?FileName=SCKX200803022&DbName=CJFQ2008. (in Chinese with English abstract). Paperna I, Vilenkin M, de Matos AP. Iridovirus infections in farm-reared tropical ornamental fish. Dis Aquat Organ. 2001;48(1):17. https://doi.org/10.3354/dao048017. Qiu L, Chen M, Wan X, Li C, Zhang Q, Wang R, Huang, J. Characterization of a new member of Iridoviridae, Shrimp hemocyte iridescent virus (SHIV), found in white leg shrimp (Litopenaeus vannamei). Sci Rep. 2017;7(1):11834–13. https://doi.org/10.1038/s41598-017-10738-8. Qiu L, Chen M, Wang R, Wan X, Li C, Zhang Q, Huang J. Complete genome sequence of shrimp hemocyte iridescent virus (SHIV) isolated from white leg shrimp, Litopenaeus vannamei. Arch Virol. 2018;163(3):781–5. https://doi.org/10.1007/s00705-017-3642-4. Qiu L, Chen X, Zhao RH, Li C, Gao W, Zhang QL, Huang J. Description of a Natural Infection with Decapod Iridescent Virus 1 in Farmed Giant Freshwater Prawn, Macrobrachium rosenbergii. Viruses. 2019;11(4). https://doi.org/10.3390/v11040354. Rahman MM, Corteel M, Dantas-Lima JJ, Wille M, Alday-Sanz V, Pensaert MB, Nauwynck HJ. Aquaculture. 2007;269(1):107–13. https://doi.org/10.1016/j.aquaculture.2007.04.056. Rahman MM, Escobedo-Bonilla CM, Corteel M, Dantas-Lima JJ, Wille M, Sanz VA, Nauwynck HJ. Aquaculture. 2006;261(3):842–9. https://doi.org/10.1016/j.aquaculture.2006.09.007. Srisala J, Sanguanrut P, Thaiue D, Laiphrom S, Siriwattano J, Khudet J, Sritunyalucksana K. Infectious myonecrosis virus (IMNV) and Decapod iridescent virus 1 (DIV1) detected in captured, wild Penaeus monodon. Aquaculture. 2021;545:737262. https://doi.org/10.1016/j.aquaculture.2021.737262. Tang KFJ, Redman RM, Pantoja CR, Groumellec ML, Duraisamy P, Lightner DV. Identification of an iridovirus in Acetes erythraeus (Sergestidae) and the development of in situ hybridization and PCR method for its detection. J Invertebr Pathol. 2007;96(3):255–60. https://doi.org/10.1016/j.jip.2007.05.006. Viet Nguyen T, Ryan LW, Nocillado J, Le Groumellec M, Elizur A, Ventura T. Transcriptomic changes across vitellogenesis in the black tiger prawn (Penaeus monodon), neuropeptides and G protein-coupled receptors repertoire curation. Gen Comp Endocrinol. 2020;298:113585. https://doi.org/10.1016/j.ygcen.2020.113585. Wang Y, Dai L, He Z, Hou D, Sun C. Recent progress in the Decapod iridescent virus 1 (DIV1) study. J Shellfish Res. 2023;42(1):8. https://doi.org/10.2983/035.042.0113. Wang Z, Zhou J, Li J, Zou J, Fan L. The immune defense response of Pacific white shrimp (Litopenaeus vannamei) to temperature fluctuation. Fish Shellfish Immunol. 2020;103:103–10. https://doi.org/10.1016/j.fsi.2020.04.053. Williams TIDE. Natural invertebrate hosts of iridoviruses (Iridoviridae). Neotrop Entomol. 2008;37(6):615–32. https://doi.org/10.1590/S1519-566X2008000600001. Williams T. Comparative studies of iridoviruses: further support for a new classification. Virus Res. 1994;33(2):99–121. https://doi.org/10.1016/0168-1702(94)90048-5. Williams T, Barbosa-Solomieu V, Chinchar VG. A decade of advances in iridovirus research. Adv Virus Res. 2005;65(173. https://doi.org/10.1016/S0065-3527(05)65006-3. Withyachumnarnkul B, Boonsaeng V, Chomsoong R, Flegel TW, Muangsin S, Nash GL. Seasonal variation in white spot syndrome virus-positive samples in broodstock and post-larvae of in Thailand. Dis Aquat Organ. 2003;53(2):167. https://doi.org/10.3354/dao053167. Wyban J, Walsh WA, Godin DM. Temperature effects on growth, feeding rate and feed conversion of the Pacific white shrimp ( Penaeus vannamei). Aquaculture. 1995;138(1):267–79. https://doi.org/10.1016/0044-8486(95)00032-1. Xeros N. A Second Virus Disease of the Leatherjacket, Tipula paludosa. Nature (London). 1954;174(4429):562–3. https://doi.org/10.1038/174562a0. Wu X, Xiong H, Du H. Advances on Possible Mechanism of Hyperthermia lnhibition of White Spot Syndrome in Shrimp. Fish Sci. 2012;31(09):568–72.https://kns.cnki.net/kcms/detail/detail.aspx?FileName=CHAN201209014&DbName=CJFQ2012. https://doi.org/10.16378/j.cnki.1003-1111.2012.09.013. (in Chinese with English abstract). Xu L, Wang T, Li F, Yang F. Isolation and preliminary characterization of a new pathogenic iridovirus from redclaw crayfish Cherax quadricarinatus. Dis Aquat Organ. 2016;120(1):17. https://doi.org/10.3354/dao03007. You X, Su Y, Mao Y, Liu M, Wang J, Zhang M, Wu C. Effect of high water temperature on mortality, immune response and viral replication of WSSV-infected Marsupenaeus japonicus juveniles and adults. Aquaculture. 2010;305(1):133–7. https://doi.org/10.1016/j.aquaculture.2010.04.024. Yuan H. Effects of Temperature and Salinity on White spotsyndrome virus (WSSV) Content in Macrobrachium nipponense. Nanjing Agricultural University; 2020. https://kns.cnki.net/kcms/detail/detail.aspx?FileName=1022022219.nh&DbName=CMFD2022. https://doi.org/10.27244/d.cnki.gnjnu.2020.000560. (in Chinese with English abstract). Zhou J, Wang L, Xin Y, Wang W, He W, Wang A, Liu, Y. Effect of temperature on antioxidant enzyme gene expression and stress protein response in white shrimp, Litopenaeus vannamei. J Therm Biol. 2010;35(6):284–9. https://doi.org/10.1016/j.jtherbio.2010.06.004. Zhang Y, Luo Y, Peng X. Advancement on the function of hemocyanin. Mar Sci. (02):77–80. https://kns.cnki.net/kcms/detail/detail.aspx?FileName=HYKX200702018&DbName=CJFQ2007. (in Chinese with English abstract). Zhang Z. Preliminary investigation and analysis of red snapper rainbow virus in some coastal areas of Fujian Province. Fujian Agriculture and Forestry University; 2014. https://go.exlibris.link/99cPz3Pj. (in Chinese with English abstract).