Abstract
The dinoflagellate Prorocentrum minimum is known to affect the normal physiological function of Exopalaemon carinicauda by inducing oxidative stress, apoptosis, and cellular injury. To study the effects of P. minimum on the immune defense system of shrimp, E. carinicauda were exposed to 5 × 103 cells mL−1 and 5 × 104 cells mL−1 of P. minimum for 336h in treatment groups, while E. carinicauda cultured in filtered seawater was employed as control. The total hemocyte counts (THC), hemocyanin concentration (HEM), and the activity of alkaline phosphatase (AKP) in hemolymph serum, as well as expressions of six immunity-related genes in hemocytes, hepatopancreases and gills were determined. The exposure of P. minimum significantly reduced the THC, HEM concentration and AKP activity in hemolymph serum. Immunity-related genes expressed differently in hemocytes, hepatopancreases and gills. Compared with the control group, the expressions of Crustin and proPO in hemocytes were significantly up-regulated in the treatment groups, while the up-regulated expressions of LGBP, Lysozyme and Serpin were only found in the group exposed to 5× 104 cells mL−1 of P. minimum. In the gills of E. carinicauda exposed to P. minimum, the down-regulation of ALF, proPO and Serpin, up-regulation of LGBP and Lysozyme, as well as unaffected Crustin were observed. In hepatopancreases, the up-regulated expressions of LGBP, Crustin, Lysozyme, Serpin and proPO (only in 5 × 103 cells mL−1 of P. minimum group) were found in the treatment groups. After exposure to P. minimum for 336 h, shrimps were injected with Vibrio parahaemolyticus and WSSV. The results showed that the mortality rates of shrimp in the treatment groups were significantly increased with a dose-dependent effect, which suggests that exposure to P. minimum may reduce the immunity of E. carinicauda. The research indicates that hemocytes and hepatopancreases play important roles in protecting the shrimp immune response to harmful algae, while the protection effect of hemolymph serum and gills may be suppressed. Since the exposure to P. minimum depressed the immunity of E. carinicauda, further studies are needed to confirm whether the presence of the algae will affect the susceptibility of shrimp to pathogens.
This is a preview of subscription content, log in via an institution to check access.
We’re sorry, something doesn't seem to be working properly.
Please try refreshing the page. If that doesn't work, please contact support so we can address the problem.
References
Alonso-Rodrıguez, R., and Páez-Osuna, F., 2003. Nutrients, phytoplankton and harmful algal blooms in shrimp ponds: A review with special reference to the situation in the Gulf of California. Aquaculture, 219: 317–336, DOI: https://doi.org/10.1016/S0044-8486(02)00509-4.
Ajani, P. A., Larsson, M. E., Woodcock, S., Rubio, A., Farrell, H., Brett, S., et al., 2018. Bloom drivers of the potentially harmful dinoflagellate Prorocentrum minimum (Pavillard) Schiller in a south eastern temperate Australian estuary. Estuarine, Coastal and Shelf Science, 215: 161–171, DOI: https://doi.org/10.1016/j.ecss.2018.09.029.
Aweya, J. J., Zheng, Z., Zheng, X., Yao, D., and Zhang, Y, 2021. The expanding repertoire of immune-related molecules with antimicrobial activity in penaeid shrimps: A review. Reviews in Aquaculture, 13: 1907–1937, DOI: https://doi.org/10.1111/raq.12551.
Azanza, R. V., Fukuyo, Y., Yap, L. G., and Takayama, H., 2005. Prorocentrum minimum bloom and its possible link to a massive fish kill in Bolinao, Pangasinan, Northern Philippines. Harmful Algae, 4: 519–524, DOI: https://doi.org/10.1016/j.hal.2004.08.006.
Cerenius, L., and Söderhäll, K., 2004. The prophenoloxidase-activating system in invertebrates. Immunological Reviews, 198: 116–126, DOI: https://doi.org/10.1111/j.0105-2896.2004.00116.x.
Chen, J., and Xie, P., 2005. Tissue distributions and seasonal dynamics of the hepatotoxic microcystins-LR and -RR in two freshwater shrimps, Palaemon modestus and Macrobrachium nipponensis, from a large shallow, eutrophic lake of the subtropical China. Toxicon, 45: 615–625, DOI: https://doi.org/10.1016/j.toxicon.2005.01.003.
Destoumieux-Garzón, D., Saulnier, D., Garnier, J., Jouffrey, C., Bulet, P., and Bachere, E., 2001. Crustacean immunity: Anti-fungal peptides are generated from the C terminus of shrimp hemocyanin in response to microbial challenge. The Journal of Biological Chemistry, 276: 47070–47077, DOI: https://doi.org/10.1074/jbc.M103817200.
Estrada, N., Lagos, N., Garcia, C., Maeda-Martinez, A., and Ascencio, F., 2007a. Effects of the toxic dinoflagellate Gymnodinium catenatum on uptake and fate of paralytic shellfish poisons in the Pacific giant lions-paw scallop Nodipecten subnodosus. Marine Biology, 151: 1205–1214, DOI: https://doi.org/10.1007/s00227-006-0568-x.
Estrada, N., Rodríguez-Jaramillo, M., Contreras, R., and Ascencio, F., 2010. Effects of induced paralysis on hemocytes and tissues of the giant lions-paw scallop by paralyzing shellfish poison. Marine Biology, 157: 1401–1415, DOI: https://doi.org/10.1007/s00227-010-1418-4.
Estrada, N., Romero, M., Campa-Córdova, A., Luna, A., and Ascencio, F., 2007b. Effects of the toxic dinoflagellate, Gymnodinium catenatum on hydrolytic and antioxidant enzymes, in tissues of the giant lions-paw scallop Nodipecten subnodosus. Comparative Biochemistry and Physiology C–Toxicology & Pharmacology, 146: 502–510, DOI: https://doi.org/10.1016/j.cbpc.2007.06.003.
Flegel, T. W., Lightner, D. V., Lo, C. F., and Owens, L., 2008. Shrimp disease control: Past, present and future. In: Diseases in Asian Aquaculture VI. Manila, Philippines: Fish Health Section. Bondad-Reantaso, M. G., et al., eds., Asian Fisheries Society, 355–378.
Galanti, L. N., Amé, M. V., and Wunderlin, D. A., 2013. Accumulation and detoxification dynamic of cyanotoxins in the freshwater shrimp Palaemonetes argentinus. Harmful Algae, 27: 88–97, DOI: https://doi.org/10.1016/j.hal.2013.05.007.
Galimany, E., Sunila, I., Hégaret, H., Ramón, M., and Wikfors, G. H., 2008. Pathology and immune response of the blue mussel (Mytilus edulis L.) after an exposure to the harmful dinoflagellate Prorocentrum minimum. Harmful Algae, 7: 630–638, DOI: https://doi.org/10.1007/s00244-005-0214-5.
Gao, J., Zuo, H., Yang, L., He, J. H., Niu, S., Weng, S., et al, 2017. Long-term influence of cyanobacterial bloom on the immune system of Litopenaeus vannamei. Fish and Shellfish Immunology, 61: 79–85, DOI: https://doi.org/10.1016/j.fsi.2016.12.015.
García-Carreño, F., Cota Ruiz, K., and Navarrete del Toro, M. A., 2008. Phenoloxidase activity of hemocyanin in whiteleg shrimp Penaeus vannamei: Conversion, characterization of catalytic properties, and role in postmortem melanosis. Journal of Agricultural and Food Chemistry, 56: 6454–6459, DOI: https://doi.org/10.1021/jf800839x.
Ge, Q., Li, J., Li, J., Wang, J., and Li, Z., 2017. Immune response of Exopalaemon carinicauda infected with an AHPND-causing strain of Vibrio parahaemolyticus. Fish and Shellfish Immunology, 74: 223–234, DOI: https://doi.org/10.1016/j.fsi.2017.12.042.
Ge, Q., Liang, J., Li, J., Li, J., Duan, Y., Zhao, F., et al., 2015. Molecular cloning and expression analysis of Relish gene from the ridgetail white prawn Exopalaemon carinicauda. Fisheries Science, 81: 699–711, DOI: https://doi.org/10.1007/s12562-015-0898-z.
Heil, C. A., Glibert, P. M., and Fan, C., 2005. Prorocentrum minimum (Pavillard) Schiller: A review of a harmful algal bloom species of growing worldwide importance. Harmful Algae, 4: 449–470, DOI: https://doi.org/10.1016/j.hal.2004.08.003.
Holland, D. S., and Leonard, J., 2020. Is a delay a disaster? economic impacts of the delay of the california dungeness crab fishery due to a harmful algal bloom. Harmful Algae, 98: 101904, DOI: https://doi.org/10.1016/j.hal.2020.101904.
Huang, Y., and Ren, Q., 2021. Innate immune responses against viral pathogens in Macrobrachium. Developmental & Comparative Immunology, 117: 103966.
Kotaki, Y., Koike, K., Yoshida, M., Thuoc, C., Huyen, N., Hoi, N., et al., 2008. Domoic acid production in Nitzschia sp (Bacillariophyceae) isolated from a shrimp-culture pond in Do Son, Vietnam. Journal of Phycology, 36: 1057–1060, DOI: https://doi.org/10.1046/j.1529-8817.2000.99209.x.
Kulkarni, A., Krishnan, S., Anand, D., Kokkattunivarthi Uthaman, S., Otta, S. K., Karunasagar, I., et al., 2021. Immune responses and immunoprotection in crustaceans with special reference to shrimp. Reviews in Aquaculture, 13: 431–459, DOI: https://doi.org/10.1111/raq.12482.
Lai, H. C., Ng, T. H., Ando, M., Lee, C. T., Chen, I. T., Chuang, J. C., et al., 2015. Pathogenesis of acute hepatopancreatic necrosis disease (AHPND) in shrimp. Fish and Shellfish Immunology, 47: 1006–1014, DOI: https://doi.org/10.1016/j.fsi.2015.11.008.
Landsberg, J., 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10: 113–390, DOI: https://doi.org/10.1080/20026491051695.
Li, J., Glibert, P. M., and Gao, Y., 2015. Temporal and spatial changes in Chesapeake Bay water quality and relationships to Prorocentrum minimum, Karlodinium veneficum, and Cyano-HAB events, 1991–2008. Harmful Algae, 42: 1–14, DOI: https://doi.org/10.1016/j.hal.2014.11.003.
Liu, C. H., and Chen, J. C., 2004. Effect of ammonia on the immune response of white shrimp Litopenaeus vannamei and it susceptibility to Vibrio alginolyticus. Fish and Shellfish Immunology, 16: 321–334, DOI: https://doi.org/10.1016/S1050-4648(03)00113-X.
Liu, F., Shao, G. Y., Tian, Q. Q., Cheng, B. X., Shen, C., Wang, A. M., et al., 2021. Enhanced growth performance, immune responses, immune-related gene expression and disease resistance of red swamp crayfish (Procambarus clarkii) fed dietary glycyrrhizic acid. Aquaculture, 533: 736202, DOI: https://doi.org/10.1016/j.aquaculture.2020.736202.
Livak, K., and Schmittgen, T., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the \({2^{- \Delta \Delta {C_{\rm{T}}}}}\) method. Methods, 25: 402–408, DOI: https://doi.org/10.1006/meth.2001.1262.
Lukwambe, B., Nicholaus, R., Zhang, D., Yang, W., Zhu, J., and Zheng, Z., 2019. Successional changes of microalgae community in response to commercial probiotics in the intensive shrimp (Litopenaeus vannamei Boone) culture systems. Aquaculture, 511: 734257, DOI: https://doi.org/10.1016/j.aquaculture.2019.734257.
Meng, F., Zhang, Y., Kong, J., and Ma, G., 1999. The research review of prophenoloxidase activating system in crustacean. Oceanologia et Limnologia Sinica, 30: 110–116.
Mu, C., Ge, Q., and Li, J., 2019. Exposure to Prorocentrum minimum induces oxidative stress and apoptosis in the ridgetail white prawn, Exopalaemon carinicauda. Journal of Ocean University of China, 18: 727–734, DOI: https://doi.org/10.1007/s11802-019-3846-1.
Mu, C., Ren, X., Ge, Q., Wang, J., and Li, J., 2017. Antioxidant response of ridgetail white prawn Exopalaemon carinicauda to harmful dinoflagellate Prorocentrum minimum exposure and its histological change. Journal of Ocean University of China, 16: 285–293, DOI: https://doi.org/10.1007/s11802-017-3170-6.
Nagai, T., Osaki, T., and Kawabata, S. I., 2001. Functional conversion of hemocyanin to phenoloxidase by horseshoe crab antimicrobial peptides. The Journal of Biological Chemistry, 276: 27166–27170, DOI: https://doi.org/10.1074/jbc.M102596200.
Paezosuna, F., 2003. Shrimp aquaculture development and the environment in the Gulf of California ecoregion. Marine Pollution Bulletin, 46: 806–815, DOI: https://doi.org/10.1016/s0025-326x(03)00107-3.
Pérez-Morales, A., Band-Schmidt, C. J., and Martínez-Díaz, S. F., 2017. Mortality on zoea stage of the Pacific white shrimp Litopenaeus vannamei caused by Cochlodinium polykrikoides (Dinophyceae) and Chattonella spp. (Raphidophyceae). Marine Biology, 164: 57, DOI: https://doi.org/10.1007/s00227-017-3083-3.
Sierra-Beltrán, A. P., Cortés-Altamirano, R., and Cortés-Lara, M. C., 2005. Occurrences of Prorocentrum minimum (Pavillard) in México. Harmful Algae, 4: 507–517, DOI: https://doi.org/10.1016/j.hal.2004.08.003.
Söderhäll, K., and Cerenius, L., 1992. Crustacean immunity. Annual Review of Fish Diseases, 2: 3–23, DOI: https://doi.org/10.1016/0959-8030(92)90053-Z.
Vazquez, L., Alpuche, J., Maldonado, G., Agundis, C., Pereyra-Morales, A., and Zenteno, E., 2009. Review: Immunity mechanisms in crustaceans. Innate Immunity, 15: 179–188, DOI: https://doi.org/10.1177/1753425909102876.
Vlamis, A., Katikou, P., Rodriguez, I., Rey, V., Alfonso, A., Papazachariou, A., et al., 2015. Tetrodotoxin detection in Greek shellfish by UPLC-MS/MS and potential link to presence of the dinoflagellate Prorocentrum minimum. Toxins, 7: 1779–1807, DOI: https://doi.org/10.3390/toxins7051779.
Xu, H., Min, G. S., Choi, J. K., and Zhu, M., 2010. Temporal population dynamics of the dinoflagellate Prorocentrum minimum in a semi-enclosed mariculture pond and its relationship to environmental factors and protozoan grazers. Chinese Journal of Oceanology and Limnology, 28: 75–81, DOI: https://doi.org/10.1007/s00343-010-9249-1.
Yang, X., Wen, X., Zhou, C., Zhu, X., Meng, R., Luo, Q., et al, 2018. Comparative study of brine shrimp bioassay-based toxic activities of three harmful microalgal species that frequently blooming in aquaculture ponds. Journal of Oceanology and Limnology, 36: 1697–1706, DOI: https://doi.org/10.1007/s00343-018-7140-7.
Yao, W., Li, X., Zhang, C., Wang, J., Cai, Y., and Leng, X., 2021. Effects of dietary synbiotics supplementation methods on growth, intestinal health, non-specific immunity and disease resistance of Pacific white shrimp, Litopenaeus vannamei. Fish and Shellfish Immunology, 112: 46–55, DOI: https://doi.org/10.1016/j.fsi.2021.02.011.
Yeganeh, V., Sharifinia, M., Mobaraki, S., Dashtiannasab, A., Aeinjamshid, K., Borazjani, J. M., et al., 2020. Survey of survival rate and histological alterations of gills and hepatopancreas of the Litopenaeus vannamei juveniles caused by exposure of Margalefidinium/Cochlodinium polykrikoides isolated from the Persian Gulf. Harmful Algae, 97: 101856, DOI: https://doi.org/10.1016/j.hal.2020.101856.
Zhang, X., Huang, C., and Qin, Q., 2004. Antiviral properties of hemocyanin isolated from Penaeus monodon. Antiviral Research, 61: 93–99, DOI: https://doi.org/10.1016/j.antiviral.2003.08.019.
Zhu, M., and Xu, J., 1993. Red tide in shrimp ponds along the Bohai Sea. In: Toxic Phytoplankton Blooms in the Sea. Smayda, T. J., and Shimizu, Y., eds., Elsevier, Amsterdam, 363–367.
Acknowledgements
This project was financially supported by the earmarked fund for National Key R & D Program of China (No. 2019YFD0900403), the Modern Agro-Industry Technology Research System (No. CARS-48), the Program of Shandong Leading Talent (No. LNJY2015002), the Central Public-Interest Scientific Institution Basal Research Fund of CAFS (No. 2020TD46), and the Scientific Research Start-Up Funding of Shandong Agricultural University (No. 72188).
Author information
Authors and Affiliations
Corresponding author
Rights and permissions
About this article
Cite this article
Mu, C., Ren, X. & Li, J. Immune Response of the Ridgetail White Prawn Exopalaemon carinicauda After Exposure to the Dinoflagellate Prorocentrum minimum. J. Ocean Univ. China 22, 821–830 (2023). https://doi.org/10.1007/s11802-023-5336-8
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s11802-023-5336-8