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Exposure to Prorocentrum minimum Induces Oxidative Stress and Apoptosis in the Ridgetail White Prawn, Exopalaemon carinicauda

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Abstract

Prorocentrum minimum is a bloom-forming, planktonic mixotrophic dinoflagellate, and can cause stress in shrimp ponds. In this study, healthy Exopalaemon carinicauda were exposed to 5 ×104 cells mL−1P. minimum for 72 hours to investigate the adverse effect of P. minimum on shrimps. Elevated superoxide dismutase (SOD) activity and malondialdehyde (MDA) content, reduced total antioxidant capacity (T-AOC) and catalase (CAT) activity, and regulatory glutathione peroxidase (GPX) activity were found in the hemolymph of E. carinicauda after exposure to P. minimum. In this study, P. minimum exposure induced oxidative stress and caused significant oxidative damage to E. carinicauda. P. minimum exposure increased the expression of HSP70 gene in the hemocyte, gills and hepatopancreas. Compared with the enhanced level of caspase-3 gene mRNA in the hemocyte and gills, the up-regulation of caspase-3 gene in the hepatopancreas was only observed from 3 to 6 h, and then the mRNA level of glutathione-S-transferase (GST) gene increased. These results indicated that GST might be involved in the shrimp hepatopancreas’ defense against P. minimum exposure. The present study demonstrates that exposure to P. minimum could induce oxidative stress and apoptosis in E. carinicauda. The SOD activity, HSP70 and GST (in the hepatopancreas) were evoked to protect cells from oxidative stress and apoptosis. This study will provide new insights into the toxic mechanism of P. minimum on shrimps.

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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 (1–4): 317–336.

    Article  Google Scholar 

  • 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 (3): 519–524.

    Article  Google Scholar 

  • Bachère, E., Gueguen, Y., Gonzalez, M., De Lorgeril, J., Garnier, J., and Romest, B., 2004. Insights into the anti-microbial defense of marine invertebrates: The penaeid shrimps and the oyster Crassostrea gigas. Immunological Reviews, 198 (1): 149–168.

    Article  Google Scholar 

  • Bermejo-Nogales, A., Nederlof, M., Benedito-Palos, L., Balles-ter-Lozano, G. F., Folkedal, O., Olsen, R. E., Sitjà-Bobadilla A., and Pérez-Sánchez, J., 2014. Metabolic and transcriptional responses of gilthead sea bream (Sparus aurata L.) to environmental stress: New insights in fish mitochondrial pheno-typing. General and Comparative Endocrinology, 205, 305–315.

    Article  Google Scholar 

  • Blanchette, B., Feng, X., and Singh, B. R., 2007. Marine glu-tathione S-transferases. Marine biotechnology, 9 (5): 513–542.

    Article  Google Scholar 

  • Bradford, M. M., 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

    Article  Google Scholar 

  • Castex, M., Lemaire, P., Wabete, N., and Chim, L., 2010. Effect of probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress of Litopenaeus stylirostris under Vibri-onigripulchritudo challenge. Fish and Shellfish Immunology, 28 (4): 622–631.

    Article  Google Scholar 

  • Cheng, C. H., Yang, F. F., Ling, R. Z., Liao, S. A., Miao, Y. T., Ye, C. X., and Wang, A. L., 2015. Effects of ammonia exposure on apoptosis, oxidative stress and immune response in pufferfish (Takifugu obscurus). Aquatic Toxicology, 164, 61–71.

    Article  Google Scholar 

  • El-Beltagi, H. S., and Mohamed, H. I., 2013. Reactive oxygen species, lipid peroxidation and antioxidative defense mechanism. Notulae Botanicae Horti Agrobotanici Cluj-Napoca, 41 (1): 44–57.

    Article  Google Scholar 

  • Franco, R., Sánchez-Olea, R., Reyes-Reyes, E. M., and Panay-iotidis, M. I., 2009. Environmental toxicity, oxidative stress and apoptosis: Menage a trois. Mutation Research/Genetic Toxicology and Environmental Mutagenesis, 674 (1): 3–22.

    Article  Google Scholar 

  • Gonçalves-Soares, D., Zanette, J., Yunes, J. S., Yepiz-Plascencia, G. M., and Bainy, A. C. D., 2012. Expression and activity of glutathione S-transferases and catalase in the shrimp Litopenaeus vannamei inoculated with a toxic Microcystis aeru-ginosa strain. Marine Environmental Research, 75, 54–61.

    Article  Google Scholar 

  • Goth, L., 1991. A simple method for determination of serum catalase activity and revision of reference range. Clinica Chimica Acta, 196(2–3): 143–151.

    Article  Google Scholar 

  • Goto, S., Kawakatsu, M., Izumi, S., Urata, Y., Kageyama, K., Ihara, Y., Koji, T., and Kondo, T., 2009. Glutathione S-trans-ferase % localizes in mitochondria and protects against oxidative stress. Free Radical Biology and Medicine, 46 (10): 1392–1403.

    Article  Google Scholar 

  • Hayes, J. D., Flanagan, J. U., and Jowsey, I. R., 2005. Glutathione transferases. Annual Review of Pharmacology and Toxicology, 45, 51–88.

    Article  Google Scholar 

  • Hégaret, H., and Wikfors, G. H., 2005. Effects of natural and field-simulated blooms of the dinoflagellate Prorocentrum minimum upon hemocytes of eastern oysters, Crassostrea vir-ginica, from two different populations. Harmful Algae, 4 (2): 201–209.

    Article  Google Scholar 

  • 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 (3): 449–470.

    Article  Google Scholar 

  • Huang, X., Chen, L., Liu, W. J., Qiao, Q., Wu, K., Wen, J., Huang, C. H., Tang, R., and Zhang, X. Z., 2015. Involvement of oxidative stress and cytoskeletal disruption in microcystin-in-duced apoptosis in CIK cells. Aquatic Toxicology, 165, 41–50.

    Article  Google Scholar 

  • Jia, R., Cao, L. P., Du, J. L., Wang, J. H., Liu, Y. J., Jeney, G., Xu, P., and Yin, G. J., 2014. Effects of carbon tetrachloride on oxidative stress, inflammatory response and hepatocyte apoptosis in common carp (Cyprinus carpio). Aquatic Toxicology, 152, 11–19.

    Article  Google Scholar 

  • Jiang, J., Shi, Y., Shan, Z., Yang, L., Wang, X., and Shi, L., 2012. Bioaccumulation, oxidative stress and HSP70 expression in Cyprinus carpio L. exposed to microcystin-LR under laboratory conditions. Comparative Biochemistry and Physiology Part C: Toxicology and Pharmacology, 155 (3): 483–490.

    Google Scholar 

  • Kim, D., Nakashima, T., Matsuyama, Y., Niwano, Y., Yamaguchi, K., and Oda, T., 2007. Presence of the distinct systems responsible for superoxide anion and hydrogen peroxide generation in red tide phytoplankton Chattonella marina and Chattonella ovata. Journal of plankton research, 29 (3): 241–247.

    Article  Google Scholar 

  • Kumar, S., 2007. Caspase function in programmed cell death. Cell Death and Differentiation, 14 (1): 32–43.

    Article  Google Scholar 

  • Landsberg, J. H, 2002. The effects of harmful algal blooms on aquatic organisms. Reviews in Fisheries Science, 10 (2): 113–390.

    Article  Google Scholar 

  • Li, N., Hou, Y. H., Ma, D. D., Jing, W. X., Dahms, H. U., and Wang, L., 2015. Lead accumulation, oxidative damage and histopathological alteration in testes and accessory glands of freshwater crab, Sinopotamon henanense, induced by acute lead exposure. Ecotoxicology and Environmental Safety, 117, 20–27.

    Article  Google Scholar 

  • Li, X. Z., Liu, R. Y., and Liang, X. Q., 2002. The zoogeography of Chinese Palaemonoidea fauna. Chinese Biodiversity, 11 (5): 393–406.

    Google Scholar 

  • Liang, Z. X., Li, J., Li, J. T. Tan, Z. J., Ren, H., and Zhao, F. Z., 2014. Toxic dinoflagellate Alexandrium tamarense induces oxidative stress and apoptosis in hepatopancreas of shrimp (Fenneropenaeus chinensis). Journal of Ocean University of China, 13 (6): 1005–1011.

    Article  Google Scholar 

  • Liu, C. H., and Chen, J. C., 2004. Effect of ammonia on the immune response of white shrimp Litopenaeus vannamei and its susceptibility to Vibrio alginolyticus. Fish and Shellfish Immunology, 16 (3): 321–334.

    Article  Google Scholar 

  • Livak, K. J., and Schmittgen, T. D., 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods, 25 (4): 402–408.

    Article  Google Scholar 

  • Luckenbach, M., Sellner, K., Shumway, S., and Greene, K., 1993. Effects of two bloom-forming dinoflagellates, Prorocentrum minimum and Gyrodinium uncatenum, on the growth and survival of the eastern oyster, Crassostrea virginica (Gmelin 1791). Journal of Shellfish Research, 12 (2): 411–415.

    Google Scholar 

  • Marklund, S., and Marklund, G., 1974. Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. European Journal of Biochemistry, 47 (3): 469–474.

    Article  Google Scholar 

  • Mayer, M., and Bukau, B., 2005. Hsp70 chaperones: Cellular functions and molecular mechanism. Cellular and Molecular Life Sciences, 62 (6): 670–684.

    Article  Google Scholar 

  • Oda, T., Akaike, T., Sato, K., Ishimatsu, A., Takeshita, S., Muramatsu, T., and Maeda, H., 1992. Hydroxyl radical generation by red tide algae. Archives of Biochemistry and Biophysics, 294 (1): 38–43.

    Article  Google Scholar 

  • Oda, T., Nakashima, T., Shikayama, M., Kawano, L., Ishimatsu, A., and Muramatsu, T., 1997. Generation of reactive oxygen species by raphidophycean phytoplankton. Bioscience, Biotechnology, and Biochemistry, 61 (10): 1658–1662.

    Article  Google Scholar 

  • Ohkawa, H., Ohishi, N., and Yagi, K., 1979. Assay for lipid peroxides in animal tissues by thiobarbituric acid reaction. Analytical Biochemistry, 95 (2): 351–358.

    Article  Google Scholar 

  • Ott, M., Gogvadze, V., Orrenius, S., and Zhivotovsky, B., 2007. Mitochondria, oxidative stress and cell death. Apoptosis, 12 (5): 913–922.

    Article  Google Scholar 

  • Páez-Osuna, F., Gracia, A., Flores-Verdugo, F., Lyle-Fritch, L. P., Alonso-Rodrı, R., Roque, A., and Ruiz-Fernández, A. C., 2003. Shrimp aquaculture development and the environment in the Gulf of California ecoregion. Marine Pollution Bulletin, 46 (7): 806–815.

    Article  Google Scholar 

  • Pinho, G. L. L., Moura da Rosa, C., Maciel, F. E., Bianchini, A., Yunes, J. S., Proença, L. A. O., and Monserrat, J. M., 2005. Antioxidant responses and oxidative stress after microcystin exposure in the hepatopancreas of an estuarine crab species. Ecotoxicology and Environmental Safety, 61 (3): 353–360.

    Article  Google Scholar 

  • Ran, Q., Liang, H., Ikeno, Y., Qi, W., Prolla, T. A., Roberts, L. J., Wolf, N., VanRemmen, H., and Richardson, A., 2007. Reduction in glutathione peroxidase 4 increases life span through increased sensitivity to apoptosis. The Journals of Gerontology Series A: Biological Sciences and Medical Sciences, 62 (9): 932–942.

    Article  Google Scholar 

  • Ren, X., Pan, L., and Wang, L., 2014. Effect of florfenicol on selected parameters of immune and antioxidant systems, and damage indexes of juvenile Litopenaeus vannamei following oral administration. Aquaculture, 432, 106–113.

    Article  Google Scholar 

  • Ren, X., Pan, L., and Wang, L., 2015a. The detoxification process, bioaccumulation and damage effect in juvenile white shrimp Litopenaeus vannamei exposed to chrysene. Ecotoxicology and Environmental Safety, 114, 44–51.

    Article  Google Scholar 

  • Ren, X., Pan, L., and Wang, L., 2015b. Toxic effects upon exposure to benzo[a]pyrene in juvenile white shrimp Litope-naeus vannamei. Environmental Toxicology and Pharmacology, 39 (1): 194–207.

    Article  Google Scholar 

  • Rotruck, J., Pope, A., Ganther, H., Swanson, A., Hafeman, D. G., and Hoekstra, W., 1973. Selenium: Biochemical role as a component of glutathione peroxidase. Science, 179 (4073): 588–590.

    Article  Google Scholar 

  • Ryter, S. W., Kim, H. P., Hoetzel, A., Park, J. W., Nakahira, K., Wang, X., and Choi, A. M., 2007. Mechanisms of cell death in oxidative stress. Antioxidants and Redox Signaling, 9 (1): 49–89.

    Article  Google Scholar 

  • Sheehan, D., Meade, G., and Foley, V. M., 2001. Structure, function and evolution of glutathione transferases: Implications for classification of non-mammalian members of an ancient enzyme superfamily. Biochemical Journal, 360 (1): 1–16.

    Article  Google Scholar 

  • Sierra-Beltrán, A. P., Cortés-Altamirano, R., and Cortés-Lara, M. C., 2005. Occurrences of Prorocentrum minimum (Pavillard) in México. Harmful Algae, 4 (3): 507–517.

    Article  Google Scholar 

  • Sies, H., 1997. Oxidative stress: Oxidants and antioxidants. Experimental Physiology, 82 (2): 291–295.

    Article  Google Scholar 

  • Sørensen, J. G., Kristensen, T. N., and Loeschcke, V., 2003. The evolutionary and ecological role of heat shock proteins. Ecology Letters, 6(11): 1025–1037.

    Article  Google Scholar 

  • Tango, P., Magnien, R., Butler, W., Luckett, C., Luckenbach, M., Lacouture, R., and Poukish, C., 2005. Impacts and potential effects due to Prorocentrum minimum blooms in Chesapeake Bay. Harmful Algae, 4 (3): 525–531.

    Article  Google Scholar 

  • Vazquez, L., Alpuche, J., Maldonado, G., Agundis, C., Per-eyra-Morales, A., and Zenteno, E., 2009. Review: Immunity mechanisms in crustaceans. Innate Immunity, 15 (3): 179–188.

    Article  Google Scholar 

  • Vlamis, A., Katikou, P., Rodriguez, I., Rey, V., Alfonso, A., Papazachariou, A., Zacharaki, T., Botana, A. M., and Botana, L. M., 2015. First detection of tetrodotoxin in Greek shellfish by UPLC-MS/MS potentially linked to the presence of the dinoflagellate Prorocentrum minimum. Toxins, 7(5): 1779–1807.

    Article  Google Scholar 

  • Wang, X. H., Qu, R. J., Huang, Q. G., Wei, Z. B., and Wang, Z. Y., 2015. Hepatic oxidative stress and catalyst metals accumulation in goldfish exposed to carbon nanotubes under different pH levels. Aquatic Toxicology, 160, 142–150.

    Article  Google Scholar 

  • Wang, X. Q., Yan, B. L., Ma, S., and Dong, S. L., 2005. Study on the biology and cultural ecology of Exopalaemon carinicauda. Shandong Fisheries, 22, 21–24.

    Google Scholar 

  • Wei, K. Q., and Yang, J. X., 2015. Oxidative damage of hepato-pancreas induced by pollution depresses humoral immunity response in the freshwater crayfish Procambarus clarkii. Fish and Shellfish Immunology, 43(2): 510–519.

    Article  Google Scholar 

  • Winston, G. W., 1991. Oxidants and antioxidants in aquatic animals. Comparative Biochemistry and Physiology Part C: Comparative Pharmacology, 100(1–2): 173–176.

    Article  Google Scholar 

  • Xu, W. J., and Pan, L. Q., 2013. Enhancement of immune response and antioxidant status of Litopenaeus vannamei juvenile in biofloc-based culture tanks manipulating high C/N ratio of feed input. Aquaculture, 412, 117–124.

    Article  Google Scholar 

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Acknowledgments

This work was supported by the Program of Shandong Leading Talent (No. LNJY2015002), the Scientific and Technological Innovation Project Financially Supported by Qingdao National Laboratory for Marine Science and Technology (No. 2015ASKJ02), and the Qingdao Planned Projects for Postdoctoral Research Funds (No. ZQ 5120 1617013).

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  1. Key Laboratory for Sustainable Utilization of Marine Fisheries Resources of Ministry of Agriculture, Yellow Sea Fisheries Research Institute, Chinese Academy of Fishery Sciences, Qingdao, 266071, China

    Cuimin Mu, Qianqian Ge & Jian Li

  2. Function Laboratory for Marine Fisheries Science and Food Production Processes, Qingdao National Laboratory for Marine Science and Technology, Qingdao, 266071, China

    Cuimin Mu, Qianqian Ge & Jian Li

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  1. Cuimin Mu
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  2. Qianqian Ge
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Correspondence to Jian Li.

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Mu, C., Ge, Q. & Li, J. Exposure to Prorocentrum minimum Induces Oxidative Stress and Apoptosis in the Ridgetail White Prawn, Exopalaemon carinicauda. J. Ocean Univ. China 18, 727–734 (2019). https://doi.org/10.1007/s11802-019-3846-1

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