Effects of fucoidan polysaccharide extracted from seaweed Cystoseira trinodis (C. Agardh, 1820) on immune responses of vannamei shrimp Litopenaeus vannamei (Boone, 1931)

Document Type : Research Paper

Authors

1 - Ph.D. in Marine Biology, Department of Marine Biology, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran

2 Associate Professor in Department of Marine Biology, Faculty of Marine Science and Technology, University of Hormozgan, Bandar Abbas, Iran

3 Assistance Professor in Department of Biotechnology, Persian Gulf Research Institute, University of Persian Gulf, Bushehr, Iran

4 Assistance Professor in Iran Shrimp Research Center, Iranian Fisheries Science Research Institute, Agricultural Research Education and Extension Organization, Bushehr, Iran

5 Associate Professor in Department of Pharmaceutics, Faculty of Pharmacy, Mazandaran University of Medical Sciences, Sari, Iran

Abstract

The present study was performed in order to use the seaweed of the Persian Gulf (brown algae Cystoseira trinodis) and also the extraction of fucoidan polysaccharide as an immunostimulant supplementation to improve and enhance some immune parameters of vannamei shrimp. Therefore, 500 shrimp with average weight of 8g were divided into four treatments in triplicate (12 tanks) in a completely randomized design and were fed with diets containing 0, 0.1, 0.2 and 0.4% of fucoidan for 30 days. Results showed a significant effect of fucoidan treatments on the measured parameters (P<0.05). The immune parameters including the number of hyaline, granular and total homocyte cells, superoxide anion, phenoloxidase, superoxide dismutase, catalase and glutathione peroxidase activities in the groups fed with diets containing different levels of fucoidan, especially 0.4% indicated a significant increase compared to the control (P<0.05), while the amount of malondialdehyde showed a significant decrease compared to the control (P<0.05). In general, according to the results of the present study, it can be stated that fucoidan extracted from brown algae Cystoseira trinodis had better performance on improve immune parameters. Therefore, this bioactive compound can be recommended as an immunostimulant in the diet of white leg shrimp.

Keywords


Amparyup P., Charoensapsri W. and Tassanakajon A. 2013. Prophenoloxidase system and its role in shrimp immune responses against major pathogens. Fish and Shellfish Immunology, 34(4): 990–1001.
Bhabak K.P. and Mugesh G. 2010. Functional mimics of glutathione peroxidase: Bioinspired synthetic antioxidants. Accounts of Chemical Research, 43(11): 1408–1419.
Biagini G., Sala D. and Zini I. 1995. Diethyldithiocarbamate, a superoxide dismutase inhibitor, counteracts the maturation of ischemic-like lesions caused by endothelin-1 intrastriatal injection. Neuroscience Letters, 190(3): 212–216.
Bilan M.I., Grachev A.A., Shashkov A.S., Nifantiev N.E. and Usov A.I. 2006. Structure of a fucoidan from the brown seaweed Fucus serratus L. Carbohydrate Research, 341(2): 238–245.
Cabello F.C. 2006. Heavy use of prophylactic antibiotics in aquaculture: A growing problem for human and animal health and for the environment. Environmental Microbiology, 8(7): 1137–1144.
Cantelli L., Goncalves P., Guertler C., Kayser M., Pilotto M.R., Barracco M.A. and Perazzolo L.M. 2019. Dietary supplementation with sulfated polysaccharides from Gracilaria birdiae promotes a delayed immunostimulation in marine shrimp challenged by the white spot syndrome virus. Aquaculture International, 27(2): 349–367.
Chang C.F., Su M.S., Chen H.Y., and Liao I.C. 2003. Dietary β-1, 3-glucan effectively improves immunity and survival of Penaeus monodon challenged with white spot syndrome virus. Fish and Shellfish Immunology, 15(4): 297–310.
Chang Z.Q., Ge Q.Q., Sun M., Wang Q., Lv H.Y. and Li J. 2018. Immune responses by dietary supplement with Astragalus polysaccharides in the Pacific white shrimp, Litopenaeus vannamei. Aquaculture Nutrition, 24(2): 702–711.
Chen G.F., Huang J. and Song X.L. 2004. General situation of the immunological capability of shrimp. Journal of Fisheries of China, 28: 209–215.
Chen Y.Y., Chen J.C., Lin Y.C., Putra D.F., Kitikiew S., Li C.C. and Yeh S.T. 2014. Shrimp that have received carrageenan via immersion and diet exhibit immunocompetence in phagocytosis despite a post-plateau in immune parameters. Fish and Shellfish Immunology, 36(2): 352–366.
Cheng W., Liu C.H., Kuo C.M. and Chen J.C. 2005. Dietary administration of sodium alginate enhances the immune ability of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish and Shellfish Immunology, 18(1): 1–12.
Guiry M.D. and Guiry G.M. 2013. Algae Base. Galway: World-Wide Electronic Publication. Retrieved March 11, 2021, National University of Ireland, from http://www.algaebase.org.
Hayyan M., Hashim M.A. and AlNashef I.M. 2016. Superoxide ion: Generation and chemical implications. Chemical Reviews, 116(5): 3029–3085.
Huynh T.G., Yeh S.T., Lin Y.C., Shyu J.F., Chen L.L. and Chen J.C. 2011. White shrimp Litopenaeus vannamei immersed in seawater containing Sargassum hemiphyllum var. chinense powder and its extract showed increased immunity and resistance against Vibrio alginolyticus and white spot syndrome virus. Fish and Shellfish Immunology, 31(2): 286–293.
Immanuel G., Sivagnanavelmurugan M., Marudhupandi T., Radhakrishnan S. and Palavesam A. 2012. The effect of fucoidan from brown seaweed Sargassum wightii on WSSV resistance and immune activity in shrimp Penaeus monodon (Fab). Fish and Shellfish Immunology, 32(4): 551–564.
Itami T., Asano M., Tokushige K., Kubono K., Nakagawa A., Takeno N. and Takahashi Y. 1998. Enhancement of disease resistance of kuruma shrimp, Penaeus japonicus, after oral administration of peptidoglycan derived from Bifidobacterium thermophilum. Aquaculture, 164(4): 277–288.
Jiravanichpaisal P., Lee B.L. and Soderhall K. 2006. Cell-mediated immunity in arthropods: Hematopoiesis, coagulation, melanization and opsonization. Immunobiology, 211(4): 213–236.
Kitikiew S., Chen J.C., Putra D.F., Lin Y.C., Yeh S.T. and Liou C.H. 2013. Fucoidan effectively provokes the innate immunity of white shrimp Litopenaeus vannamei and its resistance against experimental Vibrio alginolyticus infection. Fish and Shellfish Immunology, 34(1): 280–290.
Lin Y.C., Yeh S.T., Li C.C., Chen L.L., Cheng A.C. and Chen J.C. 2011. An immersion of Gracilaria tenuistipitata extract improves the immunity and survival of white shrimp Litopenaeus vannamei challenged with white spot syndrome virus. Fish and Shellfish Immunology, 31(6): 1239–1246.
Liu W.C., Zhou S.H., Balasubramanian B., Zeng F.Y., Sun C.B. and Pang H.Y. 2020. Dietary seaweed (Enteromorpha) polysaccharides improves growth performance involved in regulation of immune responses, intestinal morphology and microbial community in banana shrimp Fenneropenaeus merguiensis. Fish and Shellfish Immunology, 104(6): 202–212.
Liu Y., Wang W.N., Wang A.L., Wang J.M. and Sun R.Y. 2007. Effects of dietary vitamin E supplementation on antioxidant enzyme activities in Litopenaeus vannamei (Boone, 1931) exposed to acute salinity changes. Aquaculture, 265(4): 351–358.
Mandal P., Mateu C.G., Chattopadhyay K., Pujol C.A., Damonte E.B. and Ray B. 2007. Structural features and antiviral activity of sulphated fucans from the brown seaweed Cystoseira indica. Antiviral Chemistry and Chemotherapy, 18(3): 153–162.
Mir I.N., Sahu N.P., Pal A.K. and Makesh M. 2017. Synergistic effect of l-methionine and fucoidan rich extract in eliciting growth and non-specific immune response of Labeo rohita fingerlings against Aeromonas hydrophila. Aquaculture, 479 (1): 396–403.
MOA (Fisheries Bureau, Ministry of Agriculture) .2016. China Fishery Statistics Yearbook 2016. China Agriculture Press, China. 155P.
Niu J., Liu Y.J., Lin H.Z., Mai K.S., Yang H.J., Liang G.Y. and Tian L.X. 2011. Effects of dietary chitosan on growth, survival and stress tolerance of postlarval shrimp, Litopenaeus vannamei. Aquaculture Nutrition, 17(2): 406–412.
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.
Pacheco R., Ascencio F., Zarain M., Gomez G. and Campa Á. 2011. Enhancement of superoxide dismutase and catalase activity in juvenile brown shrimp, Farfantepenaeus californiensis (Holmes, 1900), fed b-1.3 glucan vitamin E, and b-carotene and infected with white spot syndrome virus. Latin American Journal of Aquatic Research, 39(3): 534–543.
Paglia D.E. and Valentine W.N. 1967. Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. The Journal of Laboratory and Clinical Medicine, 70(1): 158–169.
Sarathi M., Ahmed V.I., Venkatesan C., Balasubramanian G., Prabavathy J. and Hameed A.S. 2007. Comparative study on immune response of Fenneropenaeus indicus to Vibrio alginolyticus and white spot syndrome virus. Aquaculture, 271(1): 8–20.
Sivagnanavelmurugan M., Karthik Ramnath G., Jude Thaddaeus B., Palavesam A. and Immanuel G. 2015. Effect of Sargassum wightii fucoidan on growth and disease resistance to Vibrio parahaemolyticus in Penaeus monodon postā€larvae. Aquaculture Nutrition, 21(6): 960–969.
Sivagnanavelmurugan M., Marudhupandi T., Palavesam A. and Immanuel G. 2012. Antiviral effect of fucoidan extracted from the brown seaweed, Sargassum wightii, on shrimp Penaeus monodon postlarvae against white spot syndrome virus. Journal of the World Aquaculture Society, 43(5): 697–706.
Sivagnanavelmurugan M., Thaddaeus B.J., Palavesam A. and Immanuel G. 2014. Dietary effect of Sargassum wightii fucoidan to enhance growth, prophenoloxidase gene expression of Penaeus monodon and immune resistance to Vibrio parahaemolyticus. Fish and Shellfish Immunology, 39(2): 439–449.
Sun Y., Li M., Mitra S., Hafiz Muhammad R., Debnath B., Lu X. and Qiu D. 2018. Comparative phytochemical profiles and antioxidant enzyme activity analyses of the southern highbush blueberry (Vaccinium corymbosum) at different developmental stages. Molecules, 23(9): 1–14.
Takahashi Y., Kondo M., Itami T., Honda T., Inagawa H., Nishizawa T., and Yokomizo Y. 2000. Enhancement of disease resistance against penaeid acute viraemia and induction of virus-inactivating activity in haemolymph of kuruma shrimp, Penaeus japonicus, by oral administration of Pantoea agglomerans lipopolysaccharide (LPS). Fish and Shellfish Immunology, 10(6): 555–558.
Traifalgar R.F., Kira H., Thanh Tung H., Raafat Michael F., Laining A., Yokoyama S. and Corre V. 2010. Influence of dietary fucoidan supplementation on growth and immunological response of juvenile Marsupenaeus japonicas. Journal of the World Aquaculture Society, 41(2): 235–244.
Traifalgar R.F., Serrano A.E., Corre V., Kira H., Tung H.T., Michael F.R. and Koshio S. 2009. Evaluation of dietary fucoidan supplementation effects on growth performance and vibriosis resistance of Penaeus monodon postlarvae. Aquaculture Science, 57(2): 167–174.
Van Wyk P., Davis-Hodgkins M., Laramore C.R., Main K.L., Mountain J. and Scarpa J. 1999. Farming Marine Shrimp in Recirculating Freshwater Systems. Harbor Branch Oceanographic Institution, USA. 220P.
Yang C., Chung D. and You S. 2008. Determination of physicochemical properties of sulphated fucans from sporophyll of Undaria pinnatifida using light scattering technique. Food Chemistry, 111(2): 503–507.
Yang H.T., Yang M.C., Sun J.J., Guo F., Lan J.F., Wang X.W. and Wang J.X. 2015. Catalase eliminates reactive oxygen species and influences the intestinal microbiota of shrimp. Fish and Shellfish Immunology, 47(1): 63–73.
Yu B.P. 1994. Cellular defenses against damage from reactive oxygen species. Physiological Reviews, 74(1): 139–162.