Abstract
This study evaluated the individual effects of microcystin-LR (MC-LR) with different concentrations (0, 10, 20, 30, 40 and 50 μg L−1) and the combined influences with astaxanthin (10 and 100 μg L−1) from Haematococcus pluvialis on the survival and oxidative stress of zebrafish embryos. Results showed that the reactive oxygen species (ROS), malondialdehyde (MDA), mortality and deformity rate were increased in the presence of MC-LR accompanied with the reduction of the glutathione peroxidase (GSH), superoxide dismutase (SOD), the total antioxidant capacity (T-AOC) and hatching rate of the zebrafish embryo. The higher the MC-LR concentration was, the stronger the developmental and oxidative stress response (p < 0.05). This study confirmed that the supplementation of astaxanthin could significantly alleviate the toxic effects of MC-LR on zebrafish embryos. The mortality and deformity rates decreased significantly in the combined exposure group compared with the only MC-LR exposure group, and the decreasing rates were positively correlated with the astaxanthin concentration. Astaxanthin could also significantly improve the oxidative stress response and damage caused by MC-LR. The ROS and MDA contents of juvenile fish decreased, whereas GSH, SOD and T-AOC increased significantly with astaxanthin supplementation. Therefore, astaxanthin might be a suitable diet supplement against the MC-LR contamination of pond aquaculture.
Similar content being viewed by others
References
Aguilera A, Haakonsson S, Martin MV, Salerno GL, Echenique RO (2018) Bloom forming cyanobacteria and cyanotoxins in Argentina: a growing health and environmental concern. Limnologica 69:103–114
Ambati RR, Phang SM, Ravi S, Aswathanarayana RG (2014) Astaxanthin: sources, extraction, stability, biological activities and its commercial applications-a review. Mar Drugs 12:128–152
An ZH, Zhang YY, Sun LS (2018) Effects of dietary astaxanthin supplementation on energy budget and bioaccumulation in Procambarus clarkii (Girard, 1852) crayfish under Microcystin-LR stress. Toxins 10:277
An ZH, Yang H, Liu XD, Zhang YY (2020) Effects of astaxanthin on the immune response and reproduction of Procambarus clarkii stressed with microcystin-leucine-arginine. Fisheries Sci 86:759–766
Angell A, De Nys R, Mangott A, Vucko MJ (2018) The effects of concentration and supplementation time of natural and synthetic sources of astaxanthin on the colouration of the prawn Penaeus monodon. Algal Res 35:577–585
Antonio M, Juri R, Patrizia C, Antonietta C, Vincenzo L, Simeone C, Despina K, Sanjeet M, Angelo F, Evangelos H, Dino M (2018) Extraction of astaxanthin from microalga Haematococcus pluvialis in red phase by using generally recognized as safe solvents and accelerated extraction. J Biotechnol 283:51–61
Barclay M, Irvin S, Williams K, Smith D (2006) Comparison of diets for the tropical spiny lobster Panulirus ornatus: astaxanthin-supplemented feeds and mussel flesh. Aquacult Nutr 12:117–125
Bi XD, Dai W, Wang XY, Dong SJ, Zhang SL, Zhang DJ, Wu M (2019) Microcystins distribution, bioaccumulation, and Microcystis genotype succession in a fish culture pond. Sci Total Environ 688:380–388
Brzuzan P, Woźny M, WoliWoli L, Piasecka A (2012) Expression profiling in vivo demonstrates rapid changes in liver microRNA levels of whitefish (Coregonus lavaretus) following microcystin-LR exposure. Aquat Toxicol 122-123:188–196
Bu Q, Wang B, Huang J, Liu K, Deng S, Wang Y (2016) Estimating the use of antibiotics for humans across China. Chemosphere 11:138–144
Cabello FC (2006) Heavy use of prophylactic antibiotics in aquaculture: a growing problem for human and animal health and for the environment. Environ Microbiol 8:1137–1144
Chen R, Lochmann R, Goodwin A, Praveen K, Dabrowski K, Lee KJ (2004) Effects of dietary vitamins C and E on alternative complement activity, hematology, tissue composition, vitamin concentrations and response to heat stress in juvenile golden shiner (Notemigonus crysoleucas). Aquaculture 242:553–569
Chen J, Xie P, Li L, Xu J (2009) First identification of the hepatotoxic microcystins in the serum of a chronically exposed human population together with indication of hepatocellular damage. Toxicol Sci 108:81–89
Chen Y, Zeng SF, Cao YF (2012) Oxidative stress response in zebrafish (Danio rerio) gill experimentally exposed to subchronic microcystin-LR. Environ Monit Assess 184:6775–6787
Chen L, Wang YK, Giesy JP, Chen F, Shi T, Chen J, Xie P (2018) Microcystin-LR affects the hypothalamic-pituitary-inter-renal (HPI) axis in early life stages (embryos and larvae) of zebrafish. Environ Poll 241:540–548
Cheng CH, Guo ZX, Ye CX, Wang AL (2018) Effect of dietary astaxanthin on the growth performance, non-specific immunity, and antioxidant capacity of pufferfish (Takifugu obscurus) under high temperature stress. Fish Physiol Biochem 44:209–218
Chien YH, Shiau WC (2005) The effects of dietary supplementation of algae and synthetic astaxanthin on body astaxanthin, survival, growth, and low dissolved oxygen stress resistance of kuruma prawn, Marsupenaeus japonicus Bate. J Exp Mar Biol Ecol 318:201–211
Chien YH, Pan CH, Hunter B (2003) The resistance to physical stresses by Penaeus monodon juveniles fed diets supplemented with astaxanthin. Aquaculture 216:177–191
Cui WD, Leng XJ, Li XQ, Li XN, Xu J (2009) Effects of astaxanthin and canthaxanthin on pigmentation of muscle and total antioxidant capacity of liver in rainbow trout Oncorhynchus mykiss. J Fish China 33:987–995
Diler I, Gokoglu N (2004) Investigation of the sensory properties of the flesh of rainbow trout (Oncorhynchus mykiss) fed diets with astaxanthin, shrimp waste meal and red pepper meal. Eur Food Res Technol 219:217–222
Florczyk M, Brzuzan P, Łakomiak A, Jakimiuk E, Woźny M (2019) Microcystin -LR - triggered neuronal toxicity in whitefish does not involve MiR124-3p. Neurotoxicity Res 35:29–40
Flores M, Dıaz F, Medina R, Re AD, Licea A (2007) Physiological, metabolic and haematological responses in white shrimp Litopenaeus vannamei (Boone) juveniles fed diets supplemented with astaxanthin acclimated to low-salinity water. Aquac Res 38:740–747
Ghazali IE, Saqrane S, Carvalho AP, Ouahid Y, Oudra B, Campo FFD, Vasconcelos V (2009) Compensatory growth induced in zebrafish larvae after pre-exposure to a Microcystis aeruginosa natural bloom extract containing microcystins. Int J Mol Sci 10:133–146
Giri SS, Sen SS, Chi C, Kim HJ, Yun S, Park SC (2015) Chlorophytum borivilianum polysaccharide fraction provokes the immune function and disease resistance of Labeo rohita against Aeromonas hydrophila. J Immunol Res 11:15–25
Han T, Li X, Wang J, Wang C, Yang M, Zheng P (2018) Effects of dietary astaxanthin supplementation on pigmentation, antioxidant capacity and nutritional value of swimming crab, Portunus trituberculatus. Aquaculture 490:169–177
Ho ALFC, O’Shea SK, Pomeroy HF (2013) Dietary esterified astaxanthin effects on color, carotenoid concentrations, and compositions of clown anemonefish, Amphiprion ocellaris, skin. Aquacult Int 21:361–374
Hong ME, Hwang SK, Chang WS, Kim BW, Lee J, Sim SJ (2015) Enhanced autotrophic astaxanthin production from Haematococcus pluvialis under high temperature via heat stress-driven Haber-Weiss reaction. Appl Microbiol Biotechnol 99:5203–5215
Hu XB, Zhang RF, Ye JY, Wu X, Zhang YX, Wu CL (2018) Monitoring and research of microcystins and environmental factors in a typical artificial freshwater aquaculture pond. Environ Sci Pollut Res 25:5921–5933
Huang SH, Ma JT, Zhang NN, Ren XP (2013) Toxic effects of xylene and microcystin-LR on zebrafish embryos. J Environ Health 30:308–311 (In Chinese)
Jagruthi C, Yogeshwari G, Anbazahan SM, Mari LSS, Arockiaraj J, Mariappan P (2014) Effect of dietary astaxanthin against Aeromonas hydrophila infection in common carp, Cyprinus carpio. Fish Shellfish Immunol 41:674–680
Jiang XD, Zu L, Wang ZY, Cheng YX, Yang YH, Wu XG (2020) Micro-algal astaxanthin could improve the antioxidant capability, immunity and ammonia resistance of juvenile Chinese mitten crab, Eriocheir sinensis. Fish Shellfish Immunol 102:499–510
Ju ZY, Deng DF, Dominy WG, Forster IP (2011) Pigmentation of Pacific white shrimp, Litopenaeus vannamei, by dietary astaxanthin extracted from Haematococcus pluvialis. J World Aquacult Soc 42:633–644
Lajayer BA, Ghorbanpour M, Nikabadi S (2017) Heavy metals in contaminated environment: destiny of secondary metabolite biosynthesis, oxidative status and phytoextraction in medical plants. Ecotoxicol Environ Saf 145:377–390
Łakomiak A, Brzuzan P, Jakimiuk E, Florczy kM, Woźny M (2016) MiR-34a and bcl-2 expression in whitefish (Coregonus lavaretus) after microcystin-LR exposure. Comp Biochem Physiol B 193:47–56
Le Manach S, Khenfech N, Huet H, Qiao Q, Duval C, Marie A, Bolbach G, Clodic G, Djediat C, Bernard C, Edery M, Marie B (2016) Gender-specific toxicological effects of chronic exposure to pure microcystin-LR or complex Microcystis aeruginosa extracts on adult medaka fish. Environ Sci Technol 50:8324–8334
Li J, Li R, Li J (2017) Current research scenario for microcystins biodegradation - a review on fundamental knowledge, application prospects and challenges. Sci Total Environ 595:615–632
Li MY, Liu XY, Xia CG, Wang GQ, Zhang DM (2019) Astaxanthin enhances hematology, antioxidant and immunological parameters, immune-related gene expression, and disease resistance against in Channa argus. Aquacult Int 27:735–746
Li HM, Gu XH, Chen HH, Mao ZG, Zeng QF, Yang HT, Kan KC (2021) Comparative toxicological effects of planktonic Microcystis and benthic Oscillatoria on zebrafish embryonic development: Implications for cyanobacteria risk assessment. Environ Poll 274:115852
Lim C, Yusoff FM, Shariff M, Kamarudin MS (2018) Astaxanthin as feed supplement in aquatic animals. Rev Aquacult 10:738–773
Lin W, Guo HH, Wang LK, Zhang DD, Wu XY, Li L, Li DP, Tang R (2018) Nitrite enhances MC-LR-induced changes on splenic oxidation resistance and innate immunity in male zebrafish. Toxins 10:512
Liu ZD, Tang R, Li DP, Hu Q, Wang Y (2015) Subacute microcystin-LR exposure alters the metabolism of thyroid hormones in juvenile zebrafish (Danio rerio). Toxins 7:337–352
Liu F, Shi HZ, Guo QS, Yu YB, Wang AM, Lv F (2016) Effects of astaxanthin and emodin on the growth, stress resistance and disease resistance of yellow catfish (Pelteobagrus fulvidraco). Fish Shellfish Immunol 51:12–25
Ma J, Brookes JD, Qin B, Paerl HW, Gao G, Wu P, Zhang W, Deng J, Zhu G, Zhang Y, Xu H, Niu H (2014) Environmental factors controlling colony formation in blooms of the cyanobacteria Microcystis spp. in Lake Taihu, China. Harmful Algae 31:136–142
Merchie G, Kontara E, Lavens P, Robles R, Kurmaly K, Sorgeloos P (1998) Effect of vitamin C and astaxanthin on stress and disease resistance of postlarval tiger shrimp Penaeus monodon (Fabricius). Aquac Res 29:579–585
Naguib YM (2000) Antioxidant activities of astaxanthin and related carotenoids. J Agric Food Chem 48:1150–1154
Niu J, Tian LX, Liu YJ, Yang HJ, Ye CX, Gao W, Mai KS (2009) Effect of dietary astaxanthin on growth, survival, and stress tolerance of postlarval shrimp, Litopenaeus vannamei. J World Aquacult Soc 40:795–802
Oberemm A, Fastner J, Steinberg CEW (1997) Effects of microcystin-LR and cyanobacterial crude extracts on embryo-larval development of zebrafish (Danio rerio). Water Res 31:2921
Omidi A, Esterhuizen-Londt M, Pflugmacher S (2018) Still challenging: the ecological function of the cyanobacterial toxin microcystin- what we know so far. Toxin Rev 37:87–105
Ost RVD, Beyer J, Vermeulen NPE (2003) Fish bioaccumulation and biomarkers in environmental risk assessment: a review. Environ Toxicol Pharmacol 13:57–149
Paerl HW, Tucker CS (2010) Ecology of bluegreen algae in aquaculture ponds. J World Aquacult Soc 26:109–131
Pan CH, Chien YH, Hunter B (2003) The resistance to ammonia stress of Penaeus monodon Fabricius juvenile fed diets supplemented with astaxanthin. J Exp Mar Biol Ecol 297:107–118
Panis G, Carreon J (2016) Commercial astaxanthin production derived by green alga Haematococcus pluvialis: a microalgae process model and a techno-economic assessment all through production line. Algal Res 18:175–190
Pavagadhi S, Balasubramanian R (2013). Toxicological evaluation of microcystins in aquatic fish species: current knowledge and future directions. Aquat Toxicol 142-143C: 1-16.
Pham T, Utsumi M (2018) An overview of the accumulation of microcystins in aquatic ecosystems. J Environ Manag 213:520–529
Pradhan A, Silva CO, Silva C, Pascoal C, Cassio F (2016) Enzymatic biomarkers can portray nanoCuO-induced oxidative and neuronal stress in freshwater shredders. Aquat Toxicol 180:227–235
Qi M, Dang Y, Xu Q, Yu L, Liu C, Yuan Y, Wang J (2016) Microcystin-LR induced developmental toxicity and apoptosis in zebrafish (Danio rerio) larvae by activation of ER stress response. Chemosphere 157:166–173
Requena JR, Fu MX, Ahmed MU, Jenkins AJ, Lyons TJ, Thorpe SR (1996) Lipoxidation products as biomarkers of oxidative damage to proteins during lipid peroxidation reactions. Nephrol Dial Transpl 11:48–53
Rippka R, Deruelle J, Waterbury J, Herdman M, Stanier R (1979) Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61
Saraf SR, Frenkel A, Harke MJ, Jankowiak JG, Gobler CJ, Mcelroy AE (2018) Effects of Microcystis on development of early life stage Japanese medaka (Oryzias latipes): comparative toxicity of natural blooms, cultured microcystis and microcystin-LR. Aquat Toxicol 194:18–26
Shimada N, Okuda Y, Maeda K, Umeno D, Takaichi S, Ikeuchi M (2020) Astaxanthin production in a model cyanobacterium Synechocystis sp. PCC 6803. J Gen Appl Microbiol 66:116–120
Sinden A, Sinang SC (2016) Cyanobacteria in aquaculture systems: linking the occurrence, abundance and toxicity with rising temperatures. Int J Environ Sci Technol 13:1–8
Sommer TR, D’Souza FML, Morrissy NM (1992) Pigmentation of adult rainbow trout, Oncorhynchus mykiss, using the green alga Haematococcus pluvialis. Aquaculture 106:63–74
Song S, Zhou F, Nordquist RE, Carubelli R, Liu H, Chen WR (2009) Glycated chitosan as a new non-toxic immunological stimulant. Immunopharmacol Immunotoxicol 31:202–208
Susanne F, Verena G, Karl G (2016) Comparative effects of nodularin and microcystin-LR in zebrafish: 2. Uptake and molecular effects in eleuthero-embryos and adult liver with focus on endoplasmic reticulum stress. Aquat Toxicol 171:77–87
Wang Z, Cai CF, Cao XM, Zhu JM, He J, Wu P (2018) Supplementation of dietary astaxanthin alleviated oxidative damage induced by chronic high pH stress, and enhanced carapace astaxanthin concentration of Chinese mitten crab Eriocheir sinensis. Aquaculture 483:230–237
Wang HJ, Xu C, Liu Y, Jeppesen E, Svenning JC, Wu JG, Zhang WX, Zhou TJ, Wang P, Nangombe S, Ma JG, Duan HT, Fang JY, Xie P (2021) From unusual suspect to serial killer: cyanotoxins boosted by climate change may jeopardize African megafauna. The Innovation 2:100092
Wei J, Zhang F, Tian WJ, Kong YQ, Li Q, Yu N, Du ZY, Wu QQ, Qin JG, Chen LQ (2016) Effects of dietary folic acid on growth, antioxidant capacity, no-specific immune response and disease resistance of juvenile Chinese mitten crab Eriocheir sinensis (Milne-Edwards, 1853). Aquacult Nutr 22:567–574
Yang H, Xie P, Xu J (2006) Seasonal variation of microcystin concentration in lake Chaohu, a shallow subtropical lake in the People’s Republic of China. Bull Environ Contam Tox 77:367–374
Yao YH, He WH, Yu LN (2007) Mechanism of forming of cyanobacteria bloom and its effects on aquaculture. Acta Agr Jiangxi 19:98–100 (In Chinese)
Yarahmadi P, Ghafari H, Khazaii A, Khodadadi M, Rashidiyan G, Jalali MA (2016) Protective effects of the prebiotic on the immunological indicators of rainbow trout (Oncorhynchus mykiss) infected with Aeromonas hydrophila. Fish Shellfish Immunol 54:589–597
Zhang J, Liu YJ, Tian LX, Yang HJ, Liang GY, Yue YR, Xu DH (2013) Effects of dietary astaxanthin on growth, antioxidant capacity and gene expression in Pacific white shrimp Litopenaeus vannamei. Aquacult Nutr 19:917–927
Zhao YT, Yue CC, Ding W, Li Tao XJW, Zhao P, Ma HX, Yu XY (2018) Butylated hydroxytoluene induces astaxanthin and lipid production in Haematococcus pluvialis under high-light and nitrogen-deficiency conditions. Bioresour Technol 266:315–321
Funding
This work was financially supported by the Key Scientific Research Project of Henan Higher Education University (No. 20A240004), Young Backbone Teachers Project of Henan Province (No. 2020GGJS064), the National Natural Science Foundation of China (No. 21906046) and the Science and Technology Project of Henan Province (No. 192102310138).
Author information
Authors and Affiliations
Corresponding authors
Ethics declarations
Competing interests
The authors declare no competing interests.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Dong, J., Li, C., Dai, D. et al. Protective effects of astaxanthin from Haematococcus pluvialis on the survival and oxidative stress of zebrafish embryos induced by microcystin-LR. J Appl Phycol 33, 2261–2271 (2021). https://doi.org/10.1007/s10811-021-02448-6
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-021-02448-6