Abstract
Ammonia is the main environmental pollutant in aquaculture that has a negative impact on the healthy cultivation of common carp. The effects of antioxidant capacity, histopathology, and related gene expression of common carp (Cyprinus carpio) under ammonia stress (2.6 mM ammonia concentration, 168 h) were studied. In the study, ammonia stress can lead to oxidative stress in common carp, which is related to the regulation of SOD, GSH-PX, and CAT activities. Histopathology and TUNEL assays confirmed that apoptosis occurred in the hepatopancreas after ammonia stress, and the rate of apoptosis increased significantly with increasing exposure time (P < 0.05). We found the mRNA expression of p53, BAX, caspase-9, and caspase-3 were significantly enhanced (P < 0.05), and the transcriptional expression of BCL-2 was significantly inhibited (P < 0.05) in the late stage of ammonia exposure (96 h and 168 h). The results showed the apoptosis in the hepatopancreas of common carp under ammonia stress may be mediated by oxidative stress through the p53–BAX/BCL-2 apoptosis signal pathway.
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References
Abu-Elala NM, Reham M et al (2016) Eutrophication, ammonia intoxication, and infectious diseases: interdisciplinary factors of mass mortalities in cultured Nile tilapia. J Aquat Anim Health 28(3):187–198. https://doi.org/10.1080/08997659.2016.1185050
Chao L, Wu F, Que H, Zhang G (2019) Relationships of growth and mortality to enzymatic activity, and the relative mRNA expression of cultured scallops Patinopecten yessoensis in the Yellow Sea, China. J Oceanol Limnol 37:1409–1422. https://doi.org/10.1007/s00343-019-7257-3
Chen D, Ning F, Zhang J, Tang Y, Teng X (2020) NF-κB pathway took part in the development of apoptosis mediated by miR-15a and oxidative stress via mitochondrial pathway in ammonia-treated chicken splenic lymphocytes. Sci Total Environ 729:139017. https://doi.org/10.1016/j.scitotenv.2020.139017
Cheng CH, Yang FF, Ling RZ, Liao SA, Miao YT, Ye CX, Wang AL (2015) Effects of ammonia exposure on apoptosis, oxidative stress and immune response in pufferfish (Takifugu obscurus). Aquat Toxicol 164:61–71. https://doi.org/10.1016/j.aquatox.2015.04.004
Dabrowska HW, Asow T (1986) Sublethal effect of ammonia on certain biochemical and haematological indicators in common carp (Cyprinus carpio L.). Comparative Biochemistry and Physiology. Part C, Comparative Pharmacology 83(1):179–184. https://doi.org/10.1016/0742-8413(86)90033-2
Eddy FB (2005) Ammonia in estuaries and effects on fish. J Fish Biol 67(6):1495–1513. https://doi.org/10.1111/j.1095-8649.2005.00930.x
Emerson K, Russo RC, Lund RE, Thurston RV (1975) Aqueous ammonia equilibrium calculations: effect of pH and temperature. J Fish Res Board Can 32(12):2379–2383. https://doi.org/10.1139/f75-274
Han Q, Zhang J, Sun Q, Xu Y, Teng X (2020) Oxidative stress and mitochondrial dysfunction involved in ammonia-induced nephrocyte necroptosis in chickens. Ecotoxicol Environ Saf 203:110974. https://doi.org/10.1016/j.ecoenv.2020.11097
Ip YK, Leong MW, Sim MY et al (2005) Chronic and acute ammonia toxicity in mudskippers, Periophthalmodon schlosseri and Boleophthalmus boddaerti: brain ammonia and glutamine contents, and effects of methionine sulfoximine and MK801. J Exp Biol 208(Pt 10):1993–2004. https://doi.org/10.1242/jeb.01586
Jeney G, Nemcsók J, Jeney Z et al (1992) Acute effect of sublethal ammonia concentrations on common carp (Cyprinus carpio L.). II. Effect of ammonia on blood plasma transaminases (GOT, GPT), G1DH enzyme activity, and ATP value. aquaculture 104(1–2):149–156. https://doi.org/10.1016/0044-8486(92)90145-B
Jiang W, Du M, Fang J et al (2019) Response of yesso scallop patinopecten yessoensis to acute temperature challenge: physiological and biochemical parameters. J Oceanol Limnol 37:321–332. https://doi.org/10.1007/s00343-019-7245-
Jin JL, Wang Y, Wu ZX et al (2017) Transcriptomic analysis of liver from grass carp (Ctenopharyngodon idellus) exposed to high environmental ammonia reveals the activation of antioxidant and apoptosis pathways. Fish Shellfish Immunol 63:444–451. https://doi.org/10.1016/j.fsi.2017.02.037
Khalid A, Zubair A, Hmoud F et al (2016) Effects of a low-radiotoxicity uranium salt (uranyl acetate) on biochemical and hematological parameters of the catfish, Clarias gariepinus. Chin J Oceanol Limnol 34:109–117. https://doi.org/10.1007/s00343-015-4392-3
Kornelia P, Yong X, Jay LZ et al (1997) A model for p53-induced apoptosis. Nature 389(6648):300–305. https://doi.org/10.1038/38525
Li M, Yu N, Qin JG, Li E, du Z, Chen L (2014) Effects of ammonia stress, dietary linseed oil and Edwardsiella ictaluri challenge on juvenile darkbarbel catfish Pelteobagrus vachelli. Fish & Shellfish Immunol 38(1):158–165. https://doi.org/10.1016/j.fsi.2014.03.015
Lia YD, Zhou FL, Huang JH et al (2018) Transcriptome reveals involvement of immune defense, oxidative imbalance, and apoptosis in ammonia-stress response of the black tiger shrimp (Penaeus monodon). Fish & Shellfish Immunol 83:162–170. https://doi.org/10.1016/j.fsi.2018.09.026
Liew HJ, Sinha, et al. (2013) Differential responses in ammonia excretion, sodium fluxes and gill permeability explain different sensitivities to acute high environmental ammonia in three freshwater teleosts. Aquat Toxicol 126:63–76. https://doi.org/10.1016/j.aquatox.2012.10.012
Lin YC, Chen JC (2001) Acute toxicity of ammonia on Litopenaeus vannamei Boone juveniles at different salinity levels. J Exp Mar Biol Ecol 259(1):109–119. https://doi.org/10.1016/S0022-0981(01)00227-1
Michela P, Cosima TB (2009) Apoptosis and oxidative stress-related diseases: the p66Shc connection. Curr Mol Med 9(3):392–398. https://doi.org/10.2174/156652409787847254
Murakami M, Ohi M, Ishikawa S, Shirai M, Horiguchi H, Nishino Y, Funaba M (2015) Adaptive expression of uncoupling protein 1 in the carp liver and kidney in response to changes in ambient temperature. Comparative Biochemistry & Physiology Part A Molecular & Integrative Physiology 185:142–149. https://doi.org/10.1016/j.cbpa.2015.04.003
Ogundele OM, Sanya OJ (2015) Bax modulates neuronal survival while p53 is unaltered after cytochrome c induced oxidative stress in the adult olfactory bulb in vivo. Ann Neurosci 22:19–25. https://doi.org/10.5214/ans.0972.7531.220105
Paust LO, Foss A, Imsland AK (2011) Effects of chronic and periodic exposure to ammonia on growth, food conversion efficiency and blood physiology in juvenile Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 315(3-4):400–406. https://doi.org/10.1016/j.aquaculture.2011.03.008
Peyghan R, Takamy GA (2002) Histopathological, serum enzyme, cholesterol and urea changes in experimental acute toxicity of ammonia in common carp Cyprinus carpio and use of natural zeolite for prevention. Aquac Int 10(4):317–325. https://doi.org/10.1023/a:1022408529458
Qi XZ, Xue MY, Yang SB, Zha JW, Wang GX, Ling F (2017) Ammonia exposure alters the expression of immune-related and antioxidant enzymes-related genes and the gut microbial community of crucian carp (Carassius auratus). Fish & Shellfish Immunol 70:485–490. https://doi.org/10.1016/j.fsi.2017.09.043
Randall DJ, Tsui TKN (2002) Ammonia toxicity in fish. Mar Pollut Bull 45(1-12):17–23. https://doi.org/10.1016/s0025-326x(02)00227-8
Sinha AK, Abd EH, Giblen T et al (2014) Anti-oxidative defences are modulated differentially in three freshwater teleosts in response to ammonia-induced oxidative stress. PLoS One 9(4):e95319. https://doi.org/10.1371/journal.pone.0095319
Sinha AK, AbdElgawad H, Zinta G, Dasan AF, Rasoloniriana R, Asard H, Blust R, de Boeck G (2015) Nutritional status as the key modulator of antioxidant responses induced by high environmental ammonia and salinity stress in European sea bass (Dicentrarchus labrax). PLoS One 10(8):e0135091. https://doi.org/10.1371/journal.pone.0135091
Smart GR (1978) Investigations of the toxic mechanisms of ammonia to fish-gas exchange in rainbow trout (Salmo gairdneri) exposed to acutely lethal concentrations [J]. J Fish Biol 12(1):93–104. https://doi.org/10.1111/j.1095-8649.1978.tb04155.x
Thellin O, Zorzi W, Lakaye B, de Borman B, Coumans B, Hennen G, Grisar T, Igout A, Heinen E (1999) Housekeeping genes as internal standards: use and limits. J.Biotechnol. 75(2–3):291–295. https://doi.org/10.1016/S0168-1656(99)00163-7
Vedel NE, Korsgaard B, Jensen FB (1998) Isolated and combined exposure to ammonia and nitrite in rainbow trout (Oncorhynchus mykiss): Effects on electrolyte status, blood respiratory properties and brain glutamine/glutamate concentrations. Aquat Toxicol 41(4):325–342. https://doi.org/10.1016/s0166-445x(97)00071-4
Wang J, Li J, Xu N, Li J, Li Z, Chen Y, Yang Z (2015) Responses of Takifugu obscurus fertilized eggs and larvae to increased ammonia exposure. Environ Sci Pollut Res 44(4):15976–15984. https://doi.org/10.1007/s11356-015-4815-x
Wang SC, Zhang QJ et al (2019) Atrazine exposure triggers common carp neutrophil apoptosis via the CYP450s/ROS pathway. Fish and Shellfish Immunol 84:551–557. https://doi.org/10.1016/j.fsi.2018.10.029
Willima MF, Kazina SB (1997) Localization of superoxide dismutase activity in rat tissues. Free Radic Biol Med 22(1 /2):241–248. https://doi.org/10.1016/s0891-5849(96)00328-0
Xu P, Zhang XF, Wang XM et al (2014) Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nature Genetics, Genome sequence and genetic diversity of the common carp, Cyprinus carpio. Nat Genet 46(11):1212–1219. https://doi.org/10.1038/ng.30980
Yang HC, Chun SK (1986) Histopathological study of acute toxicity of ammonia on common carp, Cyprinus carpio. Bull Korean Fish Soc 19(3):249–256
Yuen KI, Chew SF (2010) Ammonia production, excretion, toxicity, and defense in fish: a review, Front. Physiol 1:134–139. https://doi.org/10.3389/fphys.2010.00134
Zhang Y, Ye C, Wang A, Zhu X, Chen C, Xian J, Sun Z (2015) Isolated and combined exposure to ammonia and nitrite in giant freshwater pawn (Macrobrachium rosenbergii): effects on the oxidative stress, antioxidant enzymatic activities and apoptosis in haemocytes. Ecotoxicology 24(7-8):1601–1610. https://doi.org/10.1007/s10646-015-1477-x
Zhang Z, Qi L, Cai J et al (2017) Chlorpyrifos exposure in common carp (Cyprinus carpio L.) leads to oxidative stress and immune responses. Fish Shellfish Immunol 67:604–611. https://doi.org/10.1016/j.fsi.2017.06.048
Zhang W, Sun S, Ge X, Xia S, Zhu J, Miao L, Lin Y, Liang H, Pan W, Su Y, Yu H (2018) Acute effects of ammonia exposure on the plasma and haematological parameters and histological structure of the juvenile blunt snout bream, Megalobrama amblycephala, and post-exposure recovery. Aquac Res 49:49(2)–41019. https://doi.org/10.1111/are.13548
Zhang TX, Yan ZG, Zheng X et al (2020) Effects of acute ammonia toxicity on oxidative stress, DNA damage and apoptosis in digestive gland and gill of Asian clam (Corbicula fluminea). Fish and Shellfish Immunol 99:514–525. https://doi.org/10.1016/j.fsi.2020.02.046
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This study was supported by the Ministry of Agriculture Finance Special Sub-project, Investigation of Fishery Resources and Environment in Key Waters of Northeast China, and the China Agriculture Research System (CARS-45-06).
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Shuqun Xue completed the experiment and wrote the manuscript. Jiawen Lin and Yue Han completed part of the experiment and data analysis. Ying Han provided ideas for the experiment.
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Xue, S., Lin, J., Han, Y. et al. Ammonia stress–induced apoptosis by p53–BAX/BCL-2 signal pathway in hepatopancreas of common carp (Cyprinus carpio). Aquacult Int 29, 1895–1907 (2021). https://doi.org/10.1007/s10499-021-00724-3
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DOI: https://doi.org/10.1007/s10499-021-00724-3