Effect of taurine precursor on growth and taurine content of rarine fish
Keywords:
Cysteine, Cysteamine, Cysteic acid, Soybean meal, Low fishmeal dietAbstract
Taurine is thought to be synthesized from methionine and cysteine by the cysteine sulfinic acid pathway in freshwater fish, but not in carnivorous marine fish. However, there are two biosynthetic pathways of taurine: cysteamine pathway and cysteic acid pathway. However, the synthesis via these two pathways has not been investigated by a feeding trial using these taurine precursors. We investigated possible taurine synthesis from these two pathways using freshwater fish (carp) and marine carnivorous fish such as red sea bream and Japanese flounder. As a result, it was found that taurine can be synthesized from the two pathways, and that cysteic acid has a higher potency of taurine accumulation than cysteamine. Also, there is a risk of occurrence of malformations in fish when fed excessive cysteamine in diet. Considering risk of having malformation in fish fed cysteamine, cysteic acid is a better choice as taurine precursor. We also examined effect of taurine supplementation to non-fishmeal diet on distal intestine of juvenile red sea bream. We observed that plant protein-based non-fishmeal diet caused lower growth, pathological changes of the intestine with high expression of cytokine genes of red sea bream but these changes can be ameliorated by taurine. This improvement was observed by 1-2% taurine which is beyond the requirement for red seabream estimated by growth study, suggesting that taurine supplementation is beneficial for fish fed plant-based diet in terms of ameliorating intestinal defects as well as preventing green liver syndrome in marine carnivorous fish. This paper also discusses possible inclusion of cysteamine and cysteic acid in feedstuffs, the possible mechanisms of amelioration of plant ingredient-induced intestinal damage by taurine, the response of taurine synthesizing enzyme gene expression to sulfur amino acid in fish, and new taurine source candidates for aquafeed.
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Asano K, Suzuki T, Saito A, Wei F-Y, Ikeuchi Y, Numata T, Tanaka R, Yamane Y, Yamamoto T, Goto T, Kishita Y, Murayama K, Ohtake A, Okazaki Y, Tomizawa T, Sakaguchi Y, Suzuki S. 2018. Metabolic and chemical regulation of tRNA modification associated with taurine deficiency and human disease. Nucleic Acids Research 46, 1565–1583, https://doi.org/10.1093/nar/gky068
Baeverfjord G, Krogdahl Å. 1996. Development and regression of soybean meal induced enteritis in Atlantic salmon, Salmo salar L., distal intestine: a comparison with the intestines of fasted fish. Journal of the Fish Diseases 19, 375-387.
Bakke-McKellep CM, Baeverfjord PG, Krogdahl Å, Landsverk T. 2000. Changes in immune and enzyme histochemical phenotypes of cells in the intestinal mucosa of Atlantic salmon, Salmo salar L., with soybean meal-induced enteritis. Journal of the Fish Diseases 23, 115-127.
Divakaran S, Ramanathan S, Ostrowski AC. 1992. Endogenous production of taurine in two teleost fsh: Coryphaena hippurus and red hybrid tilapia. Comparative Biochemistry and Physiology 101B, 321–322.
Dominy JE, Simmons CR, Hirschberger LH, Hwang J, Coloso RM, Stipanuk MH. 2007. Discovery and characterization of a second mammalian thiol dioxygenase, cysteamine dioxygenase. Journal of the Biological Chemistry 282, 25189-25198.
Edgar SE, Hickman MA, Marsden MM, Morris JG, Rogers QR 1994. Dietary cysteic acid serves as a precursor of taurine for cats. Journal of Nutrition 124, 103–109.
Edgar SE, Kirk CA, Rogers QR, Morris JG. 1998. Taurine status in cats is not maintained by dietary cysteinesulfnic acid. Journal of Nutrition 128, 751–757.
El-Mostafa K, El Kharrassi Y, Badreddine A, Andreoletti P, Vamecq J, El Kebbaj MS, Latruffe N, Lizard G, Nasser B, Cherkaoui-Malki M. 2014. Nopal cactus (Opuntia ficus-indica) as a source of bioactive compounds for nutrition, health and disease. Molecules 19, 14879-14901.
Fan Z, Hu J, Jiang R, Yang X, Jin X. 2018. Evaluation of cysteine dioxygenase activity in marine organisms by high performance liquid chromatography. Food Science 39, 174-178 (in Chinese with English abstract).
Gonzales MMG. 2018. Basic studies on taurine synthesizing ability and its synthetic pathways in Japanese flounder Paralichthys olivaceus and common carp Cyprinus carpio. Ph D thesis, Tokyo University of Marine Science and Technology.
Gonzales-Plasus MM, Kondo H, Hirono I, Satoh S, Haga Y. 2019. Cysteamine dioxygenase as enzymes for taurine synthesis and the negative effect of high dietary cysteamine on growth and body shape of the common carp, Cyprinus carpio. Aquaculture Science 67, 95-108.
Goto T, Matsumoto T, Murakami S, Takagi S, Hasumi F. 2003. Conversion of cysteate into taurine in liver of fsh. Fisheries Science 69, 216–218.
Goto T, Mochizuki A, Hasumi F. 2002. Distribution and activities of enzymes involved in taurine biosynthesis in liver of fsh. Aquaculture Science 50, 443–449.
Goto T, Ooya K, Yamamoto S, Onoda K, Kobayashi T, Imai K. 2021. Characterization of cysteine dioxygenase in the liver of bluegill Lepois macrochirus for the determination of enzyme activity. Aquaculture Science 69, 299-305.
Haga Y, Kondo H, Kumagai A, Satoh N, Hirono I, Satoh S .2015. Isolation, molecular characterization of cysteine sulfnic acid decarboxylase (CSD) of red sea bream Pagrus major and yellowtail Seriola quinqueradiata and expression analysis of CSD from several marine fsh species. Aquaculture 449, 8–17.
Horibe, T., Sumi, H., Teranobu, R. 2020. Zinc biofortification of the edible cactus nopalea cochenillifera grown under hydroponic conditions. Environmental Control in Biology 58, 43-47.
Huxtable RJ .1992. Physiological actions of taurine. Physiological Review 72. 101–163.
Huynh PTN, Nguyen PH, Nguyen MA. 2018. Determination of cysteamine in animal feeds by high performance liquid chromatography with diode-array detection. Science & Technology Development Journal, 21, 37-43.
Ito T, Cho JH, Nakamura K, Masuda R, Haga Y, Satoh S .2019. Sulfur amino acid metabolism and growth of juvenile red sea bream. Japanese Journal of Taurine Research 5, 32–33 (in Japanese).
Itoh T, Haga Y, Kurihara A, Kondo H, Hirono I, Satoh S. Effects of intraperitoneal injection of sulfur compounds on taurine synthesis in juvenile red sea bream (Pagrus major). International Symposium on Fish Nutrition and Feeding 2018, Las Palmas, Spain.
Jacobsen JG, Smith LH .1968. Biochemistry and physiology of taurine and taurine derivatives. Physiological Review 48, 424–511.
Kawasaki A, Ono A, Mizuta S, Kamiya M, Takenaga T, Murakami S. 2017. The taurine content of Japanese seaweed. Advances in Experimental Medicine and Biology 975, 1105-1112.
Latshaw JD. 1990. Quality of feather meal as affected by feather processing conditions. Poultry Science 69, 953-958.
Li F, Haga Y, Kondo H, Hirono I, Satoh S. 2019. Effect of graded levels of taurine supplementation to non fishmeal diet on growth, nutrient digestibility, intestinal morphology and cytokine gene expression of juvenile red seabream Pagrus major. Aquaculture Science 67, 333-346. https://doi.org/10.11233/aquaculturesci.65.239
Li L, Liu H-Y, Xie S-Q, Zhang P-Y, Yang Z-C. 2022. Effects of taurine supplementation on growth performance and feed utilization in aquatic animals: A meta-analysis. Aquaculture 551, 737896, https://doi.org/10.1016/j.aquaculture.2022.737896.
Li P, Wu, G. 2020. Composition of amino acids and related nitrogenous nutrients in feedstufs for animal diets. Amino Acids 52, 523–542, https://doi.org/10.1007/s00726-020-02833-4
Lozano I, Wacyk JM, Carrasco J, Cortez-San Martín MA. 2016. Red macroalgae Pyropia columbina and Gracilaria chilensis: sustainable feed additive in the Salmo salar diet and the evaluation of potential antiviral activity against infectious salmon anemia virus. Journal of the Applied Phycology 28, 1343–1351. https://doi.org/10.1007/s10811-015-0648-8
Matsumoto T, Akita M, Ogawa M, Goto T. 2021. Evaluation f taurine biosynthesis in the livers of the spear squid Heteroloigo bleekeri and the swodtip squid Uroteuthis edulis. Fisheries Science 87, 717-725.
Matsunari H, Furuita H, Yamamoto T, Kim S-K, Sakakura Y, Takeuchi T. 2008. Effect of dietary taurine and cystine on growth performance of juvenile red sea bream Pagrus major. Aquaculture 274, 142-147.
Nakamura K, Gozanles-Plasus MM, Itoh T, Masuda R, Haga Y, Satoh S. 2019. Growth and amino acid content in Japanese flounder ingested cysteamine. Japanese Journa of Taurine Research 5, 34-35.
Nakamura K, Gozanles-Plasus MM, Ushigusa-Itoh T, Masuda R, Kabeya N, Kondo H, Hirono I, Satoh S, Haga Y. 2021. Taurine synthesis via the cysteic acid pathway: efect of dietary cysteic acid on growth, body taurine content, and gene expression of taurine‑synthesizing enzymes, growth hormone, and insulin‑like growth factor 1 in Japanese founder Paralichthys olivaceus. Fisheries Science 87, 353–363, https://doi.org/10.1007/s12562-021-01500-1
Poppi DA, Moore SS, Wade NM, Glencross BD. 2019. Postprandial plasma free amino acid profile and hepatic gene expression in juvenile barramundi (Lates calcarifer) is more responsive to feed consumption than to dietary methionine inclusion. Aquaculture 501, 345-358. doi: 10.1016/j.aquaculture.2018.11.044
Poppi DA, Moore SS, Wade NM, Glencross BD. 2020.Adequate supply of dietary taurine stimulates expression of molecular markers of growth and protein turnover in juvenile barramundi (Lates calcarifer). Fish Physiology and Biochemistry 46, 953-969. doi: 10.1007/s10695-020-00762-3
Salze GP, Davis DA. 2015. Taurine: a critical nutrient for future fsh feeds. Aquaculture 437, 215–229.
Shen GP, Ding ZN, Dai T, Feng JH, Dong JY, Xia F, Xu JJ, Ye JD. 2021. Effect of dietary taurine supplementation on metabolome variation in plasma of Nile tilapia. Animal 15, 100167, https://doi.org/10.1016/j.animal.2020.100167.
Stacy A, Andrade-Oliveira V, McCulloch JA, Hild B, Oh J-H, Perez-Chaparro PJ, Sim CK, Lim AI, Link VM, Enamorado M, Trinchieri G, Segre JA, Rehermann B, Belkaid Y. 2021. Infection trains the host for microbiota-enhanced resistance to pathogens. Cell 184, 1-13.
Takeuchi T. 2014. Progress on larval and juvenile nutrition to improve the quality and health of seawater fish: a review. Fisheries Science 80, 389–403.
Tochino M, Nagano T, Satoh S, Shiratori M, Ueta Y. 2009. Effect of taurine supplement to low fish meal feed on yellowtail Seriola quinqueradiata in a practical net cage. Aquaculture Science 57, 595-600.
Tozawa H, Kawabata T. 1987. Mechanism of N-nitrosothiazolidine formation at the stage of fish meal preparation. Nippon Suisan Gakkaishi 53, 2209-2216.
Wang Q, He G, Wang X, Mai K, Xu W, Zhou H. 2014. Dietary sulfur amino acid modulations of taurine biosynthesis in juvenile turbot (Psetta maxima). Aquaculture 422–423, 141–145. https://doi.org/10.1016/j.aquaculture.2013.12.014
Wang X, He G, Mai K, Xu W, Zhou H. 2016. Differential regulation of taurine biosynthesis in rainbow trout and Japanese founder. Scientific Reports 6:article no. 21231
Watanabe T, Aoki H, Shimamoto K, Hadzuma M, Maita M, Yamagata Y, Kiron V, Satoh S. 1998. A trial to culture yellowtail with nonfshmeal diets. Fisheries Science 64, 505–512.
Watanabe T, Verakunpiriya V, Watanabe K, Kiron V, Satoh S. 1997. Feeding of rainbow trout with non-fish meal diets. 1997. Fisheries Science 63, 258-266.
Wei Y, Zhang Q, Xu H, Liang MQ (2020). Taurine requirement and metabolism response of tiger puffer Takifugu rubripes to graded taurine supplementation. Aquaculture 524, p.735237.
Wolber FM, McGrath M, Jackson F, Wylie K, Broomfeld A. 2016. Cysteic acid in dietary keratin is metabolized to glutathione and liver taurine in a rat model of human digestion. Nutrients 8, 104. https://doi.org/10.3390/nu8020104
Yang M-J, Xu D, Yang D-X, Li L, Peng X-X, Chen Z-G, Li H. 2020. Malate enhances survival of zebrafish against Vibrio alginolyticus infection in the same manner as taurine. Virulence 11, 349-364.
Yokoyama M, Takeuchi T, Park G-S, Nakazoe J. 2001. Hepatic cysteinesulphinate decarboxylase activity in fsh. Aquaculture Reserach 32, 216–222.
Zhang Q-W, Xu H-P, Mao L-S, Jin H-X. 2019. Evaluation of cysteine sulfinate decarboxylase activity in marine life by high performance liquid chromatography. Journal of the Anhui Agricultural Science 47, 212-215. (in Chinese with English abstract).
