Abstract
The interaction between lysine (Lys) and arginine (Arg) in the proximal intestinal region of Pacific bluefin tuna (Thunnus orientalis) was evaluated using the everted intestine method. This in vitro intestinal system has been shown to be an effective tool for studying the nutrient absorption without the need to handle the tuna fish in marine cages as needed for digestibility and amino acid (AA) absorption. We used a factorial design with two sets of variables: low and high Lys concentration (10 and 75 mM) and four different Arg concentrations (3, 10, 20, and 30 mM). Both amino acids were dissolved in marine Ringer solution with a basal amino acidic composition consisting of a tryptone solution (9 mg mL−1). No interaction was observed between the absorption of Lys and Arg during the first 10 min of the experiment when low concentration of Lys and Arg was used in the hydrolyzate solution. However, there seemed to be a positive effect on Lys absorption when both amino acids were at high concentrations (30 and 75 mM, respectively). This type of studies will led us to test different formulations and/or additives to better understand the efficiency of AA supplementation as an alternative to in situ studies that are difficult to follow to design with the Pacific Bluefin Tuna.
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References
Aguado F, Martínez FJ, García-García B (2004) In vivo total nitrogen and total phosphorus digestibility in Atlantic bluefin tuna (Thunnus thynnus thynnus Linnaeus, 1758) under industrially intensive fattening conditions in Southeast Spain Mediterranean coastal waters. Aquac Nutr 10:413–419
Bai SC, Gatlin DM III (1994) Effect of l-lysine supplementation of diet with different protein levels and sources of channel catfish Ictalurus punctatus (Rafinesque). Aquac Fish Manage 25:465–474
Bakke-McKellep AM, Nordrum S, Krogdahl Å, Buddington RK (2000) Absorption of glucose, amino acids, and dipeptides by the intestines of Atlantic salmon (Salmo salar L.). Fish Physiol Biochem 22:33–44
Ball RO, Urschel KL, Pecharz PB (2007) Nutritional consequences of interspecies differences in arginine and lysine metabolism. J Nutr 137:1626S–1641S
Berge GE, Lied E, Sveier H (1997) Nutrition of Atlantic salmon (Salmo salar): the requirement and metabolism of arginine. Comp Biochem Physiol A 117:501–509
Berge GE, Sveier H, Lied E (1998) Nutrition of Atlantic salmon (Salmo salar): the requirement and metabolic effect of lysine. Comp Biochem Physiol A 120:477–485
Berge GE, Bakke-McKellep AM, Lied E (1999) In vitro uptake and interaction between arginine and lysine in the intestine of Atlantic salmon (Salmo salar). Aquaculture 179:181–193
Bogé G, Roche H, Balocco C (2002) Amino acid transport by intestinal brush border vesicles of a marine fish, Boops salpa. Comp Biochem Physiol B 131:19–26
Bröer S (2008) Amino acid transport across mammalian intestinal and renal epithelia. Physiol Rev 88:249–286
Buddington RK, Chen JW, Diamond JM (1987) Genetic and phenotypic adaptation of intestinal nutrient transport to diet in fish. J Physiol 392:261–281
Cheng ZJ, Hardy RW, Usry JL (2003) Effects of lysine supplementation in plant protein-based diets on the performance of rainbow trout (Oncorhynchus mykiss) and apparent digestibility coefficients of nutrients. Aquaculture 215:255–265
Cowey CB, Walton MJ (1988) Studies on the uptake of (14C) amino acids derived from both dietary (14C) protein and dietary (14C) amino acids by rainbow trout, Salmo gairdneri Richardson. J Fish Biol 33:293–305
Cynober L, Le Boucher J, Vasson MP (1995) Arginine metabolism in mammals. Nutr Biochem 6:402–413
Day OJ, Plascencia-González HG (2000) Soybean protein concentrate as a protein source for turbot Scophthalmus maximus L. Aquac Nutr 6:221–228
Griffin ME, Wilson KA, Brown PB (1994) Dietary arginine requirement of juvenile hybrid striped bass. J Nutr 124:888–893
Guillaume J, Kaushik S, Bergot P, Métailler R (2001) Nutrition and feeding of fish and crustaceans. Springer Praxis Books, Chichester
Hardy RW, Barrows FT (2002) Diet formulation and manufacture. In: Halver JE, Hardy RW (eds) Fish nutrition, 3rd edn. Academic Press, San Diego, pp 505–600
Kaushik SJ, Fauconneau B (1984) Effects of lysine administration on plasma arginine and on some nitrogenous catabolites in rainbow trout. Comp Biochem Physiol A 79:459–462
Maenz DD, Chenu C, Breton S, Berteloot A (1992) pH-dependent heterogeneity of acidic amino acid transport in rabbit jejunal brush border membrane vesicles. J Biol Chem 257(3):1510–1516
Maenz DD, Chenu C, Berteloot A (1993) Heterotrophic effects of dipolar amino acids on the activity of the anionic amino acids transport system X− AG in rabbit jejunal brush-border membrane vesicles. J Biol Chem 268(21):15361–15367
Mai K, Zhang L, Ai Q, Duan Q, Zhang C, Li H, Wan J, Liufu Z (2006) Dietary lysine requirement of juvenile Japanese seabass, Lateolabrax japonicas. Aquaculture 258:535–542
Mailliard ME, Stevens BR, Mann GE (1995) Amino acid transport by small intestinal, hepatic and pancreatic epithelia. Gastroenterology 108:888–910
Martínez-Montaño E, Peña E, Focken U, Viana MT (2010) Intestinal absorption of amino acids in the Pacific bluefin tuna (Thunnus orientalis): in vitro uptake of amino acids using hydrolyzed sardine muscle at three different concentrations. Aquaculture 299:134–139
Martínez-Montaño E, Peña E, Viana MT (2011) In vitro amino acid absorption using hydrolysed sardine muscle or soybean meal at different intestinal regions of the Pacific bluefin tuna (Thunnus orientalis). Aquac Nutr 17:789–797
Matthews JC (2000) Amino acids and peptide transport systems. In: D’Mello JPF (ed) Farm animal metabolism and nutrition. CAB International, Wallingford, pp 3–20
McNamara PD, Rea CT, Segal S (1986) Lysine uptake by rat renal brush-border membrane vesicles. Am J Physiol 251:F734–F742
Mourente G, Tocher DR (2009) Tuna nutrition and feeds: current status and future perspectives. Rev Fish Sci 17:373–390
Moyano FJ, Savoie L (2001) Comparison of in vitro systems of protein digestion using either mammal or fish proteolytic enzymes. Comp Biochem Physiol A 128:359–368
National Research Council (2011) Nutritional requirements of fish and shrimps. The National Academic Press, Washington, DC, p 376
Ottolenghi F (2008) Capture-based aquaculture of bluefin tuna. In: Lovatelli A, Holthus PF (eds) Capture-based aquaculture: global overview. FAO Fisheries Technical Paper No. 508, Rome, pp 169–182
Palavesam A, Beena S, Immanuel G (2008) Effect of l-lysine supplementation with different protein levels in diets on growth, body composition and protein metabolism in pearl spot Etroplus suratensis (Bloch). Turkish J Fish Aquat Sci 8:133–139
Rosas A, Vazquez-Duhalt R, Tinoco R, Shimada A, D’Abramo LR, Viana MT (2008) Comparative intestinal absorption of amino acids in rainbow trout (Oncorhynchus mykiss), totoaba (Totoaba macdonaldi) and Pacific bluefin tuna (Thunnus orientalis). Aquac Nutr 14:481–489
Steffansen B, Nielsen CU, Brodin B, Eriksson AH, Andersen R, Frokjaer S (2004) Intestinal solute carriers: an overview of trends and strategies for improving oral drug absorption. Eur J Pharm Sci 21:3–16
Takagi S, Shimeno S, Hosokawa H, Ukawa M (2001) Effect of lysine and methionine supplementation to a soy protein concentrate diet for red sea bream Pagrus major. Fish Sci 67:1088–1096
Tesser MB, Terjesen BF, Zhang Y, Portella MC, Dabrowski K (2005) Free- and peptide-based dietary arginine supplementation for the South American fish pacu (Piaractus mesopotamicus). Aquaculture Nutr 11:443–453
Tseng Y, Hwang P (2008) Some insights into energy metabolism for osmoregulation in fish. Comp Biochem Physiol C 148:419–429
Wu G (1998) Intestinal mucosal amino acid catabolism. J Nutr 128:1249–1252
Zertuche-González JA, Sosa-Nishizaki O, Vaca-Rodríguez JG, del Moral-Simanek R, Yarish C, Costa-Pierce BA (2008) Marine science assessment of capture-based tuna (Thunnus orientalis) Aquaculture in the Ensenada Region of Northern Baja California, México. Final report to the David & Lucile Packard Foundation, Los Altos, CA
Acknowledgments
This work was supported by project numbers SAGARPA/CONACyT 109150; CB-2009-01 and UABC 403/1/C/19/15. We thank Pacífico Aquaculture SA de CV for their kind donation of fish. Emmanuel Martínez-Montaño and Emyr Peña thank CONACyT for their graduate studies fellowships. We thank Nancy Boston for her English editorial work.
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Martínez-Montaño, E., Peña, E. & Viana, M.T. Intestinal absorption of amino acids in the Pacific bluefin tuna (Thunnus orientalis): in vitro lysine–arginine interaction using the everted intestine system. Fish Physiol Biochem 39, 325–334 (2013). https://doi.org/10.1007/s10695-012-9702-5
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DOI: https://doi.org/10.1007/s10695-012-9702-5