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Dietary arginine affects growth, gut morphology, oxidation resistance and immunity of hybrid grouper (Epinephelus fuscoguttatus♀×Epinephelus lanceolatus♂) juveniles

  • Mingjuan Wu (a1) (a2) (a3), Xiaoyi Wu (a1) (a2) (a3), Senda Lu (a1) (a2) (a3), Yujie Gao (a1) (a2) (a3), Wei Yao (a1) (a2) (a3), Xiaojun Li (a1) (a2) (a3), Yu Dong (a1) (a2) (a3) and Zibo Jin (a1) (a2) (a3)...

Abstract

An 8-week growth trial was conducted to evaluate the effects of dietary arginine (Arg) levels on growth, gut morphology, oxidation resistance and immunity of hybrid grouper (Epinephelus fuscoguttatus×Epinephelus lanceolatus♂) juveniles. Seven isoenergetic (1465 kJ (350 kcal)/100-g DM), isoproteic (53·5 % of DM) and isolipidic (7 % of DM) experimental diets were formulated to contain graded Arg levels ranging from 1·9 to 4·7 % (dry weight) at approximately 0·5 % increments. Each diet was randomly assigned to triplicate groups of 16 juvenile fish (average initial body weight: 11·7 (sd 0·1) g) and was administered twice daily (08.00 and 16.00 hours). After the growth trial, all remaining fish were fed their prescribed diets for 2 d and then exposed to 4·5 mg Cu2+/l water for 36 h. Results showed that growth performance and feed utilisation of experimental fish were significantly affected by different dietary Arg levels. Weight gain % (WG%) of fish was increased as dietary Arg increased, reaching a peak value at 3·8 % dietary Arg level, and when dietary Arg level increased to 4·7 % WG% was reduced. Fish fed 1·9 and 2·2 % dietary Arg levels had higher daily feed intake compared with fish fed other dietary Arg levels. Feed conversion ratios in fish fed 1·9, 2·2, 2·7 and 4·7 % dietary Arg levels were higher than those in fish fed 3·1, 3·8 and 4·1 % dietary Arg levels. Protein efficiency ratio and protein productive value (PPV) increased with an increase in dietary Arg, up to a peak value at 3·8 % dietary Arg level, above which these parameters declined. On the basis of quadratic regression analysis of weight gain % (WG%) or PPV against dietary Arg levels, the optimal dietary Arg requirement for hybrid grouper was estimated to be 3·65 %. Fish fed 3·8 % dietary Arg had higher whole-body and muscle protein contents compared with fish fed other dietary Arg levels. Fish fed 3·8 and 4·1 % dietary Arg levels had higher levels of mRNA for insulin-like growth factor-I and target of rapamycin in the liver compared with fish fed other dietary Arg levels. Hepatic S6 kinase 1 mRNA expression in fish fed 3·8 % dietary Arg level was higher than that in fish fed any of the other dietary Arg levels. Gut morphology, hepatic antioxidant indices and immune indices in serum and head kidney were significantly influenced by dietary Arg levels. In conclusion, the optimal dietary Arg requirement for hybrid grouper was estimated to be 3·65 %, and suitable dietary Arg supplementations improved gut morphology and oxidation resistance of hybrid grouper.

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* Corresponding author: X. Wu, email wjurk@163.com

References

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1.National Research Council (2011) Nutrient Requirement of Fish. Washington, DC: National Academies Press.
2.Cheng, ZY, Buentello, A & Gatlin, DM III (2011) Effects of dietary arginine and glutamine on growth performance, immune responses and intestinal structure of red drum, Sciaenops ocellatus. Aquaculture 319, 247252.
3. Cheng, ZY, Gatlin, DM III & Buentello, A (2012) Dietary supplementation of arginine and/or glutamine influences growth performance, immune responses and intestinal morphology of hybrid striped bass (Morone chrysops×Morone saxatilis). Aquaculture 362-363, 3943.
4.Pohlenz, C, Buentello, A, Mwangi, W, et al. (2012) Arginine and glutamine supplementation to culture media improves the performance of various channel catfish immune cells. Fish Shellfish Immunol 32, 762768.
5.Zhou, QC, Jin, M, Elmada, Z C, et al. (2015) Growth, immune response and resistance to Aeromonas hydrophila of juvenile yellow catfish, Pelteobagrus fulvidraco, fed diets with different arginine levels. Aquaculture 437, 8491.
6.Buentello, JA & Gatlin, DM III (2000) The dietary arginine requirement of channel catfish (Ictalurus punctatus) is influenced by endogenous synthesis of arginine from glutamic acid. Aquaculture 188, 311321.
7.Alam, MS, Teshima, S, Koshio, S, et al. (2002) Arginine requirement of juvenile Japanese flounder Paralichthys olivaceus estimated by growth and biochemical parameters. Aquaculture 205, 127140.
8.Luo, Z, Liu, Y, Mai, KS, et al. (2007) Effects of dietary arginine levels on growth performance and body composition of juvenile grouper Epinephelus coioides . J Appl Ichthyol 23, 252257.
9.Singh, S & Khan, MA (2007) Dietary arginine requirement of fingerling hybrid Clarias (Clarias gariepinus×Clarias macrocephalus). Aquacult Res 38, 1725.
10.Zhou, F, Xiong, W, Xiao, JX, et al. (2010) Optimum arginine requirement of juvenile black sea bream, Sparus macrocephalus . Aquacult Res 41, e418e430.
11.Zhou, QC, Zeng, WP, Wang, HL, et al. (2012) Dietary arginine requirement of juvenile yellow grouper Epinephelus awoara . Aquaculture 350–353, 175182.
12.Ren, M, Ai, Q & Mai, K (2014) Dietary arginine requirement of juvenile cobia (Rachycentron canadum). Aquacult Res 45, 225233.
13.Yue, Y, Zou, Z, Zhu, J, et al. (2013) ) Effects of dietary arginine on growth performance, feed utilization, haematological parameters and non-specific immune responses of juvenile Nile tilapia (Oreochromis niloticus L.). Aquacult Res 46, 18011809.
14.Ren, M, Liao, Y, Xie, J, et al. (2013) Dietary arginine requirement of juvenile blunt snout bream, Megalobrama amblycephala . Aquaculture 414-415, 229234.
15.Tu, YQ, Xie, SQ, Han, D, et al. (2015) Dietary arginine requirement for gibel carp (Carassis auratus gibelio var. CAS III) reduces with fish size from 50 g to 150 g associated with modulation of genes involved in TOR signaling pathway. Aquaculture 449, 3747.
16.Liang, HL, Ren, MC, Habte-Tsion, HM, et al. (2016) Dietary arginine affects growth performance, plasma amino acid contents and gene expressions of the TOR signaling pathway in juvenile blunt snout bream, Megalobrama amblycephala . Aquaculture 461, 18.
17.Anthony, TG, Reiter, AK, Anthony, JC, et al. (2001) Deficiency of dietary EAA preferentially inhibits mRNA translation of ribosomal proteins in liver of meal-fed rats. Am J Physiol Endocrinol Metab 281, E430E439.
18.Holz, MK, Ballif, BA, Gygi, SP, et al. (2005) mTOR and S6K1 mediate assembly of the translation preinitiation complex through dynamic protein interchange and ordered phosphorylation events. Cell 123, 569580.
19.Kong, XF, Bie Tan, B, Yin, YL, et al. (2012) L-Arginine stimulates the mTOR signaling pathway and protein synthesis in porcine trophectoderm cells. J Nutr Biochem 23, 11781183.
20.Corl, BA, Odle, J, Niu, X, et al. (2008) Arginine activates intestinal p70(S6k) and protein synthesis in piglet rotavirus enteritis. J Nutr 138, 2429.
21.Chen, GF, Feng, L, Kuang, SY, et al. (2012) Effect of dietary arginine on growth, intestinal enzyme activities and gene expression in muscle, hepatopancreas and intestine of juvenile Jian carp (Cyprinus carpio var. Jian). Br J Nutr 108, 195207.
22.Chen, N, Jin, L, Zhou, H, et al. (2012) Effects of dietary arginine levels and carbohydrate-to-lipid ratios on mRNA expression of growth-related hormones in largemouth bass, Micropterus salmoides . Gen Comp Endocrinol 179, 121127.
23.Efstratiadis, A (1998) Genetics of mouse growth. Int J Dev Biol 42, 955976.
24.Nakae, J, Kido, Y & Accili, D (2001) Distinct and overlapping functions of insulin and IGF-I receptors. Endocr Rev 22, 818835.
25.Newsholme, P, Brennnan, L, Rubi, B, et al. (2005) New insights into amino acid metabolism, beta-cell function and diabetes. Clin Sci 108, 185194.
26.Tan, B, Yin, Y, Liu, Z, et al. (2009) Dietary L-arginine supplementation increases muscle gain and reduces body fat mass in growing-finishing pigs. Amino Acids 37, 169175.
27.Plisetskaya, EM, Buchelli-Narvaez, LI, Hardy, RW, et al. (1991) Effects of injected and dietary arginine on plasma insulin levels and growth of Pacific salmon and rainbow trout. Comp Biochem Physiol A 98, 165170.
28.Mommsen, TP, Moon, TW & Plisetskaya, EM (2001) Effects of arginine on pancreatic hormones 2 hepatic metabolism in rainbow trout. Physiol Biochem Zool 74, 668678.
29.Andoh, T (2007) Amino acids are more important insulinotropins than glucose in a teleost fish, barfin flounder (Verasper moseri). Gen Comp Endocrinol 151, 308317.
30.Uni, Z & Ferket, P (2003) Enhancement of development of oviparous species by in ovo feeding. US Regular Patent US 6,592,878 B2, Washington, DC.
31.Rhoads, JM, Chen, W, Gookin, J, et al. (2004) Arginine stimulates intestinal cell migration through a focal adhesion kinase dependent mechanism. Gut 53, 514522.
32.Li, P, Yin, YL, Li, D, et al. (2007) Amino acids and immune function. Br J Nutr 98, 237252.
33.Choi, BS, Martinez-Falero, IC, Corset, C, et al. (2009) Differential impact of l-arginine deprivation on the activation and effector functions of T cells and macrophages. J Leuk Biol 85, 268277.
34.Pohlenz, C, Buentello, A, Criscitiello, MF, et al. (2012) Synergies between vaccination and dietary arginine and glutamine supplementation improve the immune response of channel catfish against Edwardsiella ictaluri . Fish Shellfish Immunol 33, 543551.
35.Abdukalykova, S & Ruiz-Feria, CA (2006) Arginine and vitamin E improve the cellular and humoral immune response of broiler chickens. Inter J Poul Sci 5, 121127.
36.Tayade, C, Jaiswal, TN, Mishra, SC, et al. (2006) L-arginine stimulates immune response in chickens immunized with intermediate plus strain of infectious bursal disease vaccine. Vaccine 24, 552560.
37.Abdukalykova, ST, Zhao, X & Ruiz-Feria, CA (2008) Arginine and vitamin E modulate the subpopulations of T lymphocytes in broiler chickens. Poult Sci 87, 5055.
38.Ruiz-Feria, CA & Abdukalykova, ST (2009) Arginine and vitamin E improve the antibody responses to infectious bursal disease virus (IBDV) and sheep red blood cells in broiler chickens. Br Poult Sci 50, 291297.
39.Jiang, ST, Wu, XY, Li, WF, et al. (2015) Effects of dietary protein and lipid levels on growth, feed utilization, body and plasma biochemical compositions of hybrid grouper (Epinephelus lanceolatus♂×Epinephelus fuscoguttatus♀) juveniles. Aquaculture 446, 148155.
40.Jiang, ST, Wu, XY, Luo, Y, et al. (2016) Optimal dietary protein level and protein to energy ratio for hybrid grouper (Epinephelus fuscoguttatus♀×Epinephelus lanceolatus♂) juveniles. Aquaculture 465, 2836.
41.Wu, MJ, Lu, SD, Wu, XY, et al. (2017) Effects of dietary amino acid patterns on growth, feed utilization and hepatic IGF-I, TOR gene expression levels of hybrid grouper (Epinephelus fuscoguttatus♀×Epinephelus lanceolatus♂) juveniles. Aquaculture 468, 508514.
42.Lin, XY & Shiau, SY (2003) Dietary lipid requirement of grouper, Epinephelus malabaricus, and effects on immune responses. Aquaculture 225, 243250.
43.Lee, DJ & Putnam, GB (1973) The response of rainbow trout to varying protein/energy ratios in a test diet. J Nutr 103, 916922.
44.Garling, DL Jr & Wilson, RP (1977) Effects of dietary carbohydrate-to-lipid ratios on growth and body composition of fingerling channel catfish. Progr Fish Cult 39, 4347.
45.Association of Official Analytical Chemists (1990) Official Methods of Analysis. Arlington, VA: AOAC.
46.Unnikrishnan, U & Paulraj, R (2010) Dietary protein requirement of giant mud crab Scylla serrata juveniles fed iso-energetic formulated diets having graded protein levels. Aquacult Res 41, 278294.
47.Yao, CL, Kong, P, Wang, ZY, et al. (2009) Molecular cloning and expression of MyD88 in large yellow croaker, Pseudosciaena crocea . Fish Shellfish Immunol 26, 249255.
48.Davis, MJ (2010) Contrast coding in multiple regression analysis: strengths, weaknesses, and utility of popular coding structures. J Data Sci 8, 6173.
49.Kvalseth, TO (1985) Cautionary note about R2 . Am Stat 39, 279285.
50.Ngamsnae, P, De Silva, SS & Gunasekera, RM (1999) Arginine and phenylalanine requirement of juvenile silver perch Bidyanus bidyanus and validation of the use of body amino acid composition for estimating individual amino acid requirements. Aquacult Nutr 5, 173180.
51.Zehra, S & Khan, MA (2013) Dietary arginine requirement of fingerling Indian major carp, Catla catla (Hamilton). J World Aquac Soc 44, 363373.
52.Abidi, SF & Khan, MA (2009) Dietary arginine requirement of fingerling Indian major carp, Labeo rohita (Hamilton) based on growth, nutrient retention efficiencies, RNA/DNA ratio and body composition. J Appl Ichthyol 25, 707714.
53.Luzzana, U, Hardy, RW & Halver, JE (1998) Dietary arginine requirement of fingerling coho salmon (Oncorhynchus kisutch). Aquaculture 163, 137150.
54.Wilson, RP (2002) Amino acids and proteins. In Fish Nutrition, 3rd ed. pp. 144175 [JE Halver and RW Hardy, editors]. San Diego, CA: Academic Press Inc.
55.Fournier, V, Gouillou-Coustans, MF, Metailler, R, et al. (2003) Excess dietary arginine affects urea excretion but does not improve N utilisation in rainbow trout Oncorhynchus mykiss and turbot Psetta maxima . Aquaculture 217, 559576.
56.Ahmed, I & Khan, MA (2004) Dietary arginine requirement of fingerling Indian major carp, Cirrhinus mrigala (Hamilton). Aquacult Nutr 10, 217225.
57.Wan, J, Mai, KS & Ai, QH (2006) The recent advance on arginine nutritional physiology in fish. J Fish Sci 13, 679685.
58.Baoñs, N, Planas, JV, Gutierrez, J, et al. (1999) Regulation of plasma insulin-like growth factor-I levels in brown trout (Salmo trutta). Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 124, 3340.
59.Ballantyne, JS (2001) Amino acid metabolism. In Nitrogen Excretion, pp. 77107 [PA Wright and AJ Anderson, editors]. San Diego, CA: Academic Press.
60.Kim, K, McMillan, I & Bayley, HS (1983) Determination of amino acid requirements of young pigs using an indicator amino acid. Br J Nutr 50, 369382.
61.Fauconneau, B, Basseres, A & Kaushik, SJ (1992) Oxidation of phenylalanine and threonine in response to dietary arginine supply in rainbow trout (Salmo gairdneri R.). Comp Biochem Physiol A 101, 395401.
62.Klurfeld, DM (1999) Nutritional regulation of gastrointestinal growth. Front Biosci 4, 299302.
63.Hebiguchi, T, Kato, T, Yoshino, H, et al. (1997) The effect of arginine supplementation on growth hormone release and intestinal mucosal growth after massive small bowel resection in growing rats. J Pediatr Surg 32, 11491153.
64.Gurbuz, AT, Kunzelman, J & Ratzer, EE (1998) Supplemental dietary arginine accelerates intestinal mucosal regeneration and enhances bacterial clearance following radiation enteritis in rats. J Surg Res 74, 149154.
65.Liu, Y, Huang, J, Hou, Y, et al. (2008) Dietary arginine supplementation alleviates intestinal mucosal disruption induced by Escherichia coli lipopolysaccharide in weaned pigs. Br J Nutr 100, 552560.
66.Sveier, H, Raae, AJ & Lied, E (2000) Growth and protein turnover in Atlantic salmon (Salmo salar L.): the effect of dietary protein level and protein particle size. Aquaculture 185, 101120.
67.Hidetoshiban, KS, Yamatsuji, T, Gunduz, M, et al. (2004) Arginine and leucine regulate p70S6kinase and 4E-BP1 in intestinal epithelial cells. Int J Mol Med 13, 537543.
68.Wilson, RP & Poe, WE (1985) Relationship of whole body and egg essential amino acid patterns to amino acid requirement patterns in channel catfish, Ichalurus punctatus . Comp Biochem Physiol B 80, 385388.
69.Mambrini, M & Kaushik, SJ (1995) Indispensable amino acid requirements of fish: correspondence between quantitative data and amino acid profiles of tissue proteins. J Appl Ichthyol 11, 240247.
70.Cara, JB, Moyano, FJ, Zambonino, JL, et al. (2007) The whole amino acid profile as indicator of the nutritional condition in cultured marine fish larvae. Aquacult Nutr 13, 94103.
71.Wang, B, Liu, Y, Feng, L, et al. (2015) Effects of dietary arginine supplementation on growth performance, flesh quality, muscle antioxidant capacity and antioxidant-related signalling molecule expression in young grass carp (Ctenopharyngodon idella). Food Chem 167, 9199.
72.Wang, B, Feng, L, Jiang, WD, et al. (2015) Copper-induced tight junction mRNA expression changes, apoptosisand antioxidant responses via NF-ƙB, TOR and Nrf2 signaling molecules in the gills of fish: preventive role of arginine. Aquat Toxicol 158, 125137.
73.Dasgupta, T, Hebbel, RP & Kaul, DK (2006) Protective effect of arginine on oxidative stress in transgenic sickle mouse models. Free Radic Biol Med 41, 17711780.
74.Shan, LL, Wang, B, Gao, GZ, et al. (2013) L-Arginine supplementation improves antioxidant defenses through L-arginine/nitric oxide pathways in exercised rats. J Appl Physiol 115, 11461155.
75.Wallner, S, Hermetter, A, Mayer, B, et al. (2001) The alpha-amino group of L-arginine mediates its antioxidant effect. Eur J Clin Invest 31, 98102.
76.Lin, HZ, Tan, XH, Zhou, CP, et al. (2015) Effect of dietary arginine levels on the growth performance, feed utilization, non-specific immune response and disease resistance of juvenile golden pompano Trachinotus ovatus . Aquaculture 437, 382389.
77.Costas, B, Conceição, LEC, Dias, J, et al. (2011) Dietary arginine and repeated handling increase disease resistance and modulate innate immune mechanisms of Senegalese sole (Solea senegalensis Kaup, 1858). Fish Shellfish Immunol 31, 838847.
78.Chen, GF, Liu, Y, Jiang, J, et al. (2015) Effect of dietary arginine on the immune response and gene expression in head kidney and spleen following infection of Jian carp with Aeromonas hydrophila . Fish Shellfish Immunol 44, 195202.

Keywords

Dietary arginine affects growth, gut morphology, oxidation resistance and immunity of hybrid grouper (Epinephelus fuscoguttatus♀×Epinephelus lanceolatus♂) juveniles

  • Mingjuan Wu (a1) (a2) (a3), Xiaoyi Wu (a1) (a2) (a3), Senda Lu (a1) (a2) (a3), Yujie Gao (a1) (a2) (a3), Wei Yao (a1) (a2) (a3), Xiaojun Li (a1) (a2) (a3), Yu Dong (a1) (a2) (a3) and Zibo Jin (a1) (a2) (a3)...

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