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Lysine and methionine supplementation ameliorates high inclusion of soybean meal inducing intestinal oxidative injury and digestive and antioxidant capacity decrease of yellow catfish

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Abstract

The yellow catfish Pelteobagrus fulvidraco with initial average weight 16.6 ± 0.17 g were fed three extruded diets for 56 days. Fish meal (FM) diet was formulated as the normal control with 380 g FM and 200 g soybean meal (SBM) kg−1 diet. The SBM diet was prepared with 220 g FM and 360 g SBM kg−1 diet without Lys or Met supplementation. The SBM supplement (SBMS) diet was similar to SBM diet and supplemented with Lys and Met to ensure their levels similar to FM diet. The results showed fish fed SBM diet had lower percent weight gain and specific growth rate than the other two groups (P < 0.05). Whole body protein content of fish fed FM and SBMS diets were higher than that of fish fed SBM diet (P < 0.05). The hepatosomatic and intestosomatic indexes of fish fed SBM diet were significantly lower than that of fish fed FM and SBMS diets (P < 0.05). The activities of pepsin in stomach, trypsin, and chymotrypsin in intestine, alkaline phosphatase and creatine kinase in proximal intestine, Na+, K+-ATPase, and gamma-glutamyl transpeptidase in distal intestine were significantly higher in fish fed FM and SBMS diets compared to SBM diet. The activities of catalase, glutathione-S-transferase, reduced glutathione, superoxide anion scavenging, and hydroxyl radical scavenging in the intestine showed the same changes (P < 0.05). Malondialdehyde and protein carbonyl contents in intestine were significantly decreased in fish fed SBMS diet compared to SBM diet. These results indicated high inclusion of SBM induced intestinal oxidative injury and digestive and antioxidant capacity decrease. The Lys and Met supplementation could ameliorate these adverse effects on yellow catfish.

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References

  • Aebi H (1984) [13] Catalase in vitro. In: Methods in Enzymology (Packer L ed.), Vol. 105 Academic Press, New York, pp 121–126

  • Alam MS, Watanabe WO, Sullivan KB, Rezek TC, Seaton PJ (2012) Replacement of menhaden fish meal protein by solvent-extracted soybean meal protein in the diet of juvenile black sea bass supplemented with or without squid meal, krill meal, methionine, and lysine. N Am J Aquacult 74:251–265

    Article  Google Scholar 

  • Armenteros M, Heinonen M, Ollilainen V, Toldra F, Estevez M (2009) Analysis of protein carbonyls in meat products by using the DNPH-method, fluorescence spectroscopy and liquid chromatography-electrospray ionisation-mass spectrometry (LC-ESI-MS). Meat Sci 83:104–112

    Article  CAS  PubMed  Google Scholar 

  • Banuelos-Vargas I, Lopez LM, Perez-Jimenez A, Peres H (2014) Effect of fishmeal replacement by soy protein concentrate with taurine supplementation on hepatic intermediary metabolism and antioxidant status of totoaba juveniles (Totoaba macdonaldi). Comp Biochem Phys B 170:18–25

    Article  CAS  Google Scholar 

  • Bhattacharyya A, Chattopadhyay R, Mitra S, Crowe SE (2014) Oxidative stress: an essential factor in the pathogenesis of gastrointestinal mucosal diseases. Physiol Rev 94:329–354

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Borey M, Panserat S, Surget A, Cluzeaud M, Plagnes-Juan E, Herman A, Lazzarotto V, Corraze G, Medale F, Lauga B, Burel C (2016) Postprandial kinetics of gene expression of proteins involved in the digestive process in rainbow trout (O. mykiss) and impact of diet composition. Fish Physiol Biochem 42:1187–1202

    Article  CAS  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Cao JM, Chen Y, Zhu X, Huang YH, Zhao HX, Li GL, Lan HB, Chen B, Pan Q (2012) A study on dietary l-lysine requirement of juvenile yellow catfish Pelteobagrus fulvidraco. Aquac Nutr 18:35–45

    Article  CAS  Google Scholar 

  • Cao XJ, Wang WM (2009) Histology and mucin histochemistry of the digestive tract of yellow catfish, Pelteobagrus fulvidraco. Anat Histol Embryol 38:254–261

    Article  CAS  PubMed  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • Dong GF, Yang YO, Song XM, Yu L, Zhao TT, Huang GL, Hu ZJ, Zhang JL (2013a) Comparative effects of dietary supplementation with maggot meal and soybean meal in gibel carp (Carassius auratus gibelio) and darkbarbel catfish (Pelteobagrus vachelli): growth performance and antioxidant responses. Aquac Nutr 19:543–554

    Article  CAS  Google Scholar 

  • Dong GF, Yang YO, Yao F, Wan Q, Yu L, Zhou JC, Li Y (2013b) Responses of yellow catfish (Pelteobagrus fulvidraco Richardson) to low-protein diets and subsequent recovery. Aquac Nutr 19:430–439

    Article  CAS  Google Scholar 

  • Elmada CZ, Huang W, Jin M, Liang X, Mai K, Zhou Q (2016) The effect of dietary methionine on growth, antioxidant capacity, innate immune response and disease resistance of juvenile yellow catfish (Pelteobagrus fulvidraco). Aquac Nutr 22:1163–1173

    Article  CAS  Google Scholar 

  • Feng L, Xiao W, Liu Y, Jiang J, Hu K, Jiang W, Li S, Zhou X (2011) Methionine hydroxy analogue prevents oxidative damage and improves antioxidant status of intestine and hepatopancreas for juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 17:595–604

    Article  CAS  Google Scholar 

  • Fountoulaki E, Alexis MN, Nengas I, Venou B (2005) Effect of diet composition on nutrient digestibility and digestive enzyme levels of gilthead sea bream (Sparus aurata L.) Aquac Res 36:1243–1251

    Article  CAS  Google Scholar 

  • Furné M, Hidalgo MC, López A, García-Gallego M, Morales AE, Domezain A, Domezainé J, Sanz A (2005) Digestive enzyme activities in Adriatic sturgeon Acipenser naccarii and rainbow trout Oncorhynchus mykiss. A comparative study. Aquaculture 250:391–398

    Article  Google Scholar 

  • Gisbert E, Piedrahita RH, Conklin DE (2004) Ontogenetic development of the digestive system in California halibut (Paralichthys californicus) with notes on feeding practices. Aquaculture 232:455–470

    Article  Google Scholar 

  • Gu M, Bai N, Xu W, Zhou H, Zhang W, Mai K (2016) Effects of dietary β-conglycinin and glycinin on digestive enzymes activities, intestinal histology and immune responses of juvenile turbot Scophthalmus maximus. Aquac Res 47:1001–1008

    Article  CAS  Google Scholar 

  • Hakim Y, Uni Z, Hulata G, Harpaz S (2006) Relationship between intestinal brush border enzymatic activity and growth rate in tilapias fed diets containing 30% or 48% protein. Aquaculture 257:420–428

    Article  CAS  Google Scholar 

  • Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776

    Article  CAS  Google Scholar 

  • Hertrampf JW, Piedad-Pascual F (2000) Handbook on ingredients for aquaculture feeds. Springer Netherlands, Dordrecht

    Book  Google Scholar 

  • Hevrøy EM, El-Mowafi A, Taylor RG, Olsvik PA, Norberg B, Espe M (2007) Lysine intake affects gene expression of anabolic hormones in atlantic salmon, Salmo salar. Gen Comp Endocr 152:39–46

    Article  PubMed  Google Scholar 

  • Horwitz W (2000) Official methods of analysis of AOAC International, AOAC international

  • Hummel BC (1959) A modified spectrophotometric determination of chymotrypsin, trypsin, and thrombin. Can J Biochem Physiol 37:1393–1399

    Article  CAS  PubMed  Google Scholar 

  • Jiang J, Shi D, Zhou XQ, Feng L, Liu Y, Jiang WD, Wu P, Tang L, Wang Y, Zhao Y (2016a) Effects of lysine and methionine supplementation on growth, body composition and digestive function of grass carp (Ctenopharyngodon idella) fed plant protein diets using high-level canola meal. Aquac Nutr 22:1126–1133

    Article  CAS  Google Scholar 

  • Jiang J, Wu X, Zhou X, Feng L, Liu Y, Jiang W, Wu P, Zhao Y (2016b) Effects of dietary curcumin supplementation on growth performance, intestinal digestive enzyme activities and antioxidant capacity of crucian carp Carassius auratus. Aquaculture 463:174–180

    Article  Google Scholar 

  • Jiang WD, Hu K, Zhang JX, Liu Y, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2015) Soyabean glycinin depresses intestinal growth and function in juvenile Jian carp (Cyprinus carpio var Jian): protective effects of glutamine. Br J Nutr 114:1569–1583

    Article  CAS  PubMed  Google Scholar 

  • Kaushik SJ, Cravedi JP, Lalles JP, Sumpter J, Fauconneau B, Laroche M (1995) Partial or total replacement of fish meal by soybean protein on growth, protein utilization, potential estrogenic or antigenic effects, cholesterolemia and flesh quality in rainbow trout, Oncorhynchus mykiss. Aquaculture 133:257–274

    Article  CAS  Google Scholar 

  • Krogdahl Å, Bakke-Mckellep AM, Baeverfjord G (2003) Effects of graded levels of standard soybean meal on intestinal structure, mucosal enzyme activities, and pancreatic response in Atlantic salmon (Salmo salar L.) Aquac Nutr 9:361–371

    Article  Google Scholar 

  • Lansard M, Panserat S, Plagnes-Juan E, Dias K, Seiliez I, Skiba-Cassy S (2011) L-leucine, L-methionine, and L-lysine are involved in the regulation of intermediary metabolism-related gene expression in rainbow trout hepatocytes. J Nutr 141:75–80

    Article  CAS  PubMed  Google Scholar 

  • Li W, Feng L, Liu Y, Jiang WD, Kuang SY, Jiang J, Li SH, Tang L, Zhou XQ (2015) Effects of dietary phenylalanine on growth, digestive and brush border enzyme activities and antioxidant capacity in the hepatopancreas and intestine of young grass carp (Ctenopharyngodon idella). Aquac Nutr 21:913–925

    Article  CAS  Google Scholar 

  • Li X, Tang L, Hu K, Liu Y, Jiang W, Jiang J, Wu P, Chen G, Li S, Kuang S, Feng L, Zhou X (2014) Effect of dietary lysine on growth, intestinal enzymes activities and antioxidant status of sub-adult grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 40:659–671

    Article  CAS  PubMed  Google Scholar 

  • Li XY, Liu Y, Jiang WD, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2016) Co- and post-treatment with lysine protects primary fish enterocytes against Cu-induced oxidative damage. PLoS One 11:e147408

    Google Scholar 

  • Lin YH, Mui JJ (2017) Comparison of dietary inclusion of commercial and fermented soybean meal on oxidative status and non-specific immune responses in white shrimp, Litopenaeus vannamei. Fish Shellfish Immun 63:208–212

    Article  CAS  Google Scholar 

  • Liu H, Jin J, Zhu X, Han D, Yang Y, Xie S (2017) Effect of substitution of dietary fish meal by soybean meal on different sizes of gibel carp (Carassius auratus gibelio): digestive enzyme gene expressions and activities, and intestinal and hepatic histology. Aquac Nutr 23:129–147

    Article  CAS  Google Scholar 

  • Liu W, Zhang X, Wang L (2010) Digestive enzyme and alkaline phosphatase activities during the early stages of Silurus soldatovi development. Zool Res 31:627–632

    CAS  PubMed  Google Scholar 

  • Luo Z, Tan X, Zheng J, Chen Q, Liu C (2011) Quantitative dietary zinc requirement of juvenile yellow catfish Pelteobagrus fulvidraco, and effects on hepatic intermediary metabolism and antioxidant responses. Aquaculture 319:150–155

    Article  CAS  Google Scholar 

  • Martínez-álvarez RM, Morales AE, Sanz A (2005) Antioxidant defenses in fish: biotic and abiotic factors. Rev Fish Biol Fisher 15:75–88

    Article  Google Scholar 

  • Naylor RL, Hardy RW, Bureau DP, Chiu A, Elliott M, Farrell AP, Forster I, Gatlin DM, Goldburg RJ, Hua K, Nichols PD (2009) Feeding aquaculture in an era of finite resources. P Natl Acad Sci Usa 106:15103–15110

    Article  CAS  Google Scholar 

  • Niu J, Figueiredo-Silva C, Dong Y, Yue YR, Lin HZ, Wang J, Wang Y, Huang Z, Xia DM, Lu X (2016) Effect of replacing fish meal with soybean meal and of DL-methionine or lysine supplementation in pelleted diets on growth and nutrient utilization of juvenile golden pompano (Trachinotus ovatus). Aquac Nutr 22:606–614

    Article  CAS  Google Scholar 

  • Rolland M, Dalsgaard J, Holm J, Gomez-Requeni P, Skov PV (2015) Dietary methionine level affects growth performance and hepatic gene expression of GH-IGF system and protein turnover regulators in rainbow trout (Oncorhynchus mykiss) fed plant protein-based diets. Comp BiochemPhys B 181:33–41

    Article  CAS  Google Scholar 

  • Srikanth K, Pereira E, Duarte AC, Ahmad I (2013) Glutathione and its dependent enzymes’ modulatory responses to toxic metals and metalloids in fish––a review. Environ Sci Pollut R 20:2133–2149

    Article  CAS  Google Scholar 

  • Tang L, Wang GX, Jiang J, Feng L, Yang L, Li SH, Kuang SY, Zhou XQ (2009) Effect of methionine on intestinal enzymes activities, microflora and humoral immune of juvenile Jian carp (Cyprinus carpio var. Jian). Aquac Nutr 15:477–483

    Article  CAS  Google Scholar 

  • Tengjaroenkul B, Smith BJ, Caceci T, Smith SA (2000) Distribution of intestinal enzyme activities along the intestinal tract of cultured Nile tilapia, Oreochromis niloticus L. Aquaculture 182:317–327

    Article  CAS  Google Scholar 

  • Vardi N, Parlakpinar H, Ozturk F, Ates B, Gul M, Cetin A, Erdogan A, Otlu A (2008) Potent protective effect of apricot and β-carotene on methotrexate-induced intestinal oxidative damage in rats. Food Chem Toxicol 46:3015–3022

    Article  CAS  PubMed  Google Scholar 

  • Villanueva J, Vanacore R, Goicoechea O, Amthauer R (1997) Intestinal alkaline phosphatase of the fish Cyprinus carpio: regional distribution and membrane association. J Exp Zool 279:347–355

    Article  CAS  Google Scholar 

  • Wang C, Xie S, Zhu X, Lei W, Yang Y, Liu J (2006b) Effects of age and dietary protein level on digestive enzyme activity and gene expression of Pelteobagrus fulvidraco larvae. Aquaculture 254:554–562

    Article  CAS  Google Scholar 

  • Wang MH, Zhang HF, Liu JG, Huang WD (2013) A comparative study on determining methods for crude fat in extruded feed. Lab Anim Sci 30(35–37):41

    Google Scholar 

  • Wang P, Powell SR (2010) Decreased sensitivity associated with an altered formulation of a commercially available kit for detection of protein carbonyls. Free Radic Biol Med 49:119–121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang Y, Kong L, Li C, Bureau DP (2006a) Effect of replacing fish meal with soybean meal on growth, feed utilization and carcass composition of cuneate drum (Nibea miichthioides). Aquaculture 261:1307–1313

    Article  Google Scholar 

  • Wu P, Jiang W, Liu Y, Chen G, Jiang J, Li S, Feng L, Zhou X (2014) Effect of choline on antioxidant defenses and gene expressions of Nrf2 signaling molecule in the spleen and head kidney of juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immun 38:374–382

    Article  CAS  Google Scholar 

  • Zhang H, Yi L, Sun R, Zhou H, Xu W, Zhang W, Mai K (2016) Effects of dietary citric acid on growth performance, mineral status and intestinal digestive enzyme activities of large yellow croaker Larimichthys crocea (Richardson, 1846) fed high plant protein diets. Aquaculture 453:147–153

    Article  CAS  Google Scholar 

  • Zhang J, Guo L, Feng L, Jiang W, Kuang S, Liu Y, Hu K, Jiang J, Li S, Tang L, Zhou X (2013) Soybean beta-conglycinin induces inflammation and oxidation and causes dysfunction of intestinal digestion and absorption in fish. PLoS One 8:e58115

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhang X, Yang Q, Jiao B, Dai J, Zhang J, Ni W (2008) Sensitive determination of pheomelanin after 5-carboxyfluorescein succinimidyl ester precapillary derivatization and micellar electrokinetic capillary chromatography with laser-induced fluorescence detection. J Chromatogr B 861:136–139

    Article  CAS  Google Scholar 

  • Zhao Y, Hu Y, Zhou XQ, Zeng XY, Feng L, Liu Y, Jiang WD, Li SH, Li DB, Wu XQ, Wu CM, Jiang J (2015) Effects of dietary glutamate supplementation on growth performance, digestive enzyme activities and antioxidant capacity in intestine of grass carp (Ctenopharyngodon idella). Aquac Nutr 21:935–941

    Article  CAS  Google Scholar 

  • Zheng Q, Wen X, Han C, Li H, Xie X (2012) Effect of replacing soybean meal with cottonseed meal on growth, hematology, antioxidant enzymes activity and expression for juvenile grass carp, Ctenopharyngodon idellus. Fish Physiol Biochem 38:1059–1069

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This study was financially supported by the Applied Basic Research Programs of Science and Technology Commission Foundation of Sichuan Province, China (2015JY0067), and Science and Technology Support Program of Sichuan Province, China (2014FZ0026). The authors would like to express their sincere thanks to the personnel of these teams for their kind assistance.

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Correspondence to Ye Zhao or Xiaoqiu Zhou.

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Jiang, J., Xu, S., Feng, L. et al. Lysine and methionine supplementation ameliorates high inclusion of soybean meal inducing intestinal oxidative injury and digestive and antioxidant capacity decrease of yellow catfish. Fish Physiol Biochem 44, 319–328 (2018). https://doi.org/10.1007/s10695-017-0437-1

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