Skip to main content
Log in

Enzyme-treated soy protein supplementation in low protein diet improved flesh tenderness, juiciness, flavor, healthiness, and antioxidant capacity in on-growing grass carp (Ctenopharyngodon idella)

  • Published:
Fish Physiology and Biochemistry Aims and scope Submit manuscript

Abstract

An 8-week feeding trial was conducted to investigate the effects of enzyme-treated soy protein (ETSP) supplementation in low protein diets on growth performance as well as flesh sensory quality and healthiness in on-growing grass carp. A total of 540 on-growing grass carp (initial average weight 325.72 ± 0.60 g) were fed six diets, which included a normal protein diet (28% crude protein) and five low protein diets (26% crude protein) supplemented with graded levels of ETSP (0.0, 0.8, 1.2, 1.6, and 2.0%). The results showed that reducing dietary protein by 2% decreased percentage weight gain, feed intake, and flesh flavor (aspartic acid, glutamic acid, histidine, and 5′-inosinic acid contents) and healthiness-related indices (linolenic acid (LA) and docosahexaenoic acid (DHA) contents and polyunsaturated fatty acids to saturated fatty acids ratio). Under the condition of reducing dietary protein by 2%, 0.8–1.2% ETSP supplementation restored above parameters to levels equal or superior to those in 28% crude protein diet group. Although reducing dietary protein by 2% did not deteriorate flesh tenderness and juiciness, 0.8–1.2% ETSP supplementation in low protein diets also improved the two indices compared with 28% crude protein diet. Moreover, ETSP-improved flesh quality was partly related to increased muscle antioxidant enzymes activities and their mRNA levels. In addition, ESTP-enhanced antioxidant enzyme mRNA levels were partly associated with the upregulation of NF-E2-related factor 2 (Nrf2) and target of rapamycin (TOR) signaling. Collectively, 0.8–1.2% ETSP supplementation in low protein diets improved growth performance as well as flesh sensory quality and healthiness in on-growing grass carp.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1

Similar content being viewed by others

Abbreviations

ETSP:

Enzyme-treated soy protein

FAAs:

Free amino acids

IMP:

5′-inosinic acid

FAs:

Fatty acids

PUFAs:

Polyunsaturated fatty acids

MDA:

Malondialdehyde

PC:

Protein carbonyl

GSH:

Glutathione

Cu/Zn-SOD:

Copper/zinc superoxide dismutase

MnSOD:

Manganese superoxide dismutase

CAT:

Catalase

GPx:

Glutathione peroxidase

GST:

Glutathione S-transferases

GR:

Glutathione reductase

GCL:

Glutamate-cysteine ligase

Nrf2:

NF-E2-related factor 2

Keap1:

Kelch-like-ECH-associated protein1

TOR:

Target of rapamycin

CK2:

Casein kinase 2

References

  • Ahmed ST, Islam MM, Bostami ABMR, Mun H, Kim Y, Yang C (2015) Meat composition, fatty acid profile and oxidative stability of meat from broilers supplemented with pomegranate (Punica granatum L.) by-products. Food Chem 188:481–488

    Article  CAS  PubMed  Google Scholar 

  • Atti N, Rouissi H, Mahouachi M (2004) The effect of dietary crude protein level on growth, carcass and meat composition of male goat kids in Tunisia. Small Rumin Res 54:89–97

    Article  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

    CAS  PubMed  Google Scholar 

  • Damodaran S (2008) Amino acids, peptides, and proteins. CRC Press, Boca Raton, (Chapter 5, pp 217–329

    Google Scholar 

  • Deng YP, Jiang WD, Liu Y, Qu B, Jiang J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2016) Dietary leucine improves flesh quality and alters mRNA expressions of Nrf2-mediated antioxidant enzymes in the muscle of grass carp (Ctenopharyngodon idella). Aquaculture 452:380–387

    Article  CAS  Google Scholar 

  • Dickinson DA, Iles KE, Zhang HQ, Blank V, Forman J (2013) Curcumin alters EpRE and AP-1 binding complexes and elevates glutamate-cysteine ligase gene expression. FASEB J 17:473–475

    Google Scholar 

  • Feng L, Li W, Liu Y, Jiang WD, Kuang SY, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ (2015) Dietary phenylalanine-improved intestinal barrier health in young grass carp (Ctenopharyngodon idella) is associated with increased immune status and regulated gene expression of cytokines, tight junction proteins, antioxidant enzymes and related signalling molecules. Fish Shellfish Immunol 45:495–509

    Article  CAS  PubMed  Google Scholar 

  • Gan L, Jiang WD, Wu P, Liu Y, Jiang J, Li SH, Tang L, Kuang SY, Feng L, Zhou XQ (2014) Flesh quality loss in response to dietary isoleucine deficiency and excess in fish: a link to impaired Nrf2-dependent antioxidant defense in muscle. PLoS One 9:e115129

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Gardeur JN, Mathis N, Kobilinsky A, Bellut JB (2007) Simultaneous effects of nutritional and environmental factors on growth and flesh quality of Perca fluviatilis using a fractional factorial design study. Aquaculture 273:50–63

    Article  Google Scholar 

  • Gatlin DM III, Barrows FT, Brown P, Dabrowski K, Gaylord TG, Hardy RW, Herman E, Hu G, Krogdahl Å, Nelson R, Overturf K, Rust M, Sealey W, Skonberg D, Souza EJ, Stone D, Wilson R, Wurtele E (2007) Expanding the utilization of sustainable plant products in aqua-feeds: a review. Aquac Res 38:551–579

    Article  CAS  Google Scholar 

  • Gralak MA (2002) Absorption of certain trace elements in different nutritional conditions. Biol Grow Anim 1:579–604

    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 

  • Hasan MR (2016) Nutrition and feeding for sustainable aquaculture development in the third millennium. Fish Aquac Dep 13:193–219

    Google Scholar 

  • Hu K, Zhang JX, Feng L, Jiang WD, Wu P, Liu Y, Jiang J, Zhou XQ (2015) Effect of dietary glutamine on growth performance, non-specific immunity, expression of cytokine genes, phosphorylation of target of rapamycin (TOR), and anti-oxidative system in spleen and head kidney of Jian carp (Cyprinus carpio var. Jian). Fish Physiol Biochem 41:635–649

    Article  CAS  PubMed  Google Scholar 

  • Jiang WD, Wen HL, Liu Y, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2016a) Enhanced muscle nutrient content and flesh quality, resulting from tryptophan, is associated with anti-oxidative damage referred to the Nrf2 and TOR signalling factors in young grass carp (Ctenopharyngodon idella): avoid tryptophan deficiency or excess. Food Chem 199:210–219

    Article  CAS  PubMed  Google Scholar 

  • Jiang WD, Wu P, Tang RJ, Liu Y, Kuang SY, Jiang J, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2016b) Nutritive values, flavor amino acids, healthcare fatty acids and flesh quality improved by manganese referring to up-regulating the antioxidant capacity and signaling molecules TOR and Nrf2 in the muscle of fish. Food Res Int 89:670–678

    Article  CAS  PubMed  Google Scholar 

  • Jones KA (1989) The palatability of amino acids and related compounds to rainbow trout, Salmo gairdneri Richardson. J Fish Biol 34:149–160

    Article  CAS  Google Scholar 

  • Kerr BJ, Mckeith FK, Easter RA (1995) Effect on performance and carcass characteristics of nursery to finisher pigs fed reduced crude protein, amino acid-supplemented diets. J Anim Sci 73:433–440

    Article  CAS  PubMed  Google Scholar 

  • Khan N, Qureshi NA, Nasir M, Rasool F, Iqba KJ (2011) Effect of artificial diet and culture systems on sensory quality of fried fish flesh of Indian major carps. Pak J Zool 43:1177–1182

    CAS  Google Scholar 

  • Khan MR, Naushad M, Alothman ZA, Alsohaimi IH, Algamdi MS (2015) Solid phase extraction and ultra performance liquid chromatography-tandem mass spectrometric identification of carcinogenic/mutagenic heterocyclic amines in cooked camel meat. RSC Adv 5:2479–2485

    Article  CAS  Google Scholar 

  • Kouba M, Enser M, Whittington FM, Nute GR, Wood JD (2003) Effect of a high-linolenic acid diet on lipogenic enzyme activities, fatty acid composition, and meat quality in the growing pig. J Anim Sci 81:1967–1979

    Article  CAS  PubMed  Google Scholar 

  • Laver DR, Lenz GKE, Lamb GD (2001) Regulation of the calcium release channel from rabbit skeletal muscle by the nucleotides ATP, AMP, IMP and adenosine. J Physiol 537:763–778

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li WW, Gong YN, Jin XK, He L, Jiang H, Ren F, Wang Q (2010) The effect of dietary zinc supplementation on the growth, hepatopancreas fatty acid composition and gene expression in the Chinese mitten crab, Eriocheir sinensis (H. Milne-Edwards) (Decapoda: Grapsidae). Aquac Res 41:e828–e837

    Article  CAS  Google Scholar 

  • Li XK, Wang JZ, Wang CQ, Zhang CH, Li X, Tang CH, Wei XL (2016) Effect of dietary phosphorus levels on meat quality and lipid metabolism in broiler chickens. Food Chem 205:289–296

    Article  CAS  PubMed  Google Scholar 

  • Liu J, Zhao S, Xiong S, Zhang S (2009) Influence of recooking on volatile and non-volatile compounds found in silver carp Hypophthalmichthys molitrix. Fish Sci 75:1067–1075

    Article  CAS  Google Scholar 

  • Ljubojević D, Radosavljević V, Puvača N, Baloš MŽ, Ðorpević V, Jovanović R, Ćirković M (2015) Influence of diet on proximate composition and fatty acid profile in common carp (Cyprinus carpio). J Food Compos Anal 37:44–50

    Article  CAS  Google Scholar 

  • Lönnerdal BO (2000) Dietary factors influencing zinc absorption. J Nutr 130:1378S–1383S

    Article  PubMed  Google Scholar 

  • Lopparelli RM, Segato S, Corato A, Fasolato L, Andrighetto I (2004) Sensory evaluation of sea bass (Dicentrarchus labrax L.) fed two diets differing in fat content. Vet Res Commun 28:225–227

    Article  PubMed  Google Scholar 

  • Lv Y, Liu Q, Bao X, Tang W, Yang B, Guo S (2009) Identification and characteristics of iron-chelating peptides from soybean protein hydrolysates using IMAC-Fe3+. J Agric Food Chem 57:4593–4597

    Article  CAS  PubMed  Google Scholar 

  • Martin D, Antequera T, Muriel T, Perez-Palacios T, Ruiz J (2011) Effect of dietary conjugated linoleic acid in combination with monounsaturated fatty acids on the composition and quality traits of cooked loin. Food Chem 124:518–526

    Article  CAS  Google Scholar 

  • Merkel M, Eckel RH, Goldberg IJ (2002) Lipoprotein lipase genetics, lipid uptake, and regulation. J Lipid Res 43:1997–2006

    Article  CAS  PubMed  Google Scholar 

  • Okouchi M, Okayama N, Alexander JS, Aw TY (2006) NRF2-dependent glutamate-L-cysteine ligase catalytic subunit expression mediates insulin protection against hyperglycemia-induced brain endothelial cell apoptosis. Curr Neurovasc Res 3:249–261

    Article  CAS  PubMed  Google Scholar 

  • Olsen BB, Svenstrup TH, Guerra B (2012) Downregulation of protein kinase CK2 induces autophagic cell death through modulation of the mTOR and MAPK signaling pathways in human glioblastoma cells. Int J Oncol 41:1967–1976

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pan CL, Chen WH, Zhou SX, Lin CZ (2006) Effect of soybean protein hydrolysate on the growth and incretion of weaned at 21 day-old piglets. J Nanjing Agric Univ 3:69–72

    Google Scholar 

  • Pan FY, Feng L, Jiang WD, Jiang J, Wu P, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ (2016) Methionine hydroxy analogue enhanced fish immunity by modulation of NF-κB, TOR, MLCK, MAPKs and Nrf2 signaling in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 56:208–228

    Article  CAS  PubMed  Google Scholar 

  • Singh BP, Vij S, Hati S (2014) Functional significance of bioactive peptides derived from soybean. Peptides 54:171–179

    Article  CAS  PubMed  Google Scholar 

  • Teye GA, Sheard PR, Whittington FM, Nute GR, Stewart A, Wood JD (2006) Effects on muscle fatty acid composition, carcass, meat and eating quality. Meat Sci 73:157–165

    Article  CAS  PubMed  Google Scholar 

  • Tibaldi E, Hakim Y, Uni Z, Tulli F, de Francesco M, Luzzana U, Harpaz S (2006) Effects of the partial substitution of dietary fish meal by differently processed soybean meals on growth performance, nutrient digestibility and activity of intestinal brush border enzymes in the European sea bass (Dicentrarchus labrax). Aquaculture 261:182–193

    Article  CAS  Google Scholar 

  • Tie HM, Wu P, Jiang WD, Liu Y, Kuang SY, Zeng YY, Jiang J, Tang L, Zhou XQ, Feng L (2019) Dietary nucleotides supplementation affect the physicochemical properties, amino acid and fatty acid constituents, apoptosis and antioxidant mechanisms in grass carp (Ctenopharyngodon idellus) muscle. Aquaculture 502:312–325

    Article  CAS  Google Scholar 

  • Toldrá F, Flores M (1998) The role of muscle proteases and lipases in flavor development during the processing of dry-cured ham. Crit Rev Food Sci 38:331–352

    Article  Google Scholar 

  • Wang JP, Liu N, Song MY, Qin CL, Ma CS (2011) Effect of enzymolytic soybean meal on growth performance, nutrient digestibility and immune function of growing broilers. Anim Feed Sci Technol 169:224–229

    Article  CAS  Google Scholar 

  • Wang W, Xue W, Jin BQ, Zhang XX, Ma F, Xu XF (2013) Candidate gene expression affects intramuscular fat content and fatty acid composition in pigs. J Appl Genet 54:113–118

    Article  CAS  PubMed  Google Scholar 

  • Wang B, Liu Y, Feng L, Jiang WD, Kuang SY, Jiang J, Li SH, Tang L, Zhou XQ (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 167:91–99

    Article  CAS  PubMed  Google Scholar 

  • Wu PY, Feng L, Jiang WD, Liu Y, Jiang J, Li SH, Tang L, Kuang SY, Zhou XQ (2015) Influence of dietary zinc on muscle composition, flesh quality and muscle antioxidant status of young grass carp (Ctenopharyngodon idella Val.). Aquac Res 46:2360–2373

    Article  CAS  Google Scholar 

  • Xia SK, Chen L, Liang JQ (2007) Enriched selenium and its effects on growth and biochemical composition in Lactobacillus bulgaricus. J Agric Food Chem 55:2413–2417

    Article  CAS  PubMed  Google Scholar 

  • Xiao WW, Jiang WD, Feng L, Liu Y, Wu P, Jiang J, Zhang YA, Zhou XQ (2017) Supplementation of enzyme-treated soy protein saves dietary protein and promotes digestive and absorptive ability referring to TOR signaling in juvenile fish. Fish Physiol Biochem 43:1657–1675

    Article  CAS  PubMed  Google Scholar 

  • Xu J, Wu P, Jiang WD, Liu Y, Jiang J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2016) Optimal dietary protein level improved growth, disease resistance, intestinal immune and physical barrier function of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 55:64–87

    Article  CAS  PubMed  Google Scholar 

  • Yang SD, Liou CH, Liu FG (2002) Effects of dietary protein level on growth performance, carcass composition and ammonia excretion in juvenile silver perch (Bidyanus bidyanus). Aquaculture 213:363–372

    Article  CAS  Google Scholar 

  • Yi XW, Zhang F, Xu W, Li J, Zhang WB, Mai KS (2014) Effects of dietary lipid content on growth, body composition and pigmentation of large yellow croaker Larimichthys croceus. Aquaculture 434:355–361

    Article  CAS  Google Scholar 

  • Zhang L, Feng L, Jiang WD, Liu Y, Jiang J, Li SH, Tang L, Kuang SY, Zhou XQ (2016) The impaired flesh quality by iron deficiency and excess is associated with increasing oxidative damage and decreasing antioxidant capacity in the muscle of young grass carp (Ctenopharyngodon idellus). Aquac Nutr 22:191–201

    Article  CAS  Google Scholar 

  • Zhao HF, Feng L, Jiang WD, Liu Y, Jiang J, Wu P, Zhao J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ (2015) Flesh shear force, cooking loss, muscle antioxidant status and relative expression of signaling molecules (Nrf2, Keap1, TOR, and CK2) and their target genes in young grass carp (Ctenopharyngodon idella) muscle fed with graded levels of choline. PLoS One 10:e14291

    Google Scholar 

  • Zheng J, Tao N, Gong J, Gu S, Xu C (2015) Comparison of non-volatile taste-active compounds between the cooked meats of pre- and post-spawning Yangtze Coilia ectenes. Fish Sci 81:559–568

    Article  CAS  Google Scholar 

Download references

Acknowledgments

The authors would like to thank the personnel of these teams for their kind assistance.

Funding

This research was financially supported by the National Key R&D Program of China (2018YFD0900400), National Natural Science Foundation of China (31672662), National Technology System for Conventional Freshwater Fish Industries (CARS-45), Outstanding Talents and Innovative Team of Agricultural Scientific Research (Ministry of Agriculture), Foundation of Sichuan Youth Science and Technology Innovation Research Team (2017TD0002), the Earmarked Fund for China Agriculture Research System (CARS-45), Outstanding Talents and Innovative Team of Agricultural Scientific Research (Ministry of Agriculture), and Sichuan Science and Technology Program (2019YFN0036).

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to XiaoQiu Zhou.

Ethics declarations

In this study, experimental methods were approved by the Animal Care Advisory Committee of Sichuan Agricultural University.

Additional information

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Electronic supplementary material

ESM 1

(DOCX 54 kb)

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Song, Y., Yan, L., Jiang, W. et al. Enzyme-treated soy protein supplementation in low protein diet improved flesh tenderness, juiciness, flavor, healthiness, and antioxidant capacity in on-growing grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 46, 213–230 (2020). https://doi.org/10.1007/s10695-019-00710-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10695-019-00710-w

Keywords

Navigation