No CrossRef data available.
Article contents
Promotion of improved intestinal barrier health by soybean-derived bioactive peptides in Chinese mitten crab (Eriocheir sinensis) fed a low fishmeal diet
Published online by Cambridge University Press: 27 October 2023
Abstract
To alleviate the growth inhibition, and intestinal damage of Chinese mitten crab (Eriocheir sinensis) induced by low fishmeal diets (LF), an 8-week feeding trial was conducted to evaluate the addition of dietary soybean-derived bioactive peptides (SBP) in LF diets on the regulation of growth, digestion and intestinal health. The crabs were fed isonitrogenous and isoenergetic conventional diet and LF diets (10 % fishmeal replaced by soybean meal, LF) supplemented with 0, 1 %, 2 %, 4 % and 6 % SBP, respectively. The results showed that LF diet inhibited growth while inclusion of SBP quadratically remitted the growth inhibition induced by LF. For digestive function, increasing addition level of SBP quadratically improved the α-amylase and trypsin activities. For antioxidant function, LF group significantly increased the malondialdehyde content, while SBP linearly decreased the malondialdehyde level and cubically increased the anti-superoxide anion activity and total antioxidant capacity level. For intestinal health, the peritrophic membrane (PM) almost completely separated from the inner wall of the intestinal lumen, the epithelial cells reduced, the muscularis became thinner and the apoptotic signals increased in LF group; with SBP addition, the intestinal morphology was improved, with the PM adhering to the inner wall of the intestinal lumen, an increase in the number of epithelial cells and an increase in the thickness of the muscularis. Additionally, there was a decrease in apoptotic signals. Dietary SBP also increased the expression of PT and Crustin1 quadratically and decreased the expression of ALF1 linearly, ALF3 and ILF2 quadratically.
Keywords
- Type
- Research Article
- Information
- Copyright
- © The Author(s), 2023. Published by Cambridge University Press on behalf of The Nutrition Society
References
Zhou, JS, Chen, YS, Ji, H, et al. (2017) The effect of replacing fish meal with fermented meal mixture of silkworm pupae, rapeseed and wheat on growth, body composition and health of mirror carp (Cyprinus carpio var. Specularis). Aquacult Nutr 23, 741–754.CrossRefGoogle Scholar
Gatlin, DM, Barrows, FT, Brown, P, et al. (2007) Expanding the utilization of sustainable plant products in aquafeeds: a review. Aquacult Res 38, 551–579.CrossRefGoogle Scholar
Miao, SY, Zhao, CZ, Zhu, JY, et al. (2018) Dietary soybean meal affects intestinal homoeostasis by altering the microbiota, morphology and inflammatory cytokine gene expression in northern snakehead. Sci Rep 8, 113.CrossRefGoogle ScholarPubMed
Yao, W, Zhang, C, Li, X, et al. (2020) The replacement of fish meal with fermented soya bean meal or soya bean meal in the diet of Pacific white shrimp (Litopenaeus vannamei). Aquacult Res 51, 2400–2409.CrossRefGoogle Scholar
Peng, K, Chen, X, Lu, H, et al. (2022) Effect of dietary soybean meal on growth performance, apparent digestibility, intestinal digestive enzyme activity, and muscle growth-related gene expression of Litopenaeus vannamei. Front Mar Sci 9, 945417.CrossRefGoogle Scholar
Liu, Z-Y, Yang, H-L, Yan, Y-Y, et al. (2021) Supplementation of tributyrin, alone and in combination with fructooligosaccharide in high soybean meal diets for shrimp (Litopenaeus vannamei): effects on growth, innate immunity and intestinal morphology. Aquacult Nutr 27, 592–603.CrossRefGoogle Scholar
Kim, I-S, Yang, W-S & Kim, C-H (2021) Beneficial effects of soybean-derived bioactive peptides. Int J Mol Sci 22, 8570.CrossRefGoogle ScholarPubMed
Song, ZD, Li, HY, Wang, JY, et al. (2014) Effects of fishmeal replacement with soy protein hydrolysates on growth performance, blood biochemistry, gastrointestinal digestion and muscle composition of juvenile starry flounder (Platichthys stellatus). Aquaculture 426, 96–104.CrossRefGoogle Scholar
Singh, BP, Vij, S & Hati, S (2014) Functional significance of bioactive peptides derived from soybean. Peptides 54, 171–179.CrossRefGoogle ScholarPubMed
Sanjukta, S, Rai, AK, Muhammed, A, et al. (2015) Enhancement of antioxidant properties of two soybean varieties of Sikkim Himalayan region by proteolytic Bacillus subtilis fermentation. J Funct Foods 14, 650–658.CrossRefGoogle Scholar
Wang, Z, Cui, Y, Liu, P, et al. (2017) Small peptides isolated from enzymatic hydrolyzate of fermented soybean meal promote endothelium-independent vasorelaxation and ACE inhibition. J Agric Food Chem 65, 10844–10850.CrossRefGoogle ScholarPubMed
Xu, C, Liu, W, Zhang, D, et al. (2020) Effects of partial fish meal replacement with two fermented soybean meals on the growth of and protein metabolism in the Chinese mitten crab (Eriocheir sinensis). Aquacult Rep 17, 100328.Google Scholar
Cheng, A-C, Lin, H-L, Shiu, Y-L, et al. (2017) Isolation and characterization of antimicrobial peptides derived from Bacillus subtilis E20-fermented soybean meal and its use for preventing Vibrio infection in shrimp aquaculture. Fish Shellfish Immunol 67, 270–279.CrossRefGoogle ScholarPubMed
Martinez-Augustin, O, Rivero-Gutierrez, B, Mascaraque, C, et al. (2014) Food derived bioactive peptides and intestinal barrier function. Int J Mol Sci 15, 22857–22873.CrossRefGoogle ScholarPubMed
Duan, ZP, Zhang, CY, Huang, LL, et al. (2022) An evaluation of replacing fish meal with fermented soybean meal in diet of hybrid snakehead (channa argus × channa maculata): growth, nutrient utilization, serum biochemical indices, intestinal histology, microbial community. Aquacult Nutr 2022, 1–13CrossRefGoogle Scholar
Yamamoto, T, Murashita, K, Matsunari, H, et al. (2012) Influence of dietary soy protein and peptide products on bile acid status and distal intestinal morphology of rainbow trout Oncorhynchus mykiss. Fish Sci 78, 1273–1283.CrossRefGoogle Scholar
Zhao, Z-X, Song, C-Y, Xie, J, et al. (2016) Effects of fish meal replacement by soybean peptide on growth performance, digestive enzyme activities, immune responses of yellow catfish Pelteobagrus fulvidraco. Fish Sci 82, 665–673.CrossRefGoogle Scholar
Wang, S, He, Y, Wang, YY, et al. (2016) Comparison of flavour qualities of three sourced Eriocheir sinensis. Food Chem 200, 24–31.CrossRefGoogle ScholarPubMed
Jiang, HB, Chen, LQ, Qin, JG, et al. (2013) Partial or complete substitution of fish meal with soybean meal and cottonseed meal in Chinese mitten crab Eriocheir sinensis diets. Aquacult Int 21, 617–628.CrossRefGoogle Scholar
Liu, QD, Wen, B, Man, DR, et al. (2021) Substitution of fish meal with soybean meal for juvenile Chinese mitten crab (Eriocheir sinensis) reared at three salinities: effects on survival, growth, antioxidant capacity and body composition. Aquacult Res 52, 3723–3735.CrossRefGoogle Scholar
Hu, Y, Yang, G, Li, ZL, et al. (2018) Effect of dietary taurine supplementation on growth, digestive enzyme, immunity and resistant to dry stress of rice field eel (Monopterus albus) fed low fish meal diets. Aquacult Res 49, 2108–2118.CrossRefGoogle Scholar
Kesselring, J, Gruber, C, Standen, B, et al. (2021) Effect of a phytogenic feed additive on the growth performance and immunity of Pacific white leg shrimp, Litopenaeus vannamei, fed a low fishmeal diet. J World Aquacult Soc 52, 303–315.CrossRefGoogle Scholar
Serradell, A, Torrecillas, S, Makol, A, et al. (2020) Prebiotics and phytogenics functional additives in low fish meal and fish oil based diets for European sea bass (Dicentrarchus labrax): effects on stress and immune responses. Fish Shellfish Immunol 100, 219–229.CrossRefGoogle ScholarPubMed
Greene, DH & Babbitt, JK (1990) Control of muscle softening and protease-parasite interactions in arrowtooth flounder atheresthes-stomias. J Food Sci 55, 579–580.CrossRefGoogle Scholar
Matei, G, Woyann, LG, Meneguzzi, C, et al. (2017) Profiling and genotype 3 environment interactions of seed sugar contents in Brazilian soybean genotypes. Euphytica 213, 203.CrossRefGoogle Scholar
Wang, C, Wang, X, Huang, Y, et al. (2020) Effects of dietary T-2 toxin on gut health and gut microbiota composition of the juvenile Chinese mitten crab (Eriocheir sinensis). Fish Shellfish Immunol 106, 574–582.CrossRefGoogle ScholarPubMed
Han, FL, Wang, XD, Guo, JL, et al. (2019) Effects of glycinin and beta-conglycinin on growth performance and intestinal health in juvenile Chinese mitten crabs (Eriocheir sinensis). Fish Shellfish Immunol 84, 269–279.CrossRefGoogle ScholarPubMed
Sun, C, Shan, F, Liu, M, et al. (2022) High-fat-diet-induced oxidative stress in giant freshwater prawn (macrobrachium rosenbergii) via NF-kappa B/NO signal pathway and the amelioration of vitamin E. Antioxidants 11, 228-Article No.CrossRefGoogle Scholar
Lai, T, Nie, Z-Y, Zhang, X-Y, et al. (2022) Effects of starvation stress on hemolymph physiology and intestinal health of Procambarus clarkii. Acta Hydrob Sinica 46, 88–97.Google Scholar
Abbasi-Oshaghi, E, Mirzaei, F & Pourjafar, M (2019) NLRP3 inflammasome, oxidative stress, and apoptosis induced in the intestine and liver of rats treated with titanium dioxide nanoparticles: in vivo and in vitro study. Int J Nanomed 14, 1919–1936.CrossRefGoogle ScholarPubMed
Collins, SA, Overland, M, Skrede, A, et al. (2013) Effect of plant protein sources on growth rate in salmonids: meta-analysis of dietary inclusion of soybean, pea and canola/rapeseed meals and protein concentrates. Aquaculture 400, 85–100.CrossRefGoogle Scholar
Zheng, L, Park, I & Kim, SW (2016) Effects of supplemental soy peptide on growth performance and gut health of nursery pigs. J Anim Sci 94, 49–50.CrossRefGoogle Scholar
Zhang, C, Wang, XD, Su, RY, et al. (2022) Dietary-aminobutyric acid (GABA) supplementation increases food intake, influences the expression of feeding-related genes and improves digestion and growth of Chinese mitten crab (Eriocheir sinensis). Aquaculture 546, 737332.CrossRefGoogle Scholar
Long, XW, Sun, YF, Wade, NM, et al. (2020) Key metabolic and enzymatic adaptations underlie the benefits of formulated diets in the adult female Chinese mitten crabEriocheir sinensis. Aquacult Res 51, 5125–5140.CrossRefGoogle Scholar
Zhang, YL, Duan, XD, Jiang, WD, et al. (2019) Soybean glycinin decreased growth performance, impaired intestinal health, and amino acid absorption capacity of juvenile grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 45, 1589–1602.CrossRefGoogle ScholarPubMed
Domijan, A-M, Ralic, J, Brkanac, SR, et al. (2015) Quantification of malondialdehyde by HPLC-FL - application to various biological samples. Biomed Chromatogr 29, 41–46.CrossRefGoogle ScholarPubMed
Jiang, J, Xu, SX, Feng, L, et al. (2018) 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.CrossRefGoogle ScholarPubMed
Yi, G, Din, JU, Zhao, F, et al. (2020) Effect of soybean peptides against hydrogen peroxide induced oxidative stress in HepG2 cells via Nrf2 signaling. Food Funct 11, 2725–2737.CrossRefGoogle ScholarPubMed
Zhang, QZ, Tong, XH, Li, Y, et al. (2019) Purification and characterization of antioxidant peptides from alcalase-hydrolyzed soybean (Glycine max L.) hydrolysate and their cytoprotective effects in human intestinal Caco-2 cells. J Agric Food Chem 67, 5772–5781.CrossRefGoogle ScholarPubMed
Morgan, AJ, Riley, LG, Sheehy, PA, et al. (2014) The influence of protein fractions from bovine colostrum digested in vivo and in vitro on human intestinal epithelial cell proliferation. J Dairy Res 81, 73–81.CrossRefGoogle ScholarPubMed
Han, F, Xu, C, Qi, C, et al. (2020) Sodium butyrate can improve intestinal integrity and immunity in juvenile Chinese mitten crab (Eriocheir sinensis) fed glycinin. Fish Shellfish Immunol 102, 400–411.CrossRefGoogle ScholarPubMed
Jiang, WD, Hu, K, Zhang, JX, et al. (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.CrossRefGoogle ScholarPubMed
Zhao, XY, Zhang, Y, He, WT, et al. (2022) Effects of small peptide supplementation on growth performance, intestinal barrier of laying hens during the brooding and growing periods. Front Immunol 13, 925256.CrossRefGoogle ScholarPubMed
Cai, CF, Wu, P, Ye, YT, et al. (2014) Assessment of the feasibility of including high levels of oilseed meals in the diets of juvenile Chinese mitten crabs (Eriocheir sinensis): effects on growth, non-specific immunity, hepatopancreatic function, and intestinal morphology. Anim Feed Sci Technol 196, 117–127.CrossRefGoogle Scholar
Park, MJ, Kim, BY & Jin, BR (2016) Molecular characterization of a chitin-binding protein with the peritrophin-A domain from the Asiatic honeybee Apis cerana. J Asia-Pac Entomol 19, 963–968.CrossRefGoogle Scholar
Huang, Y, Ma, FT, Wang, W, et al. (2015) Identification and molecular characterization of a peritrophin-like gene, involved in the antibacterial response in Chinese mitten crab, Eriocheir sinensis. Dev Comp Immunol 50, 129–138.CrossRefGoogle ScholarPubMed
Wang, QQ, Cai, CF, Shui, DZ, et al. (2018) Identification and characterization of two novel peritrophic membrane (PM) genes in the Chinese mitten crab Eriocheir sinensis that exhibit activity against high-pH stress and Aeromonas hydrophila challenge. Aquacult Res 49, 3746–3758.CrossRefGoogle Scholar
Yang, JL, Wang, LL, Huang, MM, et al. (2011) An interleukin-2 enhancer binding factor 2 homolog involved in immune response from Chinese mitten crab Eriocheir sinensis. Fish Shellfish Immunol 30, 1303–1309.CrossRefGoogle ScholarPubMed
Wu, P, Tian, L, Zhou, XQ, et al. (2018) Sodium butyrate enhanced physical barrier function referring to Nrf2, JNK and MLCK signaling pathways in the intestine of young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 73, 121–132.CrossRefGoogle ScholarPubMed
Wang, XZ, Jiang, WD, Feng, L, et al. (2018) Low or excess levels of dietary cholesterol impaired immunity and aggravated inflammation response in young grass carp (Ctenopharyngodon idella). Fish Shellfish Immunol 78, 202–221.CrossRefGoogle ScholarPubMed
Wang, LL, Zhang, Y, Wang, LL, et al. (2011) A new anti-lipopolysaccharir (EsALF-3) from Eriocheir sinensis with antimicrobial activity. Afr J Biotechnol 10, 17678–17689.Google Scholar
Chakrabarti, S, Jahandideh, F & Wu, JP (2014) Food-derived bioactive peptides on inflammation and oxidative stress. Biomed Res Int 2014, 608979.CrossRefGoogle ScholarPubMed
Kim, JA & Kim, SK (2013) Bioactive peptides from marine sources as potential anti-inflammatory therapeutics. Curr Protein Pept Sci 14, 177–182.CrossRefGoogle ScholarPubMed
Zhou, JH, Ma, LL, Xu, HH, et al. (2014) Immunomodulating effects of casein-derived peptides QEPVL and QEPV on lymphocytes in vitro and in vivo
. Food Funct 5, 2061–2069.Google Scholar
Wen, LR, Bi, HM, Zhou, XS, et al. (2022) Structure characterization of soybean peptides and their protective activity against intestinal inflammation. Food Chem 387, 132868.CrossRefGoogle ScholarPubMed
Lin, YH & Chen, YT (2022) Lactobacillus spp. fermented soybean meal partially substitution to fish meal enhances innate immune responses and nutrient digestibility of white shrimp (Litopenaeus vannamei) fed diet with low fish meal. Aquaculture 548, 737634.CrossRefGoogle Scholar
Xuquan, X, Weilan, Z, Ruixue, D, et al. (2022) Study of enzyme-hydrolyzed soybean replacing fish meal and/or chicken meal on the growth of channel catfish (Ictalurus punctatus). Aquacult Rep 27, 101344.Google Scholar
Lin, HX, Tan, BP, Ray, GW, et al. (2022) A challenge to conventional fish meal: effects of soy protein peptides on growth, histomorphology, lipid metabolism and intestinal health for juvenile pompano trachinotus ovatus. Front Mar Sci 8, 815323.CrossRefGoogle Scholar