Abstract
The present study aimed to investigate the dynamic process of soybean β-conglycinin in digestion, absorption, and metabolism in the intestine of grass carp (Ctenopharyngodon idella). Fish fed with 80 g β-conglycinin/kg diet for 7 weeks, the intestinal digestive enzyme was extracted to hydrolyze β-conglycinin in vitro, the free amino acid and its metabolism product contents in intestinal segments were analyzed. The present study first found that β-conglycinin cannot be thoroughly digested by fish intestine digestive enzyme and produces new products (about 60- and 55-kDa polypeptides). The indigestible β-conglycinin further caused the free amino acid imbalance, especially caused free essential amino acid deficiency in the proximal intestine but excess in the distal intestine. Moreover, these results might be partly associated with the effect of β-conglycinin in amino acid transporters and tight junction-regulated paracellular pathway. Finally, dietary β-conglycinin increased the content of amino acid catabolism by-product ammonia while decreased the amino acid anabolism product carnosine content in the proximal intestine and distal intestine. Thus, the current study first and systemically explored the dynamic process of β-conglycinin in digestion, absorption, and metabolism, which further supported our previous study that dietary β-conglycinin suppressed fish growth and caused intestine injure.
Similar content being viewed by others
References
Astwood JD, Leach JN, Fuchs RL (1996) Stability of food allergens to digestion in vitro. Nat Biotechnol 14:1269–1273
Ballard ST, Hunter JH, Taylor AE (1995) Regulation of tight-junction permeability during nutrient absorption across the intestinal epithelium. Annu Rev Nutr 15:35–55
Banerjee S, Bhattacharya S (1995) Histopathological changes induced by chronic nonlethal levels of elsan, mercury and ammonia in the small intestine of Channa punctatus (Bloch). Ecotoxicol Environ Safe 31:62–68
Berge GE, Goodman M, Espe M, Lied E (2004) Intestinal absorption of amino acids in fish: kinetics and interaction of the in vitro uptake of l-methionine in Atlantic salmon (Salmo salar L.). Aquaculture 229:265–273
Chasiotis H, Kolosov D, Bui P, Kelly SP (2012) Tight junctions, tight junction proteins and paracellular permeability across the gill epithelium of fishes: a review. Respir Physiol Neurobiol 184:269–281
Dong YW, Jiang WD, Liu Y, Wu P, Jiang J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2017) Threonine deficiency decreased intestinal immunity and aggravated inflammation associated with NF-κB and target of rapamycin signalling pathways in juvenile grass carp (Ctenopharyngodon idella) after infection with Aeromonas hydrophila. Brit J Nutr 118:92–108
Duan XD, Feng L, Jiang WD, Wu P, Liu Y, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ (2019a) Dietary soybean β-conglycinin suppresses growth performance and inconsistently triggers apoptosis in the intestine of juvenile grass carp (Ctenopharyngodon idella) in association with ROS-mediated MAPK signalling. Aquac Nutr 25:770–782
Duan XD, Jiang WD, Wu P, Liu Y, Jiang J, Tan BP, Yang QH, Kuang SY, Tang L, Zhou XQ, Feng L (2019b) Soybean β-conglycinin caused intestinal inflammation and oxidative damage in association with NF-κB, TOR and Nrf2 in juvenile grass carp (Ctenopharyngodon idella): varying among different intestinal segments. Fish Shellfish Immunol 95:105–116
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
Guiotto A, Calderan A, Ruzza P, Borin G (2005) Carnosine and carnosine-related antioxidants: a review. Curr Med Chem 12:2293–2315
Han F, Wang X, Guo J, Qi C, Xu C, Luo Y, Li E, Qin JG, Chen L (2019) Effects of glycinin and β-conglycinin on growth performance and intestinal health in juvenile Chinese mitten crabs (Eriocheir sinensis). Fish Shellfish Immunol 84:269–279
Hardy RW (2010) Utilization of plant proteins in fish diets: effects of global demand and supplies of fishmeal. Aquac Res 41:770–776
Jamaluddin MS, Yan S, Lu J, Liang Z, Yao Q, Chen C (2013) Resistin increases monolayer permeability of human coronary artery endothelial cells. PLoS One 8:e84576
Jiang WD, Deng YP, Liu Y, Qu B, Jiang J, Kuang SY, Tang L, Tang WN, Wu P, Zhang YA, Zhou XQ, Feng L (2015) Dietary leucine regulates the intestinal immune status, immune-related signalling molecules and tight junction transcript abundance in grass carp (Ctenopharyngodon idella). Aquaculture 444:134–142
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lallès J, Tukur HM, Salgado P, Mills ENC, Morgan MRA, Quillien L, Levieux D, Toullec R (1999) Immunochemical studies on gastric and intestinal digestion of soybean glycinin and β-conglycinin in vivo. J Agric Food Chem 47:2797–2806
Li X, Tang L, Hu K, Liu Y, Jiang WD, Jiang J, Wu P, Chen GF, Li SH, Kuang SY, Feng L, Zhou XQ (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
Li Y, Hu H, Liu J, Yang P, Zhang Y, Ai Q, Xu W, Zhang W, Mai K (2017) Dietary soya allergen β-conglycinin induces intestinal inflammatory reactions, serum-specific antibody response and growth reduction in a carnivorous fish species, turbot Scophthalmus maximus L. Aquac Res 48:4022–4037
Liu C, Wang H, Cui Z, He X, Wang X, Zeng X, Ma H (2007) Optimization of extraction and isolation for 11S and 7S globulins of soybean seed storage protein. Food Chem 102:1310–1316
Luo J, Feng L, Jiang W, Liu Y, Wu P, Jiang J, Kuang S, Tang L, Zhang Y, Zhou X (2014) The impaired intestinal mucosal immune system by valine deficiency for young grass carp (Ctenopharyngodon idella) is associated with decreasing immune status and regulating tight junction proteins transcript abundance in the intestine. Fish Shellfish Immunol 40:197–207
Mokhtar DM, Abd-Elhafez EA, Hassan AH (2015) Light and scanning electron microscopic studies on the intestine of grass carp (Ctenopharyngodon idella): I-anterior intestine. J Aquacult Res Dev 6:374
Morales GA, Moyano FJ (2010) Application of an in vitro gastrointestinal model to evaluate nitrogen and phosphorus bioaccessibility and bioavailability in fish feed ingredients. Aquaculture 306:244–251
Morales GA, Moyano FJ, Marquez L (2011) In vitro assessment of the effects of phytate and phytase on nitrogen and phosphorus bioaccessibility within fish digestive tract. Anim Feed Sci Technol 170:209–221
Pauletti GM, Okumu FW, Borchardt RT (1997) Effect of size and charge on the passive diffusion of peptides across Caco-2 cell monolayers via the paracellular pathway. Pharm Res 14:164–168
Perez MD, Mills ENC, Lambert N, Johnson IT, Morgan MRA (2000) The use of anti-soya globulin antisera in investigating soya digestion in vivo. J Sci Food Agric 80:513–521
Rabinowitz JD, White E (2010) Autophagy and metabolism. Science 330:1344–1348
Rønnestad I, Thorsen A, Finn RN (1999) Fish larval nutrition: a review of recent advances in the roles of amino acids. Aquaculture 177:201–216
Santigosa E, Sánchez J, Médale F, Kaushik S, Pérez-Sánchez J, Gallardo MA (2008) Modifications of digestive enzymes in trout (Oncorhynchus mykiss) and sea bream (Sparus aurata) in response to dietary fish meal replacement by plant protein sources. Aquaculture 282:68–74
Stroband HWJ (1977) Growth and diet dependent structural adaptations of the digestive tract in juvenile grass carp (Ctenopharyngodon idella, Val.). J Fish Biol 11:167–174
Stroband HWJ, van der Veen FH (1981) Localization of protein absorption during transport of food in the intestine of the grass carp, Ctenopharyngodon idella (Val.). J Exp Zool 218:149–156
Stroband HWJ, van Deer MH, Timmermans LP (1979) Regional functional differentiation in the gut of the grasscarp, Ctenopharyngodon idella (Val.). Histochemistry 64:235–249
Tsukita S, Furuse M, Itoh M (2001) Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293
Van der Marel M, Propsting MJ, Battermann F, Jung-Schroers V, Hubner A, Rombout JHWM, Steinhagen D (2014) Differences between intestinal segments and soybean meal-induced changes in intestinal mucus composition of common carp Cyprinus carpio L. Aquac Nutr 20:12–24
Wang T, Qin G, Sun Z, Zhao Y (2014) Advances of research on glycinin and β-conglycinin: a review of two major soybean allergenic proteins. Crit Rev Food Sci 54:850–862
Wang T, Tan Z, Sun Z (2015) Low immunoreactive glycated soybean antigen proteins production: system-wide analysis of their immunogenicity. Food Agric Immunol 26:703–716
Wang K, Jiang W, Wu P, Liu Y, Jiang J, Kuang S, Tang L, Zhang Y, Zhou X, Feng L (2018) Gossypol reduced the intestinal amino acid absorption capacity of young grass carp (Ctenopharyngodon idella). Aquaculture 492:46–58
Wu G (2009) Amino acids: metabolism, functions, and nutrition. Amino Acids 37:1–17
Zeng YY, Jiang WD, Liu Y, Wu P, Zhao J, Jiang J, Kuang SY, Tang L, Tang WN, Zhang YA, Zhou XQ, Feng L (2016) Optimal dietary alpha-linolenic acid/linoleic acid ratio improved digestive and absorptive capacities and target of rapamycin gene expression of juvenile grass carp (Ctenopharyngodon idellus). Aquac Nutr 22:1251–1266
Zhang J, Guo L, Feng L, Jiang W, Kuang S, Liu Y, Hu K, Jiang J, Li S, Tang L, Zhou X (2013) Soybean β-conglycinin induces inflammation and oxidation and causes dysfunction of intestinal digestion and absorption in fish. PLoS One 8:e58115
Zhang Y, Duan X, Jiang W, Feng L, Wu P, Liu Y, Jiang J, Kuang S, Tang L, Tang W, Zhou X (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. https://doi.org/10.1007/s10695-019-00648-z
Zhao Y, Qin G, Sun Z, Zhang X, Bao N, Wang T, Zhang B, Zhang B, Zhu D, Sun L (2008) Disappearance of immunoreactive glycinin and beta-conglycinin in the digestive tract of piglets. Arch Anim Nutr 62:322–330
Acknowledgments
The authors would like to thank the personnel of the teams below for their kind assistance.
Funding
This research was financially supported by the National Natural Science Foundation of China (31672662), the National Key R&D Program of China (2018YFD0900400), the Earmarked Fund for China Agriculture Research System (CARS-45), the Outstanding Talents and Innovative Team of Agricultural Scientific Research (Ministry of Agriculture), the Foundation of Sichuan Youth Science and Technology Innovation Research Team (2017TD0002), the Key Research and Development Plan in Sichuan Province (2018NZ0007), and the Sichuan Science and Technology Program (2019YFN0036), and supported by the 111 project (D17015).
Author information
Authors and Affiliations
Corresponding author
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Duan, XD., Feng, L., Jiang, WD. et al. The dynamic process of dietary soybean β-conglycinin in digestion, absorption, and metabolism among different intestinal segments in grass carp (Ctenopharyngodon idella). Fish Physiol Biochem 46, 1361–1374 (2020). https://doi.org/10.1007/s10695-020-00794-9
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10695-020-00794-9