Effects of dietary chenodeoxycholic acid supplementation in a low fishmeal diet on growth performance, lipid metabolism, autophagy and intestinal health of Pacific white shrimp, Litopenaeus vannamei

Salin, 2018 Viola, 1982, Partial and complete replacement of fishmeal by soybean meal in feeds for intensive culture of carp, Aquaculture, 26, 223, 10.1016/0044-8486(82)90158-2 To, 2021, Taurine supplementation enhances the replacement level of fishmeal by soybean concentrate in diets of juvenile Pacific white shrimp (Litopenaeus vannamei Boone, 1931), Aquacult. Res., 52, 3771, 10.1111/are.15222 Song, 2022, Effects of fermented soybean meal and guanosine 5'-monophosphate on growth, intestinal health and anti-stress capability of Penaeus vannamei in low fish meal diet, Aquaculture, 548, 10.1016/j.aquaculture.2021.737591 Lusas, 1995, Soy protein products: processing and use, J. Nutr., 125, 573S Deng, 2006, Effects of replacing fish meal with soy protein concentrate on feed intake and growth of juvenile Japanese flounder, Paralichthys olivaceus, Aquaculture, 258, 503, 10.1016/j.aquaculture.2006.04.004 Morr, 1991, Processing to prevent formation of off-flavors in soy products, Comments Agric, Food Chem., 2, 247 Chen, 2017, The effects of dietary fructooligosaccharide on growth, intestinal short chain fatty acids level and hepatopancreatic condition of the giant freshwater prawn (Macrobrachium rosenbergii) post-larvae, Aquaculture, 469, 95, 10.1016/j.aquaculture.2016.11.034 Chiang, 2013, Bile acid metabolism and signaling, Compr. Physiol., 3, 1191, 10.1002/cphy.c120023 Chiang, 1998, Regulation of bile acid synthesis, Front. Biosci., 3, d176, 10.2741/A273 Goto, 1996, Bile salt composition and distribution of the D-cysteinolic acid conjugated bile salts in fish, Fish. Sci., 62, 606, 10.2331/fishsci.62.606 Kong, 2020, Physiological function of bile acid and its effect on aquatic animals Chinese, J. Anim. Sci., 56, 10 Fan, 2015, Bile acid signaling and liver regeneration, Biochim. Biophys. Acta. Gene Regul. Mech., 1849, 196, 10.1016/j.bbagrm.2014.05.021 Song, 2021, Dietary chenodeoxycholic acid improves growth performance and intestinal health by altering serum metabolic profiles and gut bacteria in weaned piglets, Anim. Nutr., 7, 365, 10.1016/j.aninu.2020.07.011 Baijal, 1998, Modulation of colonic xenobiotic metabolizing enzymes by feeding bile acids: comparative effects of cholic, deoxycholic, lithocholic and ursodeoxycholic acids, Food Chem. Toxicol., 36, 601, 10.1016/S0278-6915(98)00020-9 Lester, 1975, Crustacean intestinal detergent promotes sterol solubilization, Science, 189, 1098, 10.1126/science.1162360 Su, 2021, Effects of bile acids on the growth performance, lipid metabolism, non‐specific immunity and intestinal microbiota of Pacific white shrimp (Litopenaeus vannamei), Aquacult. Nutr., 27, 2029, 10.1111/anu.13338 Xie, 2021, Dietary supplementation of chenodeoxycholic acid improved the growth performance, immune response and intestinal health of juvenile Penaeus monodon fed a low fish-meal diet, Aquacult. Rep., 20 Peng, 2019, Supplementation exogenous bile acid improved growth and intestinal immune function associated with NF-κB and TOR signalling pathways in on-growing grass carp (Ctenopharyngodon idella): enhancement the effect of protein-sparing by dietary lipid, Fish Shellfish Immunol., 92, 552, 10.1016/j.fsi.2019.06.047 Yin, 2021, Dietary supplementation of bile acid attenuate adverse effects of high-fat diet on growth performance, antioxidant ability, lipid accumulation and intestinal health in juvenile largemouth bass (Micropterus salmoides), Aquaculture, 531, 10.1016/j.aquaculture.2020.735864 Maita, 1996, Pharmacological effect of Ursodeoxycholic acid in juvenile eel (short paper), Nihon Suisan Gakkai-Shi, 62, 129, 10.2331/suisan.62.129 Xie, 2014, Effect of glycine supplementation on growth performance, body composition and salinity stress of juvenile Pacific white shrimp, Litopenaeus vannamei fed low fishmeal diet, Aquaculture, 418, 159, 10.1016/j.aquaculture.2013.10.023 Xie, 2015, Effect of proline supplementation on anti-oxidative capacity, immune response and stress tolerance of juvenile Pacific white shrimp, Litopenaeus vannamei, Aquaculture, 448, 105, 10.1016/j.aquaculture.2015.05.040 Horwitz, 2005, vol. 45, 75 Chen, 2021, Replacement of fish meal with Methanotroph (Methylococcus capsulatus, Bath) bacteria meal in the diets of Pacific white shrimp (Litopenaeus vannamei), Aquaculture, 541, 10.1016/j.aquaculture.2021.736801 Livak, 2001, Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method, Methods, 25, 402, 10.1006/meth.2001.1262 Lim, 1990, Evaluation of soybean meal as a replacement for marine animal protein in diets for shrimp (Penaeus vannamei), Aquaculture, 87, 53, 10.1016/0044-8486(90)90210-E Sá, 2013, Dietary concentration of marine oil affects replacement of fish meal by soy protein concentrate in practical diets for the white shrimp, L itopenaeus vannamei, Aquacult. Nutr., 19, 199, 10.1111/j.1365-2095.2012.00954.x Sookying, 2012, Use of soy protein concentrate in practical diets for Pacific white shrimp (Litopenaeus vannamei) reared under field conditions, Aquacult. Int., 20, 357, 10.1007/s10499-011-9464-6 Paripatananont, 2001, Substitution of soy protein concentrate for fishmeal in diets of tiger shrimp Penaeus monodon, Aquacult. Res., 32, 369, 10.1046/j.1355-557x.2001.00045.x Amaya, 2007, Alternative diets for the Pacific white shrimp Litopenaeus vannamei, Aquaculture, 262, 419, 10.1016/j.aquaculture.2006.11.001 Cruz-Suárez, 2009, Apparent dry matter, energy, protein and amino acid digestibility of four soybean ingredients in white shrimp Litopenaeus vannamei juveniles, Aquaculture, 292, 87, 10.1016/j.aquaculture.2009.03.026 Ray, 2020, Effects of replacing fishmeal with dietary soybean protein concentrate (SPC) on growth, serum biochemical indices, and antioxidative functions for juvenile shrimp Litopenaeus vannamei, Aquaculture, 516, 10.1016/j.aquaculture.2019.734630 Richard, 2011, Availability of essential amino acids, nutrient utilisation and growth in juvenile black tiger shrimp, Penaeus monodon, following fishmeal replacement by plant protein, Aquaculture, 322–323, 109, 10.1016/j.aquaculture.2011.09.032 Rahimnejad, 2018, Chitooligosaccharide supplementation in low-fish meal diets for Pacific white shrimp (Litopenaeus vannamei): effects on growth, innate immunity, gut histology, and immune-related genes expression, Fish Shellfish Immunol., 80, 405, 10.1016/j.fsi.2018.06.025 Xie, 2016, Partial replacement of fish-meal by soy protein concentrate and soybean meal based protein blend for juvenile Pacific white shrimp, Litopenaeus vannamei, Aquaculture, 464, 296, 10.1016/j.aquaculture.2016.07.002 Xie Jinghong, 2013, Effcets of Vibrio alginolyticus peptidoglycan on astaxanthin level, immune indicators and protection in Litopenaeus vannamei, J. Guangdong. Ocean Univ., 33, 50 Gui, 2019, Effects of yeast culture on growth performance, hematological parameters, immunity and disease resistance of Litopenaeus vannamei, J. Guangdong. Ocean Univ., 39, 30 Zhang, 2018, Effects of replacing fish meal with high-protein cottonseed meal on growth performance, non-specific immune index and disease resistance for Litopenaeus vannamei, J. Guangdong. Ocean Univ., 38, 20 Yanyan, 2015, Effects of microcystin on activities of immune enzymes in the white shrimp Litopenaeus vannamei, J. Guangdong. Ocean Univ., 35, 35 Gaweł, 2004, Malondialdehyde (MDA) as a lipid peroxidation marker, Wiad. Lek., 57, 453 Yuancai, 2021, Effects of dietary small peptides on growth, antioxidant capacity, nonspecific immunity and ingut microflora structure of Litopenaeus vannamei, J. Guangdong. Ocean Univ., 41, 1 Ji, 2017, The effects of partial replacement of white fish meal by poultry by-product meal and addition of bile acid in feed on growth, digestibility, and serum enzyme activities of the Chinese soft-shelled turtle, Fish. Sci., 83, 83, 10.1007/s12562-016-1032-6 Hou, 2019, Effects of chromium yeast, tributyrin and bile acid on growth performance, digestion and metabolism of Channa argus, Aquacult. Res., 50, 836, 10.1111/are.13954 Tassanakajon, 2013, Discovery of immune molecules and their crucial functions in shrimp immunity, Fish Shellfish Immunol., 34, 954, 10.1016/j.fsi.2012.09.021 Wang, 2009, An immune deficiency homolog from the white shrimp, Litopenaeus vannamei, activates antimicrobial peptide genes, Mol. Immunol., 46, 1897, 10.1016/j.molimm.2009.01.005 Zuo, 2020, A MicroRNA-1–mediated inhibition of the NF-κB pathway by the JAK-STAT pathway in the invertebrate Litopenaeus vannamei, J. Immunol., 204, 2918, 10.4049/jimmunol.2000071 Huang, 2021, Innate immune responses against viral pathogens in Macrobrachium, Dev. Comp. Immunol., 117, 10.1016/j.dci.2020.103966 Sigang, 2022, Characterization and expression of inhibitor-κB kinase epsilon 2 in Marsupenaeus japonicus, J. Guangdong. Ocean Univ., 42, 13 Hu, 2012, Effect of chenodeoxycholic acid on fibrosis, inflammation and oxidative stress in kidney in high-fructose-fed Wistar rats, Kidney Blood Press. Res., 36, 85, 10.1159/000341485 Du, 2018, Molecular cloning and characterization of farnesoid X receptor from large yellow croaker (Larimichthys crocea) and the effect of dietary CDCA on the expression of inflammatory genes in intestine and spleen, Comp. Biochem. Physiol. B Biochem. Mol. Biol., 216, 10, 10.1016/j.cbpb.2017.09.007 Gadaleta, 2011, Farnesoid X receptor activation inhibits inflammation and preserves the intestinal barrier in inflammatory bowel disease, Gut, 60, 463, 10.1136/gut.2010.212159 Kumar, 2020, Bile acid and bile acid transporters are involved in the pathogenesis of acute hepatopancreatic necrosis disease in white shrimp Litopenaeus vannamei, Cell Microbiol., 22, 10.1111/cmi.13127 Swatson, 2002, Effect of dietary protein level, amino acid balance and feeding level on growth, gastrointestinal tract, and mucosal structure of the small intestine in broiler chickens, Anim. Res., 51, 501, 10.1051/animres:2002038 Amoah, 2019, Dietary supplementation of probiotic Bacillus coagulans ATCC 7050, improves the growth performance, intestinal morphology, microflora, immune response, and disease confrontation of Pacific white shrimp, Litopenaeus vannamei, Fish Shellfish Immunol., 87, 796, 10.1016/j.fsi.2019.02.029 Chen, 2021, Evaluation of the dietary black soldier fly larvae meal (Hermetia illucens) on growth performance, intestinal health, and disease resistance to Vibrio parahaemolyticus of the pacific white shrimp (Litopenaeus vannamei), Front. Mar. Sci., 1072 Xie, 2020, Low dietary fish meal induced endoplasmic reticulum stress and impaired phospholipids metabolism in juvenile pacific white shrimp, Litopenaeus vannamei, Front. Physiol., 1024, 10.3389/fphys.2020.01024 Cui, 2019, Untargeted LC-MS-based metabonomics revealed that aristolochic acid I induces testicular toxicity by inhibiting amino acids metabolism, glucose metabolism, β-oxidation of fatty acids and the TCA cycle in male mice, Toxicol. Appl. Pharmacol., 373, 26, 10.1016/j.taap.2019.04.014 Orrenius, 2007, Mitochondrial oxidative stress: implications for cell death, Annu. Rev. Pharmacol. Toxicol., 47, 143, 10.1146/annurev.pharmtox.47.120505.105122 Zhu, 2020, The effects of substituting fish meal with soy protein concentrate on growth performance, antioxidant capacity and intestinal histology in juvenile golden crucian carp, Cyprinus carpio × Carassius auratus, Aquacult. Rep., 18 Ribeiro, 2015, Effect of vegetable based diets on growth, intestinal morphology, activity of intestinal enzymes and haematological stress indicators in meagre (Argyrosomus regius), Aquaculture, 447, 116, 10.1016/j.aquaculture.2014.12.017 Zhang, 2022, Dietary bile acids reduce liver lipid deposition via activating farnesoid X receptor, and improve gut health by regulating gut microbiota in Chinese perch (Siniperca chuatsi), Fish Shellfish Immunol., 121, 265, 10.1016/j.fsi.2022.01.010 Yamamoto, 2007, Supplemental effect of bile salts to soybean meal-based diet on growth and feed utilization of rainbow trout Oncorhynchus mykiss, Fish. Sci., 73, 123, 10.1111/j.1444-2906.2007.01310.x Sang, 2010, Effects of mannan oligosaccharide dietary supplementation on performances of the tropical spiny lobsters juvenile (Panulirus ornatus, Fabricius 1798), Fish Shellfish Immunol., 28, 483, 10.1016/j.fsi.2009.12.011 Li, 2022, Effects of Clostridium butyricum on growth, antioxidant capacity and non-specific immunology of Litopenaeus vannamei fed with concentrated cottonseed protein replacement of fishmeal, J. Guangdong. Ocean Univ., 42, 29 Yin, 2018, Cottonseed protein concentrate (CPC) suppresses immune function in different intestinal segments of hybrid grouper ♀Epinephelus fuscoguttatus×♂Epinephelus lanceolatu via TLR-2/MyD88 signaling pathways, Fish Shellfish Immunol., 81, 318, 10.1016/j.fsi.2018.07.038 Wu, 2008, Histopathological and biochemical evidence of hepatopancreatic toxicity caused by cadmium and zinc in the white shrimp, Litopenaeus vannamei, Chemosphere, 73, 1019, 10.1016/j.chemosphere.2008.08.019 Bhavan, 2000, Histopathology of the hepatopancreas and gills of the prawn Macrobrachium malcolmsonii exposed to endosulfan, Aquat. Toxicol., 50, 331, 10.1016/S0166-445X(00)00096-5 Song, 2019, Chenodeoxycholic acid (CDCA) protects against the lipopolysaccharide-induced impairment of the intestinal epithelial barrier function via the FXR-MLCK pathway, J. Agric. Food Chem., 67, 8868, 10.1021/acs.jafc.9b03173 Gu, 2017, Taurocholate supplementation attenuates the changes in growth performance, feed utilization, lipid digestion, liver abnormality and sterol metabolism in turbot (Scophthalmus maximus) fed high level of plant protein, Aquaculture, 468, 597, 10.1016/j.aquaculture.2016.11.022 Yao, 2021, Tolerance assessment of dietary bile acids in common carp (Cyprinus carpio L.) fed a high plant protein diet, Aquaculture, 543, 10.1016/j.aquaculture.2021.737012 Chiang, 2021, Bile acid metabolism and bile acid receptor signaling in metabolic diseases and therapy, Liver Res., 5, 103, 10.1016/j.livres.2021.08.002 Wendelaar Bonga, 1997, The stress response in fish, Physiol. Rev., 77, 591, 10.1152/physrev.1997.77.3.591 Xian, 2021 Chen, 2021, Effect of black soldier fly (Hermetia illucens) larvae meal on lipid and glucose metabolism of Pacific white shrimp Litopenaeus vannamei, Br. J. Nutr., 1 Yang, 2011, Identification of fatty acid synthase from the Pacific white shrimp, Litopenaeus vannamei and its specific expression profiles during white spot syndrome virus infection, Fish Shellfish Immunol., 30, 744, 10.1016/j.fsi.2010.12.026 Ayisi, 2018, Genes, transcription factors and enzymes involved in lipid metabolism in fin fish, Agri Gene, 7, 7, 10.1016/j.aggene.2017.09.006 Eberlé, 2004, SREBP transcription factors: master regulators of lipid homeostasis, Biochimie, 86, 839, 10.1016/j.biochi.2004.09.018 Xuan, 2022, Preparation of lipid-modified hydrolyzed acylglycerol from tuna oil catalyzed by selective lipase, J. Guangdong. Ocean Univ., 42, 104 Jiang, 2018, Preliminary study to evaluate the effects of dietary bile acids on growth performance and lipid metabolism of juvenile genetically improved farmed tilapia (Oreochromis niloticus) fed plant ingredient‐based diets, Aquacult. Nutr., 24, 1175, 10.1111/anu.12656 Luo, 2020, Mechanisms and regulation of cholesterol homeostasis, Nat. Rev. Mol. Cell Biol., 21, 225, 10.1038/s41580-019-0190-7 Romano, 2020, Bile acid metabolism in fish: disturbances caused by fishmeal alternatives and some mitigating effects from dietary bile inclusions, Rev. Aquacult., 12, 1792, 10.1111/raq.12410 Qiang, 2016, Effects of dietary cholesterol level on growth performance, blood biochemical parameters and lipid metabolism of juvenile Cobia(Rachycentron canadum), J. Guangdong. Ocean Univ., 36, 35 Hosomi, 2011, Fish protein decreases serum cholesterol in rats by inhibition of cholesterol and bile acid absorption, J. Food Sci., 76, H116, 10.1111/j.1750-3841.2011.02130.x Nagata, 1982, Studies on the mechanism of antihypercholesterolemic action of soy protein and soy protein-type amino acid mixtures in relation to the casein counterparts in rats, J. Nutr., 112, 1614, 10.1093/jn/112.8.1614 Di Ciaula, 2018, Bile acid physiology, Ann. Hepatol., 16, 4 Runjia, 2021, Effects of low temperature stress on physiology and biochemistry of lipid metabolism of juvenile Cobia, Rachycentron canadum, J. Guangdong. Ocean Univ., 41, 123 Wan, 2018, The effect of replacement of fishmeal by concentrated dephenolization cottonseed protein on the growth, body composition, haemolymph indexes and haematological enzyme activities of the Pacific white shrimp (Litopenaeus vannamei), Aquacult. Nutr., 24, 1845, 10.1111/anu.12823 Tamura, 2005, Contribution of adipose tissue and de novo lipogenesis to nonalcoholic fatty liver disease, J. Clin. Investig., 115, 1139, 10.1172/JCI24930 Yun, 2011, Effects of dietary cholesterol on growth performance, feed intake and cholesterol metabolism in juvenile turbot (Scophthalmus maximus L.) fed high plant protein diets, Aquaculture, 319, 105, 10.1016/j.aquaculture.2011.06.028 Su, 2022, Interactive effects of dietary cholesterol and bile acids on the growth, lipid metabolism, immune response and intestinal microbiota of Litopenaeus vannamei: sparing effect of bile acids on cholesterol in shrimp diets, Aquaculture, 547, 10.1016/j.aquaculture.2021.737412 Mandimika, 2012, Effects of dietary broccoli fibre and corn oil on serum lipids, faecal bile acid excretion and hepatic gene expression in rats, Food Chem., 131, 1272, 10.1016/j.foodchem.2011.09.117 Schmitt, 2015, Protective effects of farnesoid X receptor (FXR) on hepatic lipid accumulation are mediated by hepatic FXR and independent of intestinal FGF15 signal, Liver Int., 35, 1133, 10.1111/liv.12456 Adewuyi, 2005, Non esterified fatty acids (NEFA) in dairy cattle, Rev. Vet. Q., 27, 117, 10.1080/01652176.2005.9695192 Roy, 2010, Effects of supplemental exogenous emulsifier on performance, nutrient metabolism, and serum lipid profile in broiler chickens, Vet. Med. Int., 2010 Dai, 2018, Chemoproteomics reveals baicalin activates hepatic CPT1 to ameliorate diet-induced obesity and hepatic steatosis, Proc. Natl. Acad. Sci. USA, 115, E5896, 10.1073/pnas.1801745115 Zhou, 2019, Effects of berberine on growth, liver histology, and expression of lipid-related genes in blunt snout bream (Megalobrama amblycephala) fed high-fat diets, Fish Physiol. Biochem., 45, 83, 10.1007/s10695-018-0536-7 Jin, 2019, Effects of supplemental dietary l-carnitine and bile acids on growth performance, antioxidant and immune ability, histopathological changes and inflammatory response in juvenile black seabream (Acanthopagrus schlegelii) fed high-fat diet, Aquaculture, 504, 199, 10.1016/j.aquaculture.2019.01.063 Liu, 2018, Mechanistic target of rapamycin inhibition with rapamycin induces autophagy and correlative regulation in white shrimp (Litopenaeus vannamei), Aquacult. Nutr., 24, 1509, 10.1111/anu.12688 Hosokawa, 2009, Atg101, a novel mammalian autophagy protein interacting with Atg13, Autophagy, 5, 973, 10.4161/auto.5.7.9296 Kabeya, 2005, Atg17 functions in cooperation with Atg1 and Atg13 in yeast autophagy, Mol. Biol. Cell, 16, 2544, 10.1091/mbc.e04-08-0669 Radoshevich, 2010, ATG12 conjugation to ATG3 regulates mitochondrial homeostasis and cell death, Cell, 142, 590, 10.1016/j.cell.2010.07.018 Shi, 2021, Dietary copper improves growth and regulates energy generation by mediating lipolysis and autophagy in hepatopancreas of Pacific white shrimp (Litopenaeus vannamei), Aquaculture, 537, 10.1016/j.aquaculture.2021.736505 Carino, 2021, The bile acid activated receptors GPBAR1 and FXR exert antagonistic effects on autophagy, Faseb. J., 35, 10.1096/fj.202001386R Panzitt, 2021, Regulation of autophagy by bile acids and in cholestasis-CholestoPHAGY or CholeSTOPagy, Biochim. Biophys. Acta (BBA) - Mol. Basis Dis., 1867, 10.1016/j.bbadis.2020.166017 Seok, 2014, Transcriptional regulation of autophagy by an FXR–CREB axis, Nature, 516, 108, 10.1038/nature13949 Song, 2010, Effects of antibacterial peptide on growth and immunity of Penaeus vannamei, J. Guangdong. Ocean Univ., 30, 28 Shi, 2008, MyD88 and Trif target Beclin 1 to trigger autophagy in macrophages, J. Biol. Chem., 283, 33175, 10.1074/jbc.M804478200