Temperature regulated nutrient sensing and metabolism of amino acids in juvenile turbot (Scophthalmus maximus L.)

Abstract

Temperature is well known as the major environmental factor that influences survival and growth of fish, which are poikilothermic animals. However, it is still unclear about the mechanism that underscores thermal-controlled fish physiology, especially nutritional utilization and metabolism, which are vitally important in aquaculture. In the present study, juvenile turbot was force-fed with amino acid mixture and its postprandial absorption, nutrient sensing and metabolism under low (12, 15 ℃), optimal (18 ℃) to high (21, 24 ℃) temperatures were explored. Intestinal trypsin and lipase activity were highly sensitive to water temperature, and highest under optimal temperatures for turbot, whereas amylase remained constant. Selective groups of intestinal amino acid transporters were upregulated in cold temperatures, but the amino acid absorption capability was increased with rising temperature. The mechanistic target of rapamycin (mTOR) signaling pathway was most active at optimal temperature. Postprandial muscle protein deposition achieved maximum level under optimal temperature. Amino acid catabolic enzymes branched-chain aminotransferase and branched-chain α-keto acid dehydrogenase activities were increased with rising temperatures. High temperature increased significantly energy metabolism and stimulated cellular stress in liver. These findings highlight the critical role of temperature in modulating amino acid dynamics, metabolic processes and stress responses in juvenile turbot, providing valuable insights for optimizing aquaculture practices.

Keywords

Temperature / Prandial amino acid dynamics / Protein deposition / mTOR / Metabolism

References

Amin M, Katersky Barnes R, Adams L. Effects of different protein and carbohydrate levels on growth performance and feed utilisation of brook trout, Salvelinus fontinalis (Mitchill, 1814), at two temperatures. J Appl Ichthyol, 2014, 30: 340-349

Attia ZI, Hegazi M, Younis EM. Effect of long-term thermal acclimation on enzymatic regulation of intermediary metabolism of Oreochromis aureus. Proc Icbs, 2004, 3: 959-975.

Bendiksen EA, Berg O, Jobling M, Arnesen A, Ma˚søval K, Digestibility, growth and nutrient utilisation of Atlantic salmon parr (Salmo salar L.) in relation to temperature, feed fat content and oil source. Aquaculture, 2003, 224: 283-299

Bian F, Jiang H, Man M, Mai K, Zhou H, Xu W, He G. Dietary gossypol suppressed postprandial TOR signaling and elevated ER stress pathways in turbot (Scophthalmus maximus L.). Am J Physiol-Endoc M, 2017, 312: E37-E47.

Bossi E, Cherubino F, Margheritis E, Oyadeyi A, Vollero A, Peres A. Temperature effects on the kinetic properties of the rabbit intestinal oligopeptide cotransporter PepT1. Pflug Arch Eur J Phy, 2012, 464: 183-191

Bowyer J, Qin J, Stone D. Protein, lipid and energy requirements of cultured marine fish in cold, temperate and warm water. Rev Aquacult, 2013, 5: 10-32

Bröer S, Fairweather SJ. Amino acid transport across the mammalian intestine. Compr Physiol, 2018, 9: 343-373

Burel C, Person-Le Ruyet J, Gaumet F, Le Roux A, Severe A, Boeuf G. Effects of temperature on growth and metabolism in juvenile turbot. J Fish Biol, 1996, 49: 678-692

Cai L, Wang L, Song K, Lu K, Zhang C, Rahimnejad S. Evaluation of protein requirement of spotted seabass (Lateolabrax maculatus) under two temperatures, and the liver transcriptome response to thermal stress. Aquaculture, 2020, 516: 734615.

Dado-Senn B, Skibiel AL, Dahl GE, Arriola Apelo SI, Laporta J. Dry period heat stress impacts mammary protein metabolism in the subsequent lactation. Animals-Basel, 2021, 11: 2676-2689

Dv D, Gislason H, Jvd H, Andersen KH. Global analysis of fish growth rates shows weaker responses to temperature than metabolic predictions. Global Ecol Biogeogr, 2020, 29: 2203-2213

Feidantsis K, Poertner H, Antonopoulou E, Michaelidis B. Synergistic effects of acute warming and low pH on cellular stress responses of the gilthead seabream Sparus aurata. J Comp Physiol B, 2015, 185: 185-205

Feidantsis K, Pörtner H, Vlachonikola E, Antonopoulou E, Michaelidis B. Seasonal changes in metabolism and cellular stress phenomena in the gilthead sea bream (Sparus aurata). Physiol Biochem Zool, 2018, 91: 878-895

Fraser K, Rogers A (2007) Protein metabolism in marine animals: The underlying mechanism of growth, in: Adv Mar Biol Academic Press, pp 267–362.

Fu L, Zhang L, Liu L, Yang H, Zhou P, Song F, Dong G, Chen J, Wang G, Dong X. Effect of heat stress on bovine mammary cellular metabolites and gene transcription related to amino acid metabolism, amino acid transportation and mammalian target of rapamycin (mTOR) signaling. Animals-Basel, 2021, 11: 3153-3169

Fuentes E, Björnsson B, Valdés J, Einarsdottir I, Lorca B, Alvarez M, Molina A. IGF-I/PI3K/Akt and IGF-I/MAPK/ERK pathways in vivo in skeletal muscle are regulated by nutrition and contribute to somatic growth in the fine flounder. Am J Physiol-Reg I, 2011, 300: R1532-R1542.

Geda F, Declercq AM, Remø SC, Waagbø R, Lourenço M, Janssens GP. The metabolic response in fish to mildly elevated water temperature relates to species-dependent muscular concentrations of imidazole compounds and free amino acids. J Therm Biol, 2017, 65: 57-63

Geffroy B, Wedekind C. Effects of global warming on sex ratios in fishes. J Fish Biol, 2020, 97: 596-606

Gracey AY (1996) Cold-adaptation of carp (Cyprinus carpio L.): lipid unsaturation and induced desaturase expression. The University of Liverpool (United Kingdom).

Guerreiro I, Enes P, Rodiles A, Merrifield D, Oliva-Teles A. Effects of rearing temperature and dietary short-chain fructooligosaccharides supplementation on allochthonous gut microbiota, digestive enzymes activities and intestine health of turbot (Scophthalmus maximus L.) juveniles. Aquacult Nutr, 2016, 22: 631-642

Hidalgo F, Alliot E. Influence of water temperature on protein requirement and protein utilization in juvenile sea bass, Dicentrarchus labrax. Aquaculture, 1988, 72: 115-129

Huang Z, Ma A, Xa W, Lei J, Li W, Wang T, Yang Z, Qu J. Interaction of temperature and salinity on the expression of immunity factors in different tissues of juvenile turbot Scophthalmus maximus based on response surface methodology. Chin J Oceanol Limn, 2015, 33: 28-36

Imsland A, Sunde L, Folkvord A, Stefansson S. The interaction of temperature and fish size on growth of juvenile turbot. J Fish Biol, 1996, 49: 926-940

Ince B, Thorpe A. The effects of starvation and force-feeding on the metabolism of the Northern pike, Esox lucius L. J Fish Biol, 1976, 8: 79-88

Kaloyianni M, Dimitriadi A, Ovezik M, Stamkopoulou D, Feidantsis K, Kastrinaki G, Gallios G, Tsiaoussis I, Koumoundouros G, Bobori D. Magnetite nanoparticles effects on adverse responses of aquatic and terrestrial animal models. J Hazard Mater, 2020, 383: 121204.

Katersky R, Carter C. High growth efficiency occurs over a wide temperature range for juvenile barramundi Lates calcarifer fed a balanced diet. Aquaculture, 2007, 272: 444-450

Kofuji P, Akimoto A, Hosokawa H, Masumoto T. Seasonal changes in proteolytic enzymes of yellowtail Seriola quinqueradiata (Temminck & Schlegel; Carangidae) fed extruded diets containing different protein and energy levels. Aquac Res, 2005, 36: 696-703

Liang Q, Ou M, Li Z, Ren Y, Wei W, Qiao X, Hu R, Wu X, Liu Y, Wang W. Functional analysis target of rapamycin (TOR) on the Penaeus vannamei in response to acute low temperature stress. Fish Shellfish Immun, 2020, 96: 53-61

Liang H, Xu H, Ge X, Zhu J, Ren M, Mi H. Water temperature affects the protein requirements, growth performance, and nutritional metabolism of grass carp (Ctenopharyngodon idella) juveniles. Aquacult Rep, 2022, 25: 101267.

Liu G, Sabatini D. mTOR at the nexus of nutrition, growth, ageing and disease. Nat Rev Mol Cell Bio, 2020, 21: 183-203

Liu C, Ding J, Gao X, Du C, Hou C, Wu X, Shen W, Zhu J. Effects of acute low temperature stress on the hormones and gene expression of glucocorticoid receptor of large yellow croaker Larimichthys crocea. J Therm Biol, 2021, 99: 103018.

Livak K, Schmittgen T. Analysis of relative gene expression data using real-time quantitative PCR and the 2− ΔΔCT method. Methods, 2001, 25: 402-408

Madeira D, Narciso L, Cabral H, Vinagre C, Diniz M. Influence of temperature in thermal and oxidative stress responses in estuarine fish. Comp Biochem Phys A, 2013, 166: 237-243

Miegel R, Pain S, Van Wettere W, Howarth G, Stone D. Effect of water temperature on gut transit time, digestive enzyme activity and nutrient digestibility in yellowtail kingfish (Seriola lalandi). Aquaculture, 2010, 308: 145-151

Murugan AK, Xu J, Strasburg GM, Reed KM, Velleman SG. Thermal stress affects proliferation and differentiation of turkey satellite cells through the mTOR/S6K pathway in a growth-dependent manner. PLoS ONE, 2022, 17: e0262576.

Nanba D, Sakabe J, Mosig J, Brouard M, Toki F, Shimokawa M, Kamiya M, Braschler T, Azzabi F, Droz-Georget Lathion S. Low temperature and mTOR inhibition favor stem cell maintenance in human keratinocyte cultures. Embo Rep, 2023, 24: e55439.

Neuheimer A, Thresher R, Lyle J, Semmens J. Tolerance limit for fish growth exceeded by warming waters. Nat Clim Change, 2011, 1: 110-113

Ohji G, Hidayat S, Nakashima A, Tokunaga C, Oshiro N, Yoshino K-i, Yokono K, Kikkawa U, Yonezawa K. Suppression of the mTOR-raptor signaling pathway by the inhibitor of heat shock protein 90 geldanamycin. J Biochem, 2006, 139: 129-135

Pörtner H. Oxygen-and capacity-limitation of thermal tolerance: a matrix for integrating climate-related stressor effects in marine ecosystems. J Exp Biol, 2010, 213: 881-893

Rizzello A, Romano A, Kottra G, Acierno R, Storelli C, Verri T, Daniel H, Maffia M. Protein cold adaptation strategy via a unique seven-amino acid domain in the icefish (Chionodraco hamatus) pept1 transporter. P Natl Acad Sci USA, 2013, 110: 7068-7073

Romano A, Barca A, Storelli C, Verri T. Teleost fish models in membrane transport research: the PEPT1(SLC15A1) H+–oligopeptide transporter as a case study. J Physiol, 2014, 592: 881-897

Skiba-Cassy S, Lansard M, Panserat S, Médale F. Rainbow trout genetically selected for greater muscle fat content display increased activation of liver TOR signaling and lipogenic gene expression. Am J Physiol-Reg I, 2009, 297: R1421-R1429.

Solovyev MM, Izvekova GI. Seasonal changes in pH values in the intestine of fish from Lake Chany (West Siberia). Inland Water Biol, 2016, 9: 400-404

Solovyev M, Kashinskaya E, Gisbert E. A meta-analysis for assessing the contributions of trypsin and chymotrypsin as the two major endoproteases in protein hydrolysis in fish intestine. Comp Biochem Phys A, 2023, 278: 111372.

Song F, Xu D, Mai K, Zhou H, Wang X, He G (2016) Comparative study on the cellular and systemic nutrient sensing and in termediary metabolism after partial replacement of fishmeal by meat an d bone meal in the diet of turbot (Scophthalmus maximus L.). PLoS ONE 11:e0165708

Sørensen M, Ljøkjel K, Storebakken T, Shearer K, Skredeb A. Apparent digestibility of protein, amino acids and energy in rainbow trout (Oncorhynchus mykiss) fed a fish meal based diet extruded at different temperatures. Aquaculture, 2001, 211: 215-225

Sui Z, Wei C, Wang X, Zhou H, Liu C, Mai K, He G. Nutrient sensing signaling and metabolic responses in shrimp Litopenaeus vannamei under acute ammonia stress. Ecotox Environ Safe, 2023, 253: 114672.

Sui Z, Wang X, Sun Y, Zhou H, Liu C, Mai K, He G. Methionine deficiency affects myogenesis and muscle macronutrient metabolism in juvenile turbot Scophthalmus maximus. Aquaculture, 2024, 578: 740013.

Sui Z, Wang N, Zhang X, Liu C, Wang X, Zhou H, Mai K, He G (2023a) Comprehensive study on the effect of dietary leucine supplementation on intestinal physiology, TOR signaling and microbiota in juvenile turbot (Scophthalmus maximus L.). Fish Shellfish Immun 141:109060

Sun Z, Tan X, Liu Q, Ye H, Zou C, Xu M, Zhang Y, Ye C. Physiological, immune responses and liver lipid metabolism of orange-spotted grouper (Epinephelus coioides) under cold stress. Aquaculture, 2019, 498: 545-555

Vinagre C, Madeira D, Narciso L, Cabral H, Diniz M. Effect of temperature on oxidative stress in fish: lipid peroxidation and catalase activity in the muscle of juvenile seabass, Dicentrarchus labrax. Ecol Indic, 2012, 23: 274-279

Volkoff H, Rønnestad I. Effects of temperature on feeding and digestive processes in fish. Temperature, 2020, 7: 307-320

Wang Y, Han G, Pham C, Koyanagi K, Song Y, Sudo R, Lauwereyns J, Cockrem J, Furuse M, Chowdhury V. An acute increase in water temperature can increase free amino acid concentrations in the blood, brain, liver, and muscle in goldfish (Carassius auratus). Fish Physiol Biochem, 2019, 45: 1343-1354

Wang N, Zhang X, Liu C, Wang X, Zhou H, Mai K, He G. Fine-tuning of postprandial responses via feeding frequency and leucine supplementation affects dietary performance in turbot (Scophthalmus maximus L.). J Nutr, 2021, 151: 2957-2966

Wang D, Tian Y, Wang Q, Zhang Y, Ye B, Zuo Z, He J, Pan Z, Sun D, Zou J. Cold stress-induced autophagy and apoptosis disorders are mainly mediated by AMPK/PPAR/PI3K/AKT/mTOR pathways. Aquaculture, 2024, 583: 740574.

Wu X, Chen J, Liu C, Wang X, Zhou H, Mai K, He G. Slc38a9 deficiency induces apoptosis and metabolic dysregulation and leads to premature death in zebrafish. Int J Mol Sci, 2022, 23: 4200

Xing S, Liang X, Zhang X, Oliva-Teles A, Peres H, Li M, Wang H, Mai K, Kaushik S, Xue M. Essential amino acid requirements of fish and crustaceans, a meta-analysis. Rev Aquacult, 2024, 16: 1069-1086

Xu D, He G, Mai K, Zhou H, Wang X, Song F. Postprandial nutrient-sensing and metabolic responses after partial dietary fishmeal replacement by soyabean meal in turbot (Scophthalmus maximus L.). Brit J Nutr, 2016, 115: 379-388

Xu D, He G, Mai K, Zhou H, Xu W, Song F. Expression pattern of peptide and amino acid genes in digestive tract of transporter juvenile turbot (Scophthalmus maximus L.). J Ocean U China, 2016, 15: 334-340

Yuan D, Wang H, Liu X, Wang S, Shi J, Cheng X, Gu H, Xiao S, Wang Z. High temperature induced metabolic reprogramming and lipid remodeling in a high-altitude fish species. Triplophysa Bleekeri Front Mar Sci, 2022, 9: 1017142

Zhao X, Mao W, Lin Z, Ling Q. Heat stress induced hepatocyte apoptosis in largemouth bass Micropterus salmoides via IRE1α/TRAF2/ASK1/JNK pathway. J Oceanol Limnol, 2024, 42: 988-1000