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Effects of dietary protein intake on the oxidation of glutamate, glutamine, glucose and palmitate in tissues of largemouth bass (Micropterus salmoides)

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Abstract

Largemouth bass (Micropterus salmoides, a carnivorous fish native to North America) prefers to utilize amino acids as energy sources rather than glucose and fatty acids. However, little is known about the nutritional regulation of substrate oxidation in the fish. Therefore, this study was conducted to determine whether the oxidation of glutamate, glutamine, glucose and palmitate in its tissues might be influenced by dietary protein intake. Juvenile largemouth bass (initial weight 18.3 ± 0.1 g) were fed three isocaloric diets containing 40%, 45% and 50% protein for 8 weeks. The growth performance, energy retention, and lipid retention of juvenile fish increased with increasing dietary protein levels. The rate of oxidation of glutamate by the intestine was much greater than that of glutamine, explaining why increasing the dietary protein content from 40% to 50% had no effect on the serum concentration of glutamate but increased that of glutamine in the fish. The liver of fish fed the 50% protein diet had a higher (P < 0.05) rate of glutamine oxidation than that in the 40% and 45% protein groups. In contrast, augmenting dietary protein content from 40% to 45% increased (P < 0.05) both glutamine and glutamate oxidation in the proximal intestine of the fish and renal glutamine oxidation, without changes in intestinal or renal AA oxidation between the 45% and 50% protein groups. Furthermore, the rates of glucose oxidation in the liver, kidney, and intestine of largemouth bass were decreased in response to an  increase in dietary  protein content   from 40% to 45% and a concomitant decrease in dietary starch content from 22.3% to 15.78%, but did not differ between the 45% and 50% protein groups.   The rates of oxidation of glucose in skeletal muscle and those of palmitate in all tissues (except for the  kidney) were not affected by the diets. Collectively, these results indicate that the largemouth bass can regulate substrate metabolism in a  tissue-specific manner to favor protein and lipid gains as dietary protein content increases from 40% to 50% and have a lower ability to oxidize fatty acids and glucose than amino acids regardless of the dietary protein intake. 

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Abbreviations

ALT:

Alanine transaminase

AST:

Aspartate transaminase

CP:

Crude protein

FCR:

Feed conversion ratio

FI:

Feed intake

HK:

Hexokinase

PK:

Pyruvate kinase

GK:

Glucokinase

GLUT:

Glucose transporter

LMB:

Largemouth bass

WG:

Weight gain

References

  • Abdel-Tawwab M, Ahmad MH, Khattab YA, Shalaby AM (2010) Effect of dietary protein level, initial body weight, and their interaction on the growth, feed utilization, and physiological alterations of Nile tilapia, Oreochromis niloticus (L.). Aquaculture 298:267–274

    CAS  Google Scholar 

  • Amoah A, Coyle SD, Webster CD, Durborow RM, Bright LA, Tidwell JH (2008) Effects of graded levels of carbohydrate on growth and survival of largemouth bass, Micropterus salmoides. J World Aquac Soc 39:397–405

    Google Scholar 

  • Anderson RJ, Kienholz EW, Flickinger SA (1981) Protein requirements of smallmouth bass and largemouth bass. J Nutr 111:1085–1097

    CAS  PubMed  Google Scholar 

  • Antony Jesu Prabhu P, Schrama JW, Kaushik SJ (2013) Quantifying dietary phosphorus requirement of fish—a meta-analytic approach. Aquac Nutr 19:233–249

    CAS  Google Scholar 

  • Ballantyne JS (2001) Amino acid metabolism. Fish Physiol 20:77–107

    CAS  Google Scholar 

  • Beaumont M, Blachier F (2020) Amino acids in intestinal physiology and health. Adv Exp Med Biol 1265:1–20

    PubMed  Google Scholar 

  • Capilla E, Díaz M, Albalat A, Navarro I, Pessin JE, Keller K, Planas JV (2004) Functional characterization of an insulin-responsive glucose transporter (GLUT4) from fish adipose tissue. Am J Physiol 287:348–357

    Google Scholar 

  • Chen YJ, Zhang TY, Chen HY, Lin SM, Luo L, Wang DS (2017) Simultaneous stimulation of glycolysis and gluconeogenesis by feeding in the anterior intestine of the omnivorous GIFT tilapia, Oreochromis niloticus. Biol Open 6:818–824

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cheng CR, Wang JT, Han T, Li XY, Jiang YD, Wen XB (2016) Effects of different dietary amino acid patterns on growth performance and body composition of juvenile giant croaker Nibea japonica. Aquac Res 47:3942–3951

    CAS  Google Scholar 

  • Clark TC, Tinsley J, Sigholt T, Macqueen DJ, Martin SAM (2020) Supplementation of arginine, ornithine and citrulline in rainbow trout (Oncorhynchus mykiss): effects on growth, amino acid levels in plasma and gene expression responses in liver tissue. Comp Biochem Physiol A 241:110632

    CAS  Google Scholar 

  • Collins JK, Wu G, Perkins-Veazie P, Spears K, Claypool PL, Baker RA, Clevidence BA (2007) Watermelon consumption increases plasma arginine concentrations in adults. Nutrition 23:261–266

    CAS  PubMed  Google Scholar 

  • Costas B, Conceição LE, Aragão C, Martos JA, Ruiz-Jarabo I, Mancera JM, Afonso A (2011) Physiological responses of Senegalese sole (Solea senegalensis Kaup, 1858) after stress challenge: effects on non-specific immune parameters, plasma free amino acids and energy metabolism. Aquaculture 316:68–76

    CAS  Google Scholar 

  • Cowey CB, Sargent JR (1977) Lipid nutrition in fish. Comp Biochem Physiol B 57:269–273

    CAS  Google Scholar 

  • Díaz M, Antonescu CN, Capilla E, Klip A, Planas JV (2007) Fish glucose transporter (GLUT)-4 differs from rat GLUT4 in its traffic characteristics but can translocate to the cell surface in response to insulin in skeletal muscle cells. Endocrinology 148:5248–5257

    PubMed  Google Scholar 

  • Enes P, Panserat S, Kaushik S, Oliva-Teles A (2006) Effect of normal and waxy maize starch on growth, food utilization and hepatic glucose metabolism in European sea bass (Dicentrarchus labrax) juveniles. Comp Biochem Physiol A 143:89–96

    CAS  Google Scholar 

  • Erfanullah, Jafri AK (1995) Protein sparing effect of dietary carbohydrate in diets for fingerlings Labeo rohita. Aquaculture 136:331–339

    CAS  Google Scholar 

  • Fauzi IA, Haga Y, Kondo H, Hirono I, Satoh S (2019) Effects of arginine supplementation on growth performance and plasma arginine, ornithine and citrulline dynamics of rainbow trout, Oncorhynchus mykiss. Aquac Res 50:1277–1290

    CAS  Google Scholar 

  • Fernández F, Miquel AG, Córdoba M, Varas M, Metón I, Caseras A, Baanante IV (2007) Effects of diets with distinct protein-to-carbohydrate ratios on nutrient digestibility, growth performance, body composition and liver intermediary enzyme activities in gilthead sea bream (Sparus aurata L.) fingerlings. J Exp Mar Biol Ecol 343:1–10

    Google Scholar 

  • Folch J, Lees M, Sloane-Stanley G (1957) A simple method for the isolation and purification of total lipids from animal tissues. J Biol Chem 226:497–509

    CAS  PubMed  Google Scholar 

  • Fu WJ, Haynes TE, Kohli R, Hu J, Shi W, Spencer TE, Carroll RJ, Meininger CJ, Wu G (2005) Dietary l-arginine supplementation reduces fat mass in Zucker diabetic fatty rats. J Nutr 135:714–721

    CAS  PubMed  Google Scholar 

  • Kaushik SJ, Seiliez I (2010) Protein and amino acid nutrition and metabolism in fish: current knowledge and future needs. Aquac Res 41:322–332

    CAS  Google Scholar 

  • Hemre GI, Mommsen TP, Krogdahl Å (2002) Carbohydrates in fish nutrition: effects on growth, glucose metabolism and hepatic enzymes. Aquac Nutr 8:175–194

    CAS  Google Scholar 

  • Hou YQ, He WL, Hu SD, Wu G (2019) Composition of polyamines and amino acids in plant-source foods for human consumption. Amino Acids 51:1153–1165

    CAS  PubMed  Google Scholar 

  • Huang D, Wu Y, Lin Y, Chen J, Karrow N, Ren X, Wang Y (2017) Dietary protein and lipid requirements for juvenile largemouth bass, Micropterus salmoides. J World Aquac Soc 48:782–790

    CAS  Google Scholar 

  • Jia SC, Li XY, Zheng SX, Wu YW (2017) Amino acids are major energy substrates for tissues of hybrid striped bass and zebrafish. Amino Acids 49:1–11

    Google Scholar 

  • Kamalam BS, Medale F, Panserat S (2017) Utilization of dietary carbohydrates in farmed fishes: new insights on influencing factors, biological limitations and future strategies. Aquaculture 467:3–27

    CAS  Google Scholar 

  • Kim KI, Grimshaw TW, Kayes TB, Amundson CH (1992) Effect of fasting or feeding diets containing different levels of protein or amino acids on the activities of the liver amino acid-degrading enzymes and amino acid oxidation in rainbow trout (Oncorhynchus mykiss). Aquaculture 107:89–105

    CAS  Google Scholar 

  • Kultz D, Jurss K (1993) Biochemical characterization of isolated branchial mitochondria-rich cells of Oreochromis mossambicus acclimated to fresh water or hypersaline sea water. J Comp Physiol 163B:406–412

    Google Scholar 

  • Li XY, Wu G (2019) Oxidation of energy substrates in tissues of Largemouth bass (Micropterus salmoides). J Anim Sci 97:68–69

    PubMed Central  Google Scholar 

  • Li P, Wu G (2020) Composition of amino acids and related nitrogenous nutrients in feedstuffs for animal diets. Amino Acids 52:523–542

    CAS  PubMed  Google Scholar 

  • Li XL, Rezaei R, Li P, Wu G (2011) Composition of amino acids in feed ingredients for animal diets. Amino Acids 40:1159–1168

    CAS  PubMed  Google Scholar 

  • Li XY, Zheng SX, Ma XK, Cheng KM, Wu GY (2020a) Oxidation of energy substrates in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52:1017–1032

    CAS  PubMed  Google Scholar 

  • Li XY, Zheng SX, Jia SC, Song F, Zhou CP, Wu GY (2020b) Effects of dietary starch and lipid levels on the protein retention and growth of largemouth bass (Micropterus salmoides). Amino Acids 52:999–1016

    CAS  PubMed  Google Scholar 

  • Li XY, Zheng SX, Ma XK, Cheng KM, Wu G (2020c) Effects of dietary protein and lipid levels on growth performance, feed utilization, and liver histology of largemouth bass (Micropterus salmoides). Amino Acids 52:1043–1061

    CAS  PubMed  Google Scholar 

  • Li XY, Zheng SX, Wu G (2020d) Nutrition and metabolism of glutamate and glutamine in fish. Amino Acids 52:671–691

    CAS  PubMed  Google Scholar 

  • Luo Z, Liu YJ, Mai KS, Tian LX, Liu DH, Tan XY (2004) Optimal dietary protein requirement of grouper Epinephelus coioides juveniles fed isoenergetic diets in floating net cages. Aquac Nutr 109:247–252

    Google Scholar 

  • Marín-Juez R, Diaz M, Morata J, Planas JV (2013) Mechanisms regulating GLUT4 transcription in skeletal muscle cells are highly conserved across vertebrates. PLoS ONE 8:e80628

    PubMed  PubMed Central  Google Scholar 

  • Metón I, Mediavilla D, Caseras A, Cantó E, Fernández F, Baanante IV (1999) Effect of diet composition and ration size on key enzyme activities of glycolysis–gluconeogenesis, the pentose phosphate pathway and amino acid metabolism in liver of gilthead sea bream (Sparus aurata). Br J Nutr 82:223–232

    PubMed  Google Scholar 

  • Miller KK, Rossi Jr W, Habte-Tsion HM (2020) Assessment of total dietary phosphorus requirement of juvenile largemouth bass, Micropterus salmoides, using soybean meal-based diets: effects on production performance, tissue mineralization, physiological parameters in plasma and intestine and expression of head-kidney genes. Aquac Nutr. https://doi.org/10.1111/anu.13169

    Article  Google Scholar 

  • Mohanta KN, Mohanty SN, Jena J, Sahu NP, Patro B (2009) Carbohydrate level in the diet of silver barb, Puntius gonionotus (Bleeker) fingerlings: effect on growth, nutrient utilization and whole body composition. Aquac Res 40:927–937

    CAS  Google Scholar 

  • Nagai M, Ikeda S (1971) Carbohydrate metabolism in fish. 2. Effect of dietary composition on metabolism of glucose-6-14C in carp. Bull Jpn Soc Sci Fish 37:410–414

    CAS  Google Scholar 

  • Nagai M, Ikeda S (1972) Carbohydrate metabolism in fish: III. Effects of dietary composition on metabolism of glucose-U-14C and glutamate-U-14C in carp. Bull Jpn Soc Sci Fish 38:137–143

    CAS  Google Scholar 

  • NRC (2011) Nutrient requirements of fish and shrimp. National Academies Press, Washington, DC

    Google Scholar 

  • Nuche-Pascua MT, Lazo JP, Ruiz-Cooley RI, Herzka SZ (2018) Amino acid-specific δ15N trophic enrichment factors in fish fed with formulated diets varying in protein quantity and quality. Ecol Evol 8:9192–9217

    Google Scholar 

  • Oliva-Teles A, Peres H, Kaushik S (2017) Dietary arginine supplementation does not improve nutrient utilisation in gilthead seabream. Aquaculture 479:690–695

    CAS  Google Scholar 

  • Polakof S, Alvarez R, Soengas JL (2010) Gut glucose metabolism in rainbow trout: implications in glucose homeostasis and glucosensing capacity. Am J Physiol 299:19–32

    Google Scholar 

  • Rawles SD, Green BW, McEntire ME, Gaylord TG, Barrows FT (2018) Reducing dietary protein in pond production of hybrid striped bass (Morone chrysops × M. saxatilis): effects on fish performance and water quality dynamics. Aquaculture 490:217–227

    CAS  Google Scholar 

  • Rossi W Jr, Davis DA (2012) Replacement of fishmeal with poultry by-product meal in the diet of Florida pompano Trachinotus carolinus L. Aquaculture 338:160–166

    Google Scholar 

  • Rossi W Jr, Moxely D, Buentello A, Pohlenz C, Gatlin DM III (2013) Replacement of fishmeal with novel plant feedstuffs in the diet of red drum Sciaenops ocellatus: an assessment of nutritional value. Aquac Nutr 19:72–81

    CAS  Google Scholar 

  • Sánchez-Muros MJ, Garcı́a-Rejón L, Garcı́a-Salguero L, Lupiáñez JA (1998) Long-term nutritional effects on the primary liver and kidney metabolism in rainbow trout. Adaptive response to starvation and a high-protein, carbohydrate-free diet on glutamate dehydrogenase and alanine aminotransferase kinetics. Int J Biochem Cell Biol 30:55–63

    PubMed  Google Scholar 

  • Shapawi R, Ebi I, Yong ASK, Ng WK (2014) Optimizing the growth performance of brown-marbled grouper, Epinephelus fuscoguttatus (Forskal), by varying the proportion of dietary protein and lipid levels. Anim Feed Sci Technol 191:98–105

    CAS  Google Scholar 

  • Soengas JL, Polakof S, Chen X, Sangiao-Alvarellos S, Moon TW (2006) Glucokinase and hexokinase expression and activities in rainbow trout tissues: changes with food deprivation and refeeding. Am J Physiol 291:810–821

    Google Scholar 

  • Tan Q, Wang F, Xie S, Zhu X, Lei W, Shen J (2009) Effect of high dietary starch levels on the growth performance, blood chemistry and body composition of gibel carp (Carassius auratus var. gibelio). Aquac Res 40:1011–1018

    CAS  Google Scholar 

  • Wang Y, Liu YJ, Tian LX, Du ZY, Wang JT, Wang S, Xiao WP (2005) Effects of dietary carbohydrate level on growth and body composition of juvenile tilapia, Oreochromis niloticus × O. aureus. Aquac Res 36:1408–1413

    CAS  Google Scholar 

  • Wang JT, Jiang YD, Li XY, Han T, Yang YX, Hu SX, Yang M (2016) Dietary protein requirement of juvenile red spotted grouper (Epinephelus akaara). Aquaculture 450:289–294

    CAS  Google Scholar 

  • Wang J, Li XY, Han T, Yang YX, Jiang YD, Yang M, Harpaz S (2016) Effects of different dietary carbohydrate levels on growth, feed utilization and body composition of juvenile grouper Epinephelus akaara. Aquaculture 459:143–147

    CAS  Google Scholar 

  • Wilson RP (1994) Utilization of dietary carbohydrate by fish. Aquaculture 124:67–80

    CAS  Google Scholar 

  • Wu G, Field C, Marliss EB (1991) Elevated glutamine metabolism in splenocytes from spontaneously diabetic BB rats. Biochem J 274:49–54

    CAS  PubMed  PubMed Central  Google Scholar 

  • Wu G (1997) Synthesis of citrulline and arginine from proline in enterocytes of postnatal pigs. Am J Physiol 272:G1382–G1390

    CAS  PubMed  Google Scholar 

  • Wu G (2013) Amino acids: biochemistry and nutrition. CRC Press, Boca Raton

    Google Scholar 

  • Wu G (2018) Principles of animal nutrition. CRC Press, Boca Raton

    Google Scholar 

  • Yang M, Wang J, Han T, Yang Y, Li X, Jiang Y (2016) Dietary protein requirement of juvenile bluegill sunfish (Lepomis macrochirus). Aquaculture 459:191–197

    CAS  Google Scholar 

  • Zhang JM, He WL, Yi D, Zhao D, Song Z, Hou YQ, Wu G (2019) Regulation of protein synthesis in porcine mammary epithelial cells by l-valine. Amino Acids 51:717–726

    CAS  PubMed  Google Scholar 

  • Zhou P, Wang M, Xie F, Deng DF, Zhou Q (2016) Effects of dietary carbohydrate to lipid ratios on growth performance, digestive enzyme and hepatic carbohydrate metabolic enzyme activities of large yellow croaker (Larmichthys crocea). Aquaculture 452:45–51

    CAS  Google Scholar 

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Acknowledgements

We thank students and research assistants in our laboratory for helpful discussions. Financial support by Guangdong Yuehai Feeds Group Co., Ltd. is gratefully appreciated.

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Authors and Affiliations

  1. Department of Animal Science, Texas A&M University, College Station, TX, 77843, USA

    Xinyu Li, Tao Han, Fei Song & Guoyao Wu

  2. Guangdong Yuehai Feeds Group Co., Ltd., Zhanjiang, 524017, Guangdong, China

    Shixuan Zheng

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  1. Xinyu Li
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  2. Shixuan Zheng
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  3. Tao Han
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  5. Guoyao Wu
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Correspondence to Guoyao Wu.

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This study was approved by the Institutional Animal Care and Use Committee of Texas A&M University.

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Li, X., Zheng, S., Han, T. et al. Effects of dietary protein intake on the oxidation of glutamate, glutamine, glucose and palmitate in tissues of largemouth bass (Micropterus salmoides). Amino Acids 52, 1491–1503 (2020). https://doi.org/10.1007/s00726-020-02907-3

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