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High dietary lipid level alters the growth, hepatic metabolism enzyme, and anti-oxidative capacity in juvenile largemouth bass Micropterus salmoides

Fish Physiology and Biochemistry volume 46, pages 125–134 (2020)Cite this article

Abstract

The present study was conducted to investigate the effects of high dietary lipid levels on growth, metabolism, antioxidant capacity, and immune responses of largemouth bass. Fish (initial body weight 13.38 ± 0.11 g) were fed three isonitrogenous semi-purified diets containing 5%, 10%, and 20% lipid, respectively. The results indicated that fish fed 10% lipid diet showed significantly better final body weight, specific growth rate (SGR), protein efficiency ratio (PER), and feed conversion ratio (FCR) compared with that fed 5% lipid diet. Meanwhile, fish fed 20% lipid diet had a significantly higher viscera ratio (VR), hepatosomatic index (HSI), intraperitoneal fat ratio (IPF), and liver lipid content than those fed the other diets. Higher alanine aminotransferase (ALT) and aspartate transaminase (AST) activities, total cholesterol (TC), triglyceride (TG), free fatty acids (FFA), high-density lipoprotein cholesterol (HDL-C), low-density lipoprotein cholesterol (LDL-C) contents, and LDL-C/HDL-C value in plasma were recorded in fish fed 20% lipid diet, while higher insulin contents were obtained in fish fed 5% lipid diet. In addition, the highest carnitine palmitoyltransferase I (CPT1), AMP-activated protein kinase (AMPK), fructose-1,6-bisphosphatase (FBPase), and phosphoenolpyruvate carboxykinase (PEPCK) activities in the liver were also observed in fish fed 20% lipid diet. However, fish fed 20% lipid diet had a significantly lower superoxide dismutase (SOD) and catalase (CAT) activities and higher MDA contents in liver than those fed the other diets. The higher nitric oxide (NO) contents and inducible nitric oxide synthase (iNOS) activity in liver were recorded in fish fed 10% lipid diet. Moreover, the alkaline phosphatase (ALP), inducible nitric oxide synthase (iNOS) and lysozyme activities, and nitric oxide (NO) contents in plasma were higher in fish fed the 10% diets than the other groups. In conclusion, high dietary lipid levels could suppress growth performance and liver anti-oxidative capacity, and reduce immune responses of largemouth bass.

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References

  • Akpınar Z, Sevgili H, Demir A, Özgen T, Emre Y, Eroldoğan OT (2012) Effects of dietary lipid levels on growth, nutrient utilization, and nitrogen and carbon balances in shi drum (Umbrina cirrosa L.). Aquac Int 20:131–143

    Google Scholar 

  • Association of Official Analytical Chemists (AOAC) (2005) Official Methods of Analysis, 18th ed. Association of Official Analytical Chemists, Gaithersburg

  • Bargut TCL, Frantz EDC, Mandarim-de-Lacerda CA, Aguila MB (2014) Effects of a diet rich in n-3 polyunsaturated fatty acids on hepatic lipogenesis and beta-oxidation in mice. Lipids 49:431–444

    CAS  PubMed  Google Scholar 

  • Bargut TCL, Mandarim-de-Lacerda CA, Aguila MB (2015) A high-fish-oil diet prevents adiposity and modulates white adipose tissue inflammation pathways in mice. J Nutr Biochem 26:960–969

    CAS  PubMed  Google Scholar 

  • Borges P, Valente LMP, Véron V, Dias K, Panserat S, Médale F (2014) High dietary lipid level is associated with persistent hyperglycaemia and downregulation of muscle akt-mTOR pathway in senegalese sole (Solea senegalensis). PLoS One 9(7):e102196

    PubMed  PubMed Central  Google Scholar 

  • Boujard T, Gélineau A, Covès D, Corraze G, Dutto G, Gasset E, Kaushik S (2004) Regulation of feed intake, growth, nutrient and energy utilisation in European sea bass (Dicentrarchus labrax) fed high fat diets. Aquaculture 231:529–545

    Google Scholar 

  • Bradford MM (1976) A refined and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein dye-binding. Anal Biochem 72:248–254

    CAS  PubMed  PubMed Central  Google Scholar 

  • Bright LA, Coyle SD, Tidwell JH (2005) Effect of dietary lipid level and protein energy ratio on growth and body composition of largemouth bass Micropterus salmoides. J World Aquacult Soc 36(1):129–134

    Google Scholar 

  • Chatzifotis S, Panagiotidou M, Papaioannou N, Pavlidis M, Nengas I, Mylonas CC (2010) Effect of dietary lipid levels on growth, feed utilization, body composition and serum metabolites of meagre (Argyrosomus regius) juveniles. Aquaculture 307:65–70

    CAS  Google Scholar 

  • Chen NS, Xiao WW, Liang QL, Zhou HY, Ma XL, Zhao M (2012) Effects of dietary lipid to protein ratios on growth performance, body composition and non-specific immunity of largemouth bass (Micropterus salmoides). J Fish China 36(8):1270–1280 [in Chinese with English abstract]

    Google Scholar 

  • Cho CY, Hynes JD, Wood KR, Yoshida HK (1994) Development of high-nutrient-dense, low-pollution diets and prediction of aquaculture wastes using biological approaches. Aquaculture 124:293–305

    Google Scholar 

  • Dias J, Alvarez MJ, Diez A, Arzel J, Corraze G, Bautista JM, Kaushik SJ (1998) Regulation of hepatic lipogenesis by dietary protein/energy in juvenile European seabass (Dicentrarchus labrax). Aquaculture 161:169–186

    CAS  Google Scholar 

  • Du ZY, Clouet P, Huang LM, Degrace P, Zheng WH, He JG, Tian LX, Liu YJ (2008) Utilization of different dietary lipid sources at high level in herbivorous grass carp (Ctenopharyngodon idella): mechanism related to hepatic fatty acid oxidation. Aquac Nutr 14:77–92

    CAS  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. In: Stolen, J.S., Fletcher, T.C., Anderson, D.P.,Robertsen, B.S., Van Muiswinkel, W.B. (Eds.), Techniques in Fish Immunology. SOS Publications, Fair Haven, pp. 101–103

  • Figueiredo-Silva AC, Panserat S, Kaushik S, Geurden I, Polakof S (2012) High levels of dietary fat impair glucose homeostasis in rainbow trout. J Exp Biol 215:169–178

    CAS  PubMed  Google Scholar 

  • Gu ZX, Mu H, Shen HH, Deng KY, Liu D, Yang MX, Zhang Y, Zhang WB, Mai KS (2019) High level of dietary soybean oil affects the glucose and lipid metabolism in large yellow croaker Larimichthys crocea through the insulin-mediated PI3K/AKT signaling pathway. Comp Biochem Physiol B 231:34–41

    CAS  PubMed  Google Scholar 

  • Gutiérrez J, Carrillo M, Zanuy S, Planas J (1984) Daily rhythms of insulin and glucose levels in the plasma of sea bass Dicentrarchus labrax after experimental feeding. Gen Comp Endocrinol 55:393–397

    PubMed  Google Scholar 

  • Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine. Oxford University Press, Oxford

    Google Scholar 

  • Han T, Li XY, Wang JT, Hu SX, Jiang YD, Zhong XD (2014) Effect of dietary lipid level on growth, feed utilization and body composition of juvenile giant croaker Nibea japonica. Aquaculture 434:145–150

    CAS  Google Scholar 

  • Hansen JØ, Berge GM, Hillestad M, Krogdahl Å, Galloway TF, Holm H, Holm J, Ruyter B (2008) Apparent digestion and apparent retention of lipid and fatty acids in Atlantic cod (Gadus morhua) fed increasing dietary lipid levels. Aquaculture 284:159–166

    CAS  Google Scholar 

  • Hillestad M, Johnsen F (1994) High-energy/low-protein diets for Atlantic salmon: effects on growth, nutrient retention and slaughter quality. Aquaculture 124:109–116

    Google Scholar 

  • Jia Y, Jing Q, Niu H, Huang B (2017) Ameliorative effect of vitamin E on hepatic oxidative stress and hypoimmunity induced by high-fat diet in turbot (Scophthalmus maximus). Fish Shellfish Immunol 67:634–642

    CAS  PubMed  Google Scholar 

  • Jiang DL, Wu YB, Huang D, Ren X, Wang Y (2017) Effects of nutritional history on stress response in gibel carp (Carassius auratus gibelio) and largemouth bass (Micropterus salmoides). Comp Biochem Phys B 210:9–17

    CAS  Google Scholar 

  • Jin JY, Zhu XM, Han D, Yang YX, Liu HK, Xie SQ (2017) Different regulation of insulin on glucose and lipid metabolism in 2 strains of gibel carp. Gen Comp Endocrinol 246:363–371

    CAS  PubMed  Google Scholar 

  • Kao Y, Youson JA, Holmes JH, Al-Mahrouki A, Sheridan MA (1999) Effects of insulin on lipid metabolism of larvae and metamorphosing landlocked sea lamprey (Petromyzon marinus). Gen Comp Endocrinol 114:405–414

    CAS  PubMed  Google Scholar 

  • Li C, Ford ES, Meng YX, Mok dad AH, Reaven GM (2008) Does the association of the triglyceride to high-density lipoprotein cholesterol ratio with fasting serum insulin differ by race/ethnicity? Cardiovasc Diabetol 7(4):1–9

    Google Scholar 

  • Lin SM, Jiang Y, Chen YJ, Luo L, Doolgindachbapornc S, Yuangsoic B (2017) Effects of Astragalus polysaccharides (APS) and chitooligosaccharides (COS) on growth, immune response and disease resistance of juvenile largemouth bass, Micropterus salmoides. Fish Shellfish Immunol 70:40–47

    CAS  PubMed  Google Scholar 

  • López LM, Durazo E, Viana MT, Drawbridge M, Bureau DP (2009) Effect of dietary lipid levels on performance, body composition and fatty acid profile of juvenile white seabass, Atractoscion nobilis. Aquaculture 289:101–105

    Google Scholar 

  • Lu KL, Xu WN, Wang LN, Zhang DD, Zhang CN, Liu WB (2014) Hepatic β-oxidation and regulation of carnitine palmitoyltransferase (CPT) I in blunt snout bream Megalobrama amblycephala fed a high fat diet. PLoS One 99(3):e93135

    Google Scholar 

  • Martin SAM, Król E (2017) Nutrigenomics and immune function in fish: new insights from omics technologies. Dev Comp Immunol 75:86–98

    CAS  PubMed  PubMed Central  Google Scholar 

  • Montero D, Mathlouthi F, Tort L, Afonso J, Torrecillas S, Fernández-Vaquero A, Negrin D, Izquierdo MS (2010) Replacement of dietary fish oil by vegetable oils affects humoral immunity and expression of pro-inflammatory cytokines genes in gilthead sea bream Sparus aurata. Fish Shellfish Immunol 29:1073–1081

    CAS  Google Scholar 

  • Moon TW (2011) Adaptation, constraint and the function of the gluconeogenic pathway. Can J Zool 66:1059–1068

    Google Scholar 

  • Morash AJ, Bureau DP, McClelland GB (2009) Effects of dietary fatty acid composition on the regulation of carnitine palmitoyltransferase (CPT) I in rainbow trout (Oncorhynchus mykiss). Comp Biochem Phys B152:85–93

    Google Scholar 

  • Mu H, Shen HH, Liu JH, Xie FL, Zhang WB, Mai KS (2018) High level of dietary soybean oil depresses the growth and anti-oxidative capacity and induces inflammatory response in large yellow croaker Larimichthys crocea. Fish Shellfish Immunol 77:465–473

    CAS  PubMed  Google Scholar 

  • Öner M, Atli G, Canli M (2008) Changes in serum biochemical parameters of freshwater fish Oreochromis niloticus following prolonged metal (Ag, Cd, Cr, Cu, Zn) exposures. Environ Toxicol Chem 27:360–366

    PubMed  Google Scholar 

  • Peres H, Oliva-Teles A (1999) Effect of dietary lipid level on growth performance and feed utilization by European sea bass juveniles (Dicentrarchus labrax). Aquaculture 179:325–334

    CAS  Google Scholar 

  • Pérez-Jiménez A, Abellán E, Arizcun M, Cardenete G, Morales AE, Hidalgo MC (2017) Dietary carbohydrates improve oxidative status of common dentex (Dentex dentex) juveniles, a carnivorous fish. Comp Biochem Phys A 203:17–23

    Google Scholar 

  • Plagnes-Juan E, Lansard M, Seiliez I, Médale F, Corraze G, Kaushik S, ... Skiba-Cassy S (2008) Insulin regulates the expression of several metabolism-related genes in the liver and primary hepatocytes of rainbow trout (Oncorhynchus mykiss). J Exp Biol 211: 2510–2518

    CAS  PubMed  Google Scholar 

  • Pohl A, Behling C, Oliver D, Kilani M, Monson P, Hassanein T (2001) Serum aminotransferase levels and platelet counts as predictors of degree of fibrosis in chronic hepatitis C virus infection. Am J Gastroenterol 96:3142–3146

    CAS  PubMed  Google Scholar 

  • Rueda-Lopez S, Lazo JP, Correa RG, Viana MT (2011) Effect of dietary protein and energy levels on growth, survival and body composition of juvenile Totoaba macdonaldi. Aquaculture 319:385–390

    CAS  Google Scholar 

  • Rui BB, Chen H, Jang L, Li Z, Yang JM, Xu WP, Wei W (2016) Melatonin upregulates the activity of AMPK and attenuates lipid accumulation in alcohol-induced rats. Alcohol Alcohol 51(1):11–19

    CAS  PubMed  Google Scholar 

  • Sakai M, Sawada T, Nishimura T, Nagatsu I (1996) Expression of nitric oxide synthase in the mouse and human nasal mucosa. Acta Histochem Cytoc 29:177–179

    CAS  Google Scholar 

  • Sevgili H, Kurtoğlu A, Oikawa M, Öztürk E, Dedebali N, Emre N, Pak F (2014) High dietary lipids elevate carbon loss without sparing protein in adequate protein-fed juvenile turbot (Psetta maxima). Aquac Int 22(2):797–810

    CAS  Google Scholar 

  • Tabarin A, Diz-Chaves Y, Carmona Mdel C, Catargi B, Zorrilla EP, Roberts AJ et al (2005) Resistance to diet-induced obesity in mu-opioid receptor-deficient mice: evidence for a “thrifty gene”. Diabetes 54:3510–3516

    CAS  PubMed  Google Scholar 

  • Tan P, Dong X, Mai K, Xu W, Ai Q (2016) Vegetable oil induced inflammatory response by altering TLR-NF-κB signalling, macrophages infiltration and polarization in adipose tissue of large yellow croaker (Larimichthys crocea). Fish Shellfish Immunol 59:398–405

    CAS  PubMed  Google Scholar 

  • Tang CC, Huang HP, Lee YJ, Tang YH, Wang CJ (2013) Hepatoprotective effect of mulberry water extracts on ethanol-induced liver injury via anti-inflammation and inhibition of lipogenesis in C57BL/6J mice. Food Chem Toxicol 62:786–796

    CAS  PubMed  Google Scholar 

  • The State Science and Technology Commission (1988) Regulations for the administration of affairs concerning experimental animals. The State Science and Technology Commission, Beijing, China.

  • Wang X, Li Y, Hou C, Gao Y, Wang Y (2015) Physiological and molecular changes in large yellow croaker (Pseudosciaena crocea R.) with high-fat diet-induced fatty liver disease. Aquac Res 46:472–482

    Google Scholar 

  • Yan J, Liao K, Wang T, Mai K, Xu W, Ai Q (2015) Dietary lipid levels influence lipid deposition in the liver of large yellow croaker (Larimichthys crocea) by regulating lipoprotein receptors, fatty acid uptake and triacylglycerol synthesis and catabolism at the transcriptional level. PLoS One 10(6):e0129937

    PubMed  PubMed Central  Google Scholar 

  • Yuan XC, Liang XF, Liu LW, Fang JG, Li J, Li AX, Cai W, Xue M, Wang J, Wang QC (2016) Fat deposition pattern and mechanism in response to dietary lipid levels in grass carp, Ctenopharyngodon idellus. Fish Physiol Biochem 42:1557–1569

    CAS  PubMed  Google Scholar 

  • Yun B, Xue M, Wang J, Fan Z, Wu XF, Zheng YH, Qin YC (2013) Effects of lipid sources and lipid peroxidation on feed intake, growth, and tissue fatty acid compositions of largemouth bass (Micropterus salmoides). Aquacult Int 21:97–110

    CAS  Google Scholar 

  • Zhang LY, Chen SY, Deng AW, Liu XY, Liang Y, Shao XF et al (2015) Association between lipid ratios and insulin resistance in a Chinese population. PLoS One 10(1):e0116110

    PubMed  PubMed Central  Google Scholar 

  • Zhao PF, Li FJ, Chen XR, Chen YJ, Lin SM, Zhang L, Li Y (2016) Effect of dietary lipid level on growth, liver function and serum biochemical indexes of snakehead (Channa argus × Channa maculata). Aquacult Int 241:353–1364

    Google Scholar 

  • Zhuo MQ, Luo Z, Wu K, Zhu QL, Zheng JL, Zhang LH, Chen QL (2014) Regulation of insulin on lipid metabolism in freshly isolated hepatocytes from yellow catfish (Pelteobagrus fulvidraco). Comp Biochem Phys B 177–178:21–28

    Google Scholar 

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Acknowledgments

We thank H. Zhao and C.M. Shi for their help during the experiment. Thanks are also due to Y. Jiang and M.Q. Song for helping with the chemical analysis.

Funding

This research was financially supported by the National Natural Science Foundation of China (No. 31672659), the Science and Technology Council of Chongqing, China (No.cstc2017shms-xdny80012), and the Chongqing Ecological Fishery Technology System (2018-2019).

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  1. Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), College of Animal Science and Technology, Southwest University, Chongqing, 400715, People’s Republic of China

    Yue-Lang Zhou, Jia-Ling Guo, Hui-Jia Ma, Yong-Jun Chen & Shi-Mei Lin

  2. Liangping District Agriculture Commission, Chongqing, 400020, People’s Republic of China

    Ren-Jun Tang

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  1. Yue-Lang Zhou
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  2. Jia-Ling Guo
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Correspondence to Shi-Mei Lin.

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Zhou, YL., Guo, JL., Tang, RJ. et al. High dietary lipid level alters the growth, hepatic metabolism enzyme, and anti-oxidative capacity in juvenile largemouth bass Micropterus salmoides. Fish Physiol Biochem 46, 125–134 (2020). https://doi.org/10.1007/s10695-019-00705-7

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Keywords

  • Lipid level
  • Growth
  • Metabolism enzyme
  • Antioxidant capacity
  • M. salmoides