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

  • Yue-Lang Zhou
  • Jia-Ling Guo
  • Ren-Jun Tang
  • Hui-Jia Ma
  • Yong-Jun Chen
  • Shi-Mei LinEmail author
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.

Keywords

Lipid level Growth Metabolism enzyme Antioxidant capacity M. salmoides 

Notes

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 information

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).

References

  1. 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 20:131–143CrossRefGoogle Scholar
  2. Association of Official Analytical Chemists (AOAC) (2005) Official Methods of Analysis, 18th ed. Association of Official Analytical Chemists, GaithersburgGoogle Scholar
  3. 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 49:431–444CrossRefPubMedGoogle Scholar
  4. 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 26:960–969CrossRefPubMedGoogle Scholar
  5. 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):e102196CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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 231:529–545CrossRefGoogle Scholar
  7. 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 72:248–254CrossRefPubMedPubMedCentralGoogle Scholar
  8. 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):129–134CrossRefGoogle Scholar
  9. 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 307:65–70CrossRefGoogle Scholar
  10. 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] CrossRefGoogle Scholar
  11. 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 124:293–305CrossRefGoogle Scholar
  12. 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 161:169–186CrossRefGoogle Scholar
  13. 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 14:77–92CrossRefGoogle Scholar
  14. 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. 101–103Google Scholar
  15. 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 215:169–178CrossRefPubMedGoogle Scholar
  16. 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 231:34–41CrossRefPubMedGoogle Scholar
  17. 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 55:393–397CrossRefPubMedGoogle Scholar
  18. Halliwell B, Gutteridge JM (1999) Free radicals in biology and medicine. Oxford University Press, OxfordGoogle Scholar
  19. 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 434:145–150CrossRefGoogle Scholar
  20. 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 284:159–166CrossRefGoogle Scholar
  21. Hillestad M, Johnsen F (1994) High-energy/low-protein diets for Atlantic salmon: effects on growth, nutrient retention and slaughter quality. Aquaculture 124:109–116CrossRefGoogle Scholar
  22. 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 67:634–642CrossRefPubMedGoogle Scholar
  23. 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 210:9–17CrossRefGoogle Scholar
  24. 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 246:363–371CrossRefPubMedGoogle Scholar
  25. 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 114:405–414CrossRefPubMedGoogle Scholar
  26. 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):1–9Google Scholar
  27. 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 70:40–47CrossRefPubMedGoogle Scholar
  28. 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 289:101–105CrossRefGoogle Scholar
  29. 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):e93135CrossRefGoogle Scholar
  30. Martin SAM, Król E (2017) Nutrigenomics and immune function in fish: new insights from omics technologies. Dev Comp Immunol 75:86–98CrossRefPubMedPubMedCentralGoogle Scholar
  31. 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 29:1073–1081CrossRefPubMedGoogle Scholar
  32. Moon TW (2011) Adaptation, constraint and the function of the gluconeogenic pathway. Can J Zool 66:1059–1068CrossRefGoogle Scholar
  33. 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 B152:85–93CrossRefGoogle Scholar
  34. 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 77:465–473CrossRefPubMedGoogle Scholar
  35. 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 27:360–366CrossRefPubMedGoogle Scholar
  36. 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 179:325–334CrossRefGoogle Scholar
  37. 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 203:17–23CrossRefGoogle Scholar
  38. 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: 2510–2518Google Scholar
  39. 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 96:3142–3146CrossRefPubMedGoogle Scholar
  40. 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 319:385–390CrossRefGoogle Scholar
  41. 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):11–19CrossRefPubMedGoogle Scholar
  42. Sakai M, Sawada T, Nishimura T, Nagatsu I (1996) Expression of nitric oxide synthase in the mouse and human nasal mucosa. Acta Histochem Cytoc 29:177–179CrossRefGoogle Scholar
  43. 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):797–810CrossRefGoogle Scholar
  44. 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 54:3510–3516CrossRefPubMedGoogle Scholar
  45. 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 59:398–405CrossRefPubMedGoogle Scholar
  46. 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 62:786–796CrossRefPubMedGoogle Scholar
  47. The State Science and Technology Commission (1988) Regulations for the administration of affairs concerning experimental animals. The State Science and Technology Commission, Beijing, China.Google Scholar
  48. 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 46:472–482CrossRefGoogle Scholar
  49. 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):e0129937CrossRefPubMedPubMedCentralGoogle Scholar
  50. 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 42:1557–1569CrossRefGoogle Scholar
  51. 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 21:97–110CrossRefGoogle Scholar
  52. 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):e0116110CrossRefPubMedPubMedCentralGoogle Scholar
  53. 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 241:353–1364Google Scholar
  54. 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 177–178:21–28CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.Key Laboratory of Freshwater Fish Reproduction and Development (Ministry of Education), College of Animal Science and TechnologySouthwest UniversityChongqingPeople’s Republic of China
  2. 2.Liangping District Agriculture CommissionChongqingPeople’s Republic of China

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