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Effect of supplementary manganese on growth performance, tissue manganese content, antioxidant activities, and cytosolic manganese superoxide dismutase gene mRNA expression in juvenile Chinese mitten crabs (Eriocheir sinensis)

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Abstract

A 50-day feeding trial was conducted to determine the dietary manganese (Mn) requirement of juvenile Chinese mitten crabs Eriocheir sinensis. Manganese sulfate monohydrate (MnSO4·H2O) was added to a semi-purified basal diet to prepare six experimental diets with graded levels of Mn (0, 10, 20, 40, 80, and 160 mg/kg) providing the actual dietary Mn value of 2.12, 12.26, 22.45, 33.78, 44.05, and 66.18 mg/kg. Results showed that Mn supplementation significantly (P < 0.05) increased the weight growth rate (WGR), feed efficiency (FE), and activities of both hepatic Mn superoxide dismutase (Mn-SOD) and total SOD (T-SOD). Survival rate was not affected by supplementary Mn (P > 0.05). Mn concentration in the whole body and hepatopancreas significantly increased with increasing levels of dietary Mn supplementation. However, crabs fed an additional 2.12 mg/kg of Mn had a significantly (P < 0.05) higher Mn retention and proportion of hepatic Mn to whole-body Mn than other groups. As biomarkers of oxidative stress, malondialdehyde content in the serum was significantly higher in crabs fed the basal diet (P < 0.05). The mRNA expression of the cytosolic Mn-SOD gene in the hepatopancreas was upregulated with increasing dietary Mn levels up to 22.45 mg/kg and then plateaued. Using the broken-line model based on WGR, the dietary Mn requirement of the juvenile Chinese mitten crab was estimated to be 30.34 mg/kg.

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References

  • Andreini C, Bertini I, Cavallaro G, Holliday GL, Thornton JM (2008) Metal ions in biological catalysis: from enzyme databases to general principles. J Biol Inorg Chem 13:1205–1218

    Article  CAS  PubMed  Google Scholar 

  • AOAC (1995) Official Methods of Analysis of AOAC International. AOAC, Arlington, VA.

  • Cai HR, Yang QH, Tan BP, Dong XH, Chi SY, Liu HY, Zhang S (2016) Effects of dietary manganese source and supplemental levels on growth performance, antioxidant enzymes activities, tissue Mn concentrations and cytosolic manganese superoxide dismutase (cMnSOD) mRNA expression level of juvenile Litopenaeus vannamei. Aquac Nutr. doi:10.1111/anu.12427

    Google Scholar 

  • Chen DW, Zhang M (2007) Non-volatile taste active compounds in the meat of Chinese mitten crab (Eriocheir sinensis). Food Chem 104:1200–1205

    Article  CAS  Google Scholar 

  • Chen K, Li E, Yu N, Du Z, Chen L (2013) Biochemical composition and nutritional value analysis of Chinese mitten crab, Eriocheir sinensis, grown in pond. Global Adv Res J Agricul Sci 2:164–173

    Google Scholar 

  • Davis CD, Wolf TL, Greger JL (1992) Varying levels of manganese and iron affect absorption and gut endogenous losses of manganese by rats. J Nutr 122(6):1300–1308

  • De Rosa G, Keen CL, Leach RM, Hurley LS (1980) Regulation of superoxide dismutase activity by dietary manganese. J Nutr 110:795–804

    CAS  PubMed  Google Scholar 

  • Elchuri S, Oberley TD, Qi W, Eisenstein RS, Jackson Roberts L, Van Remmen H, Epstein CJ, Huang TT (2005) CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24:367–380

  • Fattman CL, Schaefer LM, Oury TD (2003) Extracellular superoxide dismutase in biology and medicine. Free Radic Biol Med 35:236–256

    Article  CAS  PubMed  Google Scholar 

  • Garling jr DL, Wilson PR (1977) Effect of dietary carbohydrate to lipid ratio on growth and body composition of fingerling channel catfish. Prog Fish Cult 39:43–47

  • Gatlin DM, Wilson RP (1984) Studies on the manganese requirement of fingerling channel catfish. Aquaculture 41:85–92

    Article  CAS  Google Scholar 

  • Han D, Antunes F, Canali R, Rettori D, Cadenas E (2003) Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J Biol Chem 278:5557–5563

    Article  CAS  PubMed  Google Scholar 

  • Jiang HB, Li K, Chen LQ, Wang Q, Liu QG, Liu LH (2005) Nutritional requirement of the Chinese mitten-handed crab Eriocheir sinensis juvenile for arginine and lysine. J World Aquacult Soc 36:515–520

    Article  Google Scholar 

  • Kamunde C, Grosell M, Higgs D, Wood CM (2002) Copper metabolism in actively growing rainbow trout (Oncorhynchus mykiss): interactions between dietary and waterborne copper uptake. J Exp Biol 205:279–290

    CAS  PubMed  Google Scholar 

  • Knox D, Cowey CB, Adron JW (1981) The effect of low dietary manganese intake on rainbow trout (Salmo gairdneri). Br J Nutr 46:495–501

    Article  CAS  PubMed  Google Scholar 

  • Lebovitz RM, Zhang H, Vogel H, Cartwright J, Dionne L, Lu N, Huang S, Matzuk MM (1996) Neurodegeneration, myocardial injury, and perinatal death inmitochondrial superoxide dismutase-deficient mice. Proc Natl Acad Sci 93:9782–9787

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li HF, Hao B, Liu FY (1993) Effects of dietary manganese on Penaeus chinensis. Mar Sci 4:48–51

    CAS  Google Scholar 

  • Lin YH, Lin SM, Shiau SY (2008) Dietary manganese requirements of juvenile tilapia, Oreochromis niloticus × O. aureus. Aquaculture 284:207–210

    Article  CAS  Google Scholar 

  • Lin SM, Luo L, Ye YT (2010) Effect of dietary protein level on growth, feed utilization and digestive enzyme activity of the Chinese mitten crab, Eriocheir sinensis. Aquac Nutr 16:290–298

    Article  CAS  Google Scholar 

  • Liu K, Ai QH, Mai KS, Zhang WB, Zhang L, Zheng SX (2013) Dietary manganese requirement for juvenile cobia, Rachycentron canadum L. Aquac Nutr 19:461–467

    Article  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 22DDCT method. Methods 25:402–408

  • Lu L, Luo XG, Ji C, Liu B, Yu S (2007) Effect of manganese supplementation and source on carcass traits, meat quality, and lipid oxidation in broilers. J Anim Sci 85:812–822

    Article  CAS  PubMed  Google Scholar 

  • Ma R, Hou H, Mai K, Bharadwaj AS, Ji F, Zhang W (2015) Comparative study on the effects of chelated or inorganic manganese in diets containing tricalcium phosphate and phytate on the growth performance and physiological responses of turbot Scophthalmus maximus. Aquac Nutr 21(6):780–787

    Article  CAS  Google Scholar 

  • Maage A, Lygren B, El-Mowafic AFA (2000) Manganese requirement of Atlantic salmon (Salmo salar) fry. Fish Sci 66:1–8

    Article  CAS  Google Scholar 

  • Malecki EA, Greger J (1996) Manganese protects against heart mitochondrial lipid peroxidation in rats fed high levels of polyunsaturated fatty acids. J Nutr 126:27–33

    CAS  PubMed  Google Scholar 

  • Malecki EA, Huttner DL, Greger JL (1994) Manganese status, gut endogenous losses of manganese, and antioxidant enzyme activity in rats fed varying levels of manganese and fat. Biol Trace Elem Res 42:17–29

    Article  CAS  PubMed  Google Scholar 

  • Mu YY, Shim KF, Guo JY (1998) Effects of protein level in isocaloric diets on growth performance of the juvenile Chinese hairy crab, Eriocheir sinensis. Aquaculture 165:139–148

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Ogino C, Yang G (1980) Requirements of carp and rainbow trout for dietary manganese and copper. Bull Jpn Soc Sci Fish 46:455–458

    Article  CAS  Google Scholar 

  • Pan L, Zhu X, Xie S, Lei W, Han D, Yang Y (2008) Effects of dietary manganese on growth and tissue manganese concentrations of juvenile gibel carp, Carassius auratus gibelio. Aquac Nutr 14:459–463

    Article  CAS  Google Scholar 

  • Robbins KR, Norton HW, Baker DH (1979) Estimation of nutrient requirements from growth data. J Nutr 109:1710–1714

    CAS  PubMed  Google Scholar 

  • Sanchez-Paz A, Garca-Carreno F, Muhlia-Almazan A, Hernandez-Saavedra NY, Yepiz-Plascencia G (2003) Differential expression of trypsin mRNA in the white shrimp (Penaeus vannamei) midgut gland under starvation conditions. J Exp Mar Biol Ecol 292:1–17

    Article  CAS  Google Scholar 

  • Sun SM, Chen M, Chen LQ, Jiang HB, Li EC (2011) Optimal dietary copper and zinc requirements for juvenile Chinese mitten crab, Eriocheir sinensis. Isr J Aquacult Bamid 63(3):580–587

    Google Scholar 

  • Sun SM, Qin JG, Yu N, Ge XP, Jiang HB, Chen LQ (2013) Effect of dietary copper on the growth performance, non-specific immunity and resistance to Aeromonas hydrophila of juvenile Chinese mitten crab, Eriocheir sinensis. Fish Shellfish Immunol 34:1195–1201

    Article  CAS  PubMed  Google Scholar 

  • Tan B, Mai K (2001) Zinc methionine and zinc sulfate as sources of dietary zinc for juvenile abalone, Haliotis discus hannai Ino. Aquaculture 192:67–84

    Article  CAS  Google Scholar 

  • Tan XY, Xie P, Luo Z, Lin HZ, Zhao YH, Xi WQ (2012) Dietary manganese requirement of juvenile yellow catfish Pelteobagrus fulvidraco, and effects on whole body mineral composition and hepatic intermediary metabolism. Aquaculture 326–329:68–73

    Article  Google Scholar 

  • Wang D, Zhao L (1994) Requirement of fingerling grass carp (Ctenopharyngodon idellus) for manganese. J Shanghai Fish Univ 3:1–2 (in Chinese with English abstract)

    CAS  Google Scholar 

  • Wang MQ, Wang LL, Yi QL, Gai YC, Song LS (2015) Molecular cloning and characterization of a cytoplasmic manganese superoxide dismutase and a mitochondrial manganese superoxide dismutase from Chinese mitten crab Eriocheir sinensis. Fish Shellfish Immunol 47:407–417

    Article  CAS  PubMed  Google Scholar 

  • Wu XG, Cheng YX, Sui LY, Zeng CS, Southgate PC, Yang XZ (2007) Effect of dietary supplementation of phospholipids and highly unsaturated fatty acids on reproductive performance and offspring quality of Chinese mitten crab, Eriocheir sinensis (H. Milne-Edwards), female broodstock. Aquaculture 273(4):602–613

    Article  CAS  Google Scholar 

  • Ye CX, Tian LX, Yang HJ, Liang JJ, Niu J, Liu YJ (2009) Growth performance and tissue mineral content of juvenile grouper (Epinephelus coioides) fed diets supplemented with various levels of manganese. Aquac Nutr 15:608–614

    Article  CAS  Google Scholar 

  • Zhang HL, Sun RJ, Xu W, Zhou HH, Zhang WB, Mai KS (2016) Dietary manganese requirement of juvenile large yellow croaker Larimichthys crocea (Richardson, 1846). Aquaculture 450:74–79

    Article  CAS  Google Scholar 

  • Zidenberg-Cherr S, Keen CL, Lonnerdal B, Hurley LS (1983) Superoxide dismutase activity and lipid peroxidation in the rat: developmental correlations affected by manganese deficiency. J Nutr 113:2498–2504

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Acknowledgments

The work was supported by the National Natural Science Foundation of China (grant numbers 31560726, 31260642, 31402305), the Major Project of Science and Technology of Jiangxi Province of China (2016ACF60018), the Natural Science Foundation of Jiangxi Province of China (grant number 20132BAB214015), and the Educational Commission of Sichuan Province of China (grant number 14ZA0249).

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Correspondence to Yijiang Hong.

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Zhao, D., Mao, Z., Lin, Q. et al. Effect of supplementary manganese on growth performance, tissue manganese content, antioxidant activities, and cytosolic manganese superoxide dismutase gene mRNA expression in juvenile Chinese mitten crabs (Eriocheir sinensis). Aquacult Int 25, 893–903 (2017). https://doi.org/10.1007/s10499-016-0086-x

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  • DOI: https://doi.org/10.1007/s10499-016-0086-x

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