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Effect of dietary supplementation of vitamin C on growth, reactive oxygen species, and antioxidant enzyme activity of Apostichopus japonicus (Selenka) juveniles exposed to nitrite

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Abstract

Different amounts of vitamin C were added to diets fed to juveniles (2.5 ± 0.15 g) of sea cucumber Apostichopus japonic u s (Selenka) in an attempt to reduce the stress response of specimens exposed to nitrite stress. A commercial feed was used as the control diet and three experimental diets were made by supplementing 1 000, 1 500, or 2 000 mg vitamin C/kg diet to control diet separately in a 45-day experiment. Sea cucumbers were exposed to three different levels (0.5, 1.0, and 1.5 mg/L) of nitrite stress for 4, 8, and 12 h at four time intervals (0, 15, 30, and 45 d). Growth of the animals was recorded during the experiment. Reactive oxygen species (ROS) (i.e. hydroxyl free radical (-OH), malondialdehyde (MDA) and total antioxidant capacity (T-AOC)) and antioxidant enzyme activities (i.e., superoxide dismutase (SOD) and catalase (CAT)) were measured. Response surface methodology (RSM) was used to analyze the effect of multiple factors on ROS indices and enzyme activities. Weight gain (WG) and special growth rate (SGR) of vitamin C supplementation groups were significantly higher than those of control group (P < 0.05). The levels of -OH and MDA increased under exposure time extending and nitrite concentration increasing, whereas T-AOC level decreased. SOD and CAT activities increased at 4 h and 8 h and decreased at 12 h. During the days in which the animal consumed experimental diets, the levels of -OH and MDA decreased and that of T-AOC increased. This result suggests that diets containing vitamin C could reduce the nitrite stress response in the animals and increase their antioxidant capacity. The multifactor regression equation of growth performance, ROS indices, and duration of feeding results suggest that vitamin C supplementation of 1 400–2 000 mg/kg diet for 29–35 days could reduce effectively the effects of nitrite exposure.

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References

  • Akhtar M S, Pal A K, Sahu N P, Alexander C, Gupta S K, Choudhary A K, Jha A K. 2010. Stress mitigating and immune modulatory effect of dietary pyridoxine in Labeo rohita (Hamilton) fingerlings. Aquacult. Res., 41: 991–1 002.

    Google Scholar 

  • Bodansky O. 1951. Methemoglobinemia and methemoglobinproducing compounds. Pharmacol. Rev., 3: 144–196.

    Google Scholar 

  • Bradford M M. 1976. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principles of protein-dye binding. Anal. Biochem., 72: 248–254.

    Article  Google Scholar 

  • Chaoui A, Mazhoudi S, Ghorbal M H. 1997. Cadmium and zinc induction of lipid peroxidation and effects on antioxidant enzyme activities in bean (Phaseolus vulgaris L.). Plant Sci., 127: 139–147.

    Article  Google Scholar 

  • Chaudiere J, Ferrari-Illiou R. 1999. Intracellular antioxidant from chemical to biochemical mechanism. Food Chem. Toxicol., 37: 949–962.

    Article  Google Scholar 

  • Deng H, He C B, Zhou Z C, Liu C, Tan K F, Wang N B. 2009. Isolation and pathogenicity of pathogens from skin ulceration disease and viscera ejection syndrome of the sea cucumber Apostichopus japonicus. Aquaculture, 287: 18–27.

    Article  Google Scholar 

  • Dong Y, Dong S, Meng X. 2008. Effects of thermal and osmotic stress on growth, osmoregulation and Hsp70 in sea cucumber (Apostichopus japonicus Selenka). Aquaculture, 276: 179–186.

    Article  Google Scholar 

  • Fracalossi D M, Allen L K, Yuyama L K, Oftedal O T. 2001. Ascorbic acid biosynthesis in Amazonian fishes. Aquaculture, 192: 321–332.

    Article  Google Scholar 

  • Frank L, Massaro D. 1980. Oxygen toxicity. Am. J. Med., 69: 117–126.

    Article  Google Scholar 

  • Friede A, Bjarte L, Amund M, Rune W. 1998. Interaction between two dietary levels of iron and two forms of ascorbic acid and the effect on growth, antioxidant status and some non-specific immune parameters in Atlantic salmon (Salmo salar) smolts. Aquaculture, 161: 437–451.

    Article  Google Scholar 

  • Gao M H. 2008. Effect of VC, VE on Blood Parameters and Antioxidant Capability of Carassius auratus gibelio under Nitrite Stress. Master thesis. Huazhong Agriculture University. (in Chinese with English abstract)

    Google Scholar 

  • Ge L A. 2007. Effects of Supplemental Vitamin C and E in Ddiet under Nitrite Stress on Immune Function of Carassius auratus gibelio. Master thesis. Huazhong Agriculture University. (in Chinese with English abstract)

    Google Scholar 

  • Gouillou-Coustans M F, Bergot S J, Kaushik. 1998. Dietary ascorbic acid needs of common carp, Cyprinus carpio, larvae. Aquaculture, 161: 453–461.

    Article  Google Scholar 

  • Halliwell B, Gutteridge J M C. 1999. Free Radicals in Biology and Medicine. Oxford University Press, New York.

    Google Scholar 

  • Henriques M M F, Gomes E F et al. 1998. Influence of supplementation of practical diets with vitamin C on growth and response to hypoxic stress of seabream, Sparus aurata. Aquaculture, 161: 415–426.

    Article  Google Scholar 

  • Hermes Lima M, Storey J M, Storey K B. 1998. Antioxidant defenses and metabolic depression. The hypothesis of preparation for oxidative stress in land snails. Comp. Biochem. Physiol. B, 120: 437–448.

    Article  Google Scholar 

  • Hill W J, Hunter W G. 1966. A review of response surface methodology: a literature review. Tecimometric, 8: 571–590.

    Article  Google Scholar 

  • Hong M, Chen L, Qin J G, Sun X, Li E, Gu S, Yu N. 2009. Acute tolerance and metabolic responses of Chinese mitten crab (Eriocheir sinensis) juveniles to ambient nitrite. Comp. Biochem. Physiol. C Toxicol. Pharmacol., 149: 419–426.

    Article  Google Scholar 

  • Huang C H, Huang S L. 2004. Effect of dietary vitamin E level on growth, tissue lipid peroxidation, and liver glutathione level of juvenile hybrid tilapia, Oreochrom is niloticus × O. aureus, fed oxidized oil. Aquaculture, 237: 381–389.

    Article  Google Scholar 

  • Jensen F B. 2003. Nitrite disrupts multiple physiological functions in aquatic animals. Comp. Biochem. Physiol. A, 135: 9–24.

    Article  Google Scholar 

  • Ji J P, Wu Z B, Liu Q S, Zhang Y S, Ye M, Li M J. 1991. An ultramicro analytic and rapid method for determination of superoxide dismutase activity. J. Nanjing Railway Med. Coll., 10: 27–30. (in Chinese with English abstract)

    Google Scholar 

  • Kukreja R C, Okabe E, Schrier G M, Hess M L. 1988. Oxygen radical-mediated lipid peroxidation and inhibition of Ca2+-ATPase activity of cardiac sarcoplasmic reticulum. Arch. Biochem. Biophys., 261: 447–457.

    Article  Google Scholar 

  • Lee K J, Dabrowski K. 2004. Long-term effects and interactions of dietary vitamins C and E on growth and reproduction of yellow perch, Perca flavescens. Aquaculture, 230: 377–389.

    Article  Google Scholar 

  • Li H, Qiao G, Li Q, Zhou W, Won K M, Xu D H. 2010. Biological characteristics and pathogenicity of a highly pathogenic Shewanella marisflavi infected sea cucumber (Apostichopus japonicus). J. Fish Dis., 33: 865–877.

    Article  Google Scholar 

  • Li M, Chen L, Qin J G, Li E, Yu N, Du Z. 2013. Growth performance, antioxidant status and immune response in darkbarbel catfish Pelteobagrus vachelli fed different PUFA/vitamin E dietary levels and exposed to high or low ammonia. Aquaculture, 406–407: 18–27.

    Article  Google Scholar 

  • Li Y, Schellhorn H E. 2007. Rapid kinetic microassay for catalase activity. J. Biomol. Technol., 18: 185–187.

    Google Scholar 

  • Liao Y. 1980. The aspidochirote holothurians of China with erection of a new genus in echinoderms, present and past. In: Jangoux M ed. Proceeding of European Colloquium on Echinoderm. A. A. Balkema Publishers, Rotterdam, Netherlands. p.115–120.

    Google Scholar 

  • Liñán-Cabello. 2003. Carotenoids and retinal levels in captive and wild shrimp, Litopenaeus vannamei. Aquaculture Nutrition, 9(6): 383–389.

    Article  Google Scholar 

  • Liu Y, Wang W N, Wang A L, Wang J M, Sun R Y. 2007. Effects of dietary vitamin E supplementation on antioxidant enzyme activities in Litopenaeus vannamei (Boone, 1931) exposed to acute salinity changes. Aquaculture, 265: 351–358.

    Article  Google Scholar 

  • Livingstone D R. 2001. Contaminant-stimulated reactive oxygen species production and oxidative damage in aquatic organisms. Marine Pollution Bulletin, 42(8): 656–666.

    Article  Google Scholar 

  • Ma Y X, Xu G R, Zhang E P, Wang P, Chang Y Q. 2006. The etiology of acute peristome edema disease in cultured juveniles of Apostichopus japonicus. J. Fish China, 30: 377–382. (in Chinese with English abstract)

    Google Scholar 

  • Ma Y, Liu Z, Yang Z, Li M, Liu J, Song J. 2013. Effects of dietary live yeast Hanseniaspora opuntiae C21 on the immune and disease resistance against Vibrio splendidus infection in juvenile sea cucumber Apostichopus japonicus. Fish Shellfish Immun., 34: 66–73.

    Article  Google Scholar 

  • Mead R, Pike D J. 1975. A review of response surface methodology from a biometrics viewpoint. Biometrics, 31: 803–851.

    Article  Google Scholar 

  • Montero D et al. 1999. Effect of vitamin E and C dietary supplementation. Aquaculture, 171: 269–278.

    Article  Google Scholar 

  • Niu J, Lin H Z, Jiang S G, Chen X, Wu K C, Liu Y J, Wang S, Tian L X. 2013. Comparison of effect of chitin, chitosan, chitosan oligosaccharide and N-acetyl-d-glucosamine on growth performance, antioxidant defenses and oxidative stress status of Penaeus monodon. Aquaculture, 372–375: 1–8.

    Article  Google Scholar 

  • NRC (National Research Council). 1993. Nutrient Requirements of Fish. National Academy Press, Washington DC, USA.

    Google Scholar 

  • Ogutcu A, Uzunhisarcikli M, Kalender S, Durak D, Bayrakdar F, Kalender Y. 2006. The effects of organophosphate insecticide diazinon on malondialdehyde levels and myocardial cells in rat heart tissue and protective role of vitamin E. Pestic. Biochem. Phys., 86: 93–98.

    Article  Google Scholar 

  • Okorie O E, Ko S H, Go S, Lee S, Bae J Y, Han K, Bal S C. 2008. Preliminary study of the optimum dietary ascorbic acid level in sea cucumber, Apostichopus japonicus (Selenka). J. World Aquacult. Soc., 39: 758–765.

    Article  Google Scholar 

  • Oropesa A L, Garcia-Cambero J P, Soler F. 2009. Glutathione and malondialdehyde levels in common carp after exposure to simazine. Environ. Toxicol. Pharmacol., 27: 30–38.

    Article  Google Scholar 

  • Ortuño J, Esteban M A, Meseguer J. 2003. The effect of dietary intake of vitamins C and E on the stress response of gilthead seabream (Sparus aurata L.). Fish Shellfish Immun., 14: 145–156.

    Article  Google Scholar 

  • Pampanin D M, Camus L, Gomiero A, Marangon I, Volpato E, Nasci C. 2005. Susceptibility to oxidative stress of mussels (Mytilus galloprovincialis) in the Venice Lagoon (Italy). Mar. Pollut. Bull., 50: 1 548–1 557.

    Article  Google Scholar 

  • Pei S, Dong S, Wang F, Tian X, Gao Q. 2012. Effects of density on variation in individual growth and differentiation in endocrine response of Japanese sea cucumber (Apostichopus japonicus Selenka). Aquaculture, 356–357: 398–403.

    Article  Google Scholar 

  • Regoli F, Cerrano C, Chierici E. 2004. Seasonal variability of prooxidant pressure and antioxidant adaptation to symbiosis in the Mediterranean demosponge Petrosia ficiformis. Marine Ecology Progress Series, 275: 129–137.

    Article  Google Scholar 

  • Siers H. 1985. Oxidative Stress. Academic Press, New York. p.1–8.

    Google Scholar 

  • Sies H, Stahl W, Sundquist A. 1992. Antioxidant functions of vitamins. Ann. NYAcad. Sci., 669: 7–18.

    Article  Google Scholar 

  • Song J R, Zhang H P. 2009. Vitamin E effects on the malondialdehyde concentration and superoxide dismutase in skeletal muscle mitochondria following eccentric exercise in rats. Journal of Clinical Rehabilitative Tissue Engineering Research, 11: 2 086–2 090. (in Chinese with English abstract)

    Google Scholar 

  • Stormer J, Jensen F B, Rankin J C. 1996. Uptake of nitrite, nitrate, and bromide in rainbow trout, Oncorhynchus mykiss: effects on ionic balance. Can. J. Fish. Aquat. Sci., 53: 1 943–1 950.

    Article  Google Scholar 

  • Sun H, Liang M, Yan J, Chen B. 2004. Nutrient requirements and growth of the sea cucumber, Apostichopus japonicus. In: Lovatelli A, Conand C, Purcell S, Uthicke S, Hamel J F, Mercier A eds. Advances in Sea Cucumber Aquaculture and Management. FAO, Rome. p.327–331.

    Google Scholar 

  • Thompson I, White A, Fletcher T C, Houlihan D F, Secombes C J. 1993. The effect of stress on the immune response of Atlantic salmon Salmo salar L. fed diets containing different amounts of vitamin C. Aquaculture, 114: 1–18.

    Google Scholar 

  • Trenzado C E, Morales A E, de la Higuera M. 2008. Physiological changes in rainbow trout held under crowded conditions and fed diets with different levels of vitamins E and C and highly unsaturated fatty acids (HUFA). Aquaculture, 277: 293–302.

    Article  Google Scholar 

  • Uchiyama M, Mihara M. 1978. Determination of malonaldehyde precursor in tissues by thiobarbituric acid test. Anal. Biochem., 86: 271–278.

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Wang H, Liu C F, Qin C X, Cao S Q, Ding J. 2007. Using a macroalgae Ulva pertusa biofilter in a recirculating system for production of juvenile sea cucumber Apostichopus japonicus. Aquacult. Eng., 36: 217–224.

    Article  Google Scholar 

  • Wang J Q, Su J W, Jiang Y S, Zhang J C, Liang Z J. 2009. The effects of dietary vitamins C sources and levels on growth in juvenile sea cucumber (Apostichopus japonicus). Marine Sciences, 33: 56–63. (in Chinese with English abstract)

    Google Scholar 

  • Wang J Q, Su J W, Zhang K, Jiang Y S, Zhang J C, Liang Z J. 2010. The effects of dietary vitamin C sources and levels on immunity of juvenile sea cucumber (Apostichopus j aponicus). Fishery Sciences, 29(7): 381–386. (in Chinese with English abstract)

    Google Scholar 

  • Wang L U, Chen J C. 2005. The immune response of white shrimp Litopenaeus vann amei and its susceptibility to Vibrio alginolyticus at different salinity levels. Fish Shellfish Immun., 18: 269–278.

    Article  Google Scholar 

  • Wilson R P. 1973. Absence of ascorbic acid synthesis in channel catfish, Ictalurus punctatus and blue catfish Ictalurus furcatus. Comp. Biochem. Physiol. B, 46: 635–638.

    Google Scholar 

  • Yu F. 2011. Responeses of A postichopus japonicus (Selenka) to Chemical Stress Factors and Physiological and Ecological Mechanisim. Master thesis. Ocean University of China. (in Chinese with English abstract)

    Google Scholar 

  • Zang Y, Tian X, Dong S, Dong Y. 2012. Growth, metabolism and immune responses to evisceration and the regeneration of viscera in sea cucumber, Apostichopus japonicus. Aquaculture, 358–359: 50–60.

    Article  Google Scholar 

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Authors and Affiliations

  1. National & Local Joint Engineering Laboratory for Ecological Mariculture, Institute of Oceanology, Chinese Academy of Sciences, Qingdao, 266071, China

    Zuoyong Luo  (骆作勇), Baojie Wang  (王宝杰), Mei Liu  (刘梅), Keyong Jiang  (蒋克勇), Mingxing Liu  (刘明星) & Lei Wang  (王雷)

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Zuoyong Luo  (骆作勇)

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  1. Zuoyong Luo  (骆作勇)
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  2. Baojie Wang  (王宝杰)
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  3. Mei Liu  (刘梅)
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  4. Keyong Jiang  (蒋克勇)
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Correspondence to Lei Wang  (王雷).

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Supported by the Main Direction Program of Knowledge Innovation of Chinese Academy of Sciences (No. KZCX2-EWQ215)

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Luo, Z., Wang, B., Liu, M. et al. Effect of dietary supplementation of vitamin C on growth, reactive oxygen species, and antioxidant enzyme activity of Apostichopus japonicus (Selenka) juveniles exposed to nitrite. Chin. J. Ocean. Limnol. 32, 749–763 (2014). https://doi.org/10.1007/s00343-014-3310-4

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