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Effects of fructooligosaccharide on immune response, antioxidant capability and HSP70 and HSP90 expressions of blunt snout bream (Megalobrama amblycephala) under high ammonia stress

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Abstract

This study aimed to determine the effects of fructooligosaccharide (FOS) on immune response, antioxidant capability and HSP70 and HSP90 mRNA expressions of blunt snout bream (Megalobrama amblycephala) under high ammonia stress. A total of 360 fish were randomly distributed into three groups (each with four replicates) and were fed three levels of FOS (0, 0.4 and 0.8 %) for 8 weeks. After the feeding trial, 24 fish per tank were exposed to ammonia at 10 mg L−1. After stress, plasma cortisol and glucose levels of fish fed 0.4 % FOS were all significantly lower than that of the control group at 6 and 3 h, respectively. Plasma lysozyme and alternative complement pathway (ACH50) activities as well as nitrogen monoxide (NO) levels all increased significantly with the maximum levels being attained at 6, 6 and 3 h, respectively. Thereafter, these parameters all decreased significantly. In addition, fish fed 0.4 % FOS showed higher immune parameters under stress compared with that of control group. In addition, liver superoxide dismutase and catalase activities of fish fed 0.4 % FOS were both significantly higher than that of the control group before and after stress, while the opposite was true for malondialdehyde content. After stress, the expression of HSP70 and HSP90 of fish fed FOS was significantly higher than that of the control group at 6 and 12 h, respectively. After 12 h stress, the cumulative mortality of fish fed FOS was significantly lower than that of the control. The results indicated that the supplementation of 0.4 % FOS could increase the nonspecific immunity, antioxidant capacity and HSP70 and HSP90 expression of blunt snout bream and enhance its resistance to high ammonia stress.

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References

  • Ai Q, Xu H, Mai K, Xu W, Wang J, Zhang W (2011) Effects of dietary supplementation of Bacillus subtilis and fructooligosaccharide on growth performance, survival, non-specific immune response and disease resistance of juvenile large yellow croaker, Larimichthys crocea. Aquaculture 317:155–161

    Article  CAS  Google Scholar 

  • AOAC (1990) Official methods of analysis, 15th edn. Association of Analytical Chemists, Arlington

    Google Scholar 

  • Asadi F, Hallajian A, Asadian P, Shahriari A, Pourkabir M (2009) Serum lipid, free fatty acid, and proteins in juvenile sturgeons: Acipenser persicus and Acipenser stellatus. Comp Clin Path 18:287–289

    Article  CAS  Google Scholar 

  • Bagnyukova TV, Chahrak OI, Lushchak VI (2006) Coordinated response of goldfish antioxidant defenses to environmental stress. Aquat Toxicol 78:325–331

    Article  CAS  PubMed  Google Scholar 

  • Barton BA (2002) Stress in fishes: a diversity of responses with particular reference to changes in circulating corticosteroids. Integr Comp Biol 42:517–525

    Article  CAS  PubMed  Google Scholar 

  • Barton BA, Iwama GK (1991) Physiological changes in fish from stress in aquaculture with emphasis on the response and effects of corticosteroids. Annu Rev Fish Dis 1:3–26

    Article  Google Scholar 

  • Bonga SW (1997) The stress response in fish. Physiol Rev 77:591–625

    Google Scholar 

  • Bricknell I, Dalmo RA (2005) The use of immunostimulants in fish larval aquaculture. Fish Shellfish Immunol 19:457–472

    Article  CAS  PubMed  Google Scholar 

  • Chang CF, Su MS, Chen HY, Liao I (2003) Dietary β-1, 3-glucan effectively improves immunity and survival of Penaeus monodon challenged with white spot syndrome virus. Fish Shellfish Immunol 15:297–310

    Article  CAS  PubMed  Google Scholar 

  • Cheng AC, Cheng SA, Chen YY, Chen JC (2009) Effects of temperature change on the innate cellular and humoral immune responses of orange-spotted grouper (Epinephelus coioides) and its susceptibility to (Vibrio alginolyticus). Fish Shellfish Immunol 26:768–772

    Article  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

    Article  CAS  Google Scholar 

  • Cuesta A, Meseguer J, Esteban M (2004) Total serum immunoglobulin M levels are affected by immunomodulators in seabream (Sparus aurata L.). Vet Immunol Immunopathol 101:203–210

    Article  CAS  PubMed  Google Scholar 

  • De Maio A (1999) Heat shock proteins: facts, thoughts, and dreams. Shock 11:1–12

    Article  PubMed  Google Scholar 

  • Ellis AE (1990) Lysozyme assays. Tech fish Immunol 1:101–103

    Google Scholar 

  • Fabbri E, Capuzzo A, Moon TW (1998) The role of circulating catecholamines in the regulation of fish metabolism: an overview. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 120:177–192

    Article  CAS  PubMed  Google Scholar 

  • Farcy E, Serpentini A, Fiévet B, Lebel JM (2007) Identification of cDNAs encoding HSP70 and HSP90 in the abalone Haliotis tuberculata: transcriptional induction in response to thermal stress in hemocyte primary culture. Comp Biochem Physiol B Biochem Mol Biol 146:540–550

    Article  PubMed  Google Scholar 

  • Feder ME, Hofmann GE (1999) Heat-shock proteins, molecular chaperones, and the stress response: evolutionary and ecological physiology. Annu Rev Physiol 61:243–282

    Article  CAS  PubMed  Google Scholar 

  • Fu D, Chen J, Zhang Y, Yu Z (2011) Cloning and expression of a heat shock protein (HSP) 90 gene in the haemocytes of Crassostrea hongkongensis under osmotic stress and bacterial challenge. Fish Shellfish Immunol 31:118–125

    Article  CAS  PubMed  Google Scholar 

  • Gao Q, Zhao J, Song L, Qiu L, Yu Y, Zhang H, Ni D (2008) Molecular cloning, characterization and expression of heat shock protein 90 gene in the haemocytes of bay scallop Argopecten irradians. Fish Shellfish Immunol 24:379–385

    Article  CAS  PubMed  Google Scholar 

  • Grutter A, Pankhurst N (2000) The effects of capture, handling, confinement and ectoparasite load on plasma levels of cortisol, glucose and lactate in the coral reef fish Hemigymnus melapterus. J Fish Biol 57:391–401

    Article  CAS  Google Scholar 

  • Hall JL (2002) Heat-shock proteins, molecular chaperones, and the stress response. J Exp Bot 53:1–11

    Article  CAS  PubMed  Google Scholar 

  • Harris JO, Maguire GB, Edwards S, Hindrum SM (1998) Effect of ammonia on the growth rate and oxygen consumption of juvenile greenlip abalone, Haliotis laevigata Donovan. Aquaculture 160:259–272

    Article  CAS  Google Scholar 

  • He HJ, Liao LK, Yuan JF, Tang HY, Wu Q, Zhang GW (2006) Pathological observation of bacterial septicemia in Megalobrama amblycephala. J Southwest Agric Univ 3:483–490 (in chinese)

    Google Scholar 

  • Israeli-Weinstein D, Kimmel E (1998) Behavioral response of carp (Cyprinus carpio) to ammonia stress. Aquaculture 165:81–93

    Article  CAS  Google Scholar 

  • Janssens P, Waterman J (1988) Hormonal regulation of gluconeogenesis and glycogenolysis in carp (Cyprinus carpio) liver pieces cultured in vitro. Comp Biochem Physiol A Physiol 91:451–455

    Article  Google Scholar 

  • Jeney G, Nemcsok J, Jeney Z, Olah J (1992) Acute effect of sublethal ammonia concentrations on common carp (Cyprinus carpio L.). II. Effect of ammonia on blood plasma transaminases (GOT, GPT), G1DH enzyme activity, and ATP value. Aquaculture 104:149–156

    Article  CAS  Google Scholar 

  • Laiz-Carrión R, Sangiao-Alvarellos S, Guzmán JM, del Río MPM, Míguez JM, Soengas JL, Mancera JM (2002) Energy metabolism in fish tissues related to osmoregulation and cortisol action. Fish Physiol Biochem 27:179–188

    Article  Google Scholar 

  • Li P, Burr GS, Gatlin DM, Hume ME, Patnaik S, Castille FL, Lawrence AL (2007) Dietary supplementation of short-chain fructooligosaccharides influences gastrointestinal microbiota composition and immunity characteristics of pacific white shrimp, Litopenaeus vannamei, cultured in a recirculating system. J Nutr 137:2763–2768

    CAS  PubMed  Google Scholar 

  • Li XF, Liu WB, Lu KL, Xu WN, Wang Y (2012) Dietary carbohydrate/lipid ratios affect stress, oxidative status and non-specific immune responses of fingerling blunt snout bream, Megalobrama amblycephala. Fish Shellfish Immunol 33:316–323

    Article  CAS  PubMed  Google Scholar 

  • Li M, Chen L, Qin JG, 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 406:18–27

    Article  Google Scholar 

  • Lindquist S (1986) The heat-shock response. Annu Rev Biochem 55:1151–1191

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Lygren B, Hamre K, Waagbø R (1999) Effects of dietary pro-and antioxidants on some protective mechanisms and health parameters in Atlantic salmon. J Aquat Anim Health 11:211–221

    Article  Google Scholar 

  • Maule A, Tripp R, Kaattari S, Schreck C (1989) Stress alters immune function and disease resistance in chinook salmon (Oncorhynchus tshawytscha). J Endocrinol 120:135–142

    Article  CAS  PubMed  Google Scholar 

  • Mayer M, Bukau B (2005) Hsp70 chaperones: cellular functions and molecular mechanism. Cell Mol Life Sci 62:670–684

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Meade JW (1985) Allowable ammonia for fish culture. Prog Fish-Cultur 3:135–145

    Article  Google Scholar 

  • Ming J, Xie J, Xu P, Ge X, Liu W, Ye J (2012) Effects of emodin and vitamin C on growth performance, biochemical parameters and two HSP70s mRNA expression of Wuchang bream (Megalobrama amblycephala Yih) under high temperature stress. Fish Shellfish Immunol 32:651–661

    Article  CAS  PubMed  Google Scholar 

  • Möck A, Peters G (1990) Lysozyme activity in rainbow trout, Oncorhynchus mykiss (Walbaum), stressed by handling, transport and water pollution. J Fish Biol 37:873–885

    Article  Google Scholar 

  • Mommsen TP, Vijayan MM, Moon TW (1999) Cortisol in teleosts: dynamics, mechanisms of action, and metabolic regulation. Rev Fish Biol Fish 9:211–268

    Article  Google Scholar 

  • Montero D, Tort L, Izquierdo M, Robaina L, Vergara J (1998) Depletion of serum alternative complement pathway activity in gilthead seabream caused by α-tocopherol and n-3 HUFA dietary deficiencies. Fish Physiol Biochem 18:399–407

    Article  CAS  Google Scholar 

  • Morimoto RI (1998) Regulation of the heat shock transcriptional response: cross talk between a family of heat shock factors, molecular chaperones, and negative regulators. Genes Dev 12:3788–3796

    Article  CAS  PubMed  Google Scholar 

  • Muñoz M, Cedeño R, Rodríguez J, van der Knaap WP, Mialhe E, Bachère E (2000) Measurement of reactive oxygen intermediate production in haemocytes of the penaeid shrimp, Penaeus vannamei. Aquaculture 191:89–107

    Article  Google Scholar 

  • Niu J, Lin H-Z, Jiang SG, Chen X, Wu KC, Liu YJ, Wang S, Tian LX (2012) 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 372:1–8

    Google Scholar 

  • Nogueira C, Quinhones E, Jung E, Zeni G, Rocha J (2003) Anti-inflammatory and antinociceptive activity of diphenyl diselenide. Inflamm Res 52:56–63

    Article  CAS  PubMed  Google Scholar 

  • Nya EJ, Austin B (2009) Use of garlic, Allium sativum, to control Aeromonas hydrophila infection in rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32:963–970

    Article  CAS  PubMed  Google Scholar 

  • Ortuño J, Cuesta A, Rodríguez A, Esteban M, Meseguer J (2002) Oral administration of yeast, Saccharomyces cerevisiae, enhances the cellular innate immune response of gilthead seabream (Sparus aurata L.). Vet Immunol Immunopathol 85:41–50

    Article  PubMed  Google Scholar 

  • Pan X, Wu T, Zhang L, Cai L, Song Z (2009) Influence of oligosaccharides on the growth and tolerance capacity of lactobacilli to simulated stress environment. Lett Appl Microbiol 48:362–367

    Article  CAS  PubMed  Google Scholar 

  • Person-Le Ruyet J, Mahe K, Le Bayon N, Le Delliou H (2004) Effects of temperature on growth and metabolism in a Mediterranean population of European sea bass, Dicentrarchus labrax. Aquaculture 237:269–280

    Article  Google Scholar 

  • Pharmaceutiques UdL (1995) Dietary modulation of the human colonie microbiota: introducing the concept of prebiotics. J Nutr 125:1401–1412

    Google Scholar 

  • Pickering A, Stewart A (1984) Acclimation of the interrenal tissue of the brown trout, Salmo trutta L., to chronic crowding stress. J Fish Biol 24:731–740

    Article  Google Scholar 

  • Placer ZA, Cushman CL, Johnson BC (1966) Estimation of products of lipid peroxidation (Malonyldialdehyde) in biological fluids. Anal Biochem 16:359–364

  • Qiang J, Xu P, He J, Wang H, Li R (2011) The combined effects of external ammonia and crowding stress on growth and biochemical activities in liver of (GIFT) Nile ti-lapia juvenile (Oreochromis niloticus). J Fish China 12:1837–1848 [In Chinese]

    Google Scholar 

  • Reinhold JG (1953) Manual determination of serum total protein, albumin and globulin fractions by Biuret method. In: Reiner M (ed) Standard method of clinical chemistry. Academic Press, New York, p 83

    Google Scholar 

  • Russo RC (1985) Ammonia, nitrite, and nitrate. In: Petrocelli SR, Rand GM (eds) Fund Aquat Toxicol. Taylor & Francis, Bristol, pp 455–471

    Google Scholar 

  • Salze G, McLean E, Schwarz M, Craig S (2008) Dietary mannan oligosaccharide enhances salinity tolerance and gut development of larval cobia. Aquaculture 274:148–152

    Article  CAS  Google Scholar 

  • Santoro MG (2000) Heat shock factors and the control of the stress response. Biochem Pharmacol 59:55–63

    Article  CAS  PubMed  Google Scholar 

  • Sheikhzadeh N, Tayefi-Nasrabadi H, Oushani AK, Enferadi MHN (2012) Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:413–419

    Article  CAS  PubMed  Google Scholar 

  • Small BC (2004) Effect of isoeugenol sedation on plasma cortisol, glucose, and lactate dynamics in channel catfish Ictalurus punctatus exposed to three stressors. Aquaculture 238:469–481

    Article  CAS  Google Scholar 

  • Soleimani N, Hoseinifar SH, Merrifield DL, Barati M, Abadi ZH (2012) Dietary supplementation of fructooligosaccharide (FOS) improves the innate immune response, stress resistance, digestive enzyme activities and growth performance of Caspian roach (Rutilus rutilus) fry. Fish Shellfish Immunol 32:316–321

    Article  CAS  PubMed  Google Scholar 

  • Solorzano L (1969) Determination of ammonia in natural waters by the phenolhypochlorite method. Limnol Oceanogr 14:799–801

    Article  CAS  Google Scholar 

  • Stratford MR, Dennis MF, Cochrane R, Parkins CS, Everett SA (1997) The role of nitric oxide in cancer improved methods for measurement of nitrite and nitrate by high-performance ion chromatography. J Chromatogr A 770:151–155

    Article  CAS  PubMed  Google Scholar 

  • Sun SM, Ge XP, Xuan FJ, Zhu J, Yu N (2014) Nitrite-induced hepatotoxicity in Bluntsnout bream (Megalobrama amblycephala): the mechanistic insight from transcriptome to physiology analysis. Environ Toxicol Pharmacol 1:55–65

    Article  Google Scholar 

  • Talpur AD, Ikhwanuddin M (2012) Azadirachta indica (Neem) leaf dietary effects on the immunity response and disease resistance of Asian seabass, Lates calcarifer challenged with Vibrio harveyi. Fish Shellfish Immunol 34:254–264

    Article  PubMed  Google Scholar 

  • Wang SH, Chen JC (2005) The protective effect of chitin and chitosan against Vibrio alginolyticus in white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 19:191–204

    Article  PubMed  Google Scholar 

  • Wang X, Wang L, Yao C, Qiu L, Zhang H, Zhi Z, Song L (2012) Alternation of immune parameters and cellular energy allocation of Chlamys farreri under ammonia-N exposure and Vibrio anguillarum challenge. Fish Shellfish Immunol 32:741–749

    Article  CAS  PubMed  Google Scholar 

  • Wei T, Gao Y, Wang R, Xu T (2013) A heat shock protein 90 β isoform involved in immune response to bacteria challenge and heat shock from Miichthys miiuy. Fish Shellfish Immunol 35:429–437

    Article  CAS  PubMed  Google Scholar 

  • Winberg S, Lepage O (1998) Elevation of brain 5-HT activity, POMC expression, and plasma cortisol in socially subordinate rainbow trout. Am J Physiol Regul Integr Comp Physiol 274:R645–R654

    CAS  Google Scholar 

  • Wojtaszek Pa (1997) Oxidative burst: an early plant response to pathogen infection. Biochem J 322:681–692

    CAS  PubMed Central  PubMed  Google Scholar 

  • Wu CX, Zhao FY, Zhang Y, Zhu YJ, Ma MS, Mao HL, Hu C-Y (2012) Overexpression of Hsp90 from grass carp (Ctenopharyngodon idella) increases thermal protection against heat stress. Fish Shellfish Immunol 33:42–47

    Article  CAS  PubMed  Google Scholar 

  • Wu Y, Liu WB, Li HY, Xu WN, He JX, Li XF, Jiang GZ (2013) Effects of dietary supplementation of fructooligosaccharide (FOS) on growth performance, body composition, intestine enzymes activities and histology of blunt snout bream (Megalobrama amblycephala) fingerlings. Aquac Nutr 16:886–894

    Article  Google Scholar 

  • Zhang Q, Tan B, Mai K, Zhang W, Ma H, Ai Q, Wang X, Liufu Z (2011) Dietary administration of Bacillus (B. licheniformis and B. subtilis) and isomaltooligosaccharide influences the intestinal microflora, immunological parameters and resistance against Vibrio alginolyticus in shrimp, Penaeus japonicus (Decapoda: Penaeidae). Aquac Res 42:943–952

    Article  CAS  Google Scholar 

  • Zhang J, Liu YJ, Tian LX, Yang HJ, Liang GY, Xu DH (2012) Effects of dietary mannan oligosaccharide on growth performance, gut morphology and stress tolerance of juvenile Pacific white shrimp Litopenaeus vannamei. Fish Shellfish Immunol 4:1027–1032

    Article  Google Scholar 

  • Zhang CN, Li XF, Xu WN, Jiang GZ, Lu KL, Wang LN, Liu WB (2013) Combined effects of dietary fructooligosaccharide and Bacillus licheniformis on innate immunity, antioxidant capability and disease resistance of triangular bream (Megalobrama terminalis). Fish Shellfish Immunol 35:1380–1386

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

The present study was funded by the National Technology System for Conventional Freshwater Fish Industries of China (CARS-46-20) in collaboration with the Science and Technology Support Program from Jiangsu Province (China, BE2010394).

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  1. Key Laboratory of Aquatic Nutrition and Feed Science of Jiangsu Province, College of Animal Science and Technology, Nanjing Agricultural University, No. 1 Weigang Road, Nanjing, 210095, Jiangsu Province, People’s Republic of China

    Chun-Nuan Zhang, Xiang-Fei Li, Hong-Yan Tian, Ding-Dong Zhang, Guang-Zhen Jiang, Kang-Le Lu, Guang-Xia Liu & Wen-Bin Liu

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  1. Chun-Nuan Zhang
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Zhang, CN., Li, XF., Tian, HY. et al. Effects of fructooligosaccharide on immune response, antioxidant capability and HSP70 and HSP90 expressions of blunt snout bream (Megalobrama amblycephala) under high ammonia stress. Fish Physiol Biochem 41, 203–217 (2015). https://doi.org/10.1007/s10695-014-0017-6

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