Advertisement

Fish Physiology and Biochemistry

, Volume 45, Issue 1, pp 187–197 | Cite as

Effects of partial replacement of fish meal by yeast hydrolysate on antioxidant capability, intestinal morphology, and inflammation-related gene expression of juvenile Jian carp (Cyprinus carpio var. Jian)

  • Xiang-Yang Yuan
  • Guang-Zhen Jiang
  • Cong-Cong Wang
  • Kenneth Prudence Abasubong
  • Qing Zou
  • Yu-Yan Zhou
  • Wen-Bin LiuEmail author
Article
  • 145 Downloads

Abstract

This study aimed to evaluate the effects of fish meal (FM) replacement by yeast hydrolysate (YH) on liver antioxidant capability, intestinal morphology, and inflammation-related genes of juvenile Jian carp (Cyprinus carpio var. Jian). A total of 600 fish (average initial weight 19.44 ± 0.06 g) were randomly selected and divided into five groups. Five isonitrogenous and isocaloric diets replacing FM by YH 0% (YH0), 1% (YH1), 3% (YH3), 5% (YH5), and 7% (YH7) were formulated. Each diet was tested in four replicates for 10 weeks. The results have shown that, compared to the control group (YH0), liver total superoxide dismutase (t-SOD), catalase (CAT), glutathione peroxidase (GPX), and glutathione (GSH) activities of fish fed YH1 and YH3 diets were significantly higher (P < 0.05). Liver malondialdehyde (MDA) concentration significantly increased as supplementation levels of YH increased from 1 to 7% (P < 0.05). Moreover, intestinal microvillus length of juvenile Jian carp fed YH diets were significantly higher than that of fish fed the control diet (P < 0.05). In proximal intestine, the relative expression levels of inflammation-related genes (ALP, IL-1β, and TNF-α) in YH7 were significantly higher than that in the control group (P < 0.05). However, in midintestine, the expression levels of these genes in YH3 were significantly lower compared to the control group (P < 0.05). The results of this study indicated that dietary replacement of FM by 3%YH could improve antioxidant capability and intestinal microvillus morphology, as well as enhance the non-specific immunity of juvenile Jian carp.

Keywords

Yeast hydrolysate Cyprinus carpio var. Jian Antioxidant capacity Intestinal histology Gene expression 

Notes

Funding information

This research was funded by the earmarked fund for China Agriculture Research System (CARS-45-14), the National Natural Science Foundation of China (31502178) and the Fundamental Research Funds for the Central Universities (KJQN201612).

References

  1. AOAC (Association of Official Analytical Chemists) (1995) Official methods of analysis. AOAC, Arlington, p 1298Google Scholar
  2. Cerezuela R, Fumanal M, Tapia-Paniagua ST, Meseguer J, Moriñigo MA, Esteban MA (2012) Histological alterations and microbial ecology of the intestine in gilthead seabream (Sparus aurata L.) fed dietary probiotics and microalgae. Cell Tissue Res 350:477–489CrossRefGoogle Scholar
  3. Cerezuela R, Meseguer J, Esteban MÁ (2013) Effects of dietary inulin, bacillus subtilis and microalgae on intestinal gene expression in gilthead seabream (Sparus aurata L.). Fish Shellfish Immunol 34:843–848CrossRefGoogle Scholar
  4. Dabas A, Nagpure N, Kumar R, Kushwaha B, Kumar P, Lakra W (2012) Assessment of tissue-specific effect of cadmium on antioxidant defense system and lipid peroxidation in freshwater murrel, Channa punctatus. Fish Physiol Biochem 38:469–482CrossRefGoogle Scholar
  5. Dimitroglou A, Merrifield DL, Moate R, Davies SJ, Spring P, Sweetman J, Bradley G (2009) Dietary mannan oligosaccharide supplementation modulates intestinal microbial ecology and improves gut morphology of rainbow trout, Oncorhynchus mykiss (Walbaum). J Anim Sci 87:3226–3234CrossRefGoogle Scholar
  6. Dimitroglou A, Merrifield DL, Spring P, Sweetman J, Moate R, Davies SJ (2010) Effects of mannan oligosaccharide (MOS) supplementation on growth performance, feed utilisation, intestinal histology and gut microbiota of gilthead sea bream (Sparus aurata). Aquaculture 300:182–188CrossRefGoogle Scholar
  7. Dimitroglou A, Merrifield DL, Carnevali O, Picchietti S, Avella M, Daniels C, Güroy D, Davies SJ (2011) Microbial manipulations to improve fish health and production a Mediterranean perspective. Fish Shellfish Immunol 30:1–16CrossRefGoogle Scholar
  8. FAO (Food and Agricultural Organization of the United Nations) (2015) Fisheries and aquaculture department, Rome, Italy. http://www.fao.org/fishery/statistics/global-commodities-production/en
  9. Farombi E, Adelowo O, Ajimoko Y (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. Int J Environ Res Public Health 4:158–165CrossRefGoogle Scholar
  10. Gonzalez B, François J, Renaud M (1997) A rapid and reliable method for metabolite extraction in yeast using boiling buffered ethanol. Yeast 13:1347–1355CrossRefGoogle Scholar
  11. Halliwell B (2006) Reactive species and antioxidants redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322CrossRefGoogle Scholar
  12. He S, Zhou Z, Meng K, Zhao H, Yao B, Ringø E, Yoon I (2011) Effects of dietary antibiotic growth promoter and Saccharomyces cerevisiae fermentation product on production, intestinal bacterial community, and nonspecific immunity of hybrid tilapia (Oreochromis niloticus female×Oreochromis aureus male). J Anim Sci 89:84–92CrossRefGoogle Scholar
  13. Hu C, Xu Y, Xia M, Xiong L, Xu Z (2007) Effects of Cu2+-exchanged montmorillonite on growth performance, microbial ecology and intestinal morphology of Nile tilapia (Oreochromis niloticus). Aquaculture 70:200–206CrossRefGoogle Scholar
  14. Huttenhuis HBT, Taverne-Thiele AJ, Grou CPO, Bergsma J, Saeij JPJ, Nakayasu C, Rombout JHWM (2006) Ontogeny of the common carp (Cyprinus carpio L.) innate immune system. Dev Comp Immunol 30:557–574CrossRefGoogle Scholar
  15. Jovanović-Galović A, Blagojević DP, Grubor-Lajšić G, Worland R, Spasić MB (2004) Role of antioxidant defense during different stages of preadult life cycle in European corn borer (Ostrinia nubilalis, Hubn.): diapause and metamorphosis. Arch Insect Biochem Physiol 55:79–89CrossRefGoogle Scholar
  16. Kaneko T, Yokoyama A, Suzuki M (1995) Digestibility characteristics of isomaltooligosaccharides in comparison with several saccharides using the rat jejunum loop method. Biosci Biotechnol Biochem 59:1190–1194CrossRefGoogle Scholar
  17. Kiron V (2012) Fish immune system and its nutritional modulation for preventive health care. Anim Feed Sci Technol 173:111–133CrossRefGoogle Scholar
  18. Lara-Flores M, Olvera-Novoa MA, Guzman-Méndez BE, López-Madrid W (2003) Use of the bacteria Streptococcus faeciumand and Lactobacillus acidophilus, and the yeast Saccharomyces cerevisiae as growth promoters in Nile tilapia (Oreochromis niloticus). Aquaculture 216:193–201CrossRefGoogle Scholar
  19. Lemaire P, Matthews A, Forlin L, Livingstone DR (1994) Stimulation of oxyradical production of hepatic microsomes of flounder (Platichthys flesus) and perch (Perca fluvialis) by model and pollutant xenobiotics. Arch Environ Contam Toxicol 26:191–200CrossRefGoogle Scholar
  20. Li P, Dmiii G (2003) Evaluation of brewer’s yeast (Saccharomyces cerevisiae) as a feed supplement for hybrid striped bass (Morone chrysops×M. saxatilis). Aquaculture 219:681–692CrossRefGoogle Scholar
  21. Li XF, Liu WB, Jiang YY, Zhu H, Ge XP (2010) Effects of dietary protein and lipid levels in practical diets on growth performance and body composition of blunt snout bream (Megalobrama amblycephala) fingerlings. Aquaculture 303:65–70CrossRefGoogle Scholar
  22. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(−Delta Delta C (T)) method. Methods 25:402–408CrossRefGoogle Scholar
  23. López-López E, Sedeño-Díaz JE, Soto C, Favari L (2011) Responses of antioxidant enzymes, lipid peroxidation, and Na+/K+-ATPase in liver of the fish Goodea atripinnis exposed to Lake Yuriria water. Fish Physiol Biochem 37:511–522CrossRefGoogle Scholar
  24. Marklund S, Marklund G (1974) Involvement of the superoxide anion radical in the autoxidation of pyrogallol and a convenient assay for superoxide dismutase. Eur J Biochem 47:469–474CrossRefGoogle Scholar
  25. Merrifield DL, Dimitroglou A, Bradley G, Baker R, Davies S (2009) Soybean meal alters autochthonous microbial populations, microvilli morphology and compromises intestinal enterocyte integrity of rainbow trout, Oncorhynchus mykiss (Walbaum). J Fish Dis 32:755–766CrossRefGoogle Scholar
  26. Merrifield DL, Dimitroglou A, Foey A, Davies SJ, Baker RTM, Bøgwald J, Castex M, Ringø E (2010) The current status and future focus of probiotic and prebiotic applications for salmonids. Aquaculture 302:1–18CrossRefGoogle Scholar
  27. Mohsen A, Mamdouhaa M, Maalya M (2010) Use of live baker's yeast, Saccharomyces cerevisiae, in practical diet to enhance the growth performance of galilee tilapia, Sarotherodon galilaeus (L.), and its resistance to environmental copper toxicity. J World Aquacult Soc 41:214–223CrossRefGoogle Scholar
  28. Nayak SK (2010) Role of gastrointestinal microbiota in fish. Aquac Res 41:1553–1573CrossRefGoogle Scholar
  29. Niklasson L, Sundh H, Fridell F, Taranger G, Sundell K (2011) Disturbance of the intestinal mucosal immune system of farmed Atlantic salmon (Salmo salar), in response to long-term hypoxic conditions. Fish Shellfish Immunol 31:1072–1080CrossRefGoogle Scholar
  30. Ortuno J, Cuesta A, Rodríguez A, Esteban MA, Meseguer J (2002) Oral administration of yeast, Saccharomyces cerevisiae, enhances the cellular innate immune response of gilthead seabream (Sparus aurata L.). Vet Immunol Immunopathol 85:41–50CrossRefGoogle Scholar
  31. Parvez S, Raisuddin S (2005) Protein carbonyls: novel biomarkers of exposure to oxidative stress-inducing pesticides in freshwater fish Channa punctata (Bloch). Environ Toxicol Pharmacol 20:112–117CrossRefGoogle Scholar
  32. Péres A, Infante JLZ, Cahu C (1998) Dietary regulation of activities and mRNA levels of trypsin and amylase in sea bass (Dicentrarchus labrax) larvae. Fish Physiol Biochem 19:145–152CrossRefGoogle Scholar
  33. Pouramini M, Alghasem KA, Almajid HMA, Rasoul G, Morteza A (2008) Effect of feeding by yeast (Saccharomyces cerevisiae) as a probiotic, in contrast with salinity stress and on intestinal histology in rainbow trout (Oncorhynchus mykiss) fry. J Fisheries 2:33–40Google Scholar
  34. Prior RL (2004) Biochemical measures of antioxidant status. Top Clin Nutr 19:226–238CrossRefGoogle Scholar
  35. Ran C, Huang L, Liu Z, Xu L, Yang YL, Philippe T, Eric A, Zhou ZG (2015) A comparison of the beneficial effects of live and heat-inactivated baker’s yeast on Nile Tilapia: suggestions on the role and function of the secretory metabolites released from the yeast. PLoS One 10:e0145448CrossRefGoogle Scholar
  36. Reyes-Becerril M, Tovar-Ramírez D, Ascencio-Valle F, Civera-Cerecedo R, Gracia-López V, Barbosa-Solomieu V, Esteban MÁ (2010) Effects of dietary supplementation with probiotic live yeast Debaryomyces hansenii on the immune and antioxidant systems of leopard grouper Mycteroperca rosacea infected with Aeromonas hydrophila. Aquac Res 42:1676–1686CrossRefGoogle Scholar
  37. Reyes-Becerril M, Guardiola F, Rojas M, Ascenciovalle F, Esteban MÁ (2013) Dietary administration of microalgae Navicula sp. affects immune status and gene expression of gilthead seabream (Sparus aurata). Fish Shellfish Immunol 35:883–891CrossRefGoogle Scholar
  38. Salze G, Mclean E, Schwarz MH, Craig SR (2008) Dietary mannan oligosaccharide enhances salinity tolerance and gut development of larval cobia. Aquaculture 274:148–152CrossRefGoogle Scholar
  39. Sang HM, Ky LT, Fotedar R (2009) Dietary supplementation of mannan oligosaccharide improves the immune responses and survival of marron, Cheraxtenuimanus (Smith, 1912) when challenged with different stressors. Fish Shellfish Immunol 27:341–348CrossRefGoogle Scholar
  40. Satho K (1978) Serum lipid peroxidation in cerebrovascular disorders determined by a new colorimetric method. Clin Chim Acta 190:37–43Google Scholar
  41. Sato T, Okamoto N (2010) Induction of virus-specific cell-mediated cytotoxic responses of isogeneic ginbuna crucian carp, after oral immunization with inactivated virus. Fish Shellfish Immunol 29:414–421CrossRefGoogle Scholar
  42. Secombes CJ, Wang T, Hong S, Peddie S, Crampe M, Laing KJ, Cunningham C, Zou J (2001) Cytokines and innate immunity of fish. Dev Comp Immunol 25:713–723CrossRefGoogle Scholar
  43. Sheikhzadeh N, Tayefi-Nasrabadi H, Oushani AK, Enferadi MH (2012) Effects of Haematococcus pluvialis supplementation on antioxidant system and metabolism in rainbow trout (Oncorhynchus mykiss). Fish Physiol Biochem 38:413–419CrossRefGoogle Scholar
  44. Sinha AK (1972) Colorimetric assay of catalase. Anal Biochem 47:389–394CrossRefGoogle Scholar
  45. Teuber M (2001) Veterinary use and antibiotic resistance. Curr Opin Microbiol 4:493–499CrossRefGoogle Scholar
  46. Torrecillas S, Makol A, Caballero MJ, Montero D, Robaina L (2007) Immune stimulation and improved infection resistance in European seabass (Dicentrarchus labrax) fed mannan oligosaccharides. Fish Shellfish Immunol 23:969–981CrossRefGoogle Scholar
  47. Treadway S (1998) An Ayurvedic herbal approach to a healthy liver. Clin Nutr Insights 6:1–3Google Scholar
  48. Valavanidis A, Vlahogianni T, Dassenakis M, Scoullos M (2006) Molecular biomarkers of oxidative stress in aquatic organisms in relation to toxic environmental pollutants. Ecotoxicol Environ Saf 64:178–179CrossRefGoogle Scholar
  49. Wang LN, Liu WB, Lu KL, Xu WN, Cai DS, Zhang CN, Qian Y (2014) Effects of dietary carbohydrate/lipid ratios on non-specific immune responses, oxidative status and liver histology of juvenile yellow catfish Pelteobagrus fulvidraco. Aquaculture 426–427:41–48CrossRefGoogle Scholar
  50. Winston GW, Giulio RTD (1991) Prooxidant and antioxidant mechanisms in aquatic organisms. Aquat Toxicol 19:137–161CrossRefGoogle Scholar
  51. Yuan XY, Liu WB, Liang C, Sun CX, Xue YF, Wan ZD, Jiang GZ (2017) Effects of partial replacement of fish meal by yeast hydrolysate on complement system and stress resistance in juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 67:312–321CrossRefGoogle Scholar
  52. Zanello G, Meurens F, Berri M, Chevaleyre C, Melo S, Auclair E, Salmon H (2011) Saccharomyces cerevisiae decreases inflammatory responses induced by F4+ enterotoxigenic Escherichia coli in porcine intestinal epithelial cells. Vet Immunol Immunopathol 141:133–138CrossRefGoogle Scholar
  53. 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 33:1027–1032CrossRefGoogle Scholar
  54. Zhang YY, Liu B, Ge XP, Liu WB, Xie J, Ren MC, Cui YT, Xia SL, Chen RL, Zhou QL, Pan LK (2014) The influence of various feeding patterns of emodin on growth, non-specific immune responses, and disease resistance to Aeromonas hydrophila in juvenile Wuchang bream (Megalobrama amblycephala). Fish Shellfish Immunol 36:187–193CrossRefGoogle Scholar
  55. Zhu H, Liu H, Yan J, Wang R, Liu L (2012) Effect of yeast polysaccharide on some hematologic parameter and gut morphology in channel catfish (Ictalurus punctatus). Fish Physiol Biochem 38:1441–1447CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2018

Authors and Affiliations

  • Xiang-Yang Yuan
    • 1
  • Guang-Zhen Jiang
    • 1
  • Cong-Cong Wang
    • 1
  • Kenneth Prudence Abasubong
    • 1
  • Qing Zou
    • 2
  • Yu-Yan Zhou
    • 2
  • Wen-Bin Liu
    • 1
    Email author
  1. 1.Laboratory of Aquatic Nutrition and Ecology, College of Animal Science and TechnologyNanjing Agricultural UniversityNanjingPeople’s Republic of China
  2. 2.Guangdong Hinabiotech CO., LtdGuangzhouPeople’s Republic of China

Personalised recommendations