The effect of Spirulina platensis meal on antioxidant gene expression, total antioxidant capacity, and lipid peroxidation of rainbow trout (Oncorhynchus mykiss)

  • Mahdi TeimouriEmail author
  • Sakineh Yeganeh
  • Ghodrat Rahimi Mianji
  • Mojtaba Najafi
  • Soleiman Mahjoub


The study was conducted to investigate the effect of diets containing 0, 2.5, 5, 7.5, and 10% S. platensis meal on total antioxidant capacity (TAC) and lipid peroxidation, as well as the expression of two antioxidant enzyme genes (SOD and CAT) in rainbow trout (Oncorhynchus mykiss). One hundred and eighty fish, with an average initial weight of 101 ± 8 g, were cultured for 10 weeks. At the end of experiment, lipid peroxidation significantly decreased in serum of fish fed with S. platensis and fish fed with 5, 7.5, and 10% microalgae showed a significantly lower value compared to control and 2.5%. Inclusion of 7.5 and 10% S. platensis in diet also decreased lipid peroxidation in liver. TAC significantly increased with increasing level of S. platensis. Expression level of superoxide dismutase (SOD) and catalase (CAT) genes significantly increased in the fish liver after administration of microalgae and fish fed with 10% S. platensis in diet showed the highest level compared to the other treatments. The present study reveals that inclusion of 10% S. platensis in diet can decrease oxidative stress in rainbow trout. Therefore, S. platensis can be used as potential antioxidant for fish farming.


Spirulina platensis Total antioxidant capacity (TAC) Lipid peroxidation Antioxidant gene expression Rainbow trout (Oncorhynchus mykiss



The authors would like to thank research council of the Sari Agricultural Sciences and Natural Resources University (Project No. 08-1393-01), Sari, Iran, for supporting this research. The authors would like to acknowledge the Iranian National Elite Foundation. We are grateful to Dr. Evangeline Foronda for English editing.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abdelkhalek NK, Ghazy EW, Abdel-Daim MM (2015) Pharmacodynamic interaction of Spirulina platensis and deltamethrin in freshwater fish Nile tilapia, Oreochromis niloticus: impact on lipid peroxidation and oxidative stress. Environ Sci Pollut Res 22(4):3023–3031CrossRefGoogle Scholar
  2. AOAC (2000) Chapter 4. In: Official methods of analysis of the Association of Official Analytical Chemists, 17th edn. AOAC, Arlington, pp 1–40Google Scholar
  3. Asakawa T, Matsushita S (1979) Thiobarbituric acid test for detecting lipid peroxides. Lipids 14(4):401–406CrossRefGoogle Scholar
  4. Benedetti S, Benvenuti F, Pagliarani S, Francogli S, Scoglio S, Canestrari F (2004) Antioxidant properties of a novel phycocyanin extract from the blue-green alga Aphanizomenon flos-aquae. Life Sci 75(19):2353–2362CrossRefGoogle Scholar
  5. Benzie IF, Strain J (1996) The ferric reducing ability of plasma (FRAP) as a measure of “antioxidant power”: the FRAP assay. Anal Biochem 239(1):70–76CrossRefGoogle Scholar
  6. Bhat VB, Madyastha K (2001) Scavenging of peroxynitrite by phycocyanin and phycocyanobilin from Spirulina platensis: protection against oxidative damage to DNA. Biochem Biophys Res Commun 285(2):262–266CrossRefGoogle Scholar
  7. Bhattacharya A, Lawrence RA, Krishnan A, Zaman K, Sun D, Fernandes G (2003) Effect of dietary n-3 and n-6 oils with and without food restriction on activity of antioxidant enzymes and lipid peroxidation in livers of cyclophosphamide treated autoimmune-prone NZB/W female mice. J Am Coll Nutr 22(5):388–399CrossRefGoogle Scholar
  8. Cahu C, Infante JZ, Peres A, Quazuguel P, Le Gall M (1998) Algal addition in sea bass (Dicentrarchus labrax) larvae rearing: effect on digestive enzymes. Aquaculture 161(1):479–489CrossRefGoogle Scholar
  9. Castex M, Lemaire P, Wabete N, Chim L (2009) Effect of dietary probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress status of shrimp Litopenaeus stylirostris. Aquaculture 294(3):306–313CrossRefGoogle Scholar
  10. Castex M, Lemaire P, Wabete N, Chim L (2010) Effect of probiotic Pediococcus acidilactici on antioxidant defences and oxidative stress of Litopenaeus stylirostris under Vibrio nigripulchritudo challenge. Fish Shellfish Immunol 28(4):622–631CrossRefGoogle Scholar
  11. Chaiyapechara S, Casten MT, Hardy RW, Dong FM (2003) Fish performance, fillet characteristics, and health assessment index of rainbow trout (Oncorhynchus mykiss) fed diets containing adequate and high concentrations of lipid and vitamin E. Aquaculture 219(1):715–738CrossRefGoogle Scholar
  12. Chien YH, Pan CH, Hunter B (2003) The resistance to physical stresses by Penaeus monodon juveniles fed diets supplemented with astaxanthin. Aquaculture 216(1):177–191CrossRefGoogle Scholar
  13. Dasgupta T, Banerjee S, Yadav P, Rao A (2001) Chemomodulation of carcinogen metabolising enzymes, antioxidant profiles and skin and fore-stomach papillomagenesis by Spirulina platensis. Mol Cell Biochem 226(1):17–26CrossRefGoogle Scholar
  14. Duncan PL, Klesius PH (1996) Effects of feeding Spirulina on specific and nonspecific immune responses of channel catfish. J Aquat Anim Health 8(4):308–313CrossRefGoogle Scholar
  15. Gad AS, Khadrawy YA, El-Nekeety AA, Mohamed SR, Hassan NS, Abdel-Wahhab MA (2011) Antioxidant activity and hepatoprotective effects of whey protein and Spirulina in rats. Nutrition 27(5):582–589CrossRefGoogle Scholar
  16. Gholami M, Roushan MH, Mahjoub S, Bijani A (2012) How is total antioxidant status in plasma of patients with brucellosis? Caspian J Intern Med 3(1):363–367PubMedPubMedCentralGoogle Scholar
  17. Kawatsu H (1969) Studies on the anemia of fish-III. An example of macrocytic anemia found in brook trout, Salvelinus fontinalis. Bull Freshw Res Lab 19:161–167Google Scholar
  18. Kuang S-Y, Xiao W-W, Feng L, Liu Y, Jiang J, Jiang W-D, Hu K, Li S-H, Tang L, Zhou X-Q (2012) Effects of graded levels of dietary methionine hydroxy analogue on immune response and antioxidant status of immune organs in juvenile Jian carp (Cyprinus carpio var. Jian). Fish Shellfish Immunol 32(5):629–636CrossRefGoogle Scholar
  19. Li X-L, Xu G, Chen T, Wong Y-S, Zhao H-L, Fan R-R, Gu X-M, Tong PC, Chan JC (2009) Phycocyanin protects INS-1E pancreatic beta cells against human islet amyloid polypeptide-induced apoptosis through attenuating oxidative stress and modulating JNK and p38 mitogen-activated protein kinase pathways. Int J Biochem Cell Biol 41(7):1526–1535CrossRefGoogle Scholar
  20. Lin YH, Shiau SY (2005) Dietary vitamin E requirement of grouper, Epinephelus malabaricus, at two lipid levels, and their effects on immune responses. Aquaculture 248(1):235–244CrossRefGoogle Scholar
  21. Lin Y-C, Vaseeharan B, Chen J-C (2008) Identification and phylogenetic analysis on lipopolysaccharide and β-1, 3-glucan binding protein (LGBP) of kuruma shrimp Marsupenaeus japonicus. Dev Comp Immunol 32(11):1260–1269CrossRefGoogle Scholar
  22. Lin YC, Tayag CM, Huang CL, Tsui WC, Chen JC (2010) White shrimp Litopenaeus vannamei that had received the hot-water extract of Spirulina platensis showed earlier recovery in immunity and up-regulation of gene expressions after pH stress. Fish Shellfish Immunol 29(6):1092–1098CrossRefGoogle Scholar
  23. Liu Y, Wang WN, Wang AL, Wang JM, Sun RY (2007) Effects of dietary vitamin E supplementation on antioxidant enzyme activities in Litopenaeus vannamei (Boone, 1931) exposed to acute salinity changes. Aquaculture 265(1):351–358CrossRefGoogle Scholar
  24. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods 25(4):402–408CrossRefGoogle Scholar
  25. Lu J, Takeuchi T (2004) Spawning and egg quality of the tilapia Oreochromis niloticus fed solely on raw Spirulina throughout three generations. Aquaculture 234(1):625–640CrossRefGoogle Scholar
  26. Martins DA, Afonso LO, Hosoya S, Lewis-McCrea LM, Valente LM, Lall SP (2007) Effects of moderately oxidized dietary lipid and the role of vitamin E on the stress response in Atlantic halibut (Hippoglossus hippoglossus L.). Aquaculture 272(1):573–580CrossRefGoogle Scholar
  27. Mathew S, Kumar KA, Anandan R, Nair PV, Devadasan K (2007) Changes in tissue defence system in white spot syndrome virus (WSSV) infected Penaeus monodon. Comp Biochem Physiol C 145(3):315–320Google Scholar
  28. Miranda M, Cintra R, Barros S, Mancini-Filho J (1998) Antioxidant activity of the microalga Spirulina maxima. Braz J Med Biol Res 31(8):1075–1079CrossRefGoogle Scholar
  29. Mourente G, Tocher DR, Diaz E, Grau A, Pastor E (1999) Relationships between antioxidants, antioxidant enzyme activities and lipid peroxidation products during early development in Dentex dentex eggs and larvae. Aquaculture 179(1):309–324CrossRefGoogle Scholar
  30. Murai T, Andrews JW (1974) Interactions of dietary α-tocopherol, oxidized menhaden oil and ethoxyquin on channel catfish (Ictalurus punctatus). J Nutr 104(11):1416–1431CrossRefGoogle Scholar
  31. Mustafa MG, Takeda T, Umino T, Wakamatsu S, Nakagawa H (1994) Effects of Ascophyllum and Spirulina meal as feed additives on growth performance and feed utilization of red sea bream, Pagrus major. J Fac Appl Biol Sci 33(2):125–132Google Scholar
  32. Nakagawa K, Fujimoto K, Miyazawa T (1996) β-Carotene as a high-potency antioxidant to prevent the formation of phospholipid hydroperoxides in red blood cells of mice. Biochim Biophys Acta 1299(1):110–116CrossRefGoogle Scholar
  33. Niu J, Wen H, Li C-H, Liu Y-J, Tian L-X, Chen X, Huang Z, Lin H-Z (2014) Comparison effect of dietary astaxanthin and β-carotene in the presence and absence of cholesterol supplementation on growth performance, antioxidant capacity and gene expression of Penaeus monodon under normoxia and hypoxia condition. Aquaculture 422:8–17CrossRefGoogle Scholar
  34. Peña AA, Bols NC, Marshall SH (2010) An evaluation of potential reference genes for stability of expression in two salmonid cell lines after infection with either Piscirickettsia salmonis or IPNV. BMC Res Notes 3:101CrossRefGoogle Scholar
  35. Pinero Estrada J, Bermejo Bescos P, Villar del Fresno A (2001) Antioxidant activity of different fractions of Spirulina platensis protean extract. IL Farmaco 56(5):497–500CrossRefGoogle Scholar
  36. Pushpamali WA, De Zoysa M, Kang H-S, Oh CH, Whang I, Kim SJ, Lee J (2008) Comparative study of two thioredoxin peroxidases from disk abalone (Haliotis discus discus): cloning, recombinant protein purification, characterization of antioxidant activities and expression analysis. Fish Shellfish Immunol 24(3):294–307CrossRefGoogle Scholar
  37. Raa J (1996) The use of immunostimulatory substances in fish and shellfish farming. Rev Fish Sci 4(3):229–288CrossRefGoogle Scholar
  38. Romay C, Gonzalez R, Ledon N, Remirez D, Rimbau V (2003) C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci 4(3):207–216CrossRefGoogle Scholar
  39. Saleh R, Betancor M, Roo J, Benítez‐Dorta V, Zamorano MJ, Bell JG, Izquierdo M (2015) Effect of krill phospholipids versus soybean lecithin in microdiets for gilthead seabream (Sparus aurata) larvae on molecular markers of antioxidative metabolism and bone development Aquac Nutr 21:474_488Google Scholar
  40. Sahin K, Yazlak H, Orhan C, Tuzcu M, Akdemir F, Sahin N (2014) The effect of lycopene on antioxidant status in rainbow trout (Oncorhynchus mykiss) reared under high stocking density. Aquaculture 418:132–138CrossRefGoogle Scholar
  41. Sakai M (1999) Current research status of fish immunostimulants. Aquaculture 172(1):63–92CrossRefGoogle Scholar
  42. Sakai T, Murata H, Endo M, Yamauchi K, Tabata N, Fukudome M (1989) 2-Thiobarbituric acid values and contents of α-tocopherol and bile pigments in the liver and muscle of jaundiced yellowtail, Seriola quinqueradiata. Agric Biol Chem 53(6):1739–1740Google Scholar
  43. Shekh K, Tang S, Niyogi S, Hecker M (2017) Expression stability and selection of optimal reference genes for gene expression normalization in early life stage rainbow trout exposed to cadmium and copper. Aquat Toxicol 190:217–227CrossRefGoogle Scholar
  44. Shimidzu N, Goto M, Miki W (1996) Carotenoids as singlet oxygen quenchers in marine organisms. Fish Sci 62(1):134–137CrossRefGoogle Scholar
  45. Smith VJ, Brown JH, Hauton C (2003) Immunostimulation in crustaceans: does it really protect against infection? Fish Shellfish Immunol 15(1):71–90CrossRefGoogle Scholar
  46. Tayag CM, Lin Y-C, Li C-C, Liou C-H, Chen J-C (2010) Administration of the hot-water extract of Spirulina platensis enhanced the immune response of white shrimp Litopenaeus vannamei and its resistance against Vibrio alginolyticus. Fish Shellfish Immunol 28(5):764–773CrossRefGoogle Scholar
  47. Teimouri M, Amirkolaie AK, Yeganeh S (2013a) The effects of Spirulina platensis meal as a feed supplement on growth performance and pigmentation of rainbow trout (Oncorhynchus mykiss). Aquaculture 396:14–19CrossRefGoogle Scholar
  48. Teimouri M, Amirkolaie AK, Yeganeh S (2013b) The effects of dietary supplement of Spirulina platensis on blood carotenoid concentration and fillet color stability in rainbow trout (Oncorhynchus mykiss). Aquaculture 414:224–228CrossRefGoogle Scholar
  49. Wagner JR, Motchnik P, Stocker R, Sies H, Ames B (1993) The oxidation of blood plasma and low density lipoprotein components by chemically generated singlet oxygen. J Biol Chem 268(25):18502–18506PubMedGoogle Scholar
  50. Wang L, Li E, Qin J, Du Z, Yu N, Kong Y, Feng D, Chen L (2015) Effect of oxidized fish oil and α-tocopherol on growth, antioxidation status, serum immune enzyme activity and resistance to Aeromonas hydrophila challenge of Chinese mitten crab Eriocheir sinensis. Aquac Nutr 21(4):414–424CrossRefGoogle Scholar
  51. Watanuki H, Ota K, Tassakka ACMA, Kato T, Sakai M (2006) Immunostimulant effects of dietary Spirulina platensis on carp, Cyprinus carpio. Aquaculture 258(1):157–163CrossRefGoogle Scholar
  52. Xilan Y, Gang L, Chungen W, Baoqing H, Lirong D, Pengzu P, Yanhai X (2011) A catalase from the freshwater mussel Cristaria plicata with cloning, identification and protein characterization. Fish Shellfish Immunol 31(3):389–399CrossRefGoogle Scholar
  53. Yang S-P, Wu Z-H, Jian J-C, Zhang X-Z (2010) Effect of marine red yeast Rhodosporidium paludigenum on growth and antioxidant competence of Litopenaeus vannamei. Aquaculture 309(1):62–65CrossRefGoogle Scholar
  54. Yang SP, Liu HL, Wang CG, Yang P, Sun CB, Chan SM (2015) Effect of oxidized fish oil on growth performance and oxidative stress of Litopenaeus vannamei. Aquac Nutr 21(1):121–127CrossRefGoogle Scholar
  55. Yonar ME (2012) The effect of lycopene on oxytetracycline-induced oxidative stress and immunosuppression in rainbow trout (Oncorhynchus mykiss, W.). Fish Shellfish Immunol 32(6):994–1001CrossRefGoogle Scholar
  56. Zhang J, Liu YJ, Tian LX, Yang HJ, Liang GY, Yue YR, Xu DH (2013) Effects of dietary astaxanthin on growth, antioxidant capacity and gene expression in Pacific white shrimp Litopenaeus vannamei. Aquac Nutr 19(6):917–927CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Mahdi Teimouri
    • 1
    Email author
  • Sakineh Yeganeh
    • 1
  • Ghodrat Rahimi Mianji
    • 2
  • Mojtaba Najafi
    • 2
  • Soleiman Mahjoub
    • 3
  1. 1.Department of Fisheries, Faculty of Animal Science and FisheriesSari Agricultural Sciences and Natural Resources UniversitySariIran
  2. 2.Department of Animal Science, Faculty of Animal Science and FisheriesSari Agricultural Science and Natural Resources UniversitySariIran
  3. 3.Clinical Biochemistry, Cellular and Molecular Biology Research Center, Health Research InstituteBabol University of Medical SciencesBabolIran

Personalised recommendations