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Enhancement of antioxidant production in Spirulina platensis under oxidative stress

Abstract

The present study examined the possibility of increasing the contents of some bioactive compounds of Spirulina platensis cultivated in medium containing various hydrogen peroxide concentrations (2, 4, 6 and 8 mM) as a model for environmental stress. A positive correlation was observed between the increase of H2O2 and increasing amounts of cellular lipophilic antioxidants (total carotenoids and α-tocopherol) and hydrophilic antioxidants [glutathione (GSH) and ascorbic acid (AsA)]. HPLC profile of carotenoids revealed that algae responded to the change of H2O2 exposure by the accumulation of higher amounts of β-carotene, astaxanthine, luteine, zeaxanthin and cryptoxanthin. S. platensis showed significant linear increase in activities of antioxidant enzymes, i.e., catalase (CAT), peroxidase (PX), ascorbate peroxidase (APX) and superoxide dismutase (SOD), with increasing H2O2 concentrations. A pronounced increase of oxidative lesions’ indexes [thiobarbituric acid reactive substances (TBARS) and paramagnetic radical-EPR signal] was found in algal grown at 8 mM H2O2. These data revealed that S. platensis behaved with different strategies against H2O2 exposure which is dose dependent and their response strongly correlated with the scavenging enzymes (SOD, CAT, PX and APX) and antioxidant compounds (GSH, AsA, β-carotene, astaxanthine and α-tocopherol) in the antioxidant defense systems. Therefore, S. platensis could be considered as good candidates for successful cultivation in artificial open ponds under different environmental conditions, as high value health foods, functional foods and as source of wide spectrum of nutrients.

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References

  1. Abd El-Baky HH, El Baz FK, El-Baroty GS (2003) Spirulina species as a source of carotenoids and α-tocopherol and its anticarcinoma factors. Biotechnology 3:222–240

  2. Abd El-Baky HH, El Baz FK, El-Baroty GS (2004) Production of antioxidant by the green alga Dunaliella salina. Int J Agric Biol 6:49–57

  3. Abd El-Baky HH, El Baz FK, El-Baroty GS (2007) Production of carotenoids from marine microalgae and its evaluation as safe food colorant and lowering cholesterol agents. Am-Eurasian J Agric Environ Sci 2:792–800

  4. Alscher RG, Donahue JL, Cramer CL (1997) Reactive oxygen species and antioxidants: relationships in green cells. Physiol Plant 100:224–233. doi:10.1111/j.1399-3054.1997.tb04778.x

  5. Apostol I, Heinstein PF, Low PS (1989) Rapid stimulation of an oxidative burst during elicitation of cultured plant cells. Plant 90:109–116. doi:10.1104/pp.90.1.109

  6. Asada K, Yoshikawa K, Takahashi M, Maeda Y, Enmanji K (1975) Superoxide dismutase from a blue-green alga Plectonema boryanum. J Biol Chem 250:2801–2807

  7. Augustin J, Klein PB, Becker D, Venugopal BP (1985) Vitamin. In: Methods of vitamin assay. Academic Press, Now York, p 323

  8. Barros PM, Granbom M, Colepicolo P, Pedersėn M (2003) Temporal mismatch between induction of superoxide dismutase and ascorbate peroxidase correlates with high H2O2 concentration in seawater from clofibrate-treated red algae Kappaphycus alvarezii. Arch Biochem Biophys 420:161–168. doi:10.1016/j.abb.2003.09.014

  9. Ben-Amotz A, Shaish J (1992) In: Ben-Amotz A, Averon M (eds). Dunaliella: physiology, biochemistry and biotechnology. CRC, USA, pp 135–64

  10. Bennoun P (1998) In: Rochais JD, Goldschmidt M, Merchant S (eds) The molecular biology of chloroplasts and mitochondria in Chlamydompnas. Kluwer, Dordrecht, pp 675–83

  11. Bischof K, Hanelt D, Wiencke C (2000) Effects of ultraviolet radiation on photosynthesis and related enzyme reactions of marine macroalgae. Planta 211:555–562. doi:10.1007/s004250000313

  12. Blokhina O, Virolainen E, Fagerstedt VK (2002) Antioxidants, oxidative damage and oxygen deprivation stress: a review. Ann Bot (Lond) 91:179–194. doi:10.1093/aob/mcf118

  13. Bradford MM (1976) A rapid and sensitive method for the quantification of microgram of protein utilizing of protein–dye binding. Anal Biochem 72:248–254. doi:10.1016/0003-2697(76)90527-3

  14. Chance B, Maehly AC (1955) Assay of catalase and peroxidase. In: Colowic SP, Kaplan NO (eds) Methods of enzymology, vol 2. Academic Press, New York, p 764

  15. Demming-Adams B, Adams WW (1994) Light stress and photoprotection related to the xanthophyll cycle. In: Foyer C, Mullineaux P (eds) Causes of photooxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton, pp 105–126

  16. Dummermuth LA, Karsten U, Fisch KM, Kónig GM, Wiencke C (2003) Responses of marine macroalgae to hydrogen-peroxide stress. J Exp Mar Biol Ecol 289:103–121. doi:10.1016/S0022-0981(03)00042-X

  17. El Baz FK, Aboul-Enein AM, El-Baroty GS, Youssef AM, Abd El-Baky HH (2002) Accumulation of antioxidant vitamins in Dunaliella salina. Online J Biol Sci 2:220–223

  18. Elstner EF (1987) Metabolism of activated oxygen species. In: Davies DD (ed) Biochemistry of plants, vol II. Academic Press, London, pp 253–315

  19. Elstner EF, Osswald W (1994) Mechanisms of oxygen activation during plant stress. Proc R Soc Edinburgh 102B:131–154

  20. Foyer CH (1997) Oxygen metabolism and electron transport in photosynthesis. In: Scandalios JG (ed) Oxidative stress and the molecular biology of antioxidant defenses. Cold Spring Harbor Laboratory, New York, pp 587–621

  21. Foyer CH, Noctor G (2000) Oxygen processing in photosynthesis: regulation and signaling: a review. New Phytol 146:359–388

  22. Foyer CH, Descourvieres P, Kunert KJ (1994) Protection against oxygen radicals: important defense mechanism studied in transgenic plants. Plant Cell Environ 17:507–523

  23. Fridovich I (1978) The biology of oxygen radicals. Science 201:875–880

  24. Giasuddin ASM, Diplock AT (1981) The influence of vitamin E on membrane lipids of mouse fibroblast in culture. Arch Biochem Biophys 210:348–362

  25. Ginnopolitis NC, Ries SK (1977) Superoxide dismutase occurrence in higher plants. Plant Physiol 59:309–314

  26. Grant CM, MacIver FH, Dawes IW (1996) Glutathione is an essential metabolite required for resistance to oxidative stress in the yeast Saccharomyces cerevisiae. Curr Genet 29:511–515

  27. Hans-Luck (1970) Catalase. In: Bergmeyer HU (ed) Method of enzymatic analysis (English edition). Academic Press, New York, pp 885–888

  28. Haraguchi H, Ishikawa H, Kubo I (1997) Antioxdative action of di-terpenoids from Podocarpus nagi. Planta Med 63:213–215

  29. Henzler T, Steudle E (2000) Transport and metabolic degradation of hydrogen peroxide in Chara coralline: model calculations and measurements with the pressure probe suggest transport of H2O2 water channels. J Exp Bot 51:2053–2066

  30. Honya MK, Kinoshita T, Ishikawa M, Mori H, Nisizw K (1994) Seasonal variation in lipid content of cultured Laminaria japonica fatty acids, sterols, β-carotene and tocopherol. J Appl Phycol 6:25–29

  31. Jones DP, Coates RJ, Flagg EW, Eley JW, Block GH, Greenberg RS, Gunter EW, Jackson B (1992) Glutathione in foods listed in the national cancer institutes health habits and history food frequency questionnaire. Nutr Cancer 17:57–75

  32. Karpinski S, Reynolds H, Karpinksa B, Wingsle G, Creissen G, Mullineaux P (1999) Systemic signaling and acclimation in response to excess excitation energy in Arabidopsis. Science 284:654–657

  33. Lu I, Sung MS, Lee TM (2006) Salinity stress and hydrogen peroxide regulation of antioxidant defense system in Ulva fasciata. Mar Biol 150:1–15

  34. Manley LS (2002) Phytogenesis of halomethanes: a product of selection or a metabolic accident. Biogeochemistry 60:163–180

  35. Mittler R, Vanderauwera S, Gollery M, Van Breusegem F (2004) Reactive oxygen gene network of plants. Trends Plant Sci 9:490–498

  36. Nakano M, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880

  37. Noctor G, Foyer CH (1998) Ascorbate and glutathione: keeping active oxygen under control. Ann Rev Plant Physiol Plant Mol Biol 49:249–279

  38. Noctor G, Aris AM, Jouanin J, Kunert JK, Rennenberg H, Foyer H (1998) Glutathione: biosynthesis, metabolism and relationship to stress tolerance explored in transformed plants. J Exp Bot 321:623–647

  39. Osmond B, Badger M, Maxwell K, Björkman O, Leegod R (1997) Too many photons: photorespiration, photoinhibition and photooxidation. Trends Plant Sci 2:119–120

  40. Payer HD (1971) First report upon the organization and experimental work of the Thailand German project on the production and utilization of single cell green algae as a protein source for human nutrition. Institute of Food Research and Product Development, Kasetsar Univ, Bangkok, Thailand

  41. Peng M, Kuc J (1992) Peroxidase-generated hydrogen peroxide as a source of antifungal activity in vitro and on tobacco leaf disks. Phytopathology 82:696–699

  42. Polle A, Rennenberg H (1994) Photooxidative stress in trees. In: Foyer CH, Mullineaux PM et al (eds) Causes of photoxidative stress and amelioration of defense systems in plants. CRC Press, Boca Raton

  43. Prasad KVS, Saradhi PP, Sharmila P (1999) Concerted action of antioxidant enzymes and curtailed growth under zinc toxicity in Brassica juncea. Environ Exp Bot 42:1–10

  44. Ridnour AL, Sim EJ, Choi J, Dickinson AD, Forman HJ, Ahmad MI, Coleman CM, Hunt RC, Spitz RD (2005) Nitric oxide-induced resistance to hydrogen peroxide stress is a glutamate cysteine ligase activity-dependent process. Free Rad Biol Med 38:1361–1371

  45. Salguero A, Benito M, Vigara J, Vega JM, Vilchez C, León R (2003) Carotenoids as protective response against oxidative damage in Dunaliella bardawil. Biomol Eng 20:249–253

  46. Schneider S, Bergmann L (1995) Regulation of glutathione synthesis in suspension cultures of parsley and tobacco. Bot Acta 108:34–40

  47. Schomburg D, Salzmann M, Stephan D (eds) (1994) Enzyme handbook 7. Springer, Berlin

  48. Semenenko EV, Abdullaev AA (1980) Parametric control of β-carotene biosynthesis in Dunaliella salina cells under conditions of intensive cultivation. Fizioloiya Rastenii 27:31–41

  49. Silber R, Farber M, Papopoulos E, Nervla D, Liebes L, Bruch M, Bron R (1992) Glutathione depletion in chronic lymphocytic leukemia B-lymphocytes. Blood 80:2038–2040

  50. Suzuki N, Mittler R (2006) Reactive oxygen species and temperature stresses: a delicate balance between signaling and destruction. Physiol Plant 126:45–51

  51. Takeda T, Yokota A, Shigeoka S (1995) Resistance of photosynthesis to hydrogen peroxide in algae. Plant Cell Physiol 36:1089–1095

  52. Tausz RM, Soledad M, Grille D (1998) Antioxidative defense and photoprotection in pine needles under field conditions. A multivariate approach to evaluate patterns of physiological responses at natural sites. Physiol Plant 104:760–768

  53. Yamasaki H, Grace CS (1998) ESR detection of phytophenoxyl radicals stabilized by zinc ions: evidence for the redox coupling of plant phenolics with ascorbate in the H2O2-peroxidase system. FEBS Lett 422:377–380

  54. Zarrouk C (1966) Contribution a l’etude dune cyanophycee. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthese de Spirulina maxima (Setch. et Gardner) Geitler. Ph.D. thesis. Universite de Paris, France

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Correspondence to Hanaa H. Abd El-Baky.

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Communicated by G. Bartosz.

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Abd El-Baky, H.H., El Baz, F.K. & El-Baroty, G.S. Enhancement of antioxidant production in Spirulina platensis under oxidative stress. Acta Physiol Plant 31, 623 (2009). https://doi.org/10.1007/s11738-009-0273-8

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Keywords

  • Spirulina platensis
  • Carotenoids
  • Antioxidant enzymes
  • Ascorbic acid
  • Electron paramagnetic resonance
  • Free radicals