Skip to main content
SpringerLink
Log in

Enhancement of antioxidant production in Spirulina platensis under oxidative stress

  • Original Paper
  • Published:
Acta Physiologiae Plantarum Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1

Similar content being viewed by others

References

  • 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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

  • 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

    Article  PubMed  CAS  Google Scholar 

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

  • 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

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Chapter  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

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

    Google Scholar 

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

    Google Scholar 

  • 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

    Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • 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

    Article  Google Scholar 

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

    Article  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

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

    CAS  Google Scholar 

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

    Google Scholar 

  • 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

    CAS  Google Scholar 

  • 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

    PubMed  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • 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

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • 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

Download references

Author information

Authors and Affiliations

  1. Department of Plant Biochemistry, National Research Centre, Cairo, Dokki, Egypt

    Hanaa H. Abd El-Baky & F. K. El Baz

  2. Department of Biochemistry, Faculty of Agriculture, Cairo University, Cairo, Egypt

    Gamal S. El-Baroty

Authors
  1. Hanaa H. Abd El-Baky
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. F. K. El Baz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Gamal S. El-Baroty
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Hanaa H. Abd El-Baky.

Additional information

Communicated by G. Bartosz.

Rights and permissions

Reprints and permissions

About this article

Cite this article

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, 623–631 (2009). https://doi.org/10.1007/s11738-009-0273-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11738-009-0273-8

Keywords

Search

Navigation