Abiotic stress induced production of β-carotene, allophycocyanin and total lipids in Spirulina sp.

Awatief F. Hifney, Ahmed A. Issa, Mustafa A. Fawzy

Abstract


The present study examines the possibility of increasing the levels of some bioactive compounds (β-carotene, phycopiliprotein and total lipids) in Spirulina sp. isolated from Wadi El Natron lake (Egypt) and cultivated in modified Zarrouk's medium under standard growth condition and abiotic stress including change in culturing condition as (pH, temperature, light intensity), nutrient limitation (-N, -P, -S) and salinity. The yield production of β-carotene was enhanced with 0.9M NaCl, phosphorus deficiency and at pH 6. Total lipids were also enhanced in all conditions under tested especially with 0.9M NaCl, light intensity 14.52 µmol photon.m-2.s-1. Phycobiliproteins fractions (phycocyanin, allophycocyanine and phycoerethrine) were elevated with 0.3, 0.6M NaCl as well as phosphorus, nitrogen and sulphur deficiency. Antioxidant enzymatic activities of Spirulina sp. were elevated with all studied abiotic stress factor.


Keywords


Allophycocyanin; β-carotene; Lipids; Spirulina sp.; Antioxidant enzymes

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Wang L, Pan B, Sheng J, Juan Xu J, Hu Q. Antioxidant activity of Spirulina plantasis extracts by supercritical carbon dioxide extraction. Food Chem. 2007; 105: 36–41.

Ghosh P, Adhikari U, Ghosal PK. In vitro anti-herpetic activity of sulfated polysaccharide fractions from Caulerpa racemosa. Phytochem. 2004; 65: 3151–3157.

Prakash S, Sasikala SL, Aldous V, Huxley J. Isolation and identification of MDR-Mycobacterium tuberculosis and screening of partially characterized antimycobacterial compounds from chosen marine micro algae. Asian Pac J Trop Med. 2010; 3(8): 655–661.

Rastogi RP, Sinha RP. Biotechnological and industrial significance of cyanobacterial secondary metabolites. Biotechnol Adv. 2009; 27: 521–39.

Glazer AN, Apell GS, Hixson CS, Bryant DA, Rimon S, Brown DM. Biliproteins of cyanobacteria and Rhodophyta: homologous family of photosynthetic accessory pigments. Proc Natl Acad Sci USA. 1976; 73: 428–431.

Yamanaka G, Glazer AN, Williams RC. Cyanobacterial phycobilisomes characterization of the phycobilisomes of Synechococcus sp. 6301. J Biol Chem. 1978; 253: 8303–8301.

Dillon JC, Phuc AP, Dubacq JP. Nutritional value of the alga Spirulina. World Rev Nutr Diet. 1995; 77: 32–46.

Quoc KP, Pascaud M. Effects of dietary gammalinolenic acid on the tissue phospholipid fatty acid composition and the synthesis of eicosanoids in rats. Ann Nutr Metabol. 1996; 40: 99–108.

Hirahashi T, Matsumoto M, Hazeki K, Saeki Y, Ui M, Seya T. Activation of the human innate immune system by Spirulina augmentation of interferon production and NK cytotoxicity by oral administration of hot water extract of Spirulina platensis. Int Immunopharmacol. 2002; 2: 423–434.

Subhashini J, Mahipal SVK, Reddy MC, Reddy MM, Rachamallu A, Reddanna P. Molecular mechanisms in C-Phycocyanin induced apoptosis in human chronic myeloid leukemia cell line - K562. Biochem Pharmacol. 2004; 68: 453–462.

Sasson A. 1997. Micro Biotechnologies: Recent Developments and Prospects for Developing Countries. BIOTEC Publication 1/2542. Place de Fontenoy, Paris. France. United Nations Educational, Scientific and Cultural Organization (UNESCO): 11–31.

Costa JAV, Colla LM, Filho PFD. Improving Spirulina platensis biomass yield using a fedbatch process. Biores Technol. 2004; 92: 237–241.

Habib MAB, Huntington TC, Hasan MR. 2008. A review on culture, production and use of Spirulina as food for humans and feeds for domestic animals and fish. FAO Fisheries and Aquaculture Circular No. 1034.

Romay C, Gonzalez R, Ledon N, Remirez D, Rimbau V. C-phycocyanin: a biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr Protein Pept Sci. 2003; 4(3): 207-216.

Liu Y, Xu L, Cheng N, Lin L, Zhang C. Inhibitory effect of phycocyanin from Spirulina platensis on the growth of human leukemia K562 cells. J Appl Phycol. 2000; 12(2): 125-130.

Liu B, Zhang X, Gao M, Chu, X. Effects of CD59 on antitumoral activities of phycocyanin from Spirulina platensis. Biomed Pharmacother. 2005; 59(10): 551-560.

Pardhasaradhi BV, Ali AM, Kumari AL, Reddanna P Khar A. Phycocyanin-mediated apoptosis in AK-5 tumor cells involves down-regulation of Bcl-2 and generation of ROS. Mol Cancer Ther. 2003; 2(11): 1165-1170.

Ivanova KG, Stankova KG, Nikolov VN, Georgieva RT, Minkova KM, Gigova LG, Rupova IT, Boteva RN. The biliprotein C-phycocyanin modulates the early radiation response: A pilot study. Mutat Res. 2010; 695: 40-45.

Singh CS, Sinha PR, Hader PD. Role of lipids and fatty acids in stress tolerance in cyanobacteria. Acta Protozool. 2002; 41: 297–308.

Othes S, Pire R. Fatty acid composition of Chlorella and Spirulina microalgae species. J AOAC Int. 2001; 84: 1708–1714.

Kyle DJ, Boswell KD, Gladue RM, Reab SE. 1992. Designer oils from micro algae nutritional supplements. In: Bills DB, Kung S. (eds): Biotechnology and Nutrition. Proceeding 3rd International Symposium Butterworth, Heinemann, Boston: 468.

Carlson SE, Salem N. 1991. Essential of ω3 fatty acids in growth and development of infants. In: Simopoulus AP, Kifer RR, Barlow SM. (eds): Health Effects of ω3 Polyunsaturated Fatty Acids in Seafood. World Revue of Nutrition and Dietetics. Vol. 66. Karger, Basel: 74–86.

Innis SM. Essential fatty acids in growth and development. Progress Lipid Res. 1991; 30: 39–103.

Ogata J, Hagiwara Y, Hagiwara H, Shibamoto T. Inhibition of molonoldehyde formation by antioxidant from ω3 polyunsaturated fatty acids. J Am Oil Chem Soc. 1996; 73: 654–656.

Roughan GP. Spirulina: A source of dietary gamma-linolenic acid. J Agricult Food Chem. 1989; 47: 85–93.

Saito T, Saito T, Oka N. 1992. Scientific Reports on Chlorella in Japan. Japan Chlorella Treatment Association. Silpaque Publishing, Kyoto.

Zarrouk C. 1966. Contribution à l'étude d'une cyanophycée. Influence de divers facteurs physiques et chimiques sur la croissance et la photosynthèse de Spirulina maxima. Ph.D. Thesis, Université De Paris.

Metzner H, Rau H, Senger H. Untersuchungen zur synchronisier-barkeit ein zelner pigment managel. Mutanten von Chlorella. Planta 1965; 65: 186-194.

Marker AFH. The use of acetone and methanol in the estimation of chlorophyll in the presence of Phaeophytin. Fresh Wat Biol. 1972; 2: 361-385.

Fatma T, Sarada R, Venkataraman LV. Evaluation of selected strains of Spirulina for their constituents. Pykos 1994; 33(1-2): 89-97.

Bennet A, Bogorad L. Complementary chromatic adaptation in filamentous blue-green algae. J Cell Biol. 1973; 58: 419-435.

Lowry DH, Rosebrough NJ, Farr AL, Randall RJ. Protein measurement with the folin phenol reagent. J Biol Chem. 1951; 193: 265-275.

Aebi H. Catalase in vitro. Methods in Enzymol. 1984; 105: 121-126.

Matsumura T, Tabayashi N, Kamagata Y, Souma C, Saruyama H. Wheat catalase expressed in transgenic rice can improve tolerance against low temperature stress. Physiol Plant. 2002; 116: 317-327.

Tatiana Z, Yamashita K, Matsumoto H. Iron deficiency induced changes in ascorbate content and enzyme activities related to ascorbate metabolism in cucumber root. Plant Cell Physiol. 1999; 40: 273-280.

Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol. 1981; 22: 867-880.

Drevon B, Schmit JM. 1964. La reaction sulfophosphovanillique dans l’ét.ude des lipides seriques. Bull. Trau. Soc. Pharm. Lyon 8: 173-178.

Rousch JM, Bingham SE, Sommaerfeld MR. Change in fatty acid profiles of thermo-intolerent and thermo tolerant marine diatoms during temperature stress. Exp Mar Biol Ecol. 2003; 295: 145-156.

Ayachi A, El-Abed A, Dhifi W, Marzouk B. Chlorophylls, proteins and fatty acids amounts of Arthrospira platensis growing under saline conditions. Pakistan J Biol Sci. 2007; 10: 2286-2291.

Vonshak A, Guy R, Guy M. The response of the filamentous cyanobacterium Spirulina platensis to salt stress. Arch Microbiol. 1988; 150: 417–420.

Rafiqul Islam Md, Hassan A, Sulebele G, Orosco C, Roustaian P. Influence of temperature on growth and biochemical composition of Spirulina platensis and S. fusiformis. Iranian Int J Sci. 2003; 4(2): 97-106.

Hemlata, Fatma T. Screening of Cyanobacteria for phycobiliproteins and effect of different environmental stress on its yield. Bull Environ Contam Toxicol. 2009; 83: 509–515.

Poza-Carrion C, Fernadez-Valiente E, Fernadez-Pinas F, Leganes F. Acclimation of photosynthetic pigments and photosynthesis of the cyanobacterium Nostoc sp. Strain UAM 206 to combined fluctuations of irradiance, pH and inorganic carbon availability. Plant Physiol. 2001; 158: 1455–1461.

Abd El-Baky HH. Over production of phycocyanin pigment in blue green alga Spirulina sp. and its inhibitory effect on growth of Ehrlich ascites carcinoma cells. Med Sci. 2003; 3: 314–24.

Kassem DA. 2010. Possible therapeutic effect of Spirulina sp. on hepatotoxicity in rates. M.Sc. Thesis. Bot. Dept. Fac. of Sci. Tanta Univ., Egypt.

Incharoensakdi A, Phunpruch S. 1996. Environmental factors affecting the beta-carotene content in Spirulina platensis. In: "Proceedings of the 3rd Asia-Pacific Conference on Agricultural Biotechnology: Issues and Choices". Melia Hotel, Prachuabkhirikhan, 10-15 November: 587-592.

Uslu L, Isik O, Koc K, Göksan T. The effects of nitrogen deficiencies on the lipid and protein contents of Spirulina platensis. Afr J Biotechnol. 2011; 10(3): 386-389.

Zhila NO, Kalacheva GS, Volova TG. Influence of nitrogen deficiency on biochemical composition of the green alga Botryococcus. J Appl Phycol. 2005; 17: 309-315.

Pruvost J, Van Vooren G, Cogne G, Legrand J. Investigation of biomass and lipids production with Neochloris oleoabundans in photobioreactor. Biores Technol. 2009; 10(23): 5988-5995.

Bulut Y. 2009. The investigations on the possibility of increase lipid content of Chlorella (Master Thesis). Cukurova Univ., Institute of Science and Technology, Biotechnology Department, 62 p. Turkey.

Ramadan MF, Asker MMS, Ibrahim ZK. Functional bioactive compounds and biological activities of Spirulina platensis lipids. Czech J Food Sci. 2008; 26: 211–222.

Reddy CM, Vadiraja BB, Kiranmai G, Reddy MN, Reddanna P, Madyastha KM. Selective inhibition of cyclooxygenase-2 by C-phycocyanin, a biliprotein from Spirulina platensis. Biochem Biophys Res Commun. 2000; 277: 599-603.

Estrada JE, Bescós P, Villar Del Fresno AM. Antioxidant activity of different fractions of Spirulina platensis protean extract. Il Farmaco 2001; 56: 497-500.

Bhat V B, Madyastha KM. C-phycocyanin: a potent peroxyl radical scavenger in vivo and in vitro. Biochem Biophys Res Communic. 2000; 275: 20–25.

Benedetti S, Benveuti F, Pagliarani S, Francogli S, Scoglio S, Canestrari F. Antioxidant properties of a novel phycocyanin extract from the blue green alga Aphanizomenon flos-aquae. Life Sci. 2004; 75: 2353-2362.

Huang Z, Guo BJ, Wong RNS, Jiang Y. Characterization and antioxidant activity of selenium-containing phycocyanin isolated from Spirulina platensis. Food Chem. 2007; 100: 1137-1143.

Ge B, Qin S, Han L, Lin F, Ren Y. Antioxidant properties of recombinant allophycocyanin expressed in Escherichia coli. J Photochem Photobiol B, Biol. 2006; 84: 175-80.

Yuan YV, Carrington MF, Walsh M. Extracts from dulse (Palmaria palmata) are effective antioxidants and inhibitors of cell proliferation in vitro. Food Chem Toxicol. 2005; 43: 1073-1081.


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