Grasas y Aceites, Vol 70, No 1 (2019)

Pharmaceutical applications and consequent environmental impacts of Spirulina (Arthrospira): An overview


https://doi.org/10.3989/gya.0690181

W. Shao
School of the Environment and Safety Engineering, Jiangsu University, China
orcid http://orcid.org/0000-0001-8067-3755

R. Ebaid
School of the Environment and Safety Engineering, Jiangsu University, China
orcid http://orcid.org/0000-0002-5976-5505

M. El-Sheekh
Botany Department, Faculty of Science, Tanta University, Egypt
orcid http://orcid.org/0000-0002-2298-6312

A. Abomohra
School of Energy and Power Engineering, Jiangsu University - Botany Department, Faculty of Science, Tanta University, China
orcid http://orcid.org/0000-0003-2784-3297

H. Eladel
Botany Department, Faculty of Science, Benha University, Egypt
orcid http://orcid.org/0000-0002-2369-2965

Abstract


Recently, microalgae cultivation for different applications, including the production of nutritional and pharmaceutical active compounds has received increasing attention. Among the different genera, Spirulina (Arthrospira sp.) is one of the most promising blue-green microalgae (Cyanophyta) because it is rich in antioxidants, essential amino acids (EAAs), minerals, proteins, polyunsaturated fatty acids and vitamins. It has a high protein content (60-70% of the dry weight), which is a complete protein, i.e. containing all EAAs. Therefore, Spirulina is currently a commercial product with high nutritional value and also a significant source of complementary and alternative medicine. The objective of the present work was to review the pharmaceutical and therapeutic applications of Spirulina, especially its antioxidant, anti-inflammatory, anti-cancer, anti-microbial, anti-diabetic, anti-obesity and anti-toxicity properties. The results were obtained from experiments in the literature performed in vitro and in vivo using experimental animals. The main reported active ingredients in Spirulina include phycocyanin, tocopherol, β-carotene, caffeic acids and chlorogenic acid, which showed individual or synergetic effects. In addition, the present review discusses the future perspectives of genetically modified Spirulina as a source for industrial products while producing valuable biomass photoautotrophically. Furthermore, the consequent environmental impacts of large-scale cultivation of Spirulina are discussed.

Keywords


Arthrospira sp.; Cultivation; Environmental impacts; GMO; Pharmaceuticals; Spirulina

Full Text:


HTML PDF XML

References


Abdel-Daim M, El-Bialy B, Abdel Rahman H, Radi A, Hefny H, Hassan A. 2016. Antagonistic effects of Spirulina platensis against subacute deltamethrin toxicity in mice: Biochemical and histopathological studies. Biomed. Pharmacother. 77, 79–85.

Abomohra A, El-Sheekh M, Hanelt D. 2014. Pilot cultivation of the chlorophyte microalga Scenedesmus obliquus as a promising feedstock for biofuel. Biomass Bioenergy 64, 237–244.

Abomohra A, El-Shouny W, Sharaf M, Abo-Eleneen M. 2016. Effect of Gamma Radiation on Growth and Metabolic Activities of Arthrospira platensis. Braz. Arch. Biol. Technol. 59, e16150476.

Abomohra A, Eladel H, El-Esawi M, Wang S, Wang Q, He Z, Feng Y, Shang H, Hanelt D. 2018. Effect of lipid-free microalgal biomass and waste glycerol on growth and lipid production of Scenedesmus obliquus: Innovative waste recycling for extraordinary lipid production. Bioresour. Technol. 249, 992–999.

Arun N, Gupta S, Singh DP. 2012. Antimicrobial and antioxidant property of commonly found microalgae Spirulina platensis, Nostoc muscorum and Chlorella pyrenoidosa against some pathogenic bacteria and fungi. Int. J. Pharm. Sci. Res. 3, 4866–4875.

Baicus C, Baicus A. 2007. Spirulina did not ameliorate idiopathic chronic fatigue in four N-of-1 randomized controlled trials. Phytother. Res. 21, 570–573.

Bhunia B, Uday U, Oinam G, Mondal A, Bandyopadhyay T, Tiwari O. 2018. Characterization, genetic regulation and production of cyanobacterial exopolysaccharides and its applicability for heavy metal removal. Carbohydr. Polym. 179, 228–243.

Bini F, De Rossi E, Barbierato L, Riccardi G. 1992. Molecular cloning and sequencing of the ß-isopropylmalate dehydrogenase gene from the cyanobacterium Spirulina platensis. J. Gen. Microbiol. 138, 493–498.

Bleakley S, Hayes M. 2017. Algal proteins: Extraction, application, and challenges concerning production. Foods 6, 33.

Borowitzka M. 1995. Microalgae as sources of pharmaceuticals and other biologically active compounds. J. Appl. Phycol. 7, 3–15.

Capelli B, Cysewski GR. 2010. Potential health benefits of Spirulina microalgae. Nutrafoods 9, 19–26.

Castenholz RW. 1989. Subsection III, Order Oscillatoriales. In Stanley JT, Bryant MP, Pfenning N, Holt JG (Eds), Bergey’s Manual of Systematic Bacteriology, Vol. 3, Baltimore: William and Wilkins, p. 1771.

Centeno P, Ballentine DL. 1999. Effects of culture conditions on production of antibiotically active metabolites by the marine alga Spyridia filamentosa (Ceramiaceae, Rhodophyta), I. Light. J. Appl. Phycol. 11, 217–224.

Chagas B, DoradoC, Serapiglia M, Mullen C, Boateng A, Melo M, Ataíde C. 2016. Catalytic pyrolysis-GC/MS of Spirulina: evaluation of a highly proteinaceous biomass source for production of fuels and chemicals. Fuel 179, 124–134.

Cheevadhanarak S, Kanokslip S, Chaisawadi S, Rachdawong S, Tanticharoen M. 1993. Transformation system for Spirulina platensis. In Masojidek J, Setlik I. (Eds) Book of Abstracts of the 6th International Conference on Applied Algology, Czech Republic, p. 109.

Chen F, Zhang Y, Guo S. 1996. Growth and phycocyanin formation of Spirulina platensis in photoheterotrophic culture. Biotechnol. Lett. 18, 603–608.

Choi WY, Kang DH, Lee HY. 2013. Enhancement of immune activation activities of Spirulina maxima grown in deep sea water. Int. J. Mol. Sci. 14, 12205–12221.

Ciferri O. 1984. Spirulina, the edible microorganism. Microbiol. Rev. 47, 551–578.

Deng MD, Coleman JR. 1999. Ethanol synthesis by genetic engineering in cyanobacteria. Appl. Environ. Microbiol. 65, 523–528.

Deshnium P, Paithoonrangsarid K, Suphatrakul A, Meesapyodsuk D, Tanticharoen M, Cheevadhanarak S. 2000. Temperature-independent and -dependent expression of desaturase genes in filamentous cyanobacterium Spirulina platensis strain C1 (Arthrospira sp. PCC 9438). FEMS. Microbiol. Lett. 184, 207–213.

Doucha J, Straka F, Livansky K. 2005. Utilization of flue gas for cultivation of microalgae (Chlorella sp.) in an outdoor open thin layer photobioreactor. J. Appl. Phycol. 17, 403– 412.

Ebaid R, Elhussainy E, El-Shourbagy S, Ali S, Abomohra A. 2017. Protective effect of Arthrospira platensis against liver injury induced by copper nanoparticles. Orient. Pharm. Exp. Med. 17, 203–210.

El-Desouki N, Tabl G, Abdel-Aziz K, Salim E, Nazeeh N. 2015. Improvement in beta-islets of Langerhans in alloxan-induced diabetic rats by erythropoietin and Spirulina. J. Basic App. Zool. 71, 20–31.

Eriksen NT. 2016. Research trends in the dominating microalgal pigments, ?-carotene, astaxanthin, and phycocyanin used in feed, in foods, and in health applications. J. Nutr. Food Sci. 6, 507.

Global Energy Statistical Yearbook, Enerdata 2015. Available at https://yearbook.enerdata.net, Accessed on December 2017.

Gomont M. 1892–1893. Monographie des Oscillarièes. Ann. Sci. Nat. Bot. 15, 263–368, 16, 91–264.

Graverholt OS, Eriksen NT. 2007. Heterotrophic high-cell-density fedbatch and continuous-flZ cultures of Galdieria sulphuraria and production of phycocyanin. Appl. Microbiol. Biotechnol. 77, 69–75.

Han LK, Li DX, Xiang L, Kondo Y, Suzuki I, Okuda H.2006. Isolation of pancreatic lipase activity-inhibitory component of Spirulina platensis and it reduce postprandial triacylglycerolemia. Yakugaku. Zasshi. 126, 43–49.

Hayashi K, Hayashi T, Morita N. 1993. An extract from Spirulina platensis is a selective inhibitor of herpes simplex virus type 1 penetration into HeLa cells. Phytother. Res. 7, 76–80.

Hayashi T, Hayashi K, Maedaa M, Kojima I. 1996. Calcium spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis. J. Nat. Prod. 59, 83–87.

Henrikson R. 1994. Microalga Spirulina, superalimento del futuro. Ronore Enterprises. 2nd ed. Ediciones Urano, Barcelona, Spain, pp. 222.

Honsthong A, Deshnium P, Paithoonrangsarid K, Cheevadhanarak S, Tanticharoen M. 2003. Differential responses of three acyl-lipid desaturases to immediate temperature reduction occurring in two lipid membranes of Spirulina platensis strain C1. J. Biosci. Bioeng. 96, 519–524.

Hu J, Nagarajan D, Zhang Q, Chang J, Lee D. 2018. Heterotrophic cultivation of microalgae for pigment production: A review. Biotechnol. Adv. 36, 54–67.

Jimenez C, Cossio BR, Niell FX.2003. Relationship between physicochemical variables and productivity in open ponds for the production of Spirulina: A predictive model of algal yield. Aquaculture 221, 331–345.

Kawata Y, Yano S, Kojima H, Toyomizu M. 2004. Transformation of Spirulina platensis strain C1 (Arthrospira sp. PCC9438) with Tn5 transposase–transposon DNA–cation liposome complex. Mar. Biotechnol. 6, 355–363.

Khan Z, Bhadouria P, Bisen P. 2005. Nutritional and therapeutic potential of Spirulina. Curr. Pharm. Biotechnol. 6, 373–379.

Kim D, Kim J, Goh E, Kim W, Kim S, Seo Y, Jang C, Kang S. 2011. Antioxidant response of Arabidopsis plants to gamma irradiation: Genome-wide expression profiling of the ROS scavenging and signal transduction pathways. J. Plant. Physiol. 168, 1960–1971.

Kokou F, Makridis P, Kentouri M, Divanach P. 2012. Anti-bacterial activity in microalgae cultures. Aquacult. Res. 43, 1520– 1527.

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

Manoj G, Venkataraman LV, Srinivas L. 1992. Antioxidant properties of Spirulina (Spirulina platensis). In: Seshadri CV, Jeejibai N, editors. ETTA National Symposium on Spirulina. MCRC Publishers, New York, USA, pp. 148–154.

Márquez FJ, Sasaki K, Kakizono T, Nishio N, Nagai S. 1993. Growth characteristics of Spirulina platensis in mixotrophic and heterotrophic conditions. J. Ferment. Bioeng. 5, 408–410.

Miranda MS, Cintra RG, Barros SM, Mancini-Filho J. 1998. Antioxidant activity of the microalga Spirulina maxima. Braz. J. Med. Biol. Res. 31, 1075–1079.

Mohanty P, Srivastava M, Krishna K. 1997. The Photosynthetic Apparatus of Spirulina: Electron Transport and Energy Transfer. In: Vonshak A, Spirulina platensis (Arthrospira) Physiology, cell-biology and biotechnology. 1997, Taylor & Francis Ltd., London.

Moorhead K, Capelli B, Cysewski G. 2012. Spirulina: Nature’s Superfood. 3rd edition, Cyanotech Corporation, Kailua Kona, Hawaii, USA.

Mukherjee SB, Das M, Sudhandiran G, Shaha C. 2002. Increase in cytosolic Ca2+ levels through the activation of non-selective cation channels induced by oxidative stress causes mitochondrial depolarization leading to apoptosis-like death in Leishmania donovani promastigotes. J. Biol. Chem. 277, 24717–24727.

Murata N, Deshnium P, Tasaka Y. 1996. Biosynthesis of gamma-linolenic acid in the cyanobacterium Spirulina platensis. In Huang Y, Milles DE (Eds) Gamma-linolenic acid, metabolism and its role in nutrition and medicine, AOC Press, Champaign, Illinois, p. 22.

Nelissen B, Wilmotte A, Neefs JM, De Wachter R. 1994. Phylogenetic relationships among filamentous helical cyanobacteria investigated on the basis of 16S ribosomal RNA gene sequence analysis. Syst. App. Microbiol. 17, 206–210.

Nigma D, Shukla G, Agarwal A. 1999. Glutathione depletion and oxidative damage in mitochondria following exposure to cadmium in rat liver and kidney. Toxicol. Lett. 106, 151–157.

Özdemir G, Karabay NU, Dalay MC, Pazarbasi B. 2004. Antibacterial activity of volatile component and various extracts of Spirulina platensis. Phytother. Res. 18, 754–757.

Premkumar K, Abraham SK, Santhiya ST, Ramesh A. 2004. Protective effect of Spirulina fusiformis on chemical-induced genotoxicity. Fitoterapia 75, 24–31.

Premkumar K, Pachiappan A, Abraham SK, Santhiya ST, Gopinath PM, Ramesh A. 2001. Effect of Spirulina fusiformis on cyclophosphamide and mitomycin-C induced genotoxicity and oxidative stress in mice. Fitoterapia 72, 906–911.

Rajesh V, Kala M. 2015. Antiproliferative and chemopreventive effect of Annona muricata Linn. on Ehrlich ascites carcinoma and Benzo[a]pyrene induced lung carcinoma. Orient. Pharm. Exp. Med. 15, 239–256.

Rangsayator N, Upatham ES, KruatrachureM, Pokethitiyook P, Lanza G. 2002. Phytoremediation potential of Spirulina (Arthrospira) platensis: Biosorption and toxicity studies of cadmium. Environ. Pollut. 119, 45–53.

Rempel A, Machado T, Treichel H, Colla E, Margarites A, Colla L. 2018. Saccharification of Spirulina platensis biomass using free and immobilized amylolytic enzymes. Bioresour. Technol. 263, 163–171.

Romay C, Ledon N, Gonzalez R. 1998. Further studies on anti-inflammatory activity of phycocyanin in some animal models of inflammation. Inflamm. Res. 47, 334–338.

Romay C, Ledon N, Gonzalez R. 2000. Effects of phycocyanin extract on prostaglandin E2 levels in mouse ear inflammation test. Arzneim -Forsch. 50, 1106–1109.

Santoyo S, Herrero S, Señorans M, Cifuentes F, Ibáñez A. 2006. Functional characterization of pressurized liquid extracts of Spirulina platensis. Eur. Food Res. Technol. 224, 75–81.

Sarada DL, Kumar CS, Rengasamy R. 2011. Purified C-phycocyanin from Spirulina platensis (Nordstedt) Geitler: A novel and potent agent against drug resistant bacteria. World J. Microb. Biot. 27, 779–783.

Schmidt RA, Wiebe MG, Eriksen NT. 2005. Heterotrophic high cell density fed-batch cultures of the phycocyanin producing red alga Galdieria sulphuraria. Biotechnol. Bioeng. 90, 77–84.

Schwartz J, Shklar G. 1987. Regression of experimental hamster cancer by beta carotene and algae extracts. J. Oral. Maxillofacial Surg. 5, 510–515.

Schwartz J, Shklar G, Reid S, Trickler D. 1988. Prevention of experimental oral cancer by extracts of Spirulina- Dunaliella algae. Nutrition Cancer 11, 127–134.

Shao W, Ebaid R, Abomohra A, Shahen M. 2018. Enhancement of Spirulina biomass production and cadmium biosorption using combined static magnetic field. Bioresour. Technol. 265, 163–169.

Shastri D, Kumar MM, Kumar A. 1999. Modulation of lead toxicity by Spirulina fusiformis. Phytother. Res. 13, 258–260.

Simsek N, Karadeniz A, Kalkanc Y, Keles ON, Unal B. 2008. Spirulina platensis feeding inhibited the anemia- and leucopenia-induced lead and cadmium in rats. J. Hazard. Mater. 164, 1304–1309.

Sloth JK, Wiebe MG, Eriksen NT. 2006. Accumulation of Phycocyanin in heterotrophic and mixotrophic cultures of the acidophilic red alga Galdieria sulphuraria. Enzym. Microb. Technol. 38, 168–175.

Soni R, Sudhakar K, Rana R. 2016. Sustainable biomass production from microalgae for food, feed and biofuels: An integrated approach. Biosci. Biotech. Res. Comm. 9, 729–736.

Soni R, Sudhakar K, Rana R. 2017. Spirulina – From growth to nutritional product: A review. Trends Food Sci. Technol.69, 157–171.

Sørensen L, Hantke A, Eriksen NT. 2013. Purification of the photosynthetic pigment C-phycocyanin from heterotrophic Galdieria sulphuraria. J. Sci. Food Agric. 93, 2933– 2938.

Stizenberger E. 1854. Spirulina und Arthrospira (nov. gen.). Hedwigia 1, 32–41.

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

Subudhi S, Kurdrid P, Hongsthong A, Sirijuntarut M, Cheevadhanarak S, Tanticharoen M. 2008. Isolation and functional characterization of Spirulina D6D gene promoter: Role of a putative GntR transcription factor in transcriptional regulation of D6D gene expression. Biochem. Biophys. Res. Commun. 365, 643–649.

Sumprasit N, Wagle N, Glanpracha N, Annachhatre A. 2017. Biodiesel and biogas recovery from Spirulina platensis. Int. Biodeterior. Biodegrad. 119, 196–204.

Tomaselli L. 1997. Morphology, Ultrastructure and Taxonomy of Arthrospira (Spirulina) maxima and Arthrospira (Spirulina) platensis. In: Vonshak A, Spirulina platensis (Arthrospira) Physiology, cell-biology and biotechnology. Taylor & Francis Ltd., London.

Toyomizu M, Suzuki K, Kawata Y, Kojima H, Akiba Y. 2001a. Effective transformation of the cyanobacterium Spirulina platensis using electroporation. J. App. Phycol.13, 209–214.

Toyomizu M, Sato K, Taroda H, Kato T, Akiba Y. 2001b. Effects of dietary Spirulina on meat colour in muscle of broiler chickens. Bri. Poult. Sci. 42, 197–202.

Vachhani A, Vonshak A. 1997. Genetics of Spirulina. In: Vonshak A, Spirulina platensis (Arthrospira) Physiology, cell-biology and biotechnology. 1997, Taylor & Francis Ltd., London.

Vázquez-Velasco M, González-Torres L, López-Gasco P, Bastida S, Benedí J, Sánchez-Reus M, González-Muñoz M, Sánchez-Muniz F. 2014. Liver oxidation and inflammation in Fa/Fa rats fed glucomannan/Spirulina-surimi. Food Chem. 159, 215–221.

Whitton BA. 2000. Soils and rice-fields. In: Whitton BA, Potts M, editor. The ecology of cyanobacteria. Kluwer Academic, Dordrecht, Netherlands, pp. 233–255.

Xiong J, Kurade M, Jeon B. 2018. Can Microalgae Remove Pharmaceutical Contaminants from Water?. Trends Biotechnol. 36, 30–44.




Copyright (c) 2019 Consejo Superior de Investigaciones Científicas (CSIC)

Creative Commons License
This work is licensed under a Creative Commons Attribution 4.0 International License.


Contact us grasasyaceites@ig.csic.es

Technical support soporte.tecnico.revistas@csic.es