Abstract
Organic and water extracts of Isochrysis galbana T-ISO (=Tisochrysis lutea), Tetraselmis sp. and Scenedesmus sp. were evaluated for their antioxidant activity, acetylcholinesterase (AChE) inhibition, cytotoxicity against tumour cell lines, and fatty acids and total phenolic content (TPC). I. galbana T-ISO had the highest TPC (3.18 mg GAE g−1) and radical scavenging activity, with an IC50 value of 1.9 mg mL−1 on the acetone extract. The extracts exhibited a higher ability to chelate Fe2+ than Cu2+, and the maximum Fe2+ chelating capacity was observed in the hexane extract of Scenedesmus sp. (IC50=0.73 mg mL−1) and Scenedesmus sp. (IC50 = 0.73 mg mL−1). The highest ability to inhibit AChE was observed in the water and ether extracts of Scenedesmus sp., with IC50 values of 0.11 and 0.15 mg mL−1, respectively, and in the water extract of I. galbana (IC50 = 0.16 mg mL−1). The acetone extract of I. galbana T-ISO significantly reduced the viability of human hepatic carcinoma HepG2 cells (IC50 = 81.3 μg mL−1) as compared to the non-tumour murine stromal S17 cell line, and displayed a selectivity index of 3.1 at the highest concentration tested (125 μg mL−1). All species presented a highly unsaturated fatty acids profile. Results suggest that these microalgae, particularly I. galbana T-ISO, could be a source of biomolecules for the pharmaceutical industry and the production of functional food ingredients and can be considered as an advantageous alternative to several currently produced microalgae.
Similar content being viewed by others
References
Bendif EM, Probert I, Schroeder DC, de Vargas C (2013) On the description of Tisochrysis lutea gen. nov. sp. nov. and Isochrysis nuda sp. nov. in the Isochrysidales, and the transfer of Dicrateria to the Prymnesiales (Haptophyta). J Appl Phycol. doi:10.1007/s10811-013-0037-0
Bhakuni DS, Rawat DS (2005) Bioactive marine natural products, 1st edn. Anamaya Publishers, New Delhi
Boyd MR (1997) The NCI in vitro anticancer drug discovery screen: concept, implementation, and operation. In: Teicher BA (ed) Anticancer drug development guide: preclinical screening, clinical trials, and approval. Humana Press, Totowa
Burdge GC, Finnegan YE, Minihane AM, Williams CM, Wootton SA (2003) Effect of altered dietary n-3 fatty acid intake upon plasma lipid fatty acid composition, conversion of [13C] α-linolenic acid to longer-chain fatty acids and partitioning towards β-oxidation in older men. Brit J Nutr 90:311–321
Cerón MC, García-Malea MC, Rivas J, Acien FG, Fernández JM, Del Río E, Guerrero MG, Molina E (2007) Antioxidant activity of Haematococcus pluvialis cells grown in continuous culture as a function of their carotenoid and fatty acid content. Appl Microbiol Biotechnol 74:1112–1119
Chacón-Lee TL, González-Maríño GE (2010) Microalgae for “healthy” foods—possibilities and challenges. Crit Rev Food Sci Food Saf 9:655–675
Ciro A, Park J, Burkhard G, Yan N, Geula C (2012) Biochemical differentiation of cholinesterases from normal and Alzheimer’s disease cortex. Curr Alzheimer Res 9:138–143
Coesel SN, Baumgartner AC, Teles LM, Ramos AR, Henriques NM, Cancela L, Varela J (2008) Nutrient limitation is the main regulatory factor for carotenoid accumulation and for Psy and Pds steady state transcript levels in Dunaliella salina (Chlorophyta) exposed to high light and salt stress. Mar Biotechnol 10:601–611
Custódio L, Justo T, Silvestre L, Barradas A, Vizetto C, Pereira H, Barreira L, Rauter AP, Alberício F, Varela J (2012) Microalgae of different phyla display antioxidant, metal chelating and acetylcholinesterase inhibitory activities. Food Chem 131:134–140
Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352
Damiani MC, Popovich CA, Constenla D, Leonardi PI (2010) Lipid analysis in Haematococcus pluvialis to assess its potential use as a biodiesel feedstock. Bioresour Technol 101:3801–3807
Danielson SR, Andersen K (2008) Oxidative and nitrative protein modifications in Parkinson’s disease. Free Radic Biol Med 44:1787–1794
Duval B, Shetty K, Thomas WH (2000) Phenolic compounds and antioxidant properties in the snow alga Chlamydomonas nivalis after exposure to UV light. J Appl Phycol 11:559–566
EFSA Panel on Dietetic Products, Nutrition, and Allergies (NDA) (2010) Scientific opinion on dietary reference values for fats, including saturated fatty acids, polyunsaturated fatty acids, monounsaturated fatty acids, trans fatty acids, and cholesterol. EFSA J 8:1461
El-Baky HHA, El-Baz FK, El-Baroty GS (2004) Production of lipids rich in omega 3 fatty acids from the halotolerant alga Dunaliella salina. Biotechnology 3:102–108
El-Baky HHA, El Baz FKE, El-Baroty GSE (2009) Production of phenolic compounds from Spirulina maxima microalgae and its protective effects in vitro toward hepatotoxicity model. Afr J Pharm Pharmacol 3:133–139
Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95
El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557–2576
Fang Z, Jeong SY, Jung HA, Choi JS, Min BS, Woo MH (2010) Anticholinesterase and antioxidant constituents from Gloiopeltis furcata. Chem Pharm Bull 58:1236–1239
Fidalgo JP, Cid A, Torres E, Sukenik A, Herrero C (1998) Effects of nitrogen source and growth phase on proximate biochemical composition, lipid classes and fatty acid profile of the marine microalga Isochrysis galbana. Aquaculture 166:105–116
Filho J, Medeiros K, Diniz M, Batista L, Athayde-Filho P, Silva M, da-Cunha E (2006) Natural products inhibitors of the enzyme acetylcholinesterase. Braz J Pharmacogn 16:258–285
Franco D, Sineiro J, Rubilar M, Sánchez M, Jerez M, Pinelo M, Costoya N, Núñez MJ (2008) Polyphenols from plant materials: extraction and antioxidant power. Electron J Environ Agric Food Chem 7:3210–3216
Gaeta A, Hider RC (2005) The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Brit J Pharmacol 146:1041–1059
Gish RG, Porta C, Lazar L, Ruff P, Feld R, Croitoru A, Feun L, Jeziorski K, Leighton J, Knox J, Gallo J, Kennealey GT (2007) Phase III randomized controlled trial comparing the survival of patients with unresectable hepatocellular carcinoma treated with nolatrexed or doxorubicin. J Clin Oncol 25:3069–3075
Givens DI, Gibbs RA (2008) Current intakes of EPA and DHA in European populations and the potential of animal-derived foods to increase them. Proc Nutr Soc 67:273–280
Goiris K, Muylaert K, Fraeye I, Foubert I, Brabanter JD, Cooman LD (2012) Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol 24:1477–1486
Guedes AC, Amaro HMF, Malcata X (2011) Microalgae as sources of high added-value compounds—a brief review of recent work. Biotechnol Prog 27:597–613
Hajimahmoodi M, Faramarzi MA, Mohammadi N, Soltani N, Oveisi MR, Nafissi-Varcheh N (2010) Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J Appl Phycol 22:43–50
Huerlimann R, de Nys R, Heimann K (2010) Growth, lipid content, productivity, and fatty acid composition of tropical microalgae for scale-up production. Biotechnol Bioeng 107:245–257
Kaplan D, Cohen Z, Abeliovich A (1986) Optimal growth conditions for Isochrysis galbana. Biomass 9:37–48
Klejdus B, Kopecky J, Benesová L, Vacek J (2009) Solid-phase/supercritical-fluid extraction for liquid chromatography of phenolic compounds in freshwater microalgae and selected cyanobacterial species. J Chromatogr A 1216:763–771
Komprda T (2012) Eicosapentaenoic and docosahexaenoic acids as inflammation-modulating and lipid homeostasis influencing nutraceuticals: a review. J Funct Food 4:25–38
Lepage G, Roy CC (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396
Li H-B, Cheng K-W, Wong C-C, Fan K-W, Chen F, Jiang Y (2007) Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem 102:771–776
Lordan SR, Ross P, Stanton C (2011) Marine bioactives as functional food ingredients: potential to reduce the incidence of chronic diseases. Mar Drugs 9:1056–1100
Mahavorasirikul W, Viyanant V, Chaijaroenkul W, Itharat A, Na-Bangchang K (2010) Cytotoxic activity of Thai medicinal plants against human cholangiocarcinoma, laryngeal and hepatocarcinoma cells in vitro. BMC Complement Alternat Med 10:55
Megías C, Pastor-Cavada E, Torres-Fuentes C, Girón-Calle J, Alaiz M, Jua R, Julio P, Javier V (2009) Chelating, antioxidant and antiproliferative activity of Vicia sativa polyphenol extracts. Eur Food Res Technol 230:353–359
Mendes A, Silva TL, Reis A (2007) DHA concentration and purification from the marine heterotrophic microalga Crypthecodinium cohnii CCMP316 by winterization and urea complexation. Food Technol Biotechnol 45:38–44
Moreno S, Scheyer T, Romano C, Vojnov A (2006) Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radic Res 40:223–231
Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63
Natrah FMI, Yusoff FM, Shariff M, Abas F, Mariana NS (2007) Screening of Malaysian indigenous microalgae for antioxidant properties and nutritional value. J Appl Phycol 19:711–718
Nuño K, Villarruel-López A, Puebla-Pérez AM, Romero-Velarde E, Puebla-Mora AG, Ascencio F (2013) Effects of the marine microalgae Isochrysis galbana and Nannochloropsis oculata in diabetic rats. J Funct Foods 5:106–115
O’Neil GW, Carmichael CA, Goepfert TJ, Fulton JM, Knothe G, Lau CPL, Lindell SR, Mohammady NG-E, Van Mooy BAS, Reddy CM (2012) Beyond fatty acid methyl esters: expanding the renewable carbon profile with alkenones from Isochrysis sp. Energy Fuel 26:2434–2441
Oh SH, Ahn J, Kang DH, Lee HY (2011) The effect of ultrasonificated extracts of Spirulina maxima on the anticancer activity. Mar Biotechnol 13:205–214
Olaizola M (2003) Commercial development of microalgal biotechnology: from the test tube to the marketplace. J Biomol Eng 20:459–466
Orhan I, Kartal M, Naz Q, Ejaz A, Yilmaz G, KanY KB, Sener B, Choudhary MI (2007) Antioxidant and anticholinesterase evaluation of selected Turkish Salvia species. Food Chem 103:1247–1254
Otleş S, Pire R (2001) Fatty acid composition of Chlorella and Spirulina microalgae species. J AOAC Int 84:1708–1714
Pangestuti R, Se-Kwon Kim S-K (2011) Neuroprotective effects of marine algae Mar. Drugs 9:803-818
Pereira H, Barreira L, Figueiredo F, Custódio L, Vizetto-Duarte C, Polo C, Rešek E, Engelen A, Varela J (2012) Marine macroalgae as a source of polyunsaturated fatty acids for nutritional and pharmaceutical applications. Mar Drugs 10:1920–1935
Plaza M, Herrero M, Cifuentes A, Ibáñez E (2009) Innovative natural functional ingredients from microalgae. J Agric Food Chem 57:7159–7170
Pratoomyot J, Srivilas P, Noiraksar T (2005) Fatty acids composition of 10 microalgal species. Songklanakarin J Sci Technol 27:1179–1187
Pulok KM, Venkatesan K, Mainak M, Houghton PJ (2007) Acetylcholinesterase inhibitors from plants. Phytomedicine 14:289–300
Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648
Roncarati A, Meluzzi A, Acciarri S, Tallarico N, Melotti P (2007) Fatty acid composition of different microalgae strains (Nannochloropsis sp., Nannochloropsis oculata (Droop) Hibberd, Nannochloris atomus Butcher and Isochrysis sp.) according to the culture phase and the carbon dioxide concentration. J World Aquacult Soc 35:401–411
Ruxton CHS, Calder PC, Reed SC, Simpson MJA (2005) The impact of LC n-3 PUFA on human health. Nutr Res Rev 18:113–129
Sánchez JF, Fernández JM, Acién FG, Rueda A, Pérez-Parra J, Molina E (2008) Influence of culture conditions on the productivity and lutein content of the new strain Scenedesmus almeriensis. Process Biochem 43:398–405
Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688
Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial application of microalgae. J Biosci Bioeng 101:87–96
Stalikas CD (2007) Extraction, separation, and detection methods for phenolic acids and flavonoids. J Sep Sci 30:3268–3295
Suresh Y, Das UN (2003) Long-chain polyunsaturated fatty acids and chemically induced diabetes mellitus: effect of ω-3 fatty acids. Nutrition 19:213–228
Ulloa G, Otero A, Sánchez M, Sineiro J, Núñez MJ, Fábregas J (2012) Effect of Mg, Si, and Sr on growth and antioxidant activity of the marine microalga Tetraselmis suecica. J Appl Phycol 24:1229–1236
Uma R, Sivasubramanian V, Devaraj SN (2011) Evaluation of in vitro antioxidant activities and antiproliferative activity of green microalgae, Desmococcus olivaceous and Chlorococcum humicola L. Algal Biomass Utln 2:82–93
van Gelder BM, Tijhuis M, Kalmijn S, Kromhout D (2007) Fish consumption, n-3 fatty acids, and subsequent 5-y cognitive decline in elderly men: the Zutphen Elderly Study. Am J Clin Nutr 85:1142–1147
Velioglu YS, Mazza G, Gao L, Oomah BD (1998) Antioxidant activity and total phenolics in selected fruits, vegetables, and grain products. J Agric Food Chem 46:4113–4117
Williams P, Sorribas A, Howes M-JR (2011) Natural products as a source of Alzheimer’s drug leads. Nat Prod Rep 28:48–77
Acknowledgments
This work was supported by the SEABIOMED project (PTDC/MAR/103957/2008), funded by the Foundation for Science and Technology (FCT) and the Portuguese National Budget. LC is an FCT post-doctoral research fellow (SFRH/BPD/65116/2009). CVD is an FCT doctoral research student (SFRH/BD/81425/2011). All the algal species used in this study were provided by NECTON S.A. (Portugal). The authors would like to dedicate this article to the memory of Fernando Soares, whose untimely passing remind us all of the pressing need for novel medical treatments for cancer.
Author information
Authors and Affiliations
Corresponding authors
Rights and permissions
About this article
Cite this article
Custódio, L., Soares, F., Pereira, H. et al. Fatty acid composition and biological activities of Isochrysis galbana T-ISO, Tetraselmis sp. and Scenedesmus sp.: possible application in the pharmaceutical and functional food industries. J Appl Phycol 26, 151–161 (2014). https://doi.org/10.1007/s10811-013-0098-0
Received:
Revised:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10811-013-0098-0