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Journal of Applied Phycology

, Volume 26, Issue 1, pp 151–161 | Cite as

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

  • Luísa Custódio
  • Fernando Soares
  • Hugo Pereira
  • Luísa Barreira
  • Catarina Vizetto-Duarte
  • Maria João Rodrigues
  • Amélia Pilar Rauter
  • Fernando Alberício
  • João Varela
Article

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.

Keywords

AChE inhibitors Antioxidants Functional foods Marine natural products Microalgae Polyunsaturated fatty acids 

Notes

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.

References

  1. 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 Google Scholar
  2. Bhakuni DS, Rawat DS (2005) Bioactive marine natural products, 1st edn. Anamaya Publishers, New DelhiGoogle Scholar
  3. 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, TotowaGoogle Scholar
  4. 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 90:311–321PubMedCrossRefGoogle Scholar
  5. 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 74:1112–1119PubMedCrossRefGoogle Scholar
  6. Chacón-Lee TL, González-Maríño GE (2010) Microalgae for “healthy” foods—possibilities and challenges. Crit Rev Food Sci Food Saf 9:655–675CrossRefGoogle Scholar
  7. 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 9:138–143PubMedCentralPubMedCrossRefGoogle Scholar
  8. 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 10:601–611CrossRefGoogle Scholar
  9. 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 131:134–140CrossRefGoogle Scholar
  10. Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352PubMedCrossRefGoogle Scholar
  11. 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 101:3801–3807PubMedCrossRefGoogle Scholar
  12. Danielson SR, Andersen K (2008) Oxidative and nitrative protein modifications in Parkinson’s disease. Free Radic Biol Med 44:1787–1794PubMedCentralPubMedCrossRefGoogle Scholar
  13. 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 11:559–566CrossRefGoogle Scholar
  14. 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 8:1461Google Scholar
  15. 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 3:102–108CrossRefGoogle Scholar
  16. 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 3:133–139Google Scholar
  17. Ellman GL, Courtney KD, Andres V, Featherstone RM (1961) A new and rapid colorimetric determination of acetylcholinesterase activity. Biochem Pharmacol 7:88–95PubMedCrossRefGoogle Scholar
  18. El-Serag HB, Rudolph KL (2007) Hepatocellular carcinoma: epidemiology and molecular carcinogenesis. Gastroenterology 132:2557–2576PubMedCrossRefGoogle Scholar
  19. Fang Z, Jeong SY, Jung HA, Choi JS, Min BS, Woo MH (2010) Anticholinesterase and antioxidant constituents from Gloiopeltis furcata. Chem Pharm Bull 58:1236–1239PubMedCrossRefGoogle Scholar
  20. 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 166:105–116CrossRefGoogle Scholar
  21. 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 16:258–285Google Scholar
  22. 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 7:3210–3216Google Scholar
  23. Gaeta A, Hider RC (2005) The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Brit J Pharmacol 146:1041–1059CrossRefGoogle Scholar
  24. 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 25:3069–3075PubMedCrossRefGoogle Scholar
  25. 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 67:273–280CrossRefGoogle Scholar
  26. 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 24:1477–1486CrossRefGoogle Scholar
  27. Guedes AC, Amaro HMF, Malcata X (2011) Microalgae as sources of high added-value compounds—a brief review of recent work. Biotechnol Prog 27:597–613PubMedCrossRefGoogle Scholar
  28. 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 22:43–50CrossRefGoogle Scholar
  29. 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 107:245–257PubMedCrossRefGoogle Scholar
  30. Kaplan D, Cohen Z, Abeliovich A (1986) Optimal growth conditions for Isochrysis galbana. Biomass 9:37–48CrossRefGoogle Scholar
  31. 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 1216:763–771PubMedCrossRefGoogle Scholar
  32. Komprda T (2012) Eicosapentaenoic and docosahexaenoic acids as inflammation-modulating and lipid homeostasis influencing nutraceuticals: a review. J Funct Food 4:25–38CrossRefGoogle Scholar
  33. Lepage G, Roy CC (1984) Improved recovery of fatty acid through direct transesterification without prior extraction or purification. J Lipid Res 25:1391–1396PubMedGoogle Scholar
  34. 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 102:771–776CrossRefGoogle Scholar
  35. Lordan SR, Ross P, Stanton C (2011) Marine bioactives as functional food ingredients: potential to reduce the incidence of chronic diseases. Mar Drugs 9:1056–1100PubMedCentralPubMedCrossRefGoogle Scholar
  36. 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 10:55CrossRefGoogle Scholar
  37. 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 230:353–359CrossRefGoogle Scholar
  38. 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 45:38–44Google Scholar
  39. Moreno S, Scheyer T, Romano C, Vojnov A (2006) Antioxidant and antimicrobial activities of rosemary extracts linked to their polyphenol composition. Free Radic Res 40:223–231PubMedCrossRefGoogle Scholar
  40. Mosmann T (1983) Rapid colorimetric assay for cellular growth and survival: application to proliferation and cytotoxicity assays. J Immunol Methods 65:55–63PubMedCrossRefGoogle Scholar
  41. 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 19:711–718CrossRefGoogle Scholar
  42. 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 5:106–115CrossRefGoogle Scholar
  43. 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 26:2434–2441CrossRefGoogle Scholar
  44. Oh SH, Ahn J, Kang DH, Lee HY (2011) The effect of ultrasonificated extracts of Spirulina maxima on the anticancer activity. Mar Biotechnol 13:205–214PubMedCrossRefGoogle Scholar
  45. Olaizola M (2003) Commercial development of microalgal biotechnology: from the test tube to the marketplace. J Biomol Eng 20:459–466CrossRefGoogle Scholar
  46. 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 103:1247–1254CrossRefGoogle Scholar
  47. Otleş S, Pire R (2001) Fatty acid composition of Chlorella and Spirulina microalgae species. J AOAC Int 84:1708–1714PubMedGoogle Scholar
  48. Pangestuti R, Se-Kwon Kim S-K (2011) Neuroprotective effects of marine algae Mar. Drugs 9:803-818Google Scholar
  49. 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 10:1920–1935PubMedCentralPubMedCrossRefGoogle Scholar
  50. Plaza M, Herrero M, Cifuentes A, Ibáñez E (2009) Innovative natural functional ingredients from microalgae. J Agric Food Chem 57:7159–7170PubMedCrossRefGoogle Scholar
  51. Pratoomyot J, Srivilas P, Noiraksar T (2005) Fatty acids composition of 10 microalgal species. Songklanakarin J Sci Technol 27:1179–1187Google Scholar
  52. Pulok KM, Venkatesan K, Mainak M, Houghton PJ (2007) Acetylcholinesterase inhibitors from plants. Phytomedicine 14:289–300CrossRefGoogle Scholar
  53. Pulz O, Gross W (2004) Valuable products from biotechnology of microalgae. Appl Microbiol Biotechnol 65:635–648PubMedCrossRefGoogle Scholar
  54. 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 35:401–411CrossRefGoogle Scholar
  55. Ruxton CHS, Calder PC, Reed SC, Simpson MJA (2005) The impact of LC n-3 PUFA on human health. Nutr Res Rev 18:113–129PubMedCrossRefGoogle Scholar
  56. 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 43:398–405CrossRefGoogle Scholar
  57. Simopoulos AP (2008) The importance of the omega-6/omega-3 fatty acid ratio in cardiovascular disease and other chronic diseases. Exp Biol Med 233:674–688CrossRefGoogle Scholar
  58. Spolaore P, Joannis-Cassan C, Duran E, Isambert A (2006) Commercial application of microalgae. J Biosci Bioeng 101:87–96PubMedCrossRefGoogle Scholar
  59. Stalikas CD (2007) Extraction, separation, and detection methods for phenolic acids and flavonoids. J Sep Sci 30:3268–3295PubMedCrossRefGoogle Scholar
  60. Suresh Y, Das UN (2003) Long-chain polyunsaturated fatty acids and chemically induced diabetes mellitus: effect of ω-3 fatty acids. Nutrition 19:213–228PubMedCrossRefGoogle Scholar
  61. 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 24:1229–1236CrossRefGoogle Scholar
  62. 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 2:82–93Google Scholar
  63. 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 85:1142–1147PubMedGoogle Scholar
  64. 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 46:4113–4117CrossRefGoogle Scholar
  65. Williams P, Sorribas A, Howes M-JR (2011) Natural products as a source of Alzheimer’s drug leads. Nat Prod Rep 28:48–77PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2013

Authors and Affiliations

  • Luísa Custódio
    • 1
  • Fernando Soares
    • 1
  • Hugo Pereira
    • 1
  • Luísa Barreira
    • 1
  • Catarina Vizetto-Duarte
    • 1
  • Maria João Rodrigues
    • 1
  • Amélia Pilar Rauter
    • 2
  • Fernando Alberício
    • 3
    • 4
    • 5
    • 6
  • João Varela
    • 1
  1. 1.Centre of Marine SciencesUniversity of Algarve, Faculty of Sciences and TechnologyFaroPortugal
  2. 2.Faculty of Sciences, Center of Chemistry and Biochemistry, Department of Chemistry and BiochemistryUniversity of LisbonLisbonPortugal
  3. 3.Institute for Research in BiomedicineBarcelonaSpain
  4. 4.CIBER-BBN, Networking Centre on Bioengineering, Biomaterials and NanomedicineBarcelonaSpain
  5. 5.School of ChemistryUniversity of KwaZulu-NatalDurbanSouth Africa
  6. 6.Department of Organic ChemistryUniversity of BarcelonaBarcelonaSpain

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