Advertisement

Phenolic compounds, carotenoids, and antioxidant capacities of a thermo-tolerant Scenedesmus sp. (Chlorophyta) extracted with different solvents

  • Onur Bulut
  • Dilan Akın
  • Çağla Sönmez
  • Ayşegül Öktem
  • Meral Yücel
  • Hüseyin Avni Öktem
Article

Abstract

The human body can fight against the adverse effects of chronic exposure to environmental pollutants and stress by consumption of a diet rich in antioxidants. Although fruits and vegetables are the predominant sources, alternative sources of antioxidants such as microalgae are also being explored. Here, we investigate the antioxidant capacity, total phenolic, flavonoid, and carotenoid contents of novel thermo-resistant green microalga Scenedesmus sp. ME02. This strain has previously been shown to have a high polyunsaturated fatty acid content. Four different solvents were used for extraction and the antioxidant capacity was determined to be 3.71 ± 0.11 and 47.01 ± 3.14 μmol Trolox eq. g−1 DW in ethanol/water mixture by 2,2-diphenyl-1-picrylhydrazyl (DPPH) and ferric reducing antioxidant power (FRAP) assays, respectively. Total phenolic, flavonoid, and carotenoid contents in ethanol/water were measured as 5.40 ± 0.28 mg gallic acid eq. g−1 DW, 1.61 ± 0.76 mg quercetin eq. g−1 DW, 0.61 ± 0.05 mg g−1, respectively. This is one of the few studies that reports the presence and quantification of total flavonoids in microalgae. The correlation between the total phenolic content and FRAP assay, but not the DPPH assay, was statistically significant. Finally, 12 different phenolic compounds were analyzed by reverse-phase HPLC and ethyl acetate extract showed substantial amounts of quercetin (0.84 ± 0.12 mg g−1 DW) and rutin (0.11 ± 0.08 mg g−1 DW). Quercetin amount was also high in the ethanol/water extract along with gallic acid, 4-hydroxy benzoic acid, and chlorogenic acid. To the best of our knowledge, this is the first study that reports significant amounts of quercetin and rutin in a microalgal species.

Keywords

Green microalgae Antioxidant capacity Phenolic compounds Flavonoids Quercetin 

Notes

Acknowledgments

The authors would like to thank Konya Food and Agriculture University (KFAU) Strategic Products Research and Development Center (SARGEM) for technical support with the HPLC analysis and KFAU Research and Development Center for Diagnostic Kits (KIT-ARGEM) for the use of the facilities.

Funding

This work was supported by KFAU Research Project BAP-2017/008.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no competing interests.

References

  1. Aremu AO, Masondo NA, Molnár Z, Stirk WA, Ördög V, Van Staden J (2016) Changes in phytochemical content and pharmacological activities of three Chlorella strains grown in different nitrogen conditions. J Appl Phycol 28:149–159CrossRefGoogle Scholar
  2. Balasundram N, Sundram K, Samman S (2006) Phenolic compounds in plants and agri-industrial by-products: antioxidant activity, occurrence, and potential uses. Food Chem 99:191–203CrossRefGoogle Scholar
  3. Borrás-Linares I, Fernández-Arroyo S, Arráez-Roman D, Palmeros-Suárez PA, Del Val-Díaz R, Andrade-Gonzáles I et al (2015) Characterization of phenolic compounds, anthocyanidin, antioxidant and antimicrobial activity of 25 varieties of Mexican Roselle (Hibiscus sabdariffa). Ind Crop Prod 69:385–394CrossRefGoogle Scholar
  4. Brewer MS (2011) Natural antioxidants: sources, compounds, mechanisms of action, and potential applications. Compr Rev Food Sci Food Saf 10:221–247CrossRefGoogle Scholar
  5. Cheng Z, Moore J, Yu L (2006) High-throughput relative DPPH radical scavenging capacity assay. J Agric Food Chem 54:7429–7436CrossRefGoogle Scholar
  6. Christen Y (2000) Oxidative stress and Alzheimer disease. Am J Clin Nutr 71:621S–629SCrossRefGoogle Scholar
  7. Custódio L, Soares F, Pereira H, Barreira L, Vizetto-Duarte C, Rodrigues MJ, Rauter AP, Alberico F, Varela J (2014) 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 26:151–161CrossRefGoogle Scholar
  8. Dai J, Mumper RJ (2010) Plant phenolics: extraction, analysis and their antioxidant and anticancer properties. Molecules 15:7313–7352CrossRefGoogle Scholar
  9. Farvin KHS, Jacobsen C (2013) Phenolic compounds and antioxidant activities of selected species of seaweeds from Danish coast. Food Chem 138:1670–1681CrossRefGoogle Scholar
  10. Firuzi O, Lacanna A, Petrucci R, Marrosu G, Saso L (2005) Evaluation of the antioxidant activity of flavonoids by “ferric reducing antioxidant power” assay and cyclic voltammetry. Biochim Biophys Acta 1721:174–184CrossRefGoogle Scholar
  11. Freile-Pelegrín Y, Robledo D (2013) Bioactive phenolic compounds from algae. In: Hernández-Ledesma B, Herrero M (eds) Bioactive compounds from marine foods: plant and animal sources. Wiley, Hoboken, pp 113–129CrossRefGoogle Scholar
  12. Goiris K, Muylaert K, Fraeye I, Foubert I, De Brabanter J, De Cooman L (2012) Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J Appl Phycol 24:1477–1486CrossRefGoogle Scholar
  13. Goiris K, Muylaert K, Voorspoels S, Noten B, De Paepe D, Baart E, De Cooman L (2014) Detection of flavonoids in microalgae from different evolutionary lineages. J Phycol 50:483–492CrossRefGoogle Scholar
  14. Guedes AC, Malcata FX (2012) Nutritional value and uses of microalgae in aquaculture. In: Muchlisin ZA (ed) Aquaculture. InTech Open, Riejecka, pp 59–78Google Scholar
  15. Guedes AC, Amaro HM, Pereira RD, Malcata FX (2011) Effects of temperature and pH on growth and antioxidant content of the microalga Scenedesmus obliquus. Biotechnol Prog 27:1218–1224CrossRefGoogle Scholar
  16. 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
  17. Holt EM, Steffen LM, Moran A, Basu S, Steinberger J, Ross JA, Hong CP, Sinaiko AR (2009) Fruit and vegetable consumption and its relation to markers of inflammation and oxidative stress in adolescents. J Am Diet Assoc 109:414–421CrossRefGoogle Scholar
  18. Ito N, Hirose M, Fukushima S, Tsuda H, Shirai T, Tatematsu M (1986) Studies on antioxidants: their carcinogenic and modifying effects on chemical carcinogenesis. Food Chem Toxicol 24:1071–1082CrossRefGoogle Scholar
  19. Jagani S, Chelikani R, Kim DS (2009) Effects of phenol and natural phenolic compounds on biofilm formation by Pseudomonas aeruginosa. Biofouling 25:321–324CrossRefGoogle Scholar
  20. Jerez-Martel I, Garcia-Poza S, Rodriguez-Martel G, Rico M, Afonso-Olivares C, Gomez-Pinchetti JL (2017) Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains. J Food Qual 2017:2924508Google Scholar
  21. Landete JM (2013) Dietary intake of natural antioxidants: vitamins and polyphenols. Crit Rev Food Sci Nutr 53:706–721CrossRefGoogle Scholar
  22. Li HB, Cheng KW, Wong CC, Fan KW, 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
  23. Lichtenthaler HK, Buschmann C (2001) Chlorophylls and carotenoids: measurement and characterization by UV-VIS spectroscopy. Current protocols in food analytical chemistry. Wiley, Hoboken, pp F4.3.1–F4.3.8Google Scholar
  24. López A, Rico M, Rivero A, de Tangil MS (2011) The effects of solvents on the phenolic contents and antioxidant activity of Stypocaulon scoparium algae extracts. Food Chem 125:1104–1109CrossRefGoogle Scholar
  25. Machu L, Misurcova L, Vavra Ambrozova J, Orsavova J, Mlcek J, Sochor J, Jurikova T (2015) Phenolic content and antioxidant capacity in algal food products. Molecules 20:1118–1133CrossRefGoogle Scholar
  26. Masella R, Di Benedetto R, Varì R, Filesi C, Giovannini C (2005) Novel mechanisms of natural antioxidant compounds in biological systems: involvement of glutathione and glutathione-related enzymes. J Nutr Biochem 16:577–586CrossRefGoogle Scholar
  27. Onay M, Sonmez C, Oktem HA, Yucel AM (2014) Thermo-resistant green microalgae for effective biodiesel production: isolation and characterization of unialgal species from geothermal flora of Central Anatolia. Bioresour Technol 169:62–71CrossRefGoogle Scholar
  28. Onay M, Sonmez C, Oktem HA, Yücel M (2016) Evaluation of various extraction techniques for efficient lipid recovery from thermo-resistant microalgae, Hindakia, Scenedesmus and Micractinium species—comparison of lipid extraction methods from microalgae. Am J Anal Chem 7:141–150CrossRefGoogle Scholar
  29. Onofrejová L, Vašíčková J, Klejdus B, Stratil P, Mišurcová L, Kráčmar S, Kopecký J, Vacek J (2010) Bioactive phenols in algae: the application of pressurized-liquid and solid-phase extraction techniques. J Pharm Biomed Anal 51:464–470CrossRefGoogle Scholar
  30. Panche AN, Diwan AD, Chandra SR (2016) Flavonoids: an overview. J Nutr Sci 5:e47Google Scholar
  31. Pandey KB, Rizvi SI (2009) Plant polyphenols as dietary antioxidants in human health and disease. Oxidative Med Cell Longev 2:270–278CrossRefGoogle Scholar
  32. Pietta PG (2000) Flavonoids as antioxidants. J Nat Prod 63:1035–1042CrossRefGoogle Scholar
  33. Prior RL (2003) Fruits and vegetables in the prevention of cellular oxidative damage. Am J Clin Nutr 78:570S–578SCrossRefGoogle Scholar
  34. Prior RL, Wu X, Schaich K (2005) Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J Agric Food Chem 53:4290–4302CrossRefGoogle Scholar
  35. Rico M, Lopez A, Santana-Casiano JM, Gonzalez AG, Gonzalez-Davila M (2013) Variability of the phenolic profile in the diatom Phaeodactylum tricornutum growing under copper and iron stress. Limnol Oceanogr 58:144–152CrossRefGoogle Scholar
  36. Safafar H, van Wagenen J, Møller P, Jacobsen C (2015) Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater. Mar Drugs 13:7339–7356CrossRefGoogle Scholar
  37. Shebis Y, Iluz D, Kinel-Tahan Y, Dubinsky Z, Yehoshua Y (2013) Natural antioxidants: function and sources. Food Nutr Sci 4:643–649Google Scholar
  38. Shetty V, Sibi G (2015) Relationship between total phenolics content and antioxidant activities of microalgae under autotrophic, heterotrophic and mixotrophic growth. J Food Resour Sci 4:1–9CrossRefGoogle Scholar
  39. Singleton VL, Rossi JA (1965) Colorimetry of total phenolics with phosphomolybdic-phosphotungstic acid reagents. Am J Enol Vitic 16:144–158Google Scholar
  40. Sonmez C, Elcin E, Akın D, Oktem HA, Yucel M (2016) Evaluation of novel thermo-resistant Micractinium and Scenedesmus sp. for efficient biomass and lipid production under different temperature and nutrient regimes. Bioresour Technol 211:422–428CrossRefGoogle Scholar
  41. Sørensen M, Gong Y, Bjarnason F, Vasanth GK, Dahle D, Huntley M, Kiron V (2017) Nannochloropsis oceania-derived defatted meal as an alternative to fishmeal in Atlantic salmon feeds. PLoS One 12:e0179907CrossRefGoogle Scholar
  42. Sugamura K, Keaney JF Jr (2011) Reactive oxygen species in cardiovascular disease. Free Radical Biol Med 51:978–992CrossRefGoogle Scholar
  43. Team RC (2013) R: A language and environment for statistical computing. (Vienna, Austria: Rfoundation for statistical computing). Available from https://www.r-project.org. Accessed 2 January 2019
  44. Vacca RA, Valenti D, Caccamese S, Daglia M, Braidy N, Nabavi SM (2016) Plant polyphenols as natural drugs for the management of Down syndrome and related disorders. Neurosci Biobehav Rev 71:865–877CrossRefGoogle Scholar
  45. Wang T, Jόnsdόttir R, Ólafsdόttir G (2009) Total phenolic compounds, radical scavenging and metal chelation of extracts from Icelandic seaweeds. Food Chem 116:240–248CrossRefGoogle Scholar
  46. Wang W, Sun C, Mao L, Ma P, Liu F, Yang J, Gao Y (2016) The biological activities, chemical stability, metabolism and delivery systems of quercetin: a review. Trends Food Sci Technol 56:21–38CrossRefGoogle Scholar
  47. Waris G, Ahsan H (2006) Reactive oxygen species: role in the development of cancer and various chronic conditions. J Carcinog 5:14CrossRefGoogle Scholar
  48. Zhang L, Ravipati AS, Koyyalamudi SR, Jeong SC, Reddy N, Smith PT, Bartlett J, Shanmugam K, Münch G, Wu MJ (2011) Antioxidant and anti-inflammatory activities of selected medicinal plants containing phenolic and flavonoid compounds. J Agric Food Chem 59:12361–12367CrossRefGoogle Scholar
  49. Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Onur Bulut
    • 1
    • 2
    • 3
  • Dilan Akın
    • 2
  • Çağla Sönmez
    • 1
  • Ayşegül Öktem
    • 2
  • Meral Yücel
    • 2
  • Hüseyin Avni Öktem
    • 2
  1. 1.Department of Molecular Biology and Genetics, Faculty of Agriculture and Natural SciencesKonya Food and Agriculture UniversityKonyaTurkey
  2. 2.Department of Biological SciencesMiddle East Technical UniversityAnkaraTurkey
  3. 3.Research and Development Center for Diagnostic Kits (KIT-ARGEM)Konya Food and Agriculture UniversityKonyaTurkey

Personalised recommendations