Carotenoids, phenolic compounds and tocopherols contribute to the antioxidative properties of some microalgae species grown on industrial wastewater

Marine Drugs

Volumn 13, Issue 12, 2015, Pages 7339-7356

  Safafar, Hamed ^a   Wagenen, Jonathan Van ^a   Møller, Per ^b   Jacobsen, Charlotte ^a  

^a TECHNICAL UNIVERSITY OF DENMARK   (Denmark)

^b Kalundborg Municipality   (Denmark)

Author keywords

Antioxidants; Carotenoids; DPPH; FRAP; Microalgae; Phenolic compounds; Tocopherols; Wastewater

Indexed keywords

CAROTENOID; PHENOL DERIVATIVE; TOCOPHEROL DERIVATIVE; ANTIOXIDANT; SCAVENGER; TOCOPHEROL; WASTE WATER;

ANALYSIS OF VARIANCE; ANTIOXIDANT ACTIVITY; ARTICLE; BIOCHEMICAL OXYGEN DEMAND; BIOMASS; CHLORELLA; CONTROLLED STUDY; DESMODESMUS; DPPH RADICAL SCAVENGING ASSAY; DUNANIELLA; ELECTRON TRANSPORT; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; LIPID PEROXIDATION; LIPOPHILICITY; MICROALGA; NANNOCHLOROPSIS; NONHUMAN; OXIDATIVE STRESS; PARTICLE SIZE; PHAEODACTYLUM; PULSED ELECTRIC FIELD; REGRESSION ANALYSIS; WASTE WATER; CHEMISTRY; ISOLATION AND PURIFICATION;

ANTIOXIDANTS; BIOMASS; CAROTENOIDS; FREE RADICAL SCAVENGERS; MICROALGAE; PHENOLS; TOCOPHEROLS; WASTE WATER;

EID: 84959010276     PISSN: None     EISSN: 16603397     Source Type: Journal    
DOI: 10.3390/md13127069     Document Type: Article

References (53)

1. Stengel, D.B.; Connan, S.; Popper, Z.A. Algal chemo diversity and bioactivity: Sources of natural variability and implications for commercial application. J. Biotechnol. Adv. 2011, 29, 483-501. [CrossRef] [PubMed]
2. Rong, T. Review, Chemistry and Biochemistry of Dietary Polyphenols. Nutrients 2010, 2, 1231-1246.
3. Li, H.B.; Cheng, K.W.;Wong, C.C. Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem. 2007, 102, 771-776. [CrossRef]
4. Rao, A.R.; Sarada, R.; Baskaran, V.; Ravishankar, G.A. Antioxidant activity of Botryococcus braunii extract elucidated in vitro models. J. Agric. Food Chem. 2006, 54, 4593-4599. [CrossRef] [PubMed]
5. Wu, L.; Ho, J.A.; Shieh, M.; Lu, I. Antioxidant and antiproliferative activities of Spirulina and Chlorella water extracts. J. Agric. Food Chem. 2005, 53, 4207-4212. [CrossRef] [PubMed]
6. Manivannan, K.; Anantharaman, P.; Balasubramanian, T. Evaluation of antioxidant properties of marine microalga Chlorella marina (Butcher, 1952). Asian Pac. J. Trop. Biomed. 2012, 2, S342-S346. [CrossRef]
7. Anantharaman, P.; Hemalatha, A.; Girija, K.; Parthiban, C.; Saranya, C. Antioxidant properties and total phenolic content of a marine diatom, Navicula clavata and green microalgae, Chlorella marina and Dunaliella salina. Adv. Appl. Sci. Res. 2013, 4, 151-157.
8. Herrero, M.J.L.; Martin-Alvarez, P.J.; Cifuentes, A.; Ibanez, E. Optimization of the extraction of antioxidants from Dunaliella salina microalga by pressurized liquids. J. Agric. Food Chem. 2006, 54, 5597-5603. [CrossRef] [PubMed]
9. Choochote, W.; Suklampoo, L.; Ochaikul, D. Evaluation of antioxidant capacities of green microalgae. J. Appl. Phycol. 2014, 26, 43-48. [CrossRef]
10. Guzman, S.; Gato, A.; Galleja, J.M. Anti-inflammatory, analgesic and free radical scavenging activities of the marine microalgae Chlorella stigmatophora and Phaeodactylum tricorntum. Phytother. Res. 2001, 15, 224-230. [CrossRef] [PubMed]
11. Jaime, L.; Mendiola, J.A.; Herrero, M.; Soler-Rivas, C.; Santoyo, S.; Senorans, F.J. Separation and characterization of antioxidants from Spirulina platensis microalga combining pressurized liquid extraction, TLC and HPLC-DAD. J. Sep. Sci. 2005, 28, 2111-2119. [CrossRef] [PubMed]
12. Miranda, M.S.; Cintra, R.G.; Barros, S.B.M.; Mancini-Filho, J. Antioxidant activity of the microalga Spirulina maxima. Braz. J. Med. Biol. Res. 1998, 31, 1075-1079. [CrossRef] [PubMed]
13. Goh, S.; Yusoff, M.F.; Loh, S.P. A Comparison of the Antioxidant Properties and Total Phenolic Content in a Diatom, Chaetoceros sp. and a Green Microalga, Nannochloropsis sp. J. Agric. Sci. 2010, 2, 1-8. [CrossRef]
14. Lee, S.; Lee, J.B.; Lee, K.W.; Jeon, Y.J. Antioxidant properties of tidal pool microalgae, Halochlorococcum porphyrae and Oltamannsiellopsis unicellularis from Jeju Island, Korea. Algae 2010, 25, 45-56. [CrossRef]
15. Barredo, J.L. Microbial Carotenoids from Bacteria and Microalgae. In Methods and Protocols; Humana Press: New York, NY, USA, 2012; p. 5.
16. Goiris, K.; Muylaert, K.; Fraeye, I.; Foubert, I.; de Brabanter, J.; de Cooman, L. Antioxidant potential of microalgae in relation to their phenolic and carotenoid content. J. Appl. Phycol. 2012, 24, 1477-1486. [CrossRef]
17. Takaichi, S. Carotenoids in Algae: Distributions, Biosyntheses and Functions. Mar. Drugs 2011, 9, 1101-1118. [CrossRef] [PubMed]
18. Jahnke, L.S. Massive carotenoid accumulation in Dunaliella bardawil induced by ultraviolet-A radiation. J. Photochem. Photobiol. 1999, 48, 68-74. [CrossRef]
19. Natrah, F.M.; Yusoff, F.M.; Shariff, M.; Abbas, F.; Mariana, N.S. Screening of Malaysian indigenous microalgae for antioxidant properties and nutritional value. J. Appl. Phycol. 2007, 19, 711-718. [CrossRef]
20. Klejdus, B.; Kopeckýb, J.; Benešová, L.; Vaceka, J. Solid-phase/supercritical-fluid extraction for liquid chromatography of phenolic compounds in freshwater microalgae and selected cyanobacterial species. J. Chromatogr. 2009, 1216, 763-771. [CrossRef] [PubMed]
21. Chaudhuri, D.; Baban, N.; Deb, S.; Panja, S.; Sarkar, R.; Rout, J.; Mandal, N. Assessment of the phytochemical constituents and antioxidant activity of a bloom forming microalgae Euglena tuba. Biol. Res. 2014, 47, 24-27. [CrossRef] [PubMed]
22. Goiris, K.; Muylaert, K.; Voorspoels, S.; de Paepe, D.J.E.; Baart, G.; de Cooman, L. Detection of flavonoids in microalgae from different evolutionary lineages. J. Phycol. 2014, 50, 483-492. [CrossRef]
23. Liu, J.; Sun, Z.; Gerken, H. Potential Applications of Microalgae in Wastewater Treatments. In Recent Advances in Microalgal Biotechnology; OMICS Group e-Books: Hyderabad, India, 2014.
24. Zepka, L.Q.; Rodrigues, D.B.; Flores, E.M.M.; Barin, J.S. Production of carotenoids from microalgae cultivated using agro industrial wastes. Food Res. Int. 2014, 65, 144-148.
25. Francisco, J.B.; Grimi, N.; Vorobiev, E. New Approaches for the Use of Non-conventional Cell Disruption Technologies to Extract Potential Food Additives and Nutraceuticals from Microalgae. Food Eng. Rev. 2015, 7, 45-62.
26. Lebovka, N.; Parniakov, O.; Barba, F.J.; Grimi, N.; Marchal, L.; Jubeau, S.; Vorobiev, E. Pulsed electric field assisted extraction of nutritionally valuable compounds from microalgae Nannochloropsis spp. using the binary mixture of organic solvents and water. Innov. Food Sci. Emerg. Technol. 2015, 27, 79-85.
27. Grimi, N.; Parniakov, O.; Apicella, E.; Koubaa, M.; Barb, J.; Lebovka, N.; Pataro, G.; Ferrari, G.; Vorobiev, E. Ultrasound-assisted green solvent extraction of high-added value compounds from microalgae Nannochloropsis spp. Bioresour. Technol. 2015, 198, 262-267.
28. Craft, N.E.; Soares, J.H. Relative Solubility, Stability, and Absorptivity of Lutein and-Carotene in Organic Solvents. J. Aagric. Food Chem. 1992, 40, 431-434. [CrossRef]
29. Sava, C.; Sibru, R. Analytical study of the determination of flavonoids in Black Sea algae. Ovidius Univ. Ann. Chem. 2010, 21, 29-34.
30. Klein, B.C.; Lange, H.A.; Buchholz, R. Microalgae as natural sources for antioxidative compounds. J. Appl. Phycol. 2012, 24, 1133-1139. [CrossRef]
31. Duan, X.; Zhang, W.; Li, X.; Wang, B. Evaluation of antioxidant property of extract and fractions obtained from a red alga, Polysiphonia urceolata. Food Chem. 2006, 95, 37-43. [CrossRef]
32. Kuda, T.; Tsunekawa, M.; Hishi, T.; Araki, Y. Antioxidant properties of dried Kayamo-nori, a brown alga Scytosiphon lomentaria (Scytosiphonales, Phaeophyceae). Food Chem. 2005, 89, 617-622. [CrossRef]
33. Hajimahmoodi, M.; Faramarzi, M.A.; Mohammadi, N.; Soltani, N.; Oveisi, M.R.; Nafissi-Varcheh, N. Evaluation of antioxidant properties and total phenolic contents of some strains of microalgae. J. Appl. Phycol. 2010, 22, 43-50. [CrossRef]
34. Anantharaman, P.; Saranya, C.; Hemalatha, A.; Parthiban, C. Evaluation of Antioxidant Properties, Total Phenolic and Carotenoid Content of Chaetoceros calcitrans, Chlorella salina and Isochrysis galbana. Int. J. Curr. Microbiol. App. Sci. 2014, 3, 365-377.
35. Jimenez-Escrig, A.; Jimenez-Jimenez, I.; Pulido, R.; Saura-Calixto, F. Antioxidant activity of fresh and processed edible seaweeds. J. Sci. Food Agric. 2001, 81, 530-534. [CrossRef]
36. Everette, J.D.; Bryant, Q.M.; Green, A.M.; Abbey, Y.A.; Wangila, G.W.; Walker, R.B. Thorough Study of Reactivity of Various Compound Classes toward the Folin Ciocalteu Reagent. J. Agric. Food Chem. 2010, 58, 8139-8144. [CrossRef] [PubMed]
37. Durmaz, Y. Vitamin E (-tocopherol) production by the marine microalgae Nannochloropsis oculata (Eustigmatophyceae) in nitrogen limitation. Aquaculture 2007, 272, 717-722. [CrossRef]
38. Vismara, R.; Vestri, S.; Kusmic, C.; Brarsanti, L.; Gualtieri, P. Natural vitamin E enrichment of Artema salina fed freshwater and marine microalgae. J. Appl. Phycol. 2003, 15, 75-80. [CrossRef]
39. Solovchenko, A.E.; Chivkunova, O.B.; Semenova, L.R. Stress-induced changes in pigment and fatty acid content in the microalga Desmodesmus sp. Isolated from a White Sea hydroid. Russ. J. Plant Physiol. 2013, 60, 313-321. [CrossRef]
40. Mulders, K.J.M.; Lamers, P.P.; Martens, D.E.; Wijffels, R.H. Phototrophic pigment production with microalgae: Biological constraints and opportunitie. J. Phycol. 2014, 50, 229-242. [CrossRef]
41. Cordero, B.F.; Obraztsova, I.; Couso, I.; Leon, R.; Vargas, M.A.; Rodriguez, H. Enhancement of lutein production in Chlorella sorokiniana (Chorophyta) by improvement of culture conditions and random mutagenesis. Mar. Drugs 2011, 9, 1607-1624. [CrossRef] [PubMed]
42. Xie, Y.; Ho, S.; Chen, C.N. Phototrophic cultivation of a thermo-tolerant Desmodesmus sp. for lutein production: Effects of nitrate concentration, light intensity and fed-batch operation. Bioresour. Technol. 2013, 144, 435-440. [CrossRef] [PubMed]
43. Prior, R.L.; Wu, X.; Schaich, K. Standardized methods for the determination of antioxidant capacity and phenolics in foods and dietary supplements. J. Agric. Food Chem. 2005, 53, 4290-4302. [CrossRef] [PubMed]
44. Sindu, E.R.; Preethi, K.C.; Kuttan, R. Antioxidant activity of carotenoid lutein in vitro and in vivo. Indian J. Exp. Biol. 2010, 48, 843-848.
45. Wang, L.; Min, M.; Li, Y.; Chen, P.; Chen, Y. Cultivation of green algae Chlorella sp. in different wastewaters from municipal wastewater treatment plant. Appl. Biochem. Biotechnol. 2010, 162, 1174-1186. [CrossRef] [PubMed]
46. Fernandez, E.; Galvan, A. Inorganic nitrogen assimilation in Chlamydomonas. J. Exp. Bot. 2007, 58, 2279-2287. [CrossRef] [PubMed]
47. Chen, F.; Sun, Z.; Sun, P.; Chen, T.; Zhang, J. Microalgal carotenoids: beneficial effects and potential in human health. Food Funct. 2014, 5, 413-415.
48. Miki, W. Biological functions and activities of animal carotenoids. Pure Appl. Chem. 1991, 63, 141-146. [CrossRef]
49. Wagenen, J.V.; Mathias, L.P.; Angelidaki, I. Characterization of nutrient removal and microalgal biomass production on an industrial waste-stream by application of the deceleration-stat technique. Water Res. 2015, 75, 301-311. [CrossRef] [PubMed]
50. Van huelkem, L.; Thomas, C.S. Computer-assisted high-performance liquid chromatography method development with applications to the isolation and analysis of phytoplankton pigments. J. Chromatogr. 2001, 910, 31-49.
51. Firestone, D.; Society, A.O.C. Official Methods and Recommended Practices of the AOCS, 5th ed.; American Oil Chemists' Society: Urbana, IL, USA, 2009.
52. Pan, Y.; Zhu, J.;Wang, H.; Zhang, X.; Zhang, Y.; He, C.; Ji, X.; Li, H. Antioxidant activity of ethanolic extract of Cortex fraxini and use in peanut oil. Food Chem. 2007, 103, 913-918. [CrossRef]
53. Benzie, I.F.; Strain, J.J. Ferric reducing antioxidant power assay: Direct measure of total antioxidant activity of biological fluids and modified version for simultaneous measurement of total antioxidant power and ascorbic acid concentration. Methods Enzymol. 1999, 299, 15-27. [PubMed]