Microalgae for High-Value Products Towards Human Health and Nutrition
Abstract
:1. Introduction
2. Microalgae-Based Functional Foods
3. Biochemical Composition of Microalgae
3.1. Proteins
3.2. Carbohydrates
3.3. Lipids
3.4. High-Value Natural Products
4. Microalgal Mass Cultivation
5. Purification of Bioactive Compounds from Microalgae
5.1. Lipids
5.2. Polysaccharides
5.3. Peptides
6. Microalgal Compounds with Antioxidant Properties
6.1. Oxidative Stress and the Cell
6.2. Carotenoids
6.3. Phenolics
6.4. Peptides
7. Microalgal Compounds with Antihypertensive Properties
7.1. Hypertension and Heart Health
7.2. Peptides
8. Microalgal Compounds with Anti-Inflammatory Properties
8.1. Inflammation in the Body
8.2. Omega Fatty Acids
8.3. Carotenoids
8.4. Polysaccharides
9. Future Prospects
10. Conclusions
Funding
Acknowledgments
Conflicts of Interest
References
- McFadden, G.I. Primary and secondary endosymbiosis and the origin of plastids. J. Phycol. 2001, 37, 951–959. [Google Scholar] [CrossRef]
- Leliaert, F.; Smith, D.R.; Moreau, H.; Herron, M.D.; Verbruggen, H.; Delwiche, C.F.; De Clerck, O. Phylogeny and molecular evolution of the green algae. Crit. Rev. Plant Sci. 2012, 31, 1–46. [Google Scholar] [CrossRef]
- Hou, Y.; Lin, S. Distinct gene number-genome size relationships for eukaryotes and non-eukaryotes: Gene content estimation for dinoflagellate genomes. PLoS ONE 2009, 4, e6978. [Google Scholar] [CrossRef]
- Adl, S.M.; Simpson, A.G.; Lane, C.E.; Lukeš, J.; Bass, D.; Bowser, S.S.; Brown, M.W.; Burki, F.; Dunthorn, M.; Hampl, V.; et al. The revised classification of eukaryotes. J. Eukaryot. Microbiol. 2012, 59, 429–514. [Google Scholar] [CrossRef]
- Wright, S.W.; Jeffrey, S.W. Pigment markers for phytoplankton production. In Marine Organic Matter: Biomarkers, Isotopes and DNA; Springer: Berlin, Germany, 2006; pp. 71–104. [Google Scholar]
- Botana, L.M.; Alfonso, A. Phycotoxins: Chemistry and Biochemistry; John Wiley & Sons: Hoboken, NJ, USA, 2015. [Google Scholar]
- Manning, S.R.; Nobles, D.R. Impact of Global Warming on Water Toxicity: Cyanotoxins. Curr. Opin. Food Sci. 2017, 18, 14–20. [Google Scholar] [CrossRef]
- Demirbas, A.; Demirbas, M.F. Importance of algae oil as a source of biodiesel. Energy Conv. Manag. 2011, 52, 163–170. [Google Scholar] [CrossRef]
- Craggs, R.J.; Adey, W.H.; Jenson, K.R.; St John, M.S.; Green, F.B.; Oswald, W.J. Phosphorus removal from wastewater using an algal turf scrubber. Water Sci. Technol. 1996, 33, 191–198. [Google Scholar] [CrossRef]
- Enzing, C.; Ploeg, M.; Barbosa, M.; Sijtsma, L. Microalgae-based products for the food and feed sector: An outlook for Europe. JRC Sci. Policy Rep. 2014, 19–37. [Google Scholar] [CrossRef]
- Leu, S.; Boussiba, S. Advances in the Production of High-Value Products by Microalgae. Ind. Biotechnol. 2014, 10, 169–183. [Google Scholar] [CrossRef]
- Spolaore, P.; Joannis-Cassan, C.; Duran, E.; Isambert, A. Commercial applications of microalgae. J. Biosci. Bioeng. 2006, 101, 87–96. [Google Scholar] [CrossRef] [Green Version]
- Richardson, J.W.; Johnson, M.D.; Zhang, X.; Zemke, P.; Chen, W.; Hub, Q. A financial assessment of two alternative cultivation systems and their contributions to algae biofuel economic viability. Algal Res. 2014, 4, 96–104. [Google Scholar] [CrossRef] [Green Version]
- Borowitzka, M.A. High-value products from microalgae—Their development and commercialisation. J. Appl. Phycol. 2013, 25, 743–756. [Google Scholar] [CrossRef]
- Marketsand Markets. Carotenoids Market by Type (Astaxanthin, Beta-Carotene, Canthaxanthin, Lutein, Lycopene, & Zeaxanthin), Source (Synthetic and Natural), Application (Supplements, Food, Feed, and Cosmetics), by Region—Global Trends and Forecasts to 2021. Available online: http://www.marketsandmarkets.com/Market-Reports/carotenoid-market-158421566.html (accessed on 12 October 2017).
- Hu, G.P.; Yuan, J.; Sun, L.; She, Z.G.; Wu, J.H.; Lan, X.J.; Zhu, X.; Lin, Y.C.; Chen, S.P. Statistical research on marine natural products based on data obtained between 1985 and 2008. Mar. Drugs 2011, 9, 514–525. [Google Scholar] [CrossRef]
- de Jesus Raposo, M.F.; de Morais, R.M.S.C.; de Morais, A.M.M.B. Bioactivity and applications of sulphated polysaccharides from marine microalgae. Mar. Drugs 2013, 11, 233–252. [Google Scholar] [CrossRef]
- Pouvreau, J.B.; Morançais, M.; Taran, F.; Rosa, P.; Dufossé, L.; Guérard, F.; Pin, S.; Fleurence, J.; Pondaven, P. Antioxidant and free radical scavenging properties of marennine, a blue-green polyphenolic pigment from the diatom Haslea ostrearia (Gaillon/Bory) Simonsen responsible for the natural greening of cultured oysters. J. Agric. Food Chem. 2008, 56, 6278–6286. [Google Scholar] [CrossRef] [PubMed]
- Gammone, M.A.; Riccioni, G.; D’Orazio, N. Marine carotenoids against oxidative stress: Effects on human health. Mar. Drugs 2015, 13, 6226–6246. [Google Scholar] [CrossRef] [PubMed]
- Peng, J.; Yuan, J.P.; Wu, C.F.; Wang, J.H. Fucoxanthin, a marine carotenoid present in brown seaweeds and diatoms: Metabolism and bioactivities relevant to human health. Mar. Drugs 2011, 9, 1806–1828. [Google Scholar] [CrossRef] [PubMed]
- Haimeur, A.; Ulmann, L.; Mimouni, V.; Guéno, F.; Pineau-Vincent, F.; Meskini, N. Tremblin, G. The role of Odontella aurita, a marine diatom rich in EPA, as a dietary supplement in dyslipidemia, platelet function and oxidative stress in high-fat fed rats. Lipids Health Dis. 2012, 11, 147. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Lauritano, C.; Andersen, J.H.; Hansen, E.; Albrigtsen, M.; Escalera, L.; Esposito, F.; Helland, K.; Hanssen, K.Ø.; Romano, G.; Ianora, A. Bioactivity screening of microalgae for antioxidant, anti-Inflammatory, anticancer, anti-Diabetes, and antibacterial activities. Front. Mar. Sci. 2016, 3, 68. [Google Scholar] [CrossRef]
- Xia, S.; Gao, B.; Li, A.; Xiong, J.; Ao, Z.; Zhang, C. Preliminary characterization, antioxidant properties and production of chrysolaminarin from marine diatom Odontella aurita. Mar. Drugs 2014, 12, 4883–4897. [Google Scholar] [CrossRef]
- Lee, J.B.; Hayashi, K.; Hirata, M.; Kuroda, E.; Suzuki, E.; Kubo, Y.; Hayashi, T. Antiviral sulfated polysaccharide from Navicula directa, a diatom collected from deep-sea water in Toyama Bay. Biol. Pharm. Bull. 2006, 29, 2135–2139. [Google Scholar] [CrossRef]
- Beetul, K.; Gopeechund, A.; Kaullysing, D.; Mattan-Moorgawa, S.; Puchooa, D.; Bhagooli, R. Challenges and Opportunities in the Present Era of Marine Algal Applications. In Algae-Organisms for Imminent Biotechnology; Thajuddin, N., Dhanasekaran, D., Eds.; IntechOpen: London, UK, 2016; pp. 237–276. [Google Scholar]
- Hur, S.B.; Bae, J.H.; Youn, J.Y.; Jo, M.J. KMMCC-Korea Marine Microalgae Culture Center: List of strains. Algae 2015, 30, S1. [Google Scholar] [CrossRef]
- d’Avout d’Auerstaedt, R.; Passion Spiruline Ltd. Antenna Technologies France. Unpublished. Private Communication, 2014.
- Pulz, O.; Broneske, J.; Waldeck, P. IGV GmbH experience report, industrial production of microalgae under controlled conditions: Innovative prospects. In Handbook of Microalgal Culture: Applied Phycology and Biotechnology; Richmond, A., Hu, Q., Eds.; John Wiley & Sons: Oxford, UK, 2013; pp. 445–460. [Google Scholar]
- Abu Zaid, A.A.; Hammad, D.M.; Sharaf, E.M. Antioxidant and anticancer activity of Spirulina platensis water extracts. Int. J. Pharmacol. 2015, 11, 846–851. [Google Scholar] [CrossRef]
- Tang, G.; Suter, P.M. Vitamin A, nutrition, and health values of algae: Spirulina, Chlorella, and Dunaliella. J. Pharm. Nutr. Sci. 2011, 1, 111–118. [Google Scholar] [CrossRef]
- Hernández-Corona, A.; Nieves, I.; Meckes, M.; Chamorro, G.; Barron, B.L. Antiviral activity of Spirulina maxima against herpes simplex virus type 2. Antivir. Res. 2002, 56, 279–285. [Google Scholar] [CrossRef]
- Liu, J.; Hu, Q. Chlorella: Industrial production of cell mass and chemicals. In Handbook of Microalgal Culture: Applied Phycology and Biotechnology; Richmond, A., Hu, Q., Eds.; Wiley: Oxford, UK, 2013; pp. 327–338. [Google Scholar]
- Reyna-Martinez, R.; Gomez-Flores, R.; López-Chuken, U.; Quintanilla-Licea, R.; Caballero-Hernandez, D.; Rodríguez-Padilla, C.; Beltrán-Rocha, J.C.; Tamez-Guerra, P. Antitumor activity of Chlorella sorokiniana and Scenedesmus sp. microalgae native of Nuevo León State, México. PeerJ 2018, 6, e4358. [Google Scholar] [CrossRef]
- Ryu, N.H.; Lim, Y.; Park, J.E.; Kim, J.; Kim, J.Y.; Kwon, S.W.; Kwon, O. Impact of daily Chlorella consumption on serum lipid and carotenoid profiles in mildly hypercholesterolemic adults: A double-blinded, randomized, placebo-controlled study. Nutr. J. 2014, 13, 57. [Google Scholar] [CrossRef]
- Medina-Jaritz, N.B.; Carmona-Ugalde, L.F.; Lopez-Cedillo, J.C.; Ruiloba-De Leon, F.S.L. Antibacterial activity of methanolic extracts from Dunaliella salina and Chlorella vulgaris. FASEB J. 2013, 27, 1167-5. [Google Scholar]
- Tiberg, E.; Dreborg, S.; Björkstén, B. Allergy to green algae (Chlorella) among children. J. Allergy Clin. Immunol. 1995, 96, 257–259. [Google Scholar] [CrossRef]
- Yim, H.E.; Yoo, K.H.; Seo, W.H.; Won, N.H.; Hong, Y.S.; Lee, J.W. Acute tubulointerstitial nephritis following ingestion of Chlorella tablets. Pediat. Nephrol. 2007, 22, 887–888. [Google Scholar] [CrossRef]
- Griffith, H.W. Vitamins, Herbs, Minerals & Supplements: The Complete Guide; Fisher Books: Tucson, AZ, USA, 1998. [Google Scholar]
- Dagnelie, P.C.; van Staveren, W.A.; van den Berg, H. Vitamin B-12 from algae appears not to be bioavailable. Am. J. Clin. Nutr. 1991, 53, 695–697. [Google Scholar] [CrossRef]
- Gilroy, D.J.; Kauffman, K.W.; Hall, R.A.; Huang, X.; Chu, F.S. Assessing potential health risks from microcystin toxins in blue-green algae dietary supplements. Environ. Health Perspect. 2000, 108, 435–439. [Google Scholar] [CrossRef]
- Weiß, A. Food Supplements from Blue-Green Algae do More Harm than Good. BioLAGO 2013. Healthcare Industry BW, 2013. Available online: https://www.gesundheitsindustrie-bw.de/en/article/news/food-supplements-from-blue-green-algae-do-more-harm-than-good/ (accessed on 14 April 2018).
- Carvalho, A.P.; Malcata, F.X. Effect of culture media on production of polyunsaturated fatty acids by Pavlova lutheri. Cryptogamie Algol. 2000, 21, 59–71. [Google Scholar] [CrossRef]
- Brown, M.R.; Dunstan, G.A.; Jeffrey, S.W.; Volkman, J.K.; Barrett, S.M.; LeRoi, J.M. The influence of irradiance on the biochemical composition of the Prymnesiophyte Isochrysis sp. (clone T-ISO). J. Phycol. 1993, 29, 601–612. [Google Scholar] [CrossRef]
- Brown, M.R. The amino-acid and sugar composition of 16 species of microalgae used in mariculture. J. Exp. Mar. Biol. Ecol. 1991, 145, 79–99. [Google Scholar] [CrossRef]
- Tibbetts, S.M.; Milley, J.E.; Lall, S.P. Chemical composition and nutritional properties of freshwater and marine microalgal biomass cultured in photobioreactors. J. Appl. Phycol. 2015, 27, 1109–1119. [Google Scholar] [CrossRef]
- Becker, E.W. Micro-algae as a source of protein. Biotechnol. Adv. 2007, 25, 207–210. [Google Scholar] [CrossRef]
- Barbarino, E.; Lourenço, S.O. An evaluation of methods for extraction and quantification of protein from marine macro-and microalgae. J. Appl. Phycol. 2005, 17, 447–460. [Google Scholar] [CrossRef]
- Slocombe, S.P.; Ross, M.; Thomas, N.; McNeill, S.; Stanley, M.S. A rapid and general method for measurement of protein in micro-algal biomass. Bioresource Technol. 2013, 129, 51–57. [Google Scholar] [CrossRef] [Green Version]
- Kent, M.; Welladsen, H.M.; Mangott, A.; Li, Y. Nutritional evaluation of Australian microalgae as potential human health supplements. PLoS ONE 2015, 10, e0118985. [Google Scholar] [CrossRef]
- González López, C.V.; García, M.D.C.C.; Fernández, F.G.A.; Bustos, C.S.; Chisti, Y.; Sevilla, J.M.F. Protein measurements of microalgal and cyanobacterial biomass. Bioresource Technol. 2010, 101, 7587–7591. [Google Scholar] [CrossRef]
- Velasco, L.A.; Carrera, S.; Barros, J. Isolation, culture and evaluation of Chaetoceros muelleri from the Caribbean as food for the native scallops, Argopecten nucleus and Nodipecten nodosus. Lat. Am. J. Aquat. Res. 2016, 44, 557–568. [Google Scholar]
- Schwenzfeier, A.; Wierenga, P.A.; Gruppen, H. Isolation and characterization of soluble protein from the green microalgae Tetraselmis sp. Bioresource Technol. 2011, 102, 9121–9127. [Google Scholar] [CrossRef]
- Ricketts, T.R. On the chemical composition of some unicellular algae. Phytochemistry 1966, 5, 67. [Google Scholar] [CrossRef]
- da Silva Gorgônio, C.M.; Aranda, D.A.G.; Couri, S. Morphological and chemical aspects of Chlorella pyrenoidosa, Dunaliella tertiolecta, Isochrysis galbana and Tetraselmis gracilis microalgae. Nat. Sci. 2013, 5, 783. [Google Scholar]
- Chisti, Y. Biodiesel from microalgae. Biotechnol. Adv. 2007, 25, 294–306. [Google Scholar] [CrossRef]
- Williams, P.J.L.B.; Laurens, L.M. Microalgae as biodiesel & biomass feedstocks: Review & analysis of the biochemistry, energetics & economics. Energy Environ. Sci. 2010, 3, 554–590. [Google Scholar]
- Batista, A.P.; Gouveia, L.; Bandarra, N.M.; Franco, J.M.; Raymundo, A. Comparison of microalgal biomass profiles as novel functional ingredient for food products. Algal Res. 2013, 2, 164–173. [Google Scholar] [CrossRef] [Green Version]
- Graziani, G.; Schiavo, S.; Nicolai, M.A.; Buono, S.; Fogliano, V.; Pinto, G.; Pollio, A. Microalgae as human food: Chemical and nutritional characteristics of the thermo-acidophilic microalga Galdieria sulphuraria. Food Func. 2013, 4, 144–152. [Google Scholar] [CrossRef]
- Milovanovic, I.; Misan, A.; Saric, B.; Kos, J.; Mandic, A.; Simeunovic, J.; Kovac, D. Evaluation of protein and lipid content and determination of fatty acid profile in selected species of cyanobacteria. In Proceedings of the 6th Central European Congress on Food, CEFood2012, Novi Sad, Serbia, 23–26 May 2012. [Google Scholar]
- Plaza, M.; Herrero, M.; Cifuentes, A.; Ibanez, E. Innovative natural functional ingredients from microalgae. J. Agric. Food Chem. 2009, 57, 7159–7170. [Google Scholar] [CrossRef]
- Doucha, J.; Lívanský, K. Influence of processing parameters on disintegration of Chlorella cells in various types of homogenizers. Appl. Microbiol. Biotechnol. 2008, 81, 431. [Google Scholar] [CrossRef]
- Arad, S.M.; Levy-Ontman, O. Red microalgal cell-wall polysaccharides: Biotechnological aspects. Curr. Opin. Biotechnol. 2010, 21, 358–364. [Google Scholar] [CrossRef]
- Nakamura, Y.; Takahashi, J.I.; Sakurai, A.; Inaba, Y.; Suzuki, E.; Nihei, S.; Fujiwara, S.; Tsuzuki, M.; Miyashita, H.; Ikemoto, H.; et al. Some cyanobacteria synthesize semi-amylopectin type α-polyglucans instead of glycogen. Plant Cell Physiol. 2005, 46, 539–545. [Google Scholar] [CrossRef]
- Busi, M.V.; Barchiesi, J.; Martín, M.; Gomez-Casati, D.F. Starch metabolism in green algae. Starch-Stärke 2014, 66, 28–40. [Google Scholar] [CrossRef]
- McCracken, D.A.; Cain, J.R. Amylose in floridean starch. New Phytol. 1981, 88, 67–71. [Google Scholar] [CrossRef]
- Gügi, B.; Le Costaouec, T.; Burel, C.; Lerouge, P.; Helbert, W.; Bardor, M. Diatom-specific oligosaccharide and polysaccharide structures help to unravel biosynthetic capabilities in diatoms. Mar. Drugs 2015, 13, 5993–6018. [Google Scholar] [CrossRef]
- Dismukes, G.C.; Carrieri, D.; Bennette, N.; Ananyev, G.M.; Posewitz, M.C. Aquatic phototrophs: Efficient alternatives to land-based crops for biofuels. Curr. Opin Biotechnol. 2008, 19, 235–240. [Google Scholar] [CrossRef]
- Myklestad, S. Production of carbohydrates by marine planktonic diatoms. I. Comparison of nine different species in culture. J. Exp. Mar. Biol. Ecol. 1974, 15, 261–274. [Google Scholar] [CrossRef]
- Qu, L.; Ren, L.J.; Huang, H. Scale-up of docosahexaenoic acid production in fed-batch fermentation by Schizochytrium sp. based on volumetric oxygen-transfer coefficient. Biochem. Eng. J. 2013, 77, 82–87. [Google Scholar] [CrossRef]
- Rodolfi, L.; Chini Zittelli, G.; Bassi, N.; Padovani, G.; Biondi, N.; Bonini, G.; Tredici, M.R. Microalgae for oil: Strain selection, induction of lipid synthesis and outdoor mass cultivation in a low-cost photobioreactor. Biotechnol. Bioeng. 2009, 102, 100–112. [Google Scholar] [CrossRef]
- Dunstan, G.A.; Volkman, J.K.; Barrett, S.M.; Garland, C.D. Changes in the lipid composition and maximisation of the polyunsaturated fatty acid content of three microalgae grown in mass culture. J. Appl. Phycol. 1993, 5, 71–83. [Google Scholar] [CrossRef]
- Guschina, I.A.; Harwood, J.L. Lipids and lipid metabolism in eukaryotic algae. Prog. Lipid Res. 2006, 45, 160–186. [Google Scholar] [CrossRef]
- Richmond, A. Biological principles of mass cultivation. In Handbook of Microalgal Culture: Biotechnology and Applied Phycology; Blackwell Publishing Ltd.: Oxford, UK, 2004; pp. 83–90. [Google Scholar]
- Muller-Feuga, A.; Moal, J.; Kaas, R. The microalgae of aquaculture. In Live feeds in Marine Aquaculture; Støttrup, J.G., McEvoy, L.A., Eds.; Blackwell Science: Oxford, UK, 2003; pp. 206–252. [Google Scholar]
- Michalak, I.; Chojnacka, K.; Saeid, A. Plant Growth Biostimulants, Dietary Feed Supplements and Cosmetics Formulated with Supercritical CO2 Algal Extracts. Molecules 2017, 22, 66. [Google Scholar] [CrossRef]
- Panis, G.; Carreon, J.R. Commercial astaxanthin production derived by green alga Haematococcus pluvialis: A microalgae process model and a techno-economic assessment all through production line. Algal Res. 2016, 18, 175–190. [Google Scholar] [CrossRef]
- Oilgae. Chlorella from Algae and Its Uses. Available online: http://www.oilgae.com/non_fuel_products/chlorella.html (accessed on 27 January 2018).
- Oilgae. Comprehensive Report on Attractive Algae Product Opportunities. Available online: https://secure.clixoo.com/purchase/oilgae/alg_pdt/report.html (accessed on 27 January 2018).
- Minhas, A.K.; Hodgson, P.; Barrow, C.J.; Adholeya, A. A review on the assessment of stress conditions for simultaneous production of microalgal lipids and carotenoids. Front. Microbiol. 2016, 7, 546. [Google Scholar] [CrossRef]
- Coesel, S.N.; Baumgartner, A.C.; Teles, L.M.; Ramos, A.A.; Henriques, N.M.; Cancela, L.; Varela, J.C.S. 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. 2008, 10, 602–611. [Google Scholar] [CrossRef]
- Shah, M.M.R.; Liang, Y.; Cheng, J.J.; Daroch, M. Astaxanthin-producing green microalga Haematococcus pluvialis: From single cell to high value commercial products. Front. Plant Sci. 2016, 7, 531. [Google Scholar] [CrossRef]
- Ryckebosch, E.; Bruneel, C.; Termote-Verhalle, R.; Goiris, K.; Muylaert, K.; Foubert, I. Nutritional evaluation of microalgae oils rich in omega-3 long chain polyunsaturated fatty acids as an alternative for fish oil. Food Chem. 2014, 160, 393–400. [Google Scholar] [CrossRef] [Green Version]
- Gerber, L.R.; Karimi, R.; Fitzgerald, T.P. Sustaining seafood for public health. Front. Ecol. Environ. 2012, 10, 487–493. [Google Scholar] [CrossRef]
- Adarme-Vega, T.C.; Thomas-Hall, S.R.; Lim, D.K.; Schenk, P.M. Effects of long chain fatty acid synthesis and associated gene expression in microalga Tetraselmis sp. Mar. Drugs 2014, 12, 3381–3398. [Google Scholar] [CrossRef]
- Nauroth, J.M.; Liu, Y.C.; Van Elswyk, M.; Bell, R.; Hall, E.B.; Chung, G.; Arterburn, L.M. Docosahexaenoic Acid (DHA) and Docosapentaenoic Acid (DPAn-6) Algal Oils Reduce Inflammatory Mediators in Human Peripheral Mononuclear Cells In vitro and Paw Edema In vivo. Lipids 2010, 45, 375–384. [Google Scholar] [CrossRef]
- Wynn, J.P.; Ratledge, C. Oils from Microorganisms. In Bailey’s Industrial Oil and Fat Products; Shahidi, F., Ed.; John Wiley & Sons: Hoboken, NJ, USA, 2005. [Google Scholar]
- Martek Biosciences Corporation Annual Report. 2007. Available online: http://library.corporate-ir.net/library/11/116/116214/items/281192/MATK_2007_Annual.pdf (accessed on 25 February 2018).
- Fujitani, N.; Sakaki, S.; Yamaguchi, Y.; Takenaka, H. Inhibitory effects of microalgae on the activation of hyaluronidase. J. Appl. Phycol. 2001, 13, 489–492. [Google Scholar] [CrossRef]
- Borowitzka, M.A. Microalgae as sources of pharmaceuticals and other biologically active compounds. J. Appl. Phycol. 1995, 7, 3–15. [Google Scholar] [CrossRef]
- Ciccone, M.M.; Cortese, F.; Gesualdo, M.; Carbonara, S.; Zito, A.; Ricci, G.; De Pascalis, F.; Scicchitano, P.; Riccioni, G. Dietary intake of carotenoids and their antioxidant and anti-inflammatory effects in cardiovascular care. Mediat. Inflamm. 2013, 2013, 782137. [Google Scholar] [CrossRef]
- Del Campo, J.A.; Rodrıguez, H.; Moreno, J.; Vargas, M.A.; Rivas, J.; Guerrero, M.G. Lutein production by Muriellopsis sp. in an outdoor tubular photobioreactor. J. Biotechnol. 2001, 85, 289–295. [Google Scholar] [CrossRef]
- Sánchez, J.F.; Fernández-Sevilla, J.M.; Acién, F.G.; Cerón, M.C.; Pérez-Parra, J.; Molina-Grima, E. Biomass and lutein productivity of Scenedesmus almeriensis: Influence of irradiance, dilution rate and temperature. Appl. Microbiol. Biotechnol. 2008, 79, 719–729. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Su, G.; Jiao, K.; Chang, J.; Li, Z.; Guo, X.; Sun, Y.; Zeng, X.; Lu, Y.; Lin, L. Enhancing total fatty acids and arachidonic acid production by the red microalgae Porphyridium purpureum. Bioresources Bioprocess. 2016, 3, 33. [Google Scholar] [CrossRef]
- Solovchenko, A.E.; Khozin-Goldberg, I.; Didi-Cohen, S.; Cohen, Z.; Merzlyak, M.N. Effects of light intensity and nitrogen starvation on growth, total fatty acids and arachidonic acid in the green microalga Parietochloris incisa. J. Appl. Phycol. 2008, 20, 245–251. [Google Scholar] [CrossRef]
- Giménez, A.G.; González, M.I.; Medina, A.R.; Grima, E.M.; Salas, S.G.; Cerdán, L.E. Downstream processing and purification of eicosapentaenoic (20: 5n-3) and arachidonic acids (20: 4n-6) from the microalga Porphyridium cruentum. Bioseparation 1998, 7, 89–99. [Google Scholar] [CrossRef]
- Asgharpour, M.; Rodgers, B.; Hestekin, J.A. Eicosapentaenoic acid from Porphyridium Cruentum: Increasing growth and productivity of microalgae for pharmaceutical products. Energies 2015, 8, 10487–10503. [Google Scholar] [CrossRef]
- Molina Grima, E.; Garcia Camacho, F.; Ácien Fernandez, F.G. Production of EPA from Phaeodactylum tricornutum. In Chemicals from Microalgae; Cohen, Z., Ed.; Taylor & Francis: London, UK, 1999; pp. 57–92. [Google Scholar]
- Sukenik, A. Production of eicosapentaenoic acid by the marine eustigmatophyte Nannochloropsis. In Chemicals from Microalgae; Cohen, Z., Ed.; Taylor & Francis: London, UK, 1999; pp. 41–56. [Google Scholar]
- Chu, W.L. Biotechnological applications of microalgae. IeJSME 2012, 6, S24–S37. [Google Scholar]
- Horrocks, L.A.; Yeo, Y.K. Health benefits of docosahexaenoic acid (DHA). Pharmacol. Res. 1999, 40, 211–225. [Google Scholar] [CrossRef]
- Wang, X.; Zhang, X. Separation, antitumor activities, and encapsulation of polypeptide from Chlorella pyrenoidosa. Biotechnol. Prog. 2013, 29, 681–687. [Google Scholar] [CrossRef]
- Samarakoon, K.W.; Kwon, O.N.; Ko, J.Y.; Lee, J.H.; Kang, M.C.; Kim, D.; Lee, J.B.; Lee, J.S.; Jeon, Y.J. Purification and identification of novel angiotensin-I converting enzyme (ACE) inhibitory peptides from cultured marine microalgae (Nannochloropsis oculata) protein hydrolysate. J. Appl. Phycol. 2013, 25, 1595–1606. [Google Scholar] [CrossRef]
- Cha, T.S.; Chen, C.F.; Yee, W.; Aziz, A.; Loh, S.H. Cinnamic acid, coumarin and vanillin: Alternative phenolic compounds for efficient Agrobacterium-mediated transformation of the unicellular green alga, Nannochloropsis sp. J. Microbiol. Meth. 2011, 84, 430–434. [Google Scholar] [CrossRef]
- El-Baky, H.H.A.; El Baz, F.K.; El-Baroty, G.S. Production of phenolic compounds from Spirulina maxima microalgae and its protective effects in vitro toward hepatotoxicity model. Afr. J. Pharm. Pharmacol. 2009, 3, 133–139. [Google Scholar]
- Romay, C.H.; Gonzalez, R.; Ledon, N.; Remirez, D.; Rimbau, V. C-phycocyanin: A biliprotein with antioxidant, anti-inflammatory and neuroprotective effects. Curr. Protein Pept. Sci. 2003, 4, 207–216. [Google Scholar] [CrossRef]
- Guzman, S.; Gato, A.; Lamela, M.; Freire-Garabal, M.; Calleja, J.M. Anti-inflammatory and immunomodulatory activities of polysaccharide from Chlorella stigmatophora and Phaeodactylum tricornutum. Phytother. Res. 2003, 17, 665–670. [Google Scholar] [CrossRef]
- Huheihel, M.; Ishanu, V.; Tal, J.; Arad, S.M. Activity of Porphyridium sp. polysaccharide against herpes simplex viruses in vitro and in vivo. J. Biochem. Biophys. Methods 2002, 50, 189–200. [Google Scholar] [CrossRef]
- Tannin-Spitz, T.; Bergman, M.; van-Moppes, D.; Grossman, S.; Arad, S.M. Antioxidant activity of the polysaccharide of the red microalga Porphyridium sp. J. Appl. Phycol. 2005, 17, 215–222. [Google Scholar] [CrossRef]
- Trabelsi, L.; Chaieb, O.; Mnari, A.; Abid-Essafi, S.; Aleya, L. Partial characterization and antioxidant and antiproliferative activities of the aqueous extracellular polysaccharides from the thermophilic microalgae Graesiella sp. BMC Complement. Altern. Med. 2016, 16, 210. [Google Scholar] [CrossRef]
- Zhu, L. Biorefinery as a promising approach to promote microalgae industry: An innovative framework. Renew. Sustain. Energy Rev. 2015, 41, 1376–1384. [Google Scholar] [CrossRef]
- Greenwell, H.C.; Laurens, L.M.L.; Shields, R.J.; Lovitt, R.W.; Flynn, K.J. Placing microalgae on the biofuels priority list: A review of the technological challenges. J. R. Soc. Interface 2009, 7, 703–726. [Google Scholar] [CrossRef]
- Potumarthi, R.; Baadhe, R.R. Issues in algal biofuels for fuelling the future. In Applications of Microbial Engineering; Gupta, V.K., Schmoll, M., Maki, M., Tuohy, M., Mazutti, M.A., Eds.; CRC Press: Boca Raton, FL, USA, 2013; pp. 408–425. [Google Scholar]
- Ruiz, J.; Olivieri, G.; de Vree, J.; Bosma, R.; Willems, P.; Reith, J.H.; Eppink, M.H.; Kleinegris, D.M.; Wijffels, R.H.; Barbosa, M.J. Towards industrial products from microalgae. Energy Environ. Sci. 2016, 9, 3036–3043. [Google Scholar] [CrossRef] [Green Version]
- Padmanabhan, P. Technical insight on the requirements for CO2-saturated growth of microalgae in photobioreactors. 3 Biotech 2017, 7, 119. [Google Scholar]
- Torzillo, G.; Accolla, P.; Pinzani, E.; Masojidek, J. In situ monitoring of chlorophyll fluorescence to assess the synergistic effect of low temperature and high irradiance stresses in Spirulina cultures grown outdoors in photobioreactors. J. Appl. Phycol. 1996, 8, 283–291. [Google Scholar] [CrossRef]
- Richmond, A.; Boussiba, S.; Vonshak, A.; Kopel, R. A new tubular reactor for mass production of microalgae outdoors. J. Appl. Phycol. 1993, 5, 327–332. [Google Scholar] [CrossRef]
- Ying, K.; Gilmour, D.J.; Zimmerman, W.B. Effects of CO2 and pH on growth of the microalga Dunaliella salina. J. Microb. Biochem. Technol. 2014, 6, 167–173. [Google Scholar] [CrossRef]
- Mallick, N.; Bagchi, S.K.; Koley, S.; Singh, A.K. Progress and challenges in microalgal biodiesel production. Front. Microbiol. 2016, 7, 1019. [Google Scholar] [CrossRef]
- Maranon, E. Phytoplankton growth rates in the Atlantic subtropical gyres. Limnol. Oceanogr. 2005, 50, 299–310. [Google Scholar] [CrossRef] [Green Version]
- Chisti, Y. Raceways-based production of algal crude oil. In Microalgal Biotechnology: Potential and Production; Posten, C., Walter, C., Eds.; de Gruyter: Berlin, Germany, 2012; pp. 113–146. [Google Scholar]
- Jovine, R. Method of Culturing Algae. U.S. Patent 20130269244A1, 17 October 2013. [Google Scholar]
- Geider, R.J.; Osborne, B.A. Respiration and microalgal growth: A review of the quantitative relationship between dark respiration and growth. New Phytol. 1989, 112, 327–341. [Google Scholar] [CrossRef]
- Grobbelaar, J.U.; Soeder, C.J. Respiration losses in planktonic green algae cultivated in raceway ponds. J. Plankton Res. 1985, 7, 497–506. [Google Scholar] [CrossRef]
- Huesemann, M.; Crowe, B.; Waller, P.; Chavis, A.; Hobbs, S.; Edmundson, S.; Wigmosta, M. A validated model to predict microalgae growth in outdoor pond cultures subjected to fluctuating light intensities and water temperatures. Algal Res. 2016, 13, 195–206. [Google Scholar] [CrossRef] [Green Version]
- Günerken, E.; d’Hondt, E.; Eppink, M.H.M.; Garcia-Gonzalez, L.; Elst, K.; Wijffels, R.H. Cell disruption for microalgae biorefineries. Biotechnol. Adv. 2015, 33, 243–260. [Google Scholar] [CrossRef]
- Amaro, H.M.; Fernandes, F.; Valentão, P.; Andrade, P.B.; Sousa-Pinto, I.; Malcata, F.X.; Guedes, A. Effect of solvent system on extractability of lipidic components of Scenedesmus obliquus (M2-1) and Gloeothece sp. on antioxidant scavenging capacity thereof. Mar. Drugs 2015, 13, 6453–6471. [Google Scholar] [CrossRef] [PubMed]
- Foo, S.C.; Yusoff, F.M.; Ismail, M.; Basri, M.; Chan, K.W.; Khong, N.M.; Yau, S.K. Production of fucoxanthin-rich fraction (FxRF) from a diatom, Chaetoceros calcitrans (Paulsen) Takano 1968. Algal Res. 2015, 12, 26–32. [Google Scholar] [CrossRef]
- Ventura, S.P.M.; Nobre, B.P.; Ertekin, F.; Hayes, M.; Garcia’-Vaquero, M.; Vieira, F.; Koc, M.; Gouveia, L.; Aires-Barros, M.R.; Palavra, A.M.F. Extraction of value-added compounds from microalgae. In Microalgae-Based Biofuels and Bioproducts: From Feedstock Cultivation to End-Products; Gonalez-Fernandez, C., Munoz, R., Eds.; Woodhead Publishing: Sawston, UK, 2017; pp. 461–483. [Google Scholar]
- Lee, J.Y.; Yoo, C.; Jun, S.Y.; Ahn, C.Y.; Oh, H.M. Comparison of several methods for effective lipid extraction from microalgae. Bioresource Technol. 2010, 101, S75–S77. [Google Scholar] [CrossRef]
- dos Santos, R.R.; Moreira, D.M.; Kunigami, C.N.; Aranda, D.A.G.; Teixeira, C.M.L.L. Comparison between several methods of total lipid extraction from Chlorella vulgaris biomass. Ultrason. Sonochem. 2015, 22, 95–99. [Google Scholar] [CrossRef]
- Ryckebosch, E.; Muylaert, K.; Foubert, I. Optimization of an analytical procedure for extraction of lipids from microalgae. J. Am. Oil Chem. Soc. 2012, 89, 189–198. [Google Scholar] [CrossRef]
- Wynn, J.; Behrens, P.; Sundararajan, A.; Hansen, J.; Apt, K. Production of single cell oils by dinoflagellates. In Single Cell Oils, 2nd ed.; Cohen, Z., Ratledge, C., Eds.; AOCS Press: Urbana, IL, USA, 2010; pp. 115–129. [Google Scholar]
- Ward, O.P.; Singh, A. Omega-3/6 fatty acids: Alternative sources of production. Process Biochem. 2005, 40, 3627–3652. [Google Scholar] [CrossRef]
- Wieczorek, P.P.; Lipok, J.; Górka, B. Biologically active compounds isolated from algae and their application as a plant growth regulators. In Proceedings of the IX International Scientific Conference daRostim, Lviv, Ukraine, 7–10 October 2013. [Google Scholar]
- Zhang, Z.S.; Wang, F.; Wang, X.M.; Liu, X.L.; Hou, Y.; Zhang, Q.B. Extraction of the polysaccharides from five algae and their potential antioxidant activity in vitro. Carbohydr. Polym. 2010, 82, 118–121. [Google Scholar] [CrossRef]
- Xu, S.Y.; Huang, X.; Cheong, K.L. Recent advances in marine algae polysaccharides: Isolation, structure, and activities. Mar. Drugs 2017, 15, 388. [Google Scholar] [CrossRef]
- Yuan, Y.; Macquarrie, D. Microwave assisted extraction of sulfated polysaccharides (fucoidan) from Ascophyllum nodosum and its antioxidant activity. Carbohydr. Polym. 2015, 129, 101–107. [Google Scholar] [CrossRef]
- Tsubaki, S.; Oono, K.; Hiraoka, M.; Onda, A.; Mitani, T. Microwave-assisted hydrothermal extraction of sulfated polysaccharides from Ulva spp. and Monostroma latissimum. Food Chem. 2016, 2103, 11–316. [Google Scholar] [CrossRef]
- Rahimi, F.; Tabarsa, M.; Rezaei, M. Ulvan from green algae Ulva intestinalis: Optimization of ultrasound-assisted extraction and antioxidant activity. J. Appl. Phycol. 2016, 28, 2979–2990. [Google Scholar] [CrossRef]
- Tang, W.; Lin, L.H.; Xie, J.H.; Wang, Z.; Wang, H.J.; Dong, Y.J.; Shen, M.Y.; Xie, M.Y. Effect of ultrasonic treatment on the physicochemical properties and antioxidant activities of polysaccharide from Cyclocarya paliurus. Carbohydr. Polym. 2016, 151, 305–312. [Google Scholar] [CrossRef]
- Lim, S.J.; Aida, W.M.W.; Maskat, M.T.; Mamot, S.; Ropien, J.; Mohd, D.M. Isolation and antioxidant capacity of fucoidan from selected Malaysian seaweeds. Food Hydrocoll. 2014, 42, 280–288. [Google Scholar] [CrossRef]
- Nasri, M. Protein hydrolysates and biopeptides: Production, biological activities, and applications in foods and health benefits: A review. Adv. Food Nutr. Res. 2017, 81, 109–159. [Google Scholar]
- Thorkelsson, G.; Sigurgisladottir, S.; Geirsdottir, M.; Jóhannsson, R.; Guerard, F.; Chabeaud, A.; Bourseau, P.; Vandanjon, L.; Jaouen, P.; Chaplain-Derouiniot, M.; et al. Mild processing techniques and development of functional marine protein and peptide ingredients. In Improving Seafood Products for the Consumer; Borresen, T., Ed.; Woodhead: Cambridge, UK, 2008; p. 612. [Google Scholar]
- Clemente, A. Enzymatic protein hydrolysates in human nutrition. Trends Food Sci. Technol. 2000, 11, 254–262. [Google Scholar] [CrossRef]
- Gao, M.T.; Hirata, M.; Toorisaka, E.; Hano, T. Acid-hydrolysis of fish wastes for lactic acid fermentation. Bioresource Technol. 2006, 97, 2414–2420. [Google Scholar] [CrossRef]
- Kim, S.K.; Wijesekara, I. Development and Biological Activities of Marine-Derived Bioactive Peptides: A Review. J. Funct. Food 2010, 2, 1–9. [Google Scholar] [CrossRef]
- Nasri, R.; Chataigné, G.; Bougatef, A.; Chaâbouni, M.K.; Dhulster, P.; Nasri, M.; Nedjar-Arroume, N. Novel angiotensin I-converting enzyme inhibitory peptides from enzymatic hydrolysates of goby (Zosterisessor ophiocephalus) muscle proteins. J. Proteomics 2013, 91, 444–452. [Google Scholar] [CrossRef]
- Wijesekara, I.; Qian, Z.J.; Ryu, B.; Ngo, D.H.; Kim, S.K. Purification and identification of antihypertensive peptides from seaweed pipefish (Syngnathus schlegeli) muscle protein hydrolysate. Food Res. Int. 2011, 44, 703–707. [Google Scholar] [CrossRef]
- Maehre, H.K.; Edvinsen, G.K.; Eilertsen, K.E.; Elvevoll, E.O. Heat treatment increases the protein bioaccessibility in the red seaweed dulse (Palmaria palmata), but not in the brown seaweed winged kelp (Alaria esculenta). J. Appl. Phycol. 2016, 28, 581–590. [Google Scholar] [CrossRef]
- Waghmare, A.G.; Salve, M.K.; LeBlanc, J.G.; Arya, S.S. Concentration and characterization of microalgae proteins from Chlorella pyrenoidosa. Bioresources Bioprocess. 2016, 3, 16. [Google Scholar] [CrossRef]
- Ferreira, I.M.P.L.V.; Eça, R.; Pinho, O.; Tavares, P.; Pereira, A.; Cecília Roque, A. Development and validation of an HPLC/UV method for quantification of bioactive peptides in fermented milks. J. Liq. Chromatogr. Relat. Technol. 2007, 30, 2139–2147. [Google Scholar] [CrossRef]
- Majors, R.E. Developments in preparative-scale chromatography. LC•GC Eur. 2004, 17, 630–638. [Google Scholar]
- Bargeman, G.; Koops, G.H.; Houwing, J.; Breebaart, I.; Van der Horst, H.C.; Wessling, M. The development of electro-membrane filtration for the isolation of bioactive peptides: The effect of membrane selection and operating parameters on the transport rate. Desalination 2002, 149, 369–374. [Google Scholar] [CrossRef]
- Sun, L.; Wu, S.; Zhou, L.; Wang, F.; Lan, X.; Sun, J.; Tong, Z.; Liao, D. Separation and Characterization of Angiotensin I Converting Enzyme (ACE) Inhibitory Peptides from Saurida elongata Proteins Hydrolysate by IMAC-Ni2+. Mar. Drugs 2017, 15, 29. [Google Scholar] [CrossRef]
- Andersson, L.; Blomberg, L.; Flegel, M.; Lepsa, L.; Nilsson, B.; Verlander, M. Large-scale synthesis of peptides. Pept. Sci. 2000, 55, 227–250. [Google Scholar] [CrossRef]
- Agyei, D.; Ongkudon, C.M.; Wei, C.Y.; Chan, A.S.; Danquah, M.K. Bioprocess challenges to the isolation and purification of bioactive peptides. Food Bioprod. Process. 2016, 98, 244–256. [Google Scholar] [CrossRef]
- Rietjens, I.M.; Boersma, M.G.; de Haan, L.; Spenkelink, B.; Awad, H.M.; Cnubben, N.H.; van Zanden, J.J.; van der Woude, H.; Alink, G.M.; Koeman, J.H. The pro-oxidant chemistry of the natural antioxidants vitamin C, vitamin E, carotenoids and flavonoids. Environ. Toxicol. Pharmacol. 2002, 11, 321–333. [Google Scholar] [CrossRef]
- Xia, S.; Wang, K.; Wan, L.; Li, A.; Hu, Q.; Zhang, C. Production, characterization, and antioxidant activity of fucoxanthin from the marine diatom Odontella aurita. Mar. Drugs 2013, 11, 2667–2681. [Google Scholar] [CrossRef]
- Goiris, K.; Van Colen, W.; Wilches, I.; León-Tamariz, F.; De Cooman, L.; Muylaert, K. Impact of nutrient stress on antioxidant production in three species of microalgae. Algal Res 2015, 7, 51–57. [Google Scholar] [CrossRef]
- Halliwell, B. Oxidative stress and neurodegeneration: Where are we now? J. Neurochem. 2006, 97, 1634–1658. [Google Scholar] [CrossRef]
- Gülçin, I. Antioxidant activity of food constituents: An overview. Arch. Toxicol. 2012, 86, 345–391. [Google Scholar] [CrossRef]
- Pietta, P.G. Flavonoids as antioxidants. J. Nat. Prod 2000, 63, 1035–1042. [Google Scholar] [CrossRef]
- Gülçin, İ.; Elias, R.; Gepdiremen, A.; Boyer, L. Antioxidant activity of lignans from fringe tree (Chionanthus virginicus L.). Eur. Food Res. Technol. 2006, 223, 759. [Google Scholar] [CrossRef]
- Halliwell, B.; Gutteridge, J.M. Free Radicals in Biology and Medicine; Oxford University Press: Oxford, MA, USA, 2015. [Google Scholar]
- Marks, D.B.; Marks, A.D.; Smith, C.M. Oxygen metabolism and toxicity. In Basic Medical Biochemistry: A Clinical Approach; Williams and Wilkins: Baltimore, MD, USA, 1996; pp. 327–340. [Google Scholar]
- Reed, D.J. Toxicity of oxygen. In Molecular and Cellular Mechanisms of Toxicity; De Matteis, F., Smith, L.L., Eds.; CRC Press: Boca Raton, FL, USA, 1995; pp. 35–68. [Google Scholar]
- Pashkow, F.J. Oxidative stress and inflammation in heart disease: Do antioxidants have a role in treatment and/or prevention? Int. J. Inflamm. 2011. [Google Scholar] [CrossRef]
- Larkum, A.W.; Kühl, M. Chlorophyll d: The puzzle resolved. Trends Plant Sci. 2005, 10, 355–357. [Google Scholar] [CrossRef]
- Ioannou, E.; Roussis, V. Natural products from seaweeds. In Plant-Derived Natural Products; Springer: New York, NY, USA, 2009; pp. 51–81. [Google Scholar]
- Stahl, W.; Sies, H. Antioxidant activity of carotenoids. Mol. Aspects Med. 2003, 24, 345–351. [Google Scholar] [CrossRef]
- de Jesus Raposo, M.F.; de Morais, A.M.M.B.; de Morais, R.M.S.C. Carotenoids from marine microalgae: A valuable natural source for the prevention of chronic diseases. Mar. Drugs 2015, 13, 5128–5155. [Google Scholar] [CrossRef]
- Blas-Valdivia, V.; Ortiz-Butron, R.; Rodriguez-Sanchez, R.; Torres-Manzo, P.; Hernandez-Garcia, A.; Cano-Europa, E. Microalgae of the Chlorophyceae Class: Potential Nutraceuticals Reducing Oxidative Stress Intensity and Cellular Damage. Mar. Drugs 2014, 12, 4883–4897. [Google Scholar]
- Sachindra, N.M.; Sato, E.; Maeda, H.; Hosokawa, M.; Niwano, Y.; Kohno, M.; Miyashita, K. Radical scavenging and singlet oxygen quenching activity of marine carotenoid fucoxanthin and its metabolites. J. Agric. Food Chem. 2007, 55, 8516–8522. [Google Scholar] [CrossRef]
- Klejdus, B.; Lojková, L.; Plaza, M.; Šnóblová, M.; Štěrbová, D. Hyphenated technique for the extraction and determination of isoflavones in algae: Ultrasound-assisted supercritical fluid extraction followed by fast chromatography with tandem mass spectrometry. J. Chromatogr. A 2010, 1217, 7956–7965. [Google Scholar] [CrossRef]
- Pan, M.H.; Lai, C.S.; Ho, C.T. Anti-inflammatory activity of natural dietary flavonoids. Food Funct. 2010, 1, 15–31. [Google Scholar] [CrossRef]
- Chaudhuri, D.; Ghate, N.B.; 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. [Google Scholar] [CrossRef]
- Custódio, L.; Justo, T.; Silvestre, L.; Barradas, A.; Duarte, C.V.; Pereira, H.; Barreira, L.; Rauter, A.P.; Alberício, F.; Varela, J. Microalgae of different phyla display antioxidant, metal chelating and acetylcholinesterase inhibitory activities. Food Chem. 2012, 131, 134–140. [Google Scholar] [CrossRef]
- Geetha, B.V.; Rajendran, N.; Ekambaram, P. Investigation of antioxidant capacity and phytochemical composition of Sun Chlorella-an in vitro study. J. Aquac. Res. Dev. 2010, 1, 104. [Google Scholar] [CrossRef]
- Bravo, L. Polyphenols: Chemistry, dietary sources, metabolism, and nutritional significance. Nutr. Rev. 1998, 56, 317–333. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Li, H.B.; Cheng, K.W.; Wong, C.C.; Fan, K.W.; Chen, F.; Jiang, Y. Evaluation of antioxidant capacity and total phenolic content of different fractions of selected microalgae. Food Chem. 2007, 102, 771–776. [Google Scholar] [CrossRef]
- Cos, P.; Ying, L.; Calomme, M.; Hu, J.P.; Cimanga, K.; Van Poel, B.; Pieters, L.; Vlietinck, A.J.; Berghe, D.V. Structure-activity relationship and classification of flavonoids as inhibitors of xanthine oxidase and superoxide scavengers. J. Nat. Prod. 1998, 61, 71–76. [Google Scholar] [CrossRef]
- Machu, L.; Misurcova, L.; Vavra Ambrozova, J.; Orsavova, J.; Mlcek, J.; Sochor, J.; Jurikova, T. Phenolic content and antioxidant capacity in algal food products. Molecules 2015, 20, 1118–1133. [Google Scholar] [CrossRef]
- 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. [Google Scholar] [CrossRef]
- Norzagaray-Valenzuela, C.D.; Valdez-Ortiz, A.; Shelton, L.M.; Jiménez-Edeza, M.; Rivera-López, J.; Valdez-Flores, M.A.; Germán-Báez, L.J. Residual biomasses and protein hydrolysates of three green microalgae species exhibit antioxidant and anti-aging activity. J. Appl. Phycol. 2016, 29, 189–198. [Google Scholar] [CrossRef]
- Maadane, A.; Merghoub, N.; Ainane, T.; El Arroussi, H.; Benhima, R.; Amzazi, S.; Bakri, Y.; Wahby, I. Antioxidant activity of some Moroccan marine microalgae: Pufa profiles, carotenoids and phenolic content. J. Biotechnol. 2015, 215, 13–19. [Google Scholar] [CrossRef]
- Cha, K.H.; Kang, S.W.; Kim, C.Y.; Um, B.H.; Na, Y.R.; Pan, C.H. Effect of pressurized liquids on extraction of antioxidants from Chlorella vulgaris. J. Agric. Food Chem. 2010, 58, 4756–4761. [Google Scholar] [CrossRef]
- Jerez-Martel, I.; García-Poza, S.; Rodríguez-Martel, G.; Rico, M.; Afonso-Olivares, C.; Gómez-Pinchetti, J.L. Phenolic profile and antioxidant activity of crude extracts from microalgae and cyanobacteria strains. J. Food Qual. 2017. [Google Scholar] [CrossRef]
- Klejdus, B.; Kopecký, J.; Benešová, L.; Vacek, J. Solid-phase/supercritical-fluid extraction for liquid chromatography of phenolic compounds in freshwater microalgae and selected cyanobacterial species. J. Chromatogr. A 2009, 1216, 763–771. [Google Scholar] [CrossRef]
- Poljsak, B.; Milisav, I. The neglected significance of “antioxidative stress”. Oxid. Med. Cell. Longev. 2012, 2012. [Google Scholar] [CrossRef]
- Ejike, C.E.; Collins, S.A.; Balasuriya, N.; Swanson, A.K.; Mason, B.; Udenigwe, C.C. Prospects of microalgae proteins in producing peptide-based functional foods for promoting cardiovascular health. Trends Food Sci. Technol. 2017, 59, 30–36. [Google Scholar] [CrossRef]
- Sánchez, A.; Vázquez, A. Bioactive peptides: A review. Food Qual. Saf. 2017, 1, 29–46. [Google Scholar] [CrossRef]
- Lemes, A.C.; Sala, L.; Ores, J.D.C.; Braga, A.R.C.; Egea, M.B.; Fernandes, K.F. A review of the latest advances in encrypted bioactive peptides from protein-rich waste. Int. J. Mol. Sci. 2016, 17, 950. [Google Scholar] [CrossRef]
- Ngo, D.H.; Vo, T.S.; Ngo, D.N.; Wijesekara, I.; Kim, S.K. Biological activities and potential health benefits of bioactive peptides derived from marine organisms. Int. J. Biol. Macromol. 2012, 51, 378–383. [Google Scholar] [CrossRef]
- Maestri, E.; Marmiroli, M.; Marmiroli, N. Bioactive peptides in plant-derived foodstuffs. J. Proteomics 2016, 147, 140–155. [Google Scholar] [CrossRef]
- Alzahrani, M.A.J.; Perera, C.O.; Hemar, Y. Production of bioactive proteins and peptides from the diatom Nitzschia laevis and comparison of their in vitro antioxidant activities with those from Spirulina platensis and Chlorella vulgaris. Int. J. Food Sci. Technol. 2018, 53, 676–682. [Google Scholar] [CrossRef]
- García, M.C.; Puchalska, P.; Esteve, C.; Marina, M.L. Vegetable foods: A cheap source of proteins and peptides with antihypertensive, antioxidant, and other less occurrence bioactivities. Talanta 2013, 106, 328–349. [Google Scholar] [CrossRef]
- Alam, M.N.; Bristi, N.J.; Rafiquzzaman, M. Review on in vivo and in vitro methods evaluation of antioxidant activity. Saudi Pharm. J. 2013, 21, 143–152. [Google Scholar] [CrossRef]
- Shih, M.F.; Cherng, J.Y. Protective effects of Chlorella-derived peptide against UVC-induced cytotoxicity through inhibition of caspase-3 activity and reduction of the expression of phosphorylated FADD and cleaved PARP-1 in skin fibroblasts. Molecules 2012, 17, 9116–9128. [Google Scholar] [CrossRef]
- Lee, S.H.; Chang, D.U.; Lee, B.J.; Jeon, Y.J. Antioxidant activity of solubilized Tetraselmis suecica and Chlorella ellipsoidea by enzymatic digests. J. Food Sci. Nutr. 2009, 14, 21–28. [Google Scholar] [CrossRef]
- Ko, S.C.; Kim, D.; Jeon, Y.J. Protective effect of a novel antioxidative peptide purified from a marine Chlorella ellipsoidea protein against free radical-induced oxidative stress. Food Chem. Toxicol. 2012, 50, 2294–2302. [Google Scholar] [CrossRef]
- Sheih, I.C.; Wu, T.K.; Fang, T.J. Antioxidant properties of a new antioxidative peptide from algae protein waste hydrolysate in different oxidation systems. Bioresource Technol. 2009, 100, 3419–3425. [Google Scholar] [CrossRef] [PubMed]
- Kang, K.H.; Qian, Z.J.; Ryu, B.; Karadeniz, F.; Kim, D.; Kim, S.K. Antioxidant peptides from protein hydrolysate of microalgae Navicula incerta and their protective effects in HepG2/CYP2E1 cells induced by ethanol. Phytother. Res. 2012, 26, 1555–1563. [Google Scholar] [CrossRef] [PubMed]
- Zou, T.B.; He, T.P.; Li, H.B.; Tang, H.W.; Xia, E.Q. The structure-activity relationship of the antioxidant peptides from natural proteins. Molecules 2016, 21, 72. [Google Scholar] [CrossRef] [PubMed]
- Tian, M.; Fang, B.; Jiang, L.; Guo, H.; Cui, J.; Ren, F. Structure-activity relationship of a series of antioxidant tripeptides derived from β-Lactoglobulin using QSAR modeling. Dairy Sci. Technol. 2015, 95, 451–463. [Google Scholar] [CrossRef]
- Samaranayaka, A.G.; Li-Chan, E.C. Food-derived peptidic antioxidants: A review of their production, assessment, and potential applications. J. Funct Food 2011, 3, 229–254. [Google Scholar] [CrossRef]
- Li, Y.W.; Li, B. Characterization of structure-antioxidant activity relationship of peptides in free radical systems using QSAR models: Key sequence positions and their amino acid properties. J. Theor Biol. 2013, 318, 29–43. [Google Scholar] [CrossRef] [PubMed]
- WHO [World Health Organization]. Global Status Report on Noncommunicable Diseases; WHO: Geneve, Switzerland, 2014; p. 176. [Google Scholar]
- Melaku, L.; Mossie, A. Cardioprotective effects of angiotensin converting Enzyme II. Int. J. Clin. Exp. Physiol. 2017, 4, 57. [Google Scholar]
- Muñoz-Durango, N.; Fuentes, C.A.; Castillo, A.E.; González-Gómez, L.M.; Vecchiola, A.; Fardella, C.E.; Kalergis, A.M. Role of the renin-angiotensin-aldosterone system beyond blood pressure regulation: Molecular and cellular mechanisms involved in end-organ damage during arterial hypertension. Int. J Mol. Sci. 2016, 17, 797. [Google Scholar] [CrossRef] [PubMed]
- Murohara, T.; Buerke, M.; Lefer, A.M. Polymorphonuclear leukocyte-induced vasocontraction and endothelial dysfunction. Role of selectins. Arterioscler. Thromb. J. Vasc. Biol. 1994, 14, 1509–1519. [Google Scholar] [CrossRef]
- Majumder, K.; Wu, J. Molecular targets of antihypertensive peptides: Understanding the mechanisms of action based on the pathophysiology of hypertension. Int. J. Mol. Sci. 2014, 16, 256–283. [Google Scholar] [CrossRef]
- Solomon, S.D.; Skali, H.; Bourgoun, M.; Fang, J.; Ghali, J.K.; Martelet, M.; Wojciechowski, D.; Ansmite, B.; Skards, J.; Laks, T.; et al. Effect of angiotensin-converting enzyme or vasopeptidase inhibition on ventricular size and function in patients with heart failure: The Omapatrilat Versus Enalapril Randomized Trial of Utility in Reducing Events (OVERTURE) echocardiographic study. Am. Heart J. 2005, 150, 257–262. [Google Scholar] [CrossRef] [PubMed]
- Daemen, M.J.; Lombardi, D.M.; Bosman, F.T.; Schwartz, S.M. Angiotensin II induces smooth muscle cell proliferation in the normal and injured rat arterial wall. Circ. Res. 1991, 68, 450–456. [Google Scholar] [CrossRef]
- Norris, R.; FitzGerald, R.J. Antihypertensive peptides from food proteins. In Bioactive Food Peptides in Health and Disease; Hernandez-Ledesma, B., Hsieh, C.C., Eds.; InTech: London, UK, 2013; pp. 45–72. [Google Scholar]
- Girgih, A.T.; Alashi, A.; He, R.; Malomo, S.; Aluko, R.E. Preventive and treatment effects of a hemp seed (Cannabis sativa L.) meal protein hydrolysate against high blood pressure in spontaneously hypertensive rats. Eur. J. Nutr. 2014, 53, 1237–1246. [Google Scholar] [CrossRef] [PubMed]
- Majumder, K.; Chakrabarti, S.; Morton, J.S.; Panahi, S.; Kaufman, S.; Davidge, S.T.; Wu, J. Egg-derived tri-peptide IRW exerts antihypertensive effects in spontaneously hypertensive rats. PLoS ONE 2013, 8, e82829. [Google Scholar] [CrossRef] [PubMed]
- Fernández-Musoles, R.; Manzanares, P.; Burguete, M.C.; Alborch, E.; Salom, J.B. In vivo angiotensin I-converting enzyme inhibition by long-term intake of antihypertensive lactoferrin hydrolysate in spontaneously hypertensive rats. Food Res. Int. 2013, 54, 627–632. [Google Scholar] [CrossRef]
- Murray, B.A.; FitzGerald, R.J. Angiotensin converting enzyme inhibitory peptides derived from food proteins: Biochemistry, bioactivity and production. Curr. Pharm. Des. 2007, 13, 773–791. [Google Scholar] [CrossRef]
- Sheih, I.C.; Fang, T.J.; Wu, T.K. Isolation and characterisation of a novel angiotensin I-converting enzyme (ACE) inhibitory peptide from the algae protein waste. Food Chem. 2009, 115, 279–284. [Google Scholar] [CrossRef]
- Ko, S.C.; Kang, N.; Kim, E.A.; Kang, M.C.; Lee, S.H.; Kang, S.M.; Lee, J.B.; Jeon, B.T.; Kim, S.K.; Park, S.J.; et al. A novel angiotensin I-converting enzyme (ACE) inhibitory peptide from a marine Chlorella ellipsoidea and its antihypertensive effect in spontaneously hypertensive rats. Process Biochem. 2012, 47, 2005–2011. [Google Scholar] [CrossRef]
- Udenigwe, C.C.; Aluko, R.E. Food protein-derived bioactive peptides: Production, processing, and potential health benefits. J. Food Sci. 2012, 77, R11–R24. [Google Scholar] [CrossRef]
- Brew, K. Structure of human ACE gives new insights into inhibitor binding and design. Trends Pharmacol. Sci. 2003, 24, 391–394. [Google Scholar] [CrossRef]
- FitzGerald, R.J.; Murray, B.A.; Walsh, D.J. Hypotensive peptides from milk proteins. J. Nutr. 2004, 134, 980S–988S. [Google Scholar] [CrossRef] [PubMed]
- Cheung, H.S.; Wang, F.L.; Ondetti, M.A.; Sabo, E.F.; Cushman, D.W. Binding of peptide substrates and inhibitors of angiotensin-converting enzyme. Importance of the COOH-terminal dipeptide sequence. J. Biol Chem. 1980, 255, 401–407. [Google Scholar] [PubMed]
- Moskowitz, D.W. Is “somatic” angiotensin I-converting enzyme a mechanosensor? Diabetes Technol. Ther. 2002, 4, 841–858. [Google Scholar] [CrossRef] [PubMed]
- Talero, E.; García-Mauriño, S.; Ávila-Román, J.; Rodríguez-Luna, A.; Alcaide, A.; Motilva, V. Bioactive compounds isolated from microalgae in chronic inflammation and cancer. Mar. Drugs 2015, 13, 6152–6209. [Google Scholar] [CrossRef]
- Jellinger, K.A. Recent advances in our understanding of neurodegeneration. J. Neural Transm. (Vienna) 2009, 116, 1111–1162. [Google Scholar] [CrossRef]
- Mhatre, M.; Hensley, K. Oxidative Stress and Neuroinflammation in Alzheimer’s Disease and Amyotrophic Lateral Sclerosis: From Biology to Therapeutic Strategies. In Oxidative Stress and Neurodegenerative Disorders, 1st ed.; Qureshi, G.A., Parvez, S.H., Eds.; Elsevier: Amsterdam, The Netherlands, 2007; pp. 297–311. [Google Scholar]
- Popa-Wagner, A.; Mitran, S.; Sivanesan, S.; Chang, E.; Buga, A.M. ROS and brain diseases: The good, the bad, and the ugly. Oxid. Med. Cell. Longev. 2013, 2013, 14. [Google Scholar] [CrossRef]
- Ravipati, A.S.; Zhang, L.; Koyyalamudi, S.R.; Jeong, S.C.; Reddy, N.; Bartlett, J.; Smith, P.T.; Shanmugam, K.; Münch, G.; Wu, M.J.; et al. Antioxidant and anti-inflammatory activities of selected Chinese medicinal plants and their relation with antioxidant content. BMC Complement. Altern. Med. 2012, 12, 173. [Google Scholar] [CrossRef]
- Biswas, S.K. Does the interdependence between oxidative stress and inflammation explain the antioxidant paradox? Oxid. Med. Cell Longev. 2016, 2016, 5698931. [Google Scholar] [CrossRef]
- Montero-Lobato, Z.; Vázquez, M.; Navarro, F.; Fuentes, J.; Bermejo, E.; Garbayo, I.; Vílchez, C.; Cuaresma, M. Chemically-Induced Production of Anti-Inflammatory Molecules in Microalgae. Mar. Drugs 2018, 16, 478. [Google Scholar] [CrossRef]
- Blagojević, D.; Babić, O.; Rašeta, M.; Šibul, F.; Janjušević, L.; Simeunović, J. Antioxidant activity and phenolic profile in filamentous cyanobacteria: The impact of nitrogen. J. Appl. Phycol. 2018, 30, 2337. [Google Scholar] [CrossRef]
- Robertson, R.; Guihéneuf, F.; Bahar, B.; Schmid, M.; Stengel, D.; Fitzgerald, G.; Fitzgerald, G.; Ross, R.; Stanton, C. The anti-inflammatory effect of algae-derived lipid extracts on lipopolysaccharide (LPS)-stimulated human THP-1 macrophages. Mar. Drugs 2015, 13, 5402–5424. [Google Scholar] [CrossRef]
- Hussain, T.; Tan, B.; Yin, Y.; Blachier, F.; Tossou, M.C.; Rahu, N. Oxidative stress and inflammation: What polyphenols can do for us? Oxid. Med. Cell Longev. 2016, 2016, 7432797. [Google Scholar] [CrossRef]
- Arulselvan, P.; Fard, M.T.; Tan, W.S.; Gothai, S.; Fakurazi, S.; Norhaizan, M.E.; Kumar, S.S. Role of antioxidants and natural products in inflammation. Oxid. Med. Cell Longev. 2016, 2016, 5276130. [Google Scholar] [CrossRef]
- Yates, C.M.; Calder, P.C.; Rainger, G. Pharmacology and therapeutics of omega-3 polyunsaturated fatty acids in chronic inflammatory disease. Pharmacol. Ther. 2014, 141, 272–282. [Google Scholar] [CrossRef]
- Banskota, A.H.; Gallant, P.; Stefanova, R.; Melanson, R.; O’Leary, S.J. Monogalactosyldiacylglycerols, potent nitric oxide inhibitors from the marine microalga Tetraselmis chuii. Nat. Prod. Res. 2013, 27, 1084–1090. [Google Scholar] [CrossRef]
- Banskota, A.H.; Stefanova, R.; Gallant, P.; Osborne, J.A.; Melanson, R.; O’Leary, S.J. Nitric oxide inhibitory activity of monogalactosylmonoacylglycerols from a freshwater microalgae Chlorella sorokiniana. Nat. Prod. Res. 2013, 27, 1028–1031. [Google Scholar] [CrossRef]
- Van Beelen, V.A.; Spenkelink, B.; Mooibroek, H.; Sijtsma, L.; Bosch, D.; Rietjens, I.M.C.M.; Alink, G.M. An n-3 PUFA-rich microalgal oil diet protects to a similar extent as a fish oil-rich diet against AOM-induced colonic aberrant crypt foci in F344 rats. Food Chem. Toxicol. 2009, 47, 316–320. [Google Scholar] [CrossRef]
- Khan, M.N.; Cho, J.Y.; Lee, M.C.; Kang, J.Y.; Park, N.G.; Fujii, H.; Honh, Y.K. Isolation of two anti-inflammatory and one pro-inflammatory polyunsaturated fatty acids from the brown seaweed Undaria pinnatifida. J. Agric. Food Chem. 2007, 55, 6984–6988. [Google Scholar] [CrossRef]
- Vo, T.S.; Kim, J.A.; Wijesekara, I.; Kong, C.S.; Kim, S.K. Potent effect of brown algae (Ishige okamurae) on suppression of allergic inflammation in human basophilic KU812F cells. Food Sci. Biotechnol. 2011, 20, 1227–1234. [Google Scholar] [CrossRef]
- Ohgami, K.; Shiratori, K.; Kotake, S.; Nishida, T.; Mizuki, N.; Yazawa, K.; Ohno, S. Effects of astaxanthin on lipopolysaccharide induced inflammation in vitro and in vivo. Investig. Ophthalmol. Vis. Sci. 2003, 44, 2694–2701. [Google Scholar] [CrossRef]
- Choi, Y.; Lee, M.K.; Lim, S.Y.; Sung, S.H.; Kim, Y.C. Inhibition of inducible NO synthase, cyclooxygenase-2 and interleukin-1β by torilin is mediated by mitogen-activated protein kinases in microglial BV2 cells. Br. J. Pharmacol. 2009, 156, 933–940. [Google Scholar] [CrossRef]
- Rajapakse, N.; Kim, M.M.; Mendis, E.; Kim, S.K. Inhibition of inducible nitric oxide synthase and cyclooxygenase-2 in lipopolysaccharide-stimulated RAW264.7 cells by carboxybutyrylated glucosamine tales place via down-regulation of mitogen-activated protein kinase-mediated nuclear factor-κB signaling. Immunology 2008, 123, 348–357. [Google Scholar] [CrossRef]
- Speranza, L.; Pesce, M.; Patruno, A.; Franceschelli, S.; de Lutiis, M.A.; Grilli, A.; Felaco, M. Astaxanthin treatment reduced oxidative induced pro-inflammatory cytokines secretion in U937: SHP-1 as a novel biological target. Mar. Drugs 2012, 10, 890–899. [Google Scholar] [CrossRef]
- Macedo, R.C.; Bolin, A.P.; Marin, D.P.; Otton, R. Astaxanthin addition improves human neutrophils function: In vitro study. Eur. J. Nutr. 2010, 49, 447–457. [Google Scholar] [CrossRef]
- Bennedsen, M.; Wang, X.; Willen, R.; Wadstrom, T.; Andersen, L.P. Treatment of H. pylori infected mice with antioxidant astaxanthin reduces gastric inflammation, bacterial load and modulates cytokine release by splenocytes. Immunol. Lett. 1999, 70, 185–189. [Google Scholar] [CrossRef]
- Park, J.S.; Chyun, J.H.; Kim, Y.K.; Line, L.L.; Chew, B.P. Astaxanthin decreased oxidative stress and inflammation and enhanced immune response in humans. Nutr. MeTab. 2010, 7, 18. [Google Scholar] [CrossRef]
- Nguyen, V.D. Marine glycans in relationship with probiotic microorganisms to improve human and animal health. In Marine Glycobiology: Principles and Applications; Kim, S.K., Ed.; CRC Press: Boca Raton, FL, USA, 2016. [Google Scholar]
- de Jesus Raposo, M.; de Morais, A.; de Morais, R. Marine polysaccharides from algae with potential biomedical applications. Mar. Drugs 2015, 13, 2967–3028. [Google Scholar] [CrossRef]
- Delattre, C.; Pierre, G.; Laroche, C.; Michaud, P. Production, extraction and characterization of microalgal and cyanobacterial exopolysaccharides. Biotechnol. Adv. 2016, 34, 1159–1179. [Google Scholar] [CrossRef]
- Matsui, S.M.; Muizzudin, N.; Arad, S.M.; Marenus, K. Sulfated polysaccharides from red microalgae anti-inflammatory properties in vitro and in vivo. Appl. Biochem. Biotechnol. 2003, 104, 13–22. [Google Scholar] [CrossRef]
- Albuquerque, I.R.L.; Cordeiro, S.L.; Gomes, D.L.; Dreyfuss, J.L.; Filgueira, L.G.A.; Leite, E.L.; Nader, H.B.; Rocha, H.A.O. Evaluation of anti-nociceptive and anti-inflammatory activities of a heterofucan from Dictyota menstrualis. Mar. Drugs. 2013, 11, 2722–2740. [Google Scholar] [CrossRef]
- Kang, S.M.; Kim, K.N.; Lee, S.H.; Ahn, G.; Cha, S.H.; Kim, A.D.; Yang, X.-D.; Kang, M.-C.; Jeon, Y.-J. Anti-inflammatory activity of polysaccharide purified from AMG-assistant extract of Ecklonia cava in LPS-stimulated RAW264.7 macrophages. Carbohydr. Polym. 2011, 85, 80–85. [Google Scholar] [CrossRef]
- Li, C.; Gao, Y.; Xing, Y.; Zhu, H.; Shen, J.; Tian, J. Fucoidan, a sulfated polysaccharide from brown algae, against myocardial ischemia–reperfusion injury in rats via regulating the inflammation response. Food Chem. Toxicol. 2011, 49, 2090–2095. [Google Scholar] [CrossRef]
Microalgae (form) | Major Producer | Origin | Annual Production (tons/year) | World Production (tons/year) |
---|---|---|---|---|
Arthrospira (whole, dried microalgae) | Earthrise Nutraceuticals | USA | 450 | 4100–6700 |
Cyanotech Corporation | USA | 360 | ||
Hainan DIC Microalgae | China | 350 | ||
Japan Algae Co., Ltd. | Japan | 30–100 | ||
Parry Nutraceuticals | India | >175 | ||
FEMICO | Taiwan | 50–150 | ||
Nan Pao International Biotechnology Co. Ltd. | Taiwan | 70 | ||
Biorigin | Switzerland | 60 | ||
TAAU Australia Pty Ltd. | Australia | 50–60 | ||
Chlorella (whole, dried microalgae) | Taipei | Taiwan | 400 | 2000 |
Roquette Klötze | Germany | 130–150 | ||
Blue Biotech | Germany | * | ||
Earthrise Nutritionals | USA | * | ||
β-carotene from Dunaliella (as oleoresin) | Cognis Nutrition & Health Co. | Australia | * | 1200 |
Nature Beta Technology Ltd. | Israel | * | ||
Astaxanthin from Haematococcus (as oleoresin) | Cyanotech Corp. | USA | * | 300 |
Mera Pharmaceuticals Inc. | USA | * | ||
Fuji Chemical Industries | Japan | * | ||
BioReal AB | Sweden | * |
Species | Class | % Protein (w/w) | % Carbs (w/w) | % Fat (w/w) | References |
---|---|---|---|---|---|
Phaeodactylum tricornutum | Bacillariophyceae | 34.8 | 16.8 | 16.1 | [45,46] |
Nitzschia closterium | Bacillariophyceae | 26 | 9.8 | 13 | [45] |
Chlamydomonas reinhardtii | Chlorophyceae | 48 | 17 | 21 | [47] |
Dunaliella tertiolecta | Chlorophyceae | 11 | - | - | [48] |
Dunaliella primolecta | Chlorophyceae | 12 | - | - | [49] |
Dunaliella salina | Chlorophyceae | 57 | 32 | 6 | [47] |
Dunaliella sp. | Chlorophyceae | 34.17 | 14.57 | 14.36 | [50] |
Scenedesmus obliquus | Chlorophyceae | 48–56 | 10–17 | 12–14 | [47,51] |
Scenedesmus sp. | Chlorophyceae | 31 | 28 | 15 | [50] |
Chaetoceros calcitrans | Coscinodiscophyceae | 34 | 6.0 | 16 | [45] |
Chaetoceros calcitrans | Coscinodiscophyceae | 40 | 37 | 23 | [52] |
Chaetoceros gracilis | Coscinodiscophyceae | 12 | 4.7 | 7.2 | [45] |
Chaetoceros muelleri | Coscinodiscophyceae | 59 | 10 | 31 | [52] |
Skeletonema costatum | Coscinodiscophyceae | 25 | 4.6 | 10 | [45] |
Thalassiosira pseudonana | Coscinodiscophyceae | 34 | 8.8 | 19 | [45] |
Spirulina maxima | Cyanophyceae | 60–71 | 13–16 | 6-7 | [47] |
Synechococcus sp. | Cyanophyceae | 63 | 15 | 11 | [47] |
Nannochloropsis sp. | Eustigmatophyceae | 30 | 10 | 22 | [50] |
Nannochloropsis granulata | Eustigmatophyceae | 18–34 | 27–36 | 24–28 | [46] |
Pavlova sp. | Pavlovophyceae | 24–29 | 6–9 | 9–14 | [45,47] |
Porphyridium cruentum | Porphyridiophyceae | 28–39 | 40-57 | 9–14 | [47] |
Tetraselmis chuii | Prasinophyceae | 31–46 | 25 | 12 | [45,46] |
Tetraselmis sp. | Prasinophyceae | 36 | 24 | - | [53] |
Prymnesium sp. | Prymnesiophyceae | 28–45 | 25–33 | 22–38 | [54] |
Isochrysis galbana | Prymnesiophyceae | 27 | 34 | 11 | [55] |
Schizochytrium sp. | Thraustochytriaceae | - | - | 50–77 | [56] |
Botryococcus braunii | Trebouxiophyceae | 39–40 | 19–31 | 25–34 | [46] |
Chlorella pyrenoidosa | Trebouxiophyceae | 57 | 26 | 2 | [56] |
Chlorella vulgaris | Trebouxiophyceae | 51–58 | 12–17 | 14–22 | [47] |
Product | Price (USD kg−1) | References |
---|---|---|
Astaxanthin | 2500–7000 | [77] |
β-carotene | 300–1500 | [14] |
Omega-3 fatty acids | 80–160 | [14] |
Chlorella biomass | 44 | [78] |
Arthrospira biomass | 42 * | [79] |
Bioactive Compounds | Source | Health Benefits | References |
---|---|---|---|
Carotenoids | |||
β-carotene | Dunaliella salina | Antioxidant, pro-vitamin A, anti-allergic, anti-inflammatory | [89,90] |
Astaxanthin | Haematococcus pluvialis, C. zofingiensis | Antioxidant, anti-inflammatory | [91] |
Lutein | Scenedesmus spp., Muriellopsis sp., C. sorokiniana | Antioxidant, anti-inflammatory | [92,93,94] |
PUFAs | |||
Arachidonic acid (AA) | Porphyridium purpureum, P. cruentum,Parietochloris incisa | Improves normal growth, visual and functional development in infants | [95,96,97] |
Eicosapentaenoic acid (EPA) | Nannochloropsis sp., Phaeodactylum tricornutum, Porphyridium cruentum | Cardiovascular benefits, mental development and support, anti-inflammatory, protection against atherosclerosis | [98,99,100] |
Docosahexaenoic acid (DHA) | Crypthecodinium cohnii, Schizochytrium spp., Ulkenia spp. | Cardiovascular benefits, improves nervous system development and function of the brain | [101,102] |
Other metabolites | |||
Peptides | Chlorella pyrenoidosa, Nannochloropsis oculata | Antioxidant, anti-inflammatory, anticancer, antihypertensive | [103,104] |
Phenolics | Arthrospira maxima, Tetraselmis suecica, Botryococcus braunii, Isochrysis sp., Chlorella vulgaris, Nannochloropsis sp. | Antioxidant | [22,105,106] |
Phycocyanin | Arthrospira platensis | Antioxidant, anti-inflammatory | [107] |
Sulfated polysaccharides | C. pyrenoidosa,C. stigmatophora, Porphyridium sp., Phaeodactylum tricornutum | antioxidant, anti-inflammatory, antiviral, immunomodulatory | [108,109,110] |
“Water-soluble extract” | Chlorella stigmatophora, Phaeodactylum tricornutum, Graesiella sp. | Anti-inflammatory, analgesic, antioxidant, antiproliferative | [108,111] |
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Barkia, I.; Saari, N.; Manning, S.R. Microalgae for High-Value Products Towards Human Health and Nutrition. Mar. Drugs 2019, 17, 304. https://doi.org/10.3390/md17050304
Barkia I, Saari N, Manning SR. Microalgae for High-Value Products Towards Human Health and Nutrition. Marine Drugs. 2019; 17(5):304. https://doi.org/10.3390/md17050304
Chicago/Turabian StyleBarkia, Ines, Nazamid Saari, and Schonna R. Manning. 2019. "Microalgae for High-Value Products Towards Human Health and Nutrition" Marine Drugs 17, no. 5: 304. https://doi.org/10.3390/md17050304