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Microalgae for High-Value Products Towards Human Health and Nutrition marine drugs Review Microalgae for High-Value Products Towards Human Health and Nutrition Ines Barkia 1, Nazamid Saari 1,* and Schonna R. Manning 2 1 Department of Food Science, Universiti Putra Malaysia, Selangor 43400, Malaysia; [email protected] 2 Department of Molecular Biosciences, UTEX Culture Collection of Algae, University of Texas at Austin, Austin, TX 78712, USA; [email protected] * Correspondence: [email protected] Received: 25 March 2019; Accepted: 2 April 2019; Published: 24 May 2019 Abstract: Microalgae represent a potential source of renewable nutrition and there is growing interest in algae-based dietary supplements in the form of whole biomass, e.g., Chlorella and Arthrospira, or purified extracts containing omega-3 fatty acids and carotenoids. The commercial production of bioactive compounds from microalgae is currently challenged by the biorefinery process. This review focuses on the biochemical composition of microalgae, the complexities of mass cultivation, as well as potential therapeutic applications. The advantages of open and closed growth systems are discussed, including common problems encountered with large-scale growth systems. Several methods are used for the purification and isolation of bioactive compounds, and many products from microalgae have shown potential as antioxidants and treatments for hypertension, among other health conditions. However, there are many unknown algal metabolites and potential impurities that could cause harm, so more research is needed to characterize strains of interest, improve overall operation, and generate safe, functional products. Keywords: Microalgae; bioactive compounds; health benefits; antioxidant activity; antihypertensive activity; anti-inflammatory activity 1. Introduction Algae are a complex, polyphyletic assemblage of (mostly) photosynthetic organisms. Organisms in the algae include diverse micro- and macroscopic forms that are distributed across the tree of life, including eukaryotic and prokaryotic members [1], making algae the most genetically-diverse set of organisms on the planet. While the phylogenetic relationships continue to be resolved among groups, algae can be broadly assigned to eleven major phyla: Cyanophyta, Chlorophyta, Rhodophyta, Glaucophyta, Euglenophyta, Chlorarachniophyta, Charophyta, Cryptophyta, Haptophyta, Heterokontophyta, and Dinophyta. The major groups of eukaryotic algae arose through multiple endosymbiotic events, resulting in broadly-distributed and highly-diverse lineages. The Glaucophyta, Rhodophyta, and Chlorophyta evolved via the primary endosymbiosis of a photosynthetic cyanobacterium (Cyanophyta), which gave rise to the chloroplast. Secondary endosymbiosis of green algae led to two major groups, the Euglenophyta and photosynthetic Rhizaria, the Chlorarachniophyta [2]. Similarly, the secondary endosymbiosis of a red alga gave rise to the Cryptophyta, Heterokontophyta, Haptophyta, and Dinophyta. There are tertiary (and possibly quaternary) endosymbiotic events between the Dinophyta and Haptophyta, resulting in genomes greater than 500 Gbps [3,4]. The pigments found in the algae are diagnostic for each major group [5]. Cyanobacteria contain chlorophyll-a, -d, and -f, as well as the phycobiliproteins, phycocyanin, allophycocyanin, and phycoerythrin. Glaucophytes contain chlorophyll-a and harvest light via phycobiliproteins. Mar. Drugs 2019, 17, 304; doi:10.3390/md17050304 www.mdpi.com/journal/marinedrugs Mar. Drugs 2019, 17, 304 2 of 29 Mar. Drugs 2019, 17, x 2 of 29 The Chlorophyta contain chlorophyll-a and -b, as well as a suite of carotenoids, including β-carotene variousand various xanthophylls xanthophylls (e.g., (e.g.,astaxa astaxanthin,nthin, canthaxanthin, canthaxanthin, lutein, lutein, zeaxanthin, zeaxanthin, etc.). etc.). The The primary primary pigmentspigments of of the the Rhodophyte Rhodophyte algae algae are are phycoeryth phycoerythrinrin and and phycocyanin, phycocyanin, which which can can mask mask chlorophyll- chlorophyll-a. a.There There are are no no accessory accessory chlorophylls;chlorophylls; although,although, red algae do do produce produce a a broad broad spectrum spectrum of of carotenes carotenes andand xanthophyll xanthophyll light-harvesting light-harvesting pigments. pigments. CyanobacteriaCyanobacteria and and eukaryotic eukaryotic microalgae microalgae also also synthesize synthesize numerous numerous secondary secondary metabolites, metabolites, includingincluding potentially potentially beneficial beneficial bioactives, bioactives, such such as antioxidants, as antioxidants, as well as well as many as many compounds compounds that are that broadlyare broadly characterized characterized as toxins. as toxins. These These bioactiv bioactivee compounds compounds are areproduced produced via via the the shikimic shikimic acid, acid, mevalonic/non-mevalonicmevalonic/non-mevalonic acid,acid, and acetateand pathways,acetate pathways, e.g., anatoxins, e.g., brevetoxins, anatoxins, cylindrospermopsin, brevetoxins, cylindrospermopsin,microcystins, and prymnesins, microcystins, among and prymnesins many more, among (see [6 ]).many There more are (see greater [6]). thanThere 200 are bioactive greater thanmetabolites 200 bioactive predicted metabolites from cyanobacteria predicted from [7 ],cyan andobacteria thousands [7], moreand thousands are predicted more from are eukaryoticpredicted frommicroalgae. eukaryotic However, microalgae. there However, are very few there assays are very or reference few assays standards or reference available standards for the available detection for of themicroalgal detection metabolites, of microalgal indicating metabolites, a major indicating gap and a a major need forgap more and researcha need for in more this area. research Examples in this of area.microalgal Examples pigments of microalgal and bioactive pigments compounds and bioa discussedctive compounds in this review discussed are illustrated in this in review Figure 1are. illustrated in Figure 1. FigureFigure 1. 1. BioactiveBioactive compoundscompounds fromfrom microalgae microalgae include: include: carotenoids, carotenoids,β -caroteneβ-carotene (a ).(a astaxanthin). astaxanthin (b ), (band), and fucoxanthin fucoxanthin (c); phycobilins, (c); phycobilins, phycocyanin phycocyanin (d) and phycoerythrin (d) and (phycoerythrine); sulfated polysaccharides (e); sulfated (f ); polysaccharidesomega-3 fatty acids, (f); omega-3 docosahexaenoic fatty acids, acid docosahexaenoic (g), docosapentaenoic acid ( acidg), docosapentaenoic (h), and eicosapentaenoic acid (h), acid and (i ); eicosapentaenoicand phenolics, rutin acid ((ji)); and and eckol phenolics, (k). rutin (j) and eckol (k). MicroalgaeMicroalgae are presentedpresented as as new new model model organisms organisms for a wide for rangea wide of biotechnologicalrange of biotechnological applications, applications,including biodiesel including production biodiesel [8], wastewaterproduction bioremediation[8], wastewater [9], bioremediation and dietary supplements [9], and for dietary animal supplementsand human for nutrition animal [and10–12 human]. Recent nutrition economic [10–12] viability. Recent studies economic have viability shown studies that, due have to shown limited that,biomass due productivityto limited biomass and the costsproductivity of commercial and the algal costs production, of commercial the production algal production, of biofuels isthe not productioncost-effective of unlessbiofuels the is processnot cost-effective is coupled withunless the the commercialization process is coupled of higher-valuewith the commercialization co-products [13 ]. ofBy higher-value comparison, co-products the use of microalgae[13]. By comparison, biomass for the the use development of microalgae of biomass products for with the healthdevelopment benefits, ofsuch products as nutraceuticals with health andbenefits, functional such as foods, nutraceu is aticals rapidly and growing functional market foods, [ 14is ].a rapidly For example, growing the marketworldwide [14]. For carotenoid example, market the worldwide is expected carotenoid to increase market from is $1.24expected billion to increase USD in from 2016 to$1.24 more billion than USD$1.53 in billion 2016 to USD more by than 2021 $1.53 [15]. billion USD by 2021 [15]. A lot of funding has been invested over the last few decades to screen microalgal bioactive metabolites [16]. Several bioactive compounds have been discovered and purified from marine microalgae, including sulfated polysaccharides [17], marennine [18], various carotenoids (e.g., Mar. Drugs 2019, 17, 304 3 of 29 A lot of funding has been invested over the last few decades to screen microalgal bioactive metabolites [16]. Several bioactive compounds have been discovered and purified from marine microalgae, including sulfated polysaccharides [17], marennine [18], various carotenoids (e.g., astaxanthin, fucoxanthin, β-carotene [19,20]), omega-3 fatty acids [21], and polyphenols [22]. Some of these metabolites have demonstrated biological activities, including potent antioxidant, anti-inflammatory, anticancer, and antiviral properties [23–25]. Thus, microalgae and microalgae-derived compounds have great potential as supplements in the human diet for the prevention, management, and treatment of physiological aberrations, in addition to providing sustainable natural resources in lieu of synthetic dietary supplements [26]. However, there are emergent biological and economic challenges associated with the large-scale cultivation of microalgae
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