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Microalgae, a Potential Natural Functional Food Source – a Review

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Microalgae, a Potential Natural Functional Food Source – a Review Pol. J. Food Nutr. Sci., 2017, Vol. 67, No. 4, pp. 251–263 DOI: 10.1515/pjfns-2017-0017 http://journal.pan.olsztyn.pl Review article Section: Food Quality and Functionality Microalgae, a Potential Natural Functional Food Source – a Review Angélica Villarruel-López1, Felipe Ascencio2, Karla Nuño3* 1Laboratorio de Microbiología Sanitaria, Centro Universitario de Ciencias Exactas e Ingenierías, Universidad de Guadalajara, Marcelino García Barragán No. 1421, Guadalajara, Jalisco 44430, México 2Unidad de Patología Marina, Centro de Investigaciones Biológicas del Noroeste, Instituto Politécnico Nacional 195, Col. Playa Palo de Santa Rita Sur, La Paz, B.C.S. 23096, México 3División de Ciencias de la Salud, Centro Universitario de Tonalá, Universidad de Guadalajara, Av. Periférico Norte No. 555, Tonalá, Jalisco 48525, México Key words: microalgae, polysaccharides, fatty acids, pigments, vitamins Microalgae are a group of microorganisms used in aquaculture. The number of studies regarding their use as a functional food has recently in- creased due to their nutritional and bioactive compounds such as polysaccharides, fatty acids, bioactive peptides, and pigments. Specifi c microalgal glucans (polysaccharides) can activate the immune system or exert antioxidant and hypocholesterolemic effects. The importance of algal lipids is based on their polyunsaturated fatty acids, their anti-infl ammatory effects, their modulation of lipid pathways, and their neuroprotective action. Microalgae peptides can bind or inhibit specifi c receptors in cardiovascular diseases and cancer, while carotenoids can act as potent antioxidants. The benefi cial biological activity will depend on the specifi c microalga and its chemical constituents. Therefore, knowledge of the composition of microalgae would aid in identifying, selecting, and studying their functional effects. INTRODUCTION more than 200 species are utilized worldwide, but the most cultivated and used are the brown algae Laminaria japonica Algae are a large and diverse group of organisms growing and Undaria pinnatifi da; the red algae Porphyra, Eucheuma, in aquatic environments that are able to photosynthetically Kappapycus, and Gracilaria; and the green algae Monosotroma convert CO2 and minerals to biomass, although some species and Enteromorpha [Lüning & Pang, 2003]. do grow heterotrophically. The two main forms are macroal- The microalgae consist of a wide range of autotrophic or- gae and microalgae with the latter differentiated by their pig- ganisms that grow through photosynthesis in the same way as ments, reserve substances, cell wall, cellular division charac- do plants, and their classifi cation is in constant revision due teristics, and morphology. to new genetic evidence. Nevertheless, they can be classifi ed Macroalgae, or seaweeds, are fast-growing, multicellular, into two major groups: prokaryotic and eukaryotic [Harun macroscopic nonvascular plants that contain chlorophyll, et al., 2010]. The prokaryotic microalgae are the Cyanobac- with sizes reaching up to 60 m in length. They are classi- teria (blue-green algae), the taxonomy of which includes fi ve fi ed in groups based on their pigmentation: Chlorophyceae orders: Chroococcales, Oscillatoriales, Nostocales, Stigone- (green algae), Phaeophyceae (brown algae), and Rhodo- matales, and Pleurocapsales. The Prochlorophyta, or free- phyceae (red algae). Seaweeds have been used by humans living chloroplasts, are another collection of cyanobacteria for about 14,000 years and as food products by the Japa- that represent an artifi cial group based on their different pig- nese and Chinese cultures for centuries; the Aztec popula- mentation, which is derived from an absence of phycobilipro- tion also collected and cultivated seaweeds [Dillehay et al., teins, and in most cases, the presence of chlorophylls a and b. 2008; Mc Hugh, 2003; Pulz & Gross, 2004]. Their applica- One of the main characteristics of cyanobacteria is their fast tions in the food industry have been increasing, as well as uptake and storage of nutrients and compounds such as in the textile, pharmaceutical, cosmetic, and biotechnology phosphate, cyanophycin (a polymer of aspartic acid and ar- industries [Bartsh et al., 2008]. Seaweed biomass is used for ginine), and a branched α-1,4 polyglucan. Some of these the production of phycocolloids such as agar-agar, alginates, microorganisms can produce neurotoxins and hepatotoxins, and carrageenan. Because of their commercial potential, while others produce therapeutic compounds (e.g., antivirals, inmmunomodulators, inhibitors). The most important Cya- nobacteria used in biotechnology are Spirulina (Arhrospira) * Corresponding Author: Tel.: +52 (33)35403020, Ext: 64037; E-mail: [email protected] platensis, Nostoc commune, and Aphanizomenon fl os-aquae © Copyright by Institute of Animal Reproduction and Food Research of the Polish Academy of Sciences © 2017 Author(s). This is an open access article licensed under the Creative Commons Attribution-NonCommercial-NoDerivs License (http://creativecommons.org/licenses/by-nc-nd/3.0/). 252 Microalgae as a Source of Biocompounds with Beneficial Effects TABLE 1. Main classes and species of microalgae. 2011]. In addition, the biodiversity of microalgae would al- low for increasing the number of different sources of bioactive Class Species compounds such as carbohydrates, lipids, proteins, and pig- Chaetoceros calcitrans ments (Table 2) [Markou & Nerantzis, 2013]. Chaetoceros gracilis Nitzchia closterium Bacillariophyceae Phaeodactylum tricornutum PROTEINS Thalassiosira pseudonana Cylindrogheca fusiformis The total protein content of the biomass depends on Dunaliella tertiolecta the microbial species; however, during rapid steady-state Tetraselmis suecica Chlorophyceae growth, the protein content can range from 30% to 55% Chlorella vulgaris Dunaliella salina of the dry weight. The microalgal cell wall is often disrupted to make the protein, amino acids, and other constituents ac- Eutomatophyceae Nannochloropsis oculata cessible, or alternatively, enzymatic protein hydrolysis can Isochrysis galbana be used to obtain bioactive peptides [González-López et al., Prymnesiophyceae Pavlova lutheri Pavlova salina 2010; Kim & Wijesekara, 2010]. It has been reported that some microalgae contain soluble proteins in their cytoplasm. Crysophyceae Cryptomonas rufescens In addition, microalgae with chloroplasts contain soluble Nostoc commune protein, a central pyrenoid, and phycobiliproteins, although Cyanophyceae Spirulina platensis Aphanizomenon fl os-aquae some microalgae such as A. plantesis instead have thylakoid bundles circling the peripheral part of the cytoplasm associ- Euglenophyceae Euglena gracilis ated with phycobilisomes [Safi et al., 2014]. According to Becker [2007], the general protein com- position of the cyanobacteria Spirulina platensis is 43–63% [Pulz & Gross, 2004; Gantar & Svircev, 2010; Duong et al., (dw) with an amino acid profi le of leucine, valine, isoleu- 2012] (Table 1). cine, phenylalanine, tyrosine, methionine, cysteine, and ty- The eukaryotic microalgae include several divisions: rosine. Because of its high protein content, it is also con- Chlorophyta (green algae) is the largest group, and most are sidered a food supplement [Templeton & Laurens, 2015]. unicellular or fi lamentous freshwater forms; Euglenophyta, The Rhodophyta Porphyridium cruentum contains 28–39% which are fl agellated unicells that emerged from a second- of protein dry matter with amino acids such as aspartic acid, ary endosymbiosis between algae and a protozoan-like host; threonine, serine, glutamic acid, glycine, alanine, cysteine, Rhodophyta, or red algae, resulting from their phycoerythrin and valine, among others [Becker, 2007; Safi et al., 2014; content; Cryptophyta, in which most species are photosyn- Hempler & Maier, 2012]. thetically active motile unicells; Dinophyta or Dinofl agellata, In Heterokontophyta, the diatom Phaeodactylum tricornu- which represent a wide group, though some species are not tum ranged from 45–54% algal dry weight, with 10.3% phenyl- used due to their production of harmful toxins; Prymne- alanine as the principal amino acid. In contrast, the predomi- siophyta, also called Haptophyta; Glaucophyta, freshwater nant amino acids in six species of Bacillariophyta were serine, algae that possess an almost intact cyanelle as their photosyn- alanine, arginine, leucine, glycine, aspartate, and threonine. thetic organelle; Chlorarachniophyta, amoeboid/fl agellated The Eustomatophyta Nannochloropsis sp. has a similar amino eukaryotes; and Heterokontophyta, composed of the brown acid profi le as that of Chlorella vulgaris, with a 30% protein algae Phaeophyta, the yellow-green algae Eustimatophyta (or content of algal dry weight [Chuecas & Riley, 1969; Gatenby Xanthophyta), the golden algae Chrysophyta, and the Bacil- et al., 2003]. When Prymnesiophyta Isochrysis aff. galbana lariophyta (or Diatoms) [Duong et al., 2012; Barsanti et al., (clone T-Iso) was exposed to low and high levels of nitrate, 2008; Leblond et al., 2010; McFadden et al., 1997]. it showed protein contents ranging between 6.3% and 19.8% Microalgae are cultivated in aquaculture, and in recent (dw), and its amino acid composition did not vary with dif- years, the number of studies regarding their use as functional ferent irradiances during growth. Glutamate and aspartate foods has increased. This is due to such nutritional character- were present in the same proportions (9.0–13.5% of total istics as their cell wall polysaccharide
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