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Review Microalgae metabolites: A rich source for food and medicine Ramaraj Sathasivam a , Ramalingam Radhakrishnan b, ⇑ , Abeer Hashem c , Elsayed F. Abd_Allah d, ⇑ a Department of Biotechnology, Sangmyung University, Seoul 03016, Republic of Korea b Department of Biotechnology, Yeungnam University, Gyeongsan 38541, Republic of Korea c Botany and Microbiology, Department, College of Science, King Saud University, P.O. Box. 2460, Riyadh 11451, Saudi Arabia d Plant Production Department, College of Food and Agricultural Sciences, King Saud University, P.O. Box. 2460, Riyadh 11451, Saudi Arabia a r t i c l e i n f o Article history: Received 13 August 2017Revised 4 October 2017Accepted 2 November 2017Available online xxxx Keywords: MicroalgaeBioactive compoundsFoodMedicine a b s t r a c t Microalgae are one of the important components in food chains of aquatic ecosystems and have been usedfor human consumption as food and as medicines. The wide diversity of compounds synthesized from dif-ferentmetabolicpathwaysoffreshandmarinewateralgaeprovidepromisingsourcesoffattyacids,steroids,carotenoids, polysaccharides, lectins, mycosporine-like amino acids, halogenated compounds, polyketides,toxins, agar agar, alginic acid and carrageenan. This review discusses microalgae used to produce biologicalsubstances and its economic importance in food science, the pharmaceutical industry and public health. 2017 Production and hosting by Elsevier B.V. on behalf of King Saud University. Thisisanopenaccessarticle under the CCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/). Contents 1. Introduction . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 002. Commercial production and importance of microalgae in diet. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 003. Impact of microalgae in aquaculture . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 004. Beneficial effects of microalgae in poultry and pig farming . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005. Carotenoids as health-beneficial microalgal metabolites. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.1. b -carotene . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.2. Astaxanthin . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.3. Canthaxanthin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 005.4. Lutein. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 006. Role of microalgal amino acids and fatty acids on health. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 007. Microalgal antioxidants for human health . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 008. Secondary metabolites from microalgae for health promotion. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 008.1. Glycerol . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 008.2. Sterols . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 008.3. Stable isotopic compounds. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 008.4. Phycotoxin. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 009. Conclusions. . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00Acknowledgments . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00References . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . . 00 https://doi.org/10.1016/j.sjbs.2017.11.0031319-562X/ 2017 Production and hosting by Elsevier B.V. on behalf of King Saud University.This is anopenaccess article under the CCBY-NC-NDlicense (http://creativecommons.org/licenses/by-nc-nd/4.0/). ⇑ Corresponding authors. E-mail addresses:
[email protected] (R. Radhakrishnan),
[email protected] (E.F. Abd_Allah). Peer review under responsibility of King Saud University. Production and hosting by Elsevier Saudi Journal of Biological Sciences xxx (2017) xxx–xxx Contents lists available at ScienceDirect Saudi Journal of Biological Sciences journal homepage: www.sciencedirect.com Please cite this article in press as: Sathasivam, R., et al. Microalgae metabolites: A rich source for food and medicine. Saudi Journal of Biological Sciences(2017), https://doi.org/10.1016/j.sjbs.2017.11.003 1. Introduction Algae, a multicellular or unicellular form of living organisms,can be divided into either macro or micro algae based on its size.Microalgae are one of the earliest forms of life on the earth(Falkowski et al., 2004). When the earth’s environment formedover 3 billion years ago, microalgae existed in Earth’s oceans. Thediversityof microalgae(i.e., prokaryotic cyanobacteria andeukary-otic microalgae) is vast, but this diversity has not yet been fullyexposed (Massana et al., 2006; Fehling et al., 2007; Stern et al.,2010). There are more than 50,000 different types of microalgalspeciespresentinoceansandfreshwater(lakes,pondsandrivers);among these species, only 30,000 have been studied (Richmond,2004). Microalgae have been used as food by humans for thou-sands of years (Milledge, 2011).Microalgae can convert solar energy to chemical energy by fix-ing CO 2 , and its efficiency is ten times greater than terrestrialplants. The commercial production of microalgae is approximately5,000 tons/year of dry matter (Raja et al., 2008). There are approx-imately 110 commercial producers of microalgae present in theAsia-Pacific region, with capacities ranging from 3 to 500 tons/year. About nine-tenths of algal cultivation is located in Asia.Among these, high numbers of commercial microalgae producersarelocatedinChina,TaiwanandIndia.Veryfewspeciesofmicroal-gae have commercial importance, but those that do include Spir-ulina , Chlorella , Haematococcus , Dunaliella , Botryococcus , Phaeodactylum, Porphyridium, Chaetoceros, Crypthecodinium , Isochrysis, Nannochloris , Nitzschia , Schizochytrium , Tetraselmis, and Skeletonema. Much of the microalgal biomass has been an attractive sourcefor producing a wide range of highly valuable products, includingpolyunsaturatedfatty acids (PUFA), carotenoids, phycobiliproteins,polysaccharides and phycotoxin. However, the products frommicroalgae have been widely used as a high-protein supplementin human nutrition, aquaculture and nutraceutical purposes (Del-Campo et al., 2007). The market price of algal biomass varies andhas reported ranges of 100 € /kg for human consumption,5–20 € /kg for animal and fish feed, 1–5 € /kg for bulk chemicalsand 0.40 € /kg for biofuel (Wijffels, 2008). Wijffels and Barbosa, (2010) reported that microalgal products were composed of 40%lipids, 50% proteins and 10% carbohydrates; a quarter of the lipidsare sold to the food and chemical industry for 2 € /kg, the rest forbiodiesel at 0.50 € /kg, soluble proteins (20%) for food at 5 € /kg,and the rest (80%) for feed at 0.75 € /kg. This review focuses onthe production of potentially valuable products derived frommicroalgae and their respective applications in the food and med-ical industries. 2. Commercialproductionand importance of microalgae in diet In most developed countries, people consume high caloric fooditemsduetothemodernlife style, whichleads to healthproblems,such as obesity, heart diseases, and diabetics. A balanced nutri-tional diet is needed for health and should contain vitamins, min-erals, PUFAs, etc. Microalgae are considered as a remarkable butpoorly explored natural source for a healthy diet. Several speciesof microalgae are identified as rich in carbohydrates, proteins,lipids and nutritionally valuable components. Becker (2004)reported that microalgae are an abundant source of vitamins andminerals, such as vitamins A, B1, B2, C, and E; nicotinate; biotin;folic acid; pantothenic acid; niacin; iodine; potassium; iron; mag-nesium; and calcium (Table 1). Interestingly, the lack of polysac-charides in the cell wall of cyanobacteria makes their biomass amore easily digestible material and therefore more acceptable forhuman consumption (Richmond and Preiss, 1980). The Chinesefirst used microalgae ( Nostoc sp.) (over 2000years ago) as a foodand, later, the commercial forms of microalgae ( Chlorella sp. and Spirulina sp.) were consumed as healthy foods in Japan, Taiwanand Mexico (Tamiya, 1957; Durand-Chastel, 1980; Soong, 1980).Currently, most of the commercialized products of microalgaeare available in markets as a health food, in the forms of tablets,capsules and liquids (Pulz and Gross, 2004), and their productsare mixed with pastes, snacks, candy, gums, noodles, wine, bever-ages, and breakfast cereals (Yamaguchi, 1997; Lee, 1997; Lianget al., 2004). Aphanizomenon flos-aquae , Chlorella sp. , Dunaliella sal-ina ( D. salina ), Dunaliella tertiolecta ( D. tertiolecta ) and Spirulina plantensis ( S. plantensis ) are some of the microalgae species widelyused as a human food source because they are rich in protein con-tent and have high nutritive value (Soletto et al., 2005; Rangel-Yagui et al., 2004). Among these microalgae, Spirulina ( Arthrospira )and Chlorella are currently dominating the microalgal market. Spirulina ( Arthrospira ) has a high protein content and excellentnutrient value (Spolaore et al., 2006) and has gained worldwidepopularityasafoodsupplement(Collaetal.,2007).Ithasanaminoacidcontentof62%, anditis arichnaturalsourceofvitaminsA, B 1 ,B 2 , B 12 , as well as phytopigments, including carotenoids and xan-thophyll (Richmond, 1988). In addition, it has a considerableamount of essential fatty acids and linolenic acid, which cannotbe synthesized by humans (Becker, 1994); thus, more attentionhasbeengiventothecultivationof Spirulina .Theworldproductionof Spirulina for human consumption exceeds 1000 metric tons,annually (Ciferri and Tiboni, 1985). The world’s largest Spirulina producer is Hainan Simai Enterprising, which is located in Chinaand has an annual algal powder production of 200 tons. Thereare 20 countries in the world that produce Spirulina -based prod-ucts, such as tablets and powder. Among these countries, theUSA ranks first in Spirulina -based products, primarily in the formof pills and spray-dried powder, followed by China, Israel, Japan,Mexico,TaiwanandThailand(Spolaoreet al., 2006). Frommicroal-gae,awidevarietyofnutraceuticalsareavailableandmarketedforsale. For example, the Myanmar- Spirulina -factory (Yangon, Myan-mar) produces tablets, chips, pasta and liquid extracts. Similarly,Cyanotech (Hawaii, USA) produces pure powder under the name‘‘Spirulina pacifica”. Phycocyanin, extracted from Spirulina andcommercially known as ‘lima blue’, is used as a blue colorant forfood and cosmetics. Spirulina also acts as a functional food, feedingbeneficial intestinal flora, including Lactobacillus and Bifidus (Ciferri, 1983). In the future, these health foods are expected tobe a stable market, including products such as Spirulina liquidCO 2 -extracted antioxidant capsules (Belay et al. 1993). One gramof Spirulina contains one-half of the adult daily requirements of Vitamin A. According to human studies, total serum cholesterolwas lowered by consuming Spirulina (Gonzalez de Rivera et al.,1993).ThepurifiedPUFAsfrom Spirulina areaddedintoinfantmilkformulas in European countries for health promoting purposes. Chlorella are also known as healthy foods to humans and usedfornutrient-richfeedforaquaticanimals. Morethan70companieswere involved in the cultivation of Chlorella , and the largest pro-ducer is Taiwan Chlorella Manufacturing and Co. (Taipei, Taiwan),which produces 400 tons of dried biomass/year. A significant pro-duction of Chlorella was achieved in a German company (Klotze,Germany) by using a tubular photobioreactor, and it produces130–150tonsdrybiomass/year.Theworldannualsalesof Chlorella exceed 38 billion US$ (Yamaguchi, 1997). Barrow and Shahidie(2008) notedthat the extractof Chlorella sp. showedseveral healthbenefits. For instance, it can increase hemoglobin concentration,lower blood sugar levels and act as hypocholesterolemic and hep-atoprotective agents during malnutrition and ethionine intoxica-tion. The most important substance in Chlorella is b -1,3-glucan,which is an active immunostimulator, a free radical scavengerand a reducer of blood lipids. Plankton soup primarily consisting 2 R. Sathasivam et al./Saudi Journal of Biological Sciences xxx (2017) xxx–xxx Please cite this article in press as: Sathasivam, R., et al. Microalgae metabolites: A rich source for food and medicine. Saudi Journal of Biological Sciences(2017), https://doi.org/10.1016/j.sjbs.2017.11.003 Table 1 ( continued ) Microalgal valuable metabolites Microalgal producers Uses References C. vulgaris, C. zofingiensis,Chlorococcum spp ., C.citriforme, C. nivalis, C. proboscideum, D. tertiolecta,M. aurantiaca, Muriellopsis sp .,, N. gelatinosum,Pyramimonas spp ., P.urceolata, S. almeriensis, S.armatus,T. intermedium, T.tetrasporum, Tetraselmis spp ., T. wettsteinii (2003); Egeland et al. (1995)Zeaxanthin C. ellipsiodea, D. salina, C.nivalis, D. salina, Protect eye cells; Antioxidantactivity; Neutralizing the freeradicalsCha et al. (2008); Leya et al. (2009); Bhosale and Bernstein(2005) 4. Glutathione Glutathione Dunaliella spp ., Lowering the heart attck;Antioxdiant properties;Anticancer activity; Anti-Parkinson’s disease; Detoxifythemetals; Lowering the bloodpressureLi et al. (2004)5. GlycerolGlycerol C. pulsatilla, Chlamydomonasspp., C. pulsatilla, C.reinhardtii, C. submarinum,Dunaliella spp., D. salina Moisture to the skin and helpskin smoothAhmad and Hellebust (1986); Miyasaka et al. (1998); Leonand Galvan (1999); Blackwell and Gilmour (1991); Kackaand Donmez (2008); Hadi et al. (2008) 6. Lipids Triglycerides and hydrocarbons B. braunii, C. calcitrans, C.muelleri, C. californicum, C.oviforme, C. rheinhardii, C.emersonii, C. luteo-viridis, C. protothecoides, C.sorokiniana, C. vulgaris, C.neglecta, C. simplex, C.costazygoticum, C.infusionum, C. chodati, C.striolata, C. cohnii,Cylindrotheca spp., Ellipsoidion spp., E. gracillis,H. pluvialis, I. galbana, L.culleus, L. segnis, M. salina,M. subterraneus, M.arcuatum, M. contortum, M.dybowskii, M. griffithii, M.neglectum, M. terrestre, M.tortile, M. aurantiaca, N.eucaryotum, Nannochloris spp., N. oculata, N. salinicola,N. oleoabundans, Nitzschia spp., P. kessleri, P. lutheri, P.salina, P. tricornutum, P.insigne Biofuels Chu(2012); Ramaraj et al. (2014);Rodolfietal. (2009), Mataet al. (2010), Mutanda et al. (2011), and Bogen et al. (2013) 4 R . 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