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Review ArticleBiologically Active Metabolites Synthesized by Microalgae

Michele Greque de Morais,1 Bruna da Silva Vaz,1

Etiele Greque de Morais,2 and Jorge Alberto Vieira Costa2

Laboratory of Microbiology and Biochemistry, College of Chemistry and Food Engineering,Federal University of Rio Grande, P.O. Box , - Rio Grande, RS, Brazil

Laboratory of Biochemical Engineering, College of Chemistry and Food Engineering,Federal University of Rio Grande, P.O. Box , - Rio Grande, RS, Brazil

Correspondence should be addressed to Michele Greque de Morais; [email protected]

Received September ; Revised December ; Accepted January

Academic Editor: Olga Genilloud

Copyright Michele Greque de Morais et al. Tis is an open access article distributed under the Creative CommonsAttribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work isproperly cited.

Microalgae are microorganismsthat havedifferent morphological, physiological, and genetic traits thatconer the ability to producedifferent biologically active metabolites. Microalgal biotechnology has become a subject o study or various elds, due to thevaried bioproducts that can be obtained rom these microorganisms. When microalgal cultivation processes are better understood,microalgae can become an environmentally riendly and economically viable source o compounds o interest, because production

can be optimized in a controlled culture. Te bioactive compounds derived rom microalgae have anti-inammatory, antimicrobial,and antioxidant activities, among others. Furthermore, these microorganisms have the ability to promote health and reduce the risko the development o degenerative diseases. In this context, the aim o this review is to discuss bioactive metabolites produced bymicroalgae or possible applications in the lie sciences.

1. Introduction

Microalgae are unicellular microorganisms that grow in reshor salt water and have varied shapes with a diameter or lengtho approximately m. Te term microalgae includes

prokaryotic and eukaryotic organisms []. Cyanobacteria andbacteria have very similar structural characteristics; however,they are classied as microalgae because they contain chloro-phyll and compounds related to photosynthesis. Te so-called green algae are so named because o the presence ochlorophyll and chlorophyll in the same proportions as inhigher plants [].

Microalgae are photosynthetic organisms that play a keyrole in aquatic ecosystems. Approximately % o global pho-tosynthesis is due to these microorganisms []. Microalgalmetabolism reacts to changes in the external environmentwith changes in its intracellular environment. Tus, themanipulation o the culture conditions, or the presence or

absence o certain nutrients, stimulates the biosynthesis ospecic compounds.

Several studies have been conducted to investigate theproducts o microalgal metabolism not only to understand itsnature but also to search or substances with possible appli-

cations to humans in different elds o interest. Screening oextracts or isolation o metabolites rom different microalgaeis a common method or determining the biological activityo these components. Microalgae have been described as richsources o various biocompounds o commercial interest [].

Bioactive compoundso microalgal origin can be sourceddirectly rom primary metabolism, such as proteins, attyacids, vitamins, and pigments, or can be synthesized romsecondary metabolism. Such compounds can presentantiungal, antiviral, antialgal, antienzymatic, or antibioticactions []. Many o these compounds (cyanovirin, oleic acid,linolenic acid, palmitoleic acid, vitamin E, B,-carotene,phycocyanin, lutein, and zeaxanthin) have antimicrobial

Hindawi Publishing CorporationBioMed Research InternationalVolume 2015, Article ID 835761, 15 pageshttp://dx.doi.org/10.1155/2015/835761
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BioMed Research International

: Principal bioactive compounds extracted rom microalgae.

Microalgae Bioactive compounds Reerence

Spirulinasp. Polysaccharides []

Spirulina platensisPhycocyanin, C-phycocyanin, Phenolic acids, tocopherols(vitamin E), neophytadiene, phytol, PUFAs (n-) attyacids, oleic acid, linolenic acid, palmitoleic acid

[,,]

Spirulina fusiformis Diacylglycerols []

Haematococcus pluvialis Astaxanthin, lutein, zeaxanthin, canthaxanthin, lutein,

-carotene, oleic acid [,,]

Chlorellasp. Carotenoids, sulated polysaccharides, sterols, PUFAs

(n-) atty acids []

Chlorella vulgaris Canthaxanthin, astaxanthin, peptide, oleic acid [,,]

Chlorella minutissima Eicosapentaenoic acid (EPA) []

Chlorella ellipsoidea Zeaxanthin, violaxanthin []

Dunaliella salina trans-Betacarotene,cis-betacarotene,-carotene, oleic

acid, linolenic acid, palmitic acid [,,]

Dunaliella Diacylglycerols []

Botryococcus braunii Linear alkadienes (C, C, C, and C), triene (C) []

Chlorella zongiensis Astaxanthin []

Chlorella protothecoides Lutein, zeaxanthin, canthaxanthin [,]

Chlorella pyrenoidosa Lutein, sulated polysaccharide []

Nostoc linckiaand Nostoc spongiaeforme Borophycin []

Nostocsp. Cryptophycin []

antioxidant, and anti-inammatory capacities, with thepotential or the reduction and prevention o diseases [].In most microalgae, the bioactive compounds are accu-mulated in the biomass; however, in some cases, thesemetabolites are excreted into the medium; these are knownas exometabolites.

Bioactive metabolites o microalgal origin are o specialinterest in the development o new products or medi-cal, pharmaceutical, cosmetic, and ood industries. Furtherresearch should be conducted with these bioactive com-pounds to veriy their benecial effects or humans, theirdegradability when released into the environment, and theireffects when used in animals []. In this context, the aim othis review is to discuss bioactive metabolites produced bymicroalgae or possible applications in the lie sciences.

2. Microalgae with Potential for Obtaining

Bioactive Compounds

Microalgae are a group o heterogeneous microorganismsthat have a great biodiversity o colors, shapes, and cellcharacteristics, and their manipulation is encompassed bythe eld o marine biotechnology. Among the thousands ospecies o microalgae believed to exist, only a small numbero them are retained in collections around the world, andit is estimated that only a ew hundreds are investigated orcompounds present in their biomass. O these, only and aew are industrially cultivated []. Tis untapped diversityresults in potential applications or these microorganisms inseveral biotechnological elds, such as the production o

biocompounds used in ood, medicine, cosmetics, and phar-maceuticals and even in the energy industry [].

Microalgae are a natural source o highly interesting bio-logically active compounds. Tese compounds have receivedmuch attention rom researchers and companies in recentyears due to their potential applications in different liescience elds. Te applications range rom the productiono biomass or ood and eed to the production o bioactivecompounds or the medical and pharmaceutical industries[]. Considering the enormous biodiversity o microalgaeand recent developments in genetic engineering, this groupo microorganisms is one o the most promising sources ornew products and applications [].

Microalgae are autotrophic microorganisms that use lightenergy and inorganic nutrients (carbon dioxide, nitrogen,phosphorus, etc.) to develop and synthesize biocompoundsthat have high aggregated nutritional value and therapeuticunctions, such as lipids, proteins, carbohydrates, pigments,

and polymers. Recent studies have reported that microalgaecan produce different chemical compounds with differentbiological activities, suchas carotenoids, phycobilins, polyun-saturated atty acids, proteins, polysaccharides, vitamins, andsterols among other chemicals [,,].

Components o microalgal origin with antimicrobial,antiviral, anticoagulant antienzymatic, antioxidant, antiun-gal, anti-inammatory, and anticancer activity, among oth-ers, were identied []. Te study o the extractiono bioactive compounds rom various microalgae, such as

Arthrospira (Spirulina), Botryococcus braunii, Chlorella vul-garis, Dunaliella salina, Haematococcus pluvialis, and Nostoc(able ), has been investigated [,,].

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F :Spirulinasp. LEB rom LEB/FURG strains bank.

.. Spirulina. Spirulina(Arthrospira) is prokaryotic cyano-bacteria (Figure ) that belongs to Cyanophyta, which arosemore than million years ago, orming the current oxygenatmosphere, and has been important in the regulation o theplanetary biosphere []. In ,Spirulinawas approved bythe FDA (Food Drug Administration) by the issuance o aGRAS (generally recognized as sae) certicate. Te FDA hasstated that Spirulina can be legally marketed as a ood or oodsupplement without risk to human health [].

Spirulinahas a high protein value and high digestibilityand contains signicantamounts o essential polyunsaturatedatty acids and phenolic compounds []. Due to proper-ties such as its high nutritional value and the presence oactive biocompounds, this microorganism is one o the moststudied microalgae worldwide []. Te Spirulina proteincontent ranges rom to % (w/w) o its dry weight, thecarbohydrate content rom to % (w/w), and the lipidcontent rom to % (w/w).

Tis microalga is rich in vitamins B, B, B, and E (espe-cially vitamin B). Furthermore, Spirulina has a highcontento pigments, minerals, and oligoelements (approximately to % (w/w) biomass dry weight), o which the most impor-tant are iron, calcium, magnesium, phosphorus, and potas-sium []. Some studies have demonstrated the use o thismicroalga or the production o pigments due to its antiox-idant properties []. -Carotene represents approxi-mately % o the carotenoids present in Spirulina, andother components, such as tocopherols, phycocyanin, andphycoerythrin, are also part o its composition [].able shows some o the bioactive compounds that have beenextracted romSpirulina.

Cyanobacteria are known to produce intracellular andextracellular metabolites with potential biological activities,such as antibacterial, antiungal, antiviral, antitumor, anti-HIV, anti-inammatory, antioxidant, antimalarial, herbici-dal, and immunosuppressant effects [,,]. Te thera-peutic importance oSpirulinahas been reported in severalstudies. Tese include its use in the treatment o hyperlipi-demia, cancer, HIV, diabetes, obesity, and hypertension, theimprovement o immune response in renal protection againstheavy metals and drugs, and the reduction in serum levels oglucose and lipids, among others [,,,].

Te worlds largest producer, Hainan Simai Pharmacy Co.(China), annually produces tonnes oSpirulina biomass

F : MicroalgaNostoc ellipsosporumrom LEB/FURG strainsbank.

[]. One o the largest industries in the world is EarthriseFarms (Caliornia, USA) (http://www.earthrise.com/). Manyother companies market a wide variety o nutraceuticalproducts produced rom these microalgae. For example, the

Myanmar Spirulina Factory (Yangon, Myanmar) producespills, French ries, and pasta. Cyanotech (Hawaii, USA)produces and markets products under the name SpirulinaPacica (http://www.cyanotech.com/). In Brazil, the OlsonMicroalgas Macronutricao company (Camaqua, Rio Grandedo Sul) produces Spirulinasp. LEB capsules or sale as adietary supplement (http://www.olson.com.br/).

.. Nostoc. Nostocis an edible microalga that belongs to theNostocaceae group Cyanophyta that orms spherical coloniesthat link together as laments. Tis microalga has heterocystswith a pattern o homogeneous cells and a regular distancebetween cells that compose the lament (Figure ) []. Teheterocysts x atmospheric nitrogen or amino acid synthesisin the microalgal biomass. In the absence o a nitrogen sourceduring microalgal cultivation, heterocysts orm, avoiding thelimitation o this nutrient or cell growth [].

Nostoc microalgal biomass has been used in the medicaleld and as a dietary supplement because o its protein,

vitamin, and atty acid content. Te medical value o thismicroalga was evidenced by its use in the treatment o stulaand or some orms o cancer []. Historically, the biomass othis microorganism is described as anti-inammatory, and italso aids in digestion, blood pressure control, and immuneboosting. Several studies suggest that Nostoc produces severalcompounds with antimicrobial, antiviral, and anticancer

activity. Tese results have encouraged its cultivation on alarge scale, and it has great economic potential due to itsnutritional and pharmaceutical importance []. able presents some bioactive compounds that have been extractedrom the microalga o theNostocgenus.

Cyanovirin, a potential protein molecule produced by aNostocmicroalga, showed a positive effect in the treatment oHIV [] and Inuenza A (HN) []. Nostoc contains aspectrum o polyunsaturated atty acids (PUFAs) that includeessential atty acids, such as linoleic,-linolenic,-linolenic,octadecatetraenoic, and eicosapentaenoic acid []. Essentialatty acids are precursors o prostaglandins, engenderingsignicant interest rom the pharmaceutical industry.

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: Bioactive compounds extracted romSpirulinagenus.

Microalga Bioactive compound Concentration (%, w/w) Reerence

Spirulina fusiformis C-phycocyanin . []

Spirulina platensis C-phycocyanin . []

Spirulina platensis Allophycocyanin . []

Spirulinasp. C-phycocyanin . []Spirulinasp. Allophycocyanin . []

Spirulina platensis Phenolic . []

Spirulina platensis erpenoids . []

Spirulina platensis Alkaloids . []

Spirulina maxima Phenolic . []

Spirulina maxima Flavonoids . []

: Bioactive compounds extracted rom theNostocgenus.

Microalga Bioactive compound Concentration (%) Reerence

Nostocsp. Phycocyanin . (p/p) []

Nostoc muscorum Phenolic . (p/p) []

Nostoc muscorum erpenoids . (p/p) []

Nostoc muscorum Alkaloids . (p/p) []

Nostoc muscorum Phycobilins . (p/v) []

Nostoc humifusum Phenolic . (p/p) []

Nostoc humifusum erpenoids . (p/p) []

Nostoc humifusum Alkaloids . (p/p) []

Nostoc humifusum Phycobilins . (p/v) []

F : Microalga Chlorella fusca LEB rom LEB/FURG strainsbank.

.. Chlorella. SpirulinaandChlorellarepresent the majorityo the microalgal biomass market, with an annual productiono , and , tons, respectively []. Chlorella sp. isa eukaryotic genus o green unicellular microalgae thatbelongs to the Chlorophyta group (Figure ) [].

Tis microalga was discovered by the Japanese, tradi-tional consumers o algae, who usually enjoy it and use itas a ood supplement. Te microalga Chlorella is rich inchlorophyll, proteins, polysaccharides, vitamins, minerals,and essential amino acids. Tis microalga is % (w/w)protein, % (w/w) carbohydrate, % (w/w) lipids, and %(w/w) minerals and oligoelements [].

Tese nutrient concentrations can be varied by manipu-lation o culture conditions. Te biomass o this microalga is

also rich in B complex vitamins, especially B, which arevital in the ormation and regeneration o blood cells. LikeSpirulina,Chlorellahas a GRAS certicate issued by the FDAand can thus be used as a ood without risk to human healthwhen grown in a suitable environment with proper hygieneand good manuacturing practices [,].

Chlorella contains bioactive substances with medicinalproperties. Experimental studies with Chlorella demon-strated their antitumor, anticoagulant, antibacterial, antiox-idant, and antihiperlipidemia effects in addition to a hepato-protective property and the immunostimulatory activity oenzymatic protein hydrolyzate [,].

Many antioxidant compounds may be responsible or

Chlorella unctional activities. Antioxidants such as lutein,-carotene,-carotene, ascorbic acid, and-tocopherol, whichare active against ree radicals, were identied. Some o thesecompounds not only are important as natural colorants oradditives but also may be useul in reducing the incidence ocancerand in the prevention o macular degeneration [, ](able ).

Te most important bioactive compound in Chlorellais -, glucan, an active immunostimulator that reducesree radicals and blood cholesterol. Te efficacy o thiscompound against gastric ulcers, sores, and constipation hasbeen reported. It also has been demonstrated to have preven-tive action against atherosclerosis and hypercholesterolemia,

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: Bioactive compounds extracted rom the microalgae o theChlorellagenus.


Chlorella protothecoides Lutein . []

Chlorella zongiensis Astaxanthin . []

Chlorella vulgaris Phenolic . []

Chlorella vulgaris erpenoids . []Chlorella vulgaris Alkaloids . []

Chlorella minutissima Phytol . []

Chlorella minutissima Phenol . []

5m

F :Dunaliellasp. microalga [].

as well as antitumor activity []. Chlorella is produced by

more than companies. aiwan Chlorella ManuacturingCo. (aipei, aiwan) is the worlds largest producer oChlorella, with over , tons o biomass producedper year (http://www.taiwanchlorella.com/index.php). Sig-nicant production also occurs in Klotze (Germany) (

tyr1 o dry biomass) [].

.. Dunaliella. Dunaliella is a green unicellular halotol-erant microalga that belongs to the Chlorophyceae group(Figure ). Tis microalga is widely studied due to its tol-erance o extreme habitat conditions, physiological aspects,and its many biotechnological applications. Dunaliella is asource o carotenoids, glycerol, lipids, and other bioactive

compounds, such as enzymes and vitamins [,].Tis microalga is a major source o natural -carotene,

able to produce up to % o its dry weight under conditionso high salinity, light, and temperature as well as nutrientlimitation []. In addition to -carotene, this microalgais rich in protein and essential atty acids, which can beconsumed saely, as evidenced by GRAS recognition [].able presents some compounds that have been extractedrom microalgae o theDunaliellagenus.

Compounds in theDunaliellabiomass have various bio-logical activities, such as antioxidant, antihypertensive, bron-chodilatory, analgesic, muscle relaxant, hepatoprotective, andantiedemal properties. Te microalgal biomass can also be

used directly in ood and pharmaceutical ormulations [,].

Chang et al. [] showed that Dunaliellacells containedantibiotic substances. According to these authors, the crudeextract o this microalga strongly inhibited the growtho Staphylococcus aureus, Bacillus cereus, Bacillus subtilis,and Enterobacter aerogenes. In another study, Dunaliellamicroalga also showed antibacterial activity against variousmicroorganisms o importance to the ood industry, includ-ingEscherichia coli,Staphylococcus aureus,Candida albicans,andAspergillus niger[,].

Under ideal growing conditions,Dunaliellacan be stim-ulated to produce approximately mg o-carotene persquare meter o growing area. Te cultivation o Dunaliellaor the production o -carotene has been conducted inseveral countries, including Australia, Israel, the USA, andChina []. An ingredient o Dunaliella with a strongability to stimulate cell prolieration and improve the energymetabolism o the skin was released by Pentapharm (Basel,Switzerland) []. New pilot plants are under development in

India, Chile, Mexico, Cuba, Iran, aiwan, Japan, Spain, andKuwait [].

3. Cultivation Conditions

Te conditions or microalgal cultivation are important ac-tors that inuence the metabolism o these microorganisms,thus directing the synthesis o specic compounds o interest.Several researchers have noted the inuence o incubationtemperature, the pH o the medium, the period o cultivation,as well as salinity, lightintensity, and medium constituents, onthe synthesis o antimicrobial agents [].

.. pH, emperature, and Luminescence. pH adjustments arethe primary measures used to prevent contamination bymicroorganisms, such as other microalgae species. pH con-trol is also essential or effective absorption o the compo-nents o the culture medium because it directly affects theavailability o various chemical elements []. Te reductiono some nutrients in the culture medium can lead the produc-ing o specic biocompounds. Te difficulty o consuminga nitrogen source, or example, can lead microalgae to shifyour metabolism or lipids or carbohydrates production [].

Light is an indispensable actor or photosynthesis, caus-ing the cells to reproduce and thereby increasing the cell

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: Bioactive compounds extracted rom the microalgae o theDunaliellagenus.


Dunaliella salina -Carotene % []

Dunaliella salina All-trans--carotene .% []

Dunaliella salina All-trans-zeaxanthin .% []

Dunaliella salina All-trans-lutein .% []Dunaliella tertiolecta Sterols .% []

Dunaliella salina Sterols .% []

concentration []. Te illuminance also inuences the bio-chemical composition o the biomass []. Te atty acidcontent canbe reduced with increasing light incidence. Tisisbecause lipids are the major components o chloroplasts andthe increased light energy demand greater activity o chloro-plasts []. Studies also show the inuence o illuminanceon the microalgae antioxidants. According to Madhyastha[], the application o blue light in the cultivation o the

microalga Spirulina fusiformisthrough a phenomenon wherethe microalgae cells alter the sequence o amino acids withcysteine repeats enhanced the antioxidant capacity.

One o the most important actors or the growth o allliving organisms is the temperature. Te specic growth rateo the microalgae is directly correlated with the gross rate oCO

2xation/O

2production (photosynthesis) and the respi-

ration rate. Photosynthesis and respiration are temperature-dependent, with the respiration rate increasing exponentiallywith temperature []. emperature has a great inuenceon the production o biomass, proteins, lipids, and phenoliccompounds rom microalgae. Te optimum temperature orcultivation o microalgae is C []. In studies con-ducted by Noaman [] that were perormed to veriywhich culture conditions stimulated the greatest produc-tion o antimicrobial agents by the microalga Synechococcusleopoliensis,it was observed that a temperature o C andpH produced a maximum concentration o this bioactivecompound.

.. Bioreactors. Microalgae have attracted much interest orproduction o bioactive compounds, and in order to growand tap the potentials o algae, efficient photobioreactors arerequired. A good number o photobioreactors can be used inproduction o various algal products []. Innovative culti-

vation systems and modication o biochemical composition

o microalgae by simple changes in the growth media andcultivation conditions (nutrients, light intensity, temperature,pH, mixing, etc.) can lead to higher productivity o thetargeted products [].

Bioreactors can be classied as open or closed. Closedphotobioreactors have attracted much interest because theyallow a better control o the cultivation conditions than opensystems. One o the major advantages o open ponds is thatthey are easier to construct and operate than most closedsystems [].

In open systems, temperature is a main limiting actor,as are variations in solar radiation that lead to low biomassconcentrations. However, open systems are the most widely

used due to their economic viability. Closed systems aregenerally used on a pilot scale or investigating problemsrelated to economic viability. Furthermore, the use o closedsystems is primarily used or microalgal species that do notgrow in a highly selective medium, avoiding contaminationo the cultures [].

Closed bioreactors can provide high productivity, gen-erating greater microalgal biomass per unit time. Other

advantages o the use o closed bioreactors compared withopen systems include the ollowing: (i) virtually zero losses inconnection with evaporation; (ii) a marked reduction oproblems related to culture contamination by heterotrophicalgae or other microorganisms; (iii) ease o biomass collectionprocedures due to smaller volumes o culture medium; (iv)greater control o gas exchange between the culture andthe atmosphere; (v) a smaller occupied space; (vi) a highsurace:volume ratio, which helpsto increase the illuminationo the system; and(vii) the possibility o obtaining highpuritycultures [].

.. Nutrients. Te metabolism o microalgae can beautotrophic or heterotrophic. Te ormer requires onlyinorganic compounds, such as CO

2, salts, and solar energy;

the latter is not photosynthetic, requiring an external sourceo organic compoundsor useas a nutrient and energy source.Some photosynthetic species are mixotrophic, having theability to perorm photosynthesis and use exogenous organicsources simultaneously [].

Microalgaereactto changes in theirexternal environmentwith changes in their intracellular environment. Tus, themanipulation o the culture conditions or the presence orabsence o nutrients stimulates the biosynthesis o speciccompounds. Tis act was rst reerenced by Richmond[], who changed the composition o Chlorella biomass,

particularly in their protein and lipid content, by varyingcultivation conditions.

Noaman [] ound that leucine combined with citrateor acetate is the sources o nitrogen and carbon that pro-duced higher concentrations o antimicrobial agents in themicroalgaSynechococcus leopoliensis. Coca et al. [], study-ing the cultivation oSpirulina platensis in a medium sup-plemented with vinasse, obtained an increased protein yieldcompared to the unsupplemented culture medium. Ip andChen [], studying the cultivation oChlorella zongiensisunder mixotrophic cultivation conditions, ound that lowconcentrations o nitrate and a high glucose concentrationavored the production o astaxanthin in this microalga.

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Alonso et al. [], studying the inuence o nitrogen con-centration in continuous cultivation on lipid concentrationin Phaeodactylum tricornutum, noted that there was accu-mulation o saturated and unsaturated atty acids when thenitrogen source was reduced.

Culture media are chemical preparations that are ormu-

lated to contain the nutrients necessary or the microorgan-isms to multiply and/or survive. Te culture media shouldmeet the nutritional needs o the microorganism, assist inprocess control, and have a reasonably xed composition[].

Among different microalgae, variations in the culturemedium are mainly related to the amount o necessary nutri-ents. Even so, nutritional needs are dependent on environ-mental conditions []. Microalgae require macronutrients,such as C, N, O, H, P, Ca, Mg, S, and K, or their growth.Te micronutrients that are generally required are Fe, Mn,Cu, Mo, and Co. Additionally, some species require lowerconcentrations o vitamins in the culture medium [].

4. Advantages of Using Microalgae to ObtainBioactive Compounds

Microalgae are important sources o bioactive natural sub-stances. Many metabolites isolated rom these microorgan-isms have shown biological activities and potential healthbenets []. Microalgae accumulate specic secondarymetabolites (such as pigments and vitamins) which are high

value products that have applications in the cosmetic, ood,or pharmaceutical industries [,].

Microalgae live in complex habitats and are subjectedto stress and/or extreme conditions, such as changes insalinity, temperature, and nutrients. Tus, these microorgan-isms must rapidly adapt to new environmental conditions tosurvive and thus produce a great variety o biologically activesecondary metabolites that are not ound in other organisms[]. Some o the advantages o microalgal cultivation maybe associated with taxonomic diversity, the diverse chemicalcomposition, the potential or growth in a bioreactor undercontrolled conditions, and the ability to produce activesecondary metabolites in response to the stress induced byextreme exposure conditions [,].

In addition to their natural characteristics, other impor-tant aspects related to microalgae are the use o solar energyand carbon dioxide (CO

2) and a high growth rate which

can produce higher yields compared to higher plants. Inaddition, microalgae can be grown in areas and climates thatare unsuitable or agriculture; thereore, microalgae do notcompete with arable ood production land. Te possibility ocontrolling the production o certain bioactive compoundsby manipulation o culture conditions is another advantageo using microalgae [,].

Te cultivation o microalgae is a major mechanism orreducing excess carbon dioxide (CO

2) in the atmosphere by

bioxation, in which an industrial process uses a CO2-rich

gasas a carbon sourceor microalgal growth. Tismechanismcontributes to a reduction o the greenhouse effect and globalwarming, urther reducing the costs o the carbon source

or growth, which is the greatest nutrient requirement ormicroalgae [,].

Te cultivation o microalgae is not seasonal; they areimportant or ood in aquaculture systems and can effectivelyremove pollutants, such as nitrogen and phosphorus, romwastewater. Moreover, they are the most efficient solar energy

biomass converters. Microalgae cultivation via sunlight-dependent systems contributes to sustainable developmentand natural resource management [].

Te integration o the production process o bioactivemetabolites in a biorenery is a sustainable means o energyproduction, ood production, andthe production o productswith high added value []. Te biorenery concept based onmicroalgae depends on the efficient use o biomass throughractionation, resulting in several isolated products. Tis con-cept encompasses a biorenery platorm, which is capable ooffering a wide variety o different products, such as productswith applications in pharmaceuticals, medicine, ood (pro-tein, ber), and biouels [,]. Tese benets contribute tothe economic viability o microalgal production [,].

5. Bioactive Compounds

Bioactive compounds are physiologically active substanceswith unctional properties in the human body. Tere is greatenthusiasm or the development and manuacture o variousbiocompounds that can potentially be used as unctionalingredients, such as carotenoids, phycocyanins, polyphenols,atty acids, and polyunsaturated compounds [].

An interest in the production o bioactive compoundsrom natural sources has recently emerged, driven by agrowing number o scientic studies that demonstrate thebenecial effects o these compounds on health []. Naturalproducts are important in the search or new pharmaco-logically active compounds. In general, they play a role indrug discovery or the treatment o human diseases [].Many clinically viable and commercially available drugs withantitumor and antiinective activity originated as naturalproducts.

Microalgae are a natural source o interesting biocom-pounds. Microalgae are known to produce various therapeu-tically effective biocompounds that can be obtained rom thebiomass or released extracellularly into the medium [].Tese microorganisms contain many bioactive compounds,such as proteins, polysaccharides, lipids, vitamins, enzymes,

sterols, and other high-value compounds with pharmaceu-tical and nutritional importance that can be employed orcommercial use [].

.. Compounds with Antioxidant Function. Oxidative dam-age caused by reactive oxygen species to lipids, proteins, andnucleic acids can cause many chronic diseases such as heartdisease, atherosclerosis, cancer, and aging. Epidemiologicalstudies have demonstrated an inverse association between theintake o ruits and vegetables and mortality rom diseasessuch as cancer. Tis phenomenon can be attributed to theantioxidant activity o these oods [].

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Microalgal biomass is considered a rich natural source oantioxidants, with potential applications in ood, cosmet-ics, and medicine []. Antioxidant compounds, such asdimethylsuloniopropionate and mycosporine amino acids,were isolated rom microalgae andare potentchemical block-ers oUV radiation []. Inadditionto these compounds, pig-

ments, lipids, and polysaccharides with antioxidant activitycan also be ound in microalgal biomass.Carotenoids and phycocyanins are the pigments most

used in scientic research. C-phycocyanin (C-PC) is a bluephotosynthetic pigment that belongs to the group o phyco-biliproteins ound in large quantities in the cyanobacteria,Rhodophyta, and Cryptophyte []. Phycocyanin has appli-cations as a nutrient and natural ood colorants and cosmet-ics. It is usually extracted rom the biomass oSpirulina[]andPorphyridium cruentum[] andSynechococcus[].

Among the carotenoid compounds, -carotene andastaxanthin are prominent. Tese compounds have appli-cation in the ood and pharmaceutical industries becauseo their antioxidant properties and pigmentation ability. Inmicroalgal metabolism, they protect photosynthetic tissuesagainst damage caused by light and oxygen []. Dunaliellasalinais a microalga recognized as a major biological sourceo -carotene pigment, producing more than % in drybiomass [].H. pluvialis is a source o the pigment astax-anthin, producing % o astaxanthin as dry biomass [].

Polysaccharides represent a class o high value-addedcomponents with applications in ood, cosmetics, abrics, sta-bilizers, emulsiers, and medicine []. Microalgal polysac-charides contain sulphate esters, are reerred to as sulatedpolysaccharides, and possess unique medical applications.Te basic mechanism o therapeutic action is based on thestimulation o macrophages and modulation. Te biologicalactivity o sulur polysaccharides is linked to their sugarcomposition, position, and degree o sulation []. Amongthe microalgae capable o producing these compounds areChlorella vulgaris, Scenedesmus quadricauda [], and Por-

phyridiumsp. [].

.. Compounds with Antimicrobial Activity. Te importanceo discovering new compounds with antimicrobial activityis driven by the development o antibiotic resistance inhumans due to constant clinical use o antibiotics. Microalgaeare an important source o antibiotics with a broad andefficient antibacterial activity []. Te antimicrobial activity

o these microorganisms is due to the ability to synthesizecompounds, such as atty acids, acrylic acids, halogenatedaliphatic compounds, terpenoids, sterols, sulur-containingheterocyclic compounds, carbohydrates, acetogenins, andphenols [].

Te antimicrobial activity o extracts rom microalgae isrelated to its lipid composition. Te antimicrobial action omicroalgae is also noteworthy because o the potential toproduce compounds such as- and-ionone,-cyclocitral,neophytadiene, and phytol []. Microalgae antimicrobialactivity against human pathogens, such as Escherichia coli,Pseudomonas aeruginosa, Staphylococcus aureus,andStaphy-lococcus epidermidis, has been attributed to -linolenic acid,

eicosapentaenoic acid, hexadecatrienoic acid, docosahex-aenoic acid, palmitoleic acid, lauric acid, oleic acid, lacticacid, and arachidonic acid [,].

Te mechanism o action o atty acids affects variousstructures in microorganisms; however cell membranes arethe most impacted. Membrane damage most likely leads

to a loss o internal substances rom the cells, and theentry o harmul components reduces nutrient absorption, inaddition to inhibiting cellular respiration. Te ability o attyacids to interere with bacterial growth depends on boththeir chain length and the degree o unsaturation. Fatty acidswith more than carbon atoms apparently induce lysis obacterial protoplasts [].

Microbial polysaccharides and other biological com-pounds have antiviral and antimicrobial action. Microalgaeproduce extracellular sulated polysaccharide (EPS) withacidic characteristics that has a potential as a therapeuticagent []. Highly sulated antiviral polysaccharides romseveral species o microalgae consist mainly o xylose, glu-cose, and galactose. Te EPS sulate groups determine somecharacteristics o polysaccharides; it has been ound thathigher sulphate contents induced higher antiviral activities[,]. Te inhibitory effect o polysaccharides o microal-gal origin is due to viral interactions or positive charges onthe cell surace, thereby preventing penetration o the virusinto host cells [].

Te cyanobacteriumSpirulina(Arthrospira) can producesulated polysaccharides that have already ound applicationsas antiviral agents, bothin vivoandin vitro[]. Eukaryoticmicroalgae, such asChlorellasp. andDunaliellasp., produceand secrete polysaccharides at relatively high levels []. Teantibacterial ability oSpirulina has been correlated withtheir volatile composition, resulting in the identication o elements, which constitutes % o total compounds. Temajor volatile components produced bySpirulinaconsist oheptadecane (%) and tetradecane (%) [].

Some studies have reported that sulated polysaccharidesderived rom microalgae inhibit viral inection, such asencephalomyocarditis virus, Herpes simplex virus types and (HSV, HSV), human immunodeciency virus (HIV),hemorrhagic septicemia in salmonid virus, swine ever virus,and varicella virus [, ]. Carrageenan is a sulatedpolysaccharide that can directly bind to human papillo-mavirus to inhibit not only the viral adsorption process butalso the input and subsequent process o the uncoating o the

virus [].

.. Compounds with Anti-Inammatory Action. Inam-mation is an immediate reaction to a cell or tissueinjury caused by noxious stimuli, such as toxins andpathogens. In this situation, the body recognizes theagents responsible or the attack and attempts to neu-tralize them as quickly as possible. Inammation causesredness, swelling, heat, and pain, usually located at thesite o inection []. Ingestion o anti-inammatory com-pounds enhances the bodys immune response and helpsto prevent disease and aids the healing process. Microal-gae produce several anti-inammatory compounds in their

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biomass that may exert a protective unction in the bodywhen consumed as ood or used as pharmaceuticals andcosmetics.

Because o its anti-inammatory capabilities, microalgalbiomass is being considered or applications in tissue engi-neering or the development o scaffolds, or use in reconsti-

tution o organs and tissues [,]. Tis is an importantapplication or humans, especially in patients with burnsin which the skin was completely lost []. Among themost important microalgal compounds with such prop-erties are long-chain polyunsaturated atty acids (PUFAs)[, ], sulurized polysaccharides [], and pigments[].

Many microalgal polysaccharides possess the ability tomodulate the immune system through the activation omacrophage unctions and the induction o reactive oxy-gen species (ROS), nitric oxide (NO), and various othertypes o cytokines/chemokines []. Macrophages are ableto regulate several innate responses and secrete cytokines

and chemocytokines that serve as signals or immune andinammatory molecular reactions []. Sulur polysaccha-rides with anti-inammatory activity can be applied inskin treatments inhibiting the migration and adhesion opolymorphonuclear leukocytes []. Guzman et al. []studied the anti-inammatory capacity o the microalgaChlorella stigmatophoraandPhaeodactylum tricomutumandconcluded that both microalgae showed positive responses inthe test o paw edema by carrageenan.

Te PUFAs, especially and as eicosapentaenoic(EPA), docosahexaenoic (DHA), and arachidonic (AA) acids,have been applied in the treatment o chronic inammationsuch as rheumatism and skin diseases []. Ryckebosch et

al. [] evaluated the nutritional value o the total lipidsextracted rom different PUFAs produced by microalgae. Inthis study, the microalgaeIsochrysis,Nannochloropsis, Phaeo-dactylum, Pavlova,and Talassiosiraproduced PUFA asan alternative to sh oil in ood.

Among the pigments with anti-inammatory activity,ucoxanthin carotenoid ound in diatoms [,] is capableo stimulating apoptosis in human cancer cells []. A phy-cocyanin, ound in cyanobacteria, has an anti-inammatoryactivity that occurs through the inhibition o histaminerelease [,].

.. Compounds with Potentiality over Degenerative Dis-

eases. In humans, the oxidation reactions driven by reactiveoxygen species (ROS) can lead to irreversible damage tocellular components, including lipids, proteins, and DNAdegradation and/or mutation. Consequently, this damagecan lead to several syndromes, such as cardiovascular dis-ease, some cancers, and the degenerative diseases o aging[].

Chronic age-related diseases involve oxidative stress andinammation and theirconsequences. Chronic inammationplays a signicant role in the mediation o neurodegenerativediseases such as Parkinsons disease, Alzheimers disease,multiple sclerosis, acquired immunodeciency syndrome(AIDS), and dementia complex [].

Natural pigments derived rom microalgae (NPs) haveneuroprotective properties, being valuable sources as unc-tional ingredients in oods and pharmaceutical products thatshow efficient action in the treatment and/or prevention oneurodegenerative diseases. Vitamin E has preventive effectsor many diseases, such as atherosclerosis and heart disease,

as well as neurodegenerative diseases, such as multiplesclerosis [].

Carotenoids have great potential benets to humanhealth, including the treatment o degenerative diseases, suchas macular degeneration and cataract development. Tesecompounds act as antioxidants, reducing oxidative damageby ROS. Studies indicated that increased intake o phenolsdecreased the occurrence o degenerative diseases. Phenoliccompounds rom microalgae with the potential to ght reeradicals have been reported [].

Dunaliella salinais a natural source o-carotene, whichproduced a reduced risk o cancer and degenerative diseasesin humans. Lutein is effective against various diseases, includ-

ing cataracts and macular degeneration, and in the earlystages o atherosclerosis. Extracts oChlorellasp. containing-carotene and lutein signicantly prevented the cognitivedisability that accompanies Alzheimers disease in rats. It wasalso reported that lutein extracted rom Chlorella reducedthe incidence o cancer. Likewise, carotenoids extractedromChlorella ellipsoideaandChlorella vulgarisinhibited thegrowth o colon cancer []. A lycopene extracted romthe microalgae Chlorella marina signicantly reduced theprolieration o prostate cancer in mice []. Tis compoundalso reduced total cholesterol and low-density lipoprotein(LDL) levels [] and improved rheumatoid arthritis [].

Low plasma levels o lutein have also been associated

with an increased tendency o myocardial inarction, whereashigh intake o lutein was related to a decreased risk ostroke. In addition, high levels o carotenoids with provi-tamin A activity, including -carotene, -carotene, and -cryptoxanthin, have been associated with reduction in therisk o angina pectoris. Macular degeneration, the lead-ing cause o irreversible vision loss, has also been associ-ated with very low consumption o lutein and zeaxanthin[].

Scientic ndings indicate astaxanthin or multimodalintervention or many orms o degenerative diseases, includ-ing cardiovascular diseases, cancer, metabolic syndrome,cognitive impairment, age-related immune dysunction,

stomach and ocular diseases (macular degeneration, cataract,glaucoma, diabetic retinopathy, and retinitis pigmentosa),and skin damage []. High levels o lycopene in plasmaand tissues were inversely related to coronary heart disease,myocardial inarction, and the risk o atherosclerosis [].

.. Compounds with Health Promoting Function. Te impor-tance o microalgae as sources o unctional ingredients hasbeen recognized because o their benecial health effects.Natural pigments are valuable sources o bioactive com-pounds. Tese pigments have various benecial biologicalactivities such as antioxidant, anticancer, anti-inammatory,antiobesity, antiangiogenic, and neuroprotective action and

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are indicated or the treatment or prevention o severalchronic diseases [].

Te antioxidant potential o carotenoid pigments andtheir ability to prevent cancer, aging, atherosclerosis, coro-nary heart disease, and degenerative diseases have beendescribed. -Carotene has higher provitamin A activity,

which is essential or vision and the correct unctioning othe immune system. Astaxanthin is linked to many healthbenets such as protection against lipid peroxidation, age-related macular degeneration, reduced atherosclerosis, andan increased immune response [].

Fucoxanthin is considered as a promising dietary andweight loss supplement and or the treatment o obesity.Clinical studies by Abidov et al. [] demonstrated the effecto xanthigen, a ucoxanthin based antiobesity supplement.Furthermore, ucoxanthin maybe useul or the prevention obone diseases such as osteoporosis and rheumatoid arthritis.It has also been reported to be effective or the therapeutictreatment o diabetic diseases, suppressing insulin and hyper-glycemia [].

Microalgae proteins are o great interest as a source obioactive peptides due to their therapeutic potential in thetreatment o various diseases []. Proteins, peptides, andamino acids have unctions that contribute to health benets.Tese compoundscan include growth actors, hormones, andimmunomodulators and can help to replace damaged tissues,in addition to providing nutritional benets. Microalgae,such as Chlorella and Spirulina (Arthrospira), may be usedas nutraceuticals or included in unctional oods to preventdiseases and damage to cells and tissues due to their richprotein content and amino acid prole [].

Te antimicrobial action o certain enzymes (e.g.,lysozyme) and immunoglobulins has been reported andrecommended or people with different diseases (e.g.,Crohns disease) due to the existence o ormulations withpeptides and ree amino acids. Studies o the healtheffects o lysozyme have been reported in the microalgaeSpirulina platensis [], Chlorella [], and Dunaliellasalina []. Spirulina (Arthrospira) and Chlorella biomasspills are marketed, as is Hawaiian Spirulina Pacica(http://spirulina.greennutritionals.com.au/). Other proteinscan also increase the production o cholecystokinin involvedin appetite suppression and the reduction o LDL-cholesterol.Protein peptides rom Chlorella have a potential as dietarysupplements or the prevention o oxidative stress-relateddiseases, such as atherosclerosis, coronary heart disease, and

cancer [].Te essential atty acids, - and - in particular, are

important or the integrity o tissues. -Linolenic acid hastherapeutic applications in cosmetics, to revitalize the skinand thus slow aging. Linoleic and linolenic acids are essentialnutrients or the immune system and other related tissueregeneration processes. Linoleic acid is also used or thetreatment o hyperplasia o the skin [].

Te most studied microalgal lipid compounds are thepolyunsaturated atty acids (PUFAs) docosahexaenoic acid(- C:) (DHA), eicosapentaenoic acid (C -:)(EPA), andarachidonic acid (- C:) (ARA). Studies haveshown that dietary- PUFAs have a protective effect against

atherosclerotic heart disease []. DHA and EPA showed theability to reduce problems associated with strokes and arthri-tis, besides reducing hypertension, lipid content (a decreasein triglycerides and an increase o HDL) and acting asanti-inammatory agents. DHA is also important in thedevelopment and unction o the nervous system. Further-

more, ARA and EPA are platelet aggregators, vasoconstric-tors, and vasodilators and have antiaggregative action on theendothelium, as well as chemostatic activity in neutrophils[].

Other lipid compounds with interesting bioactive prop-erties are the microalgal sterols. Phytosterols have demon-strated reduction o total cholesterol (LDL) in humans byinhibiting its absorption rom the intestine []. Polysac-charides can be considered as dietary bers associatedwith different physiological effects. Insoluble ber (cellulose,hemicellulose, and lignin) mainly promotes the movemento material through the digestive system, thereby improvinglaxation andincreasing satiety. Tey can also be considered asprebiotics because theypromote thegrowth o gutmicroora,including probiotic species. Soluble ber (oligosaccharides,pectins, and-glucans) may reduce cholesterol and regulateblood glucose [,].

6. Conclusion

Te proven ability o microalgae to produce bioactive com-pounds places these microorganisms in the biotechnologicalspotlight or applications in various areas o study, especiallyin the lie sciences. Te production o microalgal metabolites,which stimulate deense mechanisms in the human body,has spurred intense study o the application o microalgal

biomass in various oods and pharmacological and medicalproducts. Tere is obviously a need or urther study o theidentied compounds and their activities in the treatmentand prevention o various diseases, in addition to an ongoingsearch or other, as yet undetected, metabolites.

Conflict of Interests

Te authors declare that there is no conict o interestsregarding the publication o this paper.

Acknowledgment

Te authors thank the National Counsel o echnologicaland Scientic Development (CNPq) or the Productivityin echnological Development and Innovative ExtensionScholarship.

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