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Pigments Content (Chlorophylls, Fucoxanthin and Phycobiliproteins) of Different Commercial Dried Algae

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Pigments Content (Chlorophylls, Fucoxanthin and Phycobiliproteins) of Different Commercial Dried Algae separations Article Pigments Content (Chlorophylls, Fucoxanthin and Phycobiliproteins) of Different Commercial Dried Algae Catarina Osório y, Susana Machado y, Juliana Peixoto ,Sílvia Bessada, Filipa B. Pimentel, Rita C. Alves * and M. Beatriz P. P. Oliveira REQUIMTE/LAQV, Department of Chemical Sciences, Faculty of Pharmacy, University of Porto, Rua Jorge Viterbo Ferreira, 228, 4050-313 Porto, Portugal; [email protected] (C.O.); [email protected] (S.M.); [email protected] (J.P.); [email protected] (S.B.); fi[email protected] (F.B.P.); beatoliv@ff.up.pt (M.B.P.P.O.) * Correspondence: rcalves@ff.up.pt Both authors contributed equally to this work. y Received: 30 April 2020; Accepted: 6 June 2020; Published: 11 June 2020 Abstract: Algae are a complex, polyphyletic group of organisms, affordable and naturally rich in nutrients, but also valuable sources of structurally diverse bioactive substances such as natural pigments. The aim of this work was to evaluate the polar and non-polar pigment contents of different commercial dried algae (brown: Himanthalia elongata, Undaria pinnatifida, Laminaria ochroleuca; red: Porphyra spp.; and a blue-green microalga: Spirulina spp.). The pigment extraction was carried out using different solvents (100% methanol, 100% methanol acid free, 100% ethanol, 90% acetone, N,N-dimethylformamide, dimethyl sulfoxide-water (4:1, v/v) and pH 6.8 phosphate buffer), selected according to their affinity for each class of pigments. Acetone proved to be an efficient solvent to extract chlorophylls from brown and red algae, but not from Spirulina spp. Porphyra spp. presented considerably higher levels of all pigments compared to brown algae, although Spirulina spp. presented significantly higher (p < 0.05) levels of chlorophylls, carotenoids and phycobiliproteins, compared to all macroalgae. The content of fucoxanthin extracted from the three brown algae was highly correlated to the carotenoid content. Within this group, Himanthalia elongata presented the highest fucoxanthin/total carotenoids ratio. Although the yield of extraction depended on the solvent used, the algae studied herein are an interesting source of pigments of great value for a wide range of applications. Keywords: algae; Himanthalia elongata; Undaria pinnatifida; Laminaria ochroleuca; Porphyra spp.; Spirulina spp.; pigments extraction 1. Introduction The oceans cover more than 70% of the Earth’s surface and contain a wide diversity of species (approximately half of the total global biodiversity), including marine algae [1,2]. Algae are a complex, polyphyletic group of (mostly) photoautotrophic organisms that include prokaryotic and eukaryotic members. With over 40,000 species already identified, algae are currently classified into several taxonomic groups such as Chlorophyceae (green algae), Rhodophyceae (red algae), Phaeophyceae (brown algae), Cyanophyceae (cyanobacteria), Xanthophyceae (yellow-green algae), Bacillariophyceae (diatoms) and Dinophyceae (dinoflagellates) [2,3]. Due to their global distribution, accessibility, diversity and nutritional value, algae have been a traditional food source for thousands of years, especially in Asian countries. However, recently, the interest by Western cultures has been growing since algae started to be seen not only as affordable Separations 2020, 7, 33; doi:10.3390/separations7020033 www.mdpi.com/journal/separations Separations 2020, 7, x FOR PEER REVIEW 2 of 14 Separations 2020, 7, 33 2 of 14 interest by Western cultures has been growing since algae started to be seen not only as affordable products and naturally rich in nutrients (such as proteins, dietary fiber, polyunsaturated fatty acids, mineralsproducts and and vitamins), naturally richbut also in nutrients as valuable (such sources as proteins, of structurally dietary fiber,diverse polyunsaturated bioactive substances fatty acids,(e.g., polysaccharides,minerals and vitamins), phenolic but compounds, also as valuable or natural sources pigments) of structurally with diversepotential bioactive health benefits substances [2,4]. (e.g., In fact,polysaccharides, a wide range phenolic of bioactivities compounds, have or natural been pigments) described with for potentialthese compounds, health benefits such [2,4 ].as In anti- fact, hyperlipidemica wide range of bioactivities [5,6], anti-obesity have been [7,8], described anti-dia forbetic these [9,10], compounds, antioxidant such as[11,12], anti-hyperlipidemic anti-inflammatory [5,6], [13–15],anti-obesity antiviral [7,8], anti-diabetic [16,17], antibacterial [9,10], antioxidant [18–20], [11,12 ],antitumoral anti-inflammatory [21,22], [13 –antiallergic15], antiviral [23,24], [16,17], neuroprotectiveantibacterial [18 –[25,26],20], antitumoral cardiovascular [21,22 protective], antiallergic [27,28], [23,24 among], neuroprotective others. [25,26], cardiovascular protectiveIn the [27last,28 few], among years, others. the interest in the natural pigments has been growing exponentially not only Indue the to last their few pharmaceutical years, the interest and in biomedical the natural po pigmentstential [7,13,15,18,21–23,25 has been growing exponentially,29], but also notbecause only theydue tocan their be used pharmaceutical as substitutes and of biomedical artificial dyes/colorants potential [7,13 ,[29–31].15,18,21 The–23, 25basic,29], classes but also of becausepigments they found can inbe algae used asare substitutes chlorophylls, of artificial carotenoids dyes and/colorants phycobilipro [29–31].teins, The characteristics basic classes of that pigments contribute found to in cluster algae algaeare chlorophylls, in different carotenoidsphyla since andthey phycobiliproteins, are, respectively, the characteristics most prevalent that pigments contribute in to Chlorophyceae, cluster algae in Ochrophytadifferent phyla and since Rhodophyceae. they are, respectively, In Cyanobacteri the most prevalenta, phycocyanin pigments is inthe Chlorophyceae, most common Ochrophyta pigment [2,32,33].and Rhodophyceae. In Cyanobacteria, phycocyanin is the most common pigment [2,32,33]. Chlorophylls (chls)(chls) are are greenish, greenish, non-polar non-pola pigmentsr pigments which contain which a porphyrin contain ora hydroporphyrinporphyrin or hydroporphyrinrings centrally bound rings centrally to a magnesium bound to atom a magnesium found in allatom autotrophic found in algae,all autotrophic since they algae, allow since the theyconversion allow the of light conversion into biological of light energy.into biological Figure1 en showsergy. theFigure four 1 kinds shows of the chls four present kinds in of marine chls present algae: inChl marinea, the algae: major Chl and a most, the major important and most chl for important photosynthesis, chl for photosynthesis, and chls b, c and andd [ 34chls,35 b,c]. and d [34,35]. (c) (a) (b) (d) (e) Figure 1. The chemical structure of the chlorophylls present in marine algae: (a) Chlorophyll a; Figure(b) Chlorophyll 1. The chemicalb;(c) Chlorophyll structure ofc1 ;(thed) chloro Chlorophyllphylls c2present;(e) Chlorophyll in marine dalgae:. (a) Chlorophyll a; (b) Chlorophyll b; (c) Chlorophyll c1; (d) Chlorophyll c2; (e) Chlorophyll d. Carotenoids are also non-polar pigments and play a key role in photoprotection by inactivating reactiveCarotenoids oxygen species are also (ROS) non-polar formed pigments during light and exposure.play a key Structurally, role in photoprotection they belong toby the inactivating terpenoid reactiveclass of pigmentsoxygen species and have (ROS) highly formed conjugated during polyene light chainsexposure. which Structurally give them, distinct they belong colors suchto the as terpenoidpurple, red, class orange of pigments or yellow. and They have can highly be classified conjugated into twopolyene different chains groups: which carotenes, give them which distinct are colorsunsaturated such as hydrocarbons purple, red, (e.g., orangeβ-carotene or yellow. and lycopene);They can andbe classified xanthophylls, into whichtwo different are very groups: similar carotenes,to carotenes which but have, are unsaturated at least, one hydrocarbons functional group (e.g., containing β-carotene oxygen and lycopene); (e.g., lutein, and zeaxanthin, xanthophylls, and whichfucoxanthin) are very [36 similar]. Fucoxanthin to carotene (Figures but2) have, is one at of least, the most one abundantfunctional carotenoids group containing (approximately oxygen (e.g., 10% lutein,of the estimatedzeaxanthin, total and production fucoxanthin) of carotenoids [36]. Fucoxanthin in nature) and(Figure is the 2) pigment is one thatof the confers most the abundant color to carotenoidsbrown algae (approximately [37]. 10% of the estimated total production of carotenoids in nature) and is the pigment that confers the color to brown algae [37]. Separations 2020, 7, 33 3 of 14 SeparationsSeparations 20202020,, 77,, xx FORFOR PEERPEER REVIEWREVIEW 33 ofof 1414 Figure 2.2. ChemicalChemical structure structure of of the the fucoxanthin fucoxanthin.fucoxanthin.. Phycobiliproteins are a groupgroup ofof water-solublewater-soluble fluorescentfluorescent compoundscompounds composedcomposed ofof proteinsproteins covalentlycovalently bound bound to to linearlinear tetrapyrrolestetrapyrroles known known as as phycobilinsphycobilins and and areare usedused asas accessoryaccessory pigmentspigments forfor photosyntheticphotosynthetic lightlight light collectioncollection collection [38].[38]. [38 ]. InIn Incyanobacteria,cyanobacteria, cyanobacteria, suchsuch such asas Spirulina as Spirulina,, andand,
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