Seaweeds as a Functional Ingredient

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This entry is adapted from the peer-reviewed paper 10.3390/md18060301

Seaweeds are autotrophic organisms of simple structure with little or no cellular differentiation and complex tissues, so they are talophytes. They are classified taxonomically into three groups—Chlorophyta, Phaeophyceae, and Rhodophyta, corresponding to green, brown, and red algae, respectively.

seaweeds lipids proteins dietary fibre polyphenols functional food

1. Introduction

For several centuries, there has been a traditional use of seaweed as food in China, Japan, and Korea, as well as in some Latin American countries such as Mexico. The migration of the people from these countries around the world has meant that this custom has moved with them, so today, there are many more countries where seaweed consumption is not unusual. In recent years, there has been a strong movement in France to introduce seaweed into European cuisine, with some success, although it is still considered an exotic component of the menu. It has gained more acceptance in regions such as California and Hawaii, where Japanese communities are larger, and the taste for seaweed is spreading to the surrounding population as it is found in restaurant dishes and on supermarket menus. In fact, in Austria and Germany, seaweeds are being used to produce a highly prized bread—algenbrot, a blend of cereals whose composition is up to 3% seaweed. In Brittany, dulse and kombu are used to make the bara mor or “bread of the sea,” and minced seaweed in butter (beurre des algues) is used for cooking fish or spreading on bread to accompany shellfish ^[1].

2. Nutritional Evaluation of Algae

The chemical composition of algae depends on the species, place of cultivation, atmospheric conditions, and harvesting period. From a nutritional point of view (Table 1), algae are an important source of proteins and lipids. In general, protein contents was higher in green and red seaweeds (10–47% of dry weight—DW) than those found in brown seaweeds (5–24% DW); in lipids (from 0.79% to 7.87% dry matter), ω-3 and ω-6 polyunsaturated fatty acids (PUFAs) constitute a significant part of the lipid profile of seaweeds ^[2]^[3]^[4]^[5]^[6]^[7]^[8].

On the other hand, dietary fiber is recognized today as an important element for healthy nutrition. However, there is no universal definition or analytical method that measures the food components that exert the physiological effects of fiber, but there is consensus that the definition should include the physiological role of dietary fiber ^[9]. Therefore, it can be said that dietary fiber consists of a series of compounds comprising a broad mixture of carbohydrates and polymers present in plants, including both oligosaccharides and polysaccharides, such as cellulose, hemicellulose, pectic substances, gums, resistant starch, and inulin, which may be associated with lignin and/or other non-carbohydrate components (polyphenols, waxes, saponins, cutins, and resistant protein) ^[10].

Table 1. Chemical composition of different algae (g/100 g dry weight—DW).

Seaweed	Protein	Lipids	Ashes	Ref.
Chlorophyta
Caulerpa lentillifera	9.26 ± 0.03	1.57 ± 0.02	22.20 ± 0.27	^[11]
Ulva clathrata	27.2 ± 1.1	2.2 ± 0.1	27.5 ± 0.2	^[3]
Ulva lactuca	8.46 ± 0.01	7.87 ± 0.10	19.59 ± 0.51	^[4]
Rhodophyta
Chondrus crispus	27.2 ± 1.4	2.0 ± 0.1	21.1 ± 0.1	^[12]^[13]^[14]
Garateloupia turuturu	22.9 ± 2.0	2.6 ± 0.1	18.5 ± 0.6	^[2]
Jania rubens	11.28 ± 0.10	2.05 ± 0.09	44.03 ± 0.45	^[15]
Porphyra/Pyropia spp.	26.6 ± 6.3	2.1 ± 1.2	20.6 ± 0.2	^[7]^[12]
Pterocladia capillacea (formerly Pterocladia capillacea)	20.67 ± 0.03	2.19 ± 0.09	17.50 ± 0.28	^[15]
Phaeophyceae
Ascophyllum nodosum	8.70 ± 0.07	3.62 ± 0.17	30.89 ± 0.06	^[16]
Bifurcaria bifurcata	8.92 ± 0.09	6.54 ± 0.27	31.68 ± 0.41	^[16]
Durvillaea antarctica	11.6 ± 0.9	4.3 ± 0.6	25.7 ± 2.5	^[5]
Fucus vesiculosus	12.99 ± 0.04	3.75 ± 0.20	20.71 ± 0.04	^[16]
Laminaria spp.	6.3 ± 3.8	1.0 ± 0.3	37.6 ± 0.4	^[7]^[12]
Saccharina latissima	25.70 ± 0.11	0.79 ± 0.07	34.78 ± 0.08	^[6]
Sargassum fusiforme	10.9 ± 1.0	1.4 ± 0.1	-	^[7]
Undaria pinnatifida	18.9 ± 9.8	4.5 ± 0.7	39.3 ± 0.2	^[7]^[12]

Dietary fiber consists of two fractions (soluble and insoluble), and its properties are mainly determined by the proportion of these two fractions. Thus, soluble fiber is characterized by its ability to form viscous gels, in contact with water, in the intestinal tract. Insoluble fiber does not form gels in contact with water but is capable of retaining water in its structural matrix, producing an increase in fecal mass that accelerates intestinal transit. These differences in the behavior of the fibers in the intestinal transit result in different properties. Insoluble fiber is sparsely fermented and has a marked laxative and intestinal regulating effect, while soluble fiber is fermented in high proportion, and its main properties are related to the decrease of cholesterol and glucose in blood and the development of intestinal microbiota ^[17].

Algae are distinguished by the composition of the structural polysaccharides of the cell wall and reserve. Most of these polysaccharides can be considered as fiber, as they are not digested by human enzyme equipment, although some are degradable by enzymes produced by colonic bacteria ^[18]. The proportion of dietary fiber is considerable, ranging from 36% to 60% of its dry matter ^[19], with soluble dietary fiber being very high (approximately 55–70%) compared to terrestrial vegetables ^[20]. Within algae, the soluble fiber content is usually higher in red algae (15–22% dry weight) as in Chondrus and Porphyra (Nori) ^[21]^[22]. On the other hand, brown algae such as Fucus or Laminaria/Saccharina, have a higher insoluble fiber content (27–40% dry weight) ^[21]^[23]. Table 2 presents the dietary fiber values of different algae. Seaweeds have a high proportion of soluble fiber ^[24]^[25], with an average content of 24.5 g/100 g and 21.8 g/100 g for insoluble fiber. Finally, the ratio fiber soluble/fiber insoluble (S/I) is greater than the values observed in terrestrial vegetables.

Table 2. Dietary fiber content in different algae (g/100 g).

Seaweed	Soluble Fiber	Insoluble Fiber	Ref.
Chlorophyta
Caulerpa lentillifera	17.21 ± 0.87	15.78 ± 1.20	^[26]
Enteromorpha spp.	17.2	16.2	^[27]
Ulva spp. (formerly Enteromorpha spp.)	21.9 ± 0.9	18.7 ± 2.1	^[3]
Ulva spp. (formerly Enteromorpha spp.)	20.53 ± 0.28	34.37 ± 0.7	^[4]
Rhodophyta
Chondrus crispus	22.25 ± 0.99	12.04 ± 2.89	^[22]
Garateloupia turuturu	48.1 ± 1.0	12.3 ± 1.2	^[2]
Porphyra/Pyropia spp.	17.9	16.8	^[27]
Phaeophyceae
Durvillaea antarctica	27.7 ± 1.2	43.7 ± 0.3	^[5]
Himanthalia elongata	23.63 ± 0.48	13.51 ± 0.45	^[6]
Himantalia elongata	25.7	7.0	^[27]
Saccharina latissima	17.12 ± 0.84	13.11 ± 0.56	^[6]
Sargassum fusiforme	32.9	16.3	^[27]
Undaria pinnatifida	30.0	5.3	^[27]

Marine algae, because they live in an environment with a very high concentration of salts, need to accumulate solutes that allow to regulate the osmotic balance between their cells and the environment. Many ions such as sodium, chlorine, and potassium are involved in this process, but certain low molecular weight carbohydrates are also involved ^[28]. These include, for example, sucrose in green algae, alditols such as mannitol in brown and red algae ^[28], and hexitols such as digeneasides and fluorosides in red algae ^[29]. In addition, the main low molecular weight carbohydrate present in many species of brown algae, especially in Laminaria and Ecklonia, is mannitol. Mannitol content is <10% of dry weight in Ascophyllyum nodosum and Laminaria hyperborea species, although it is also subject to many seasonal variations, reaching maximum levels of up to 25% of dry weight in autumn ^[21]. Finally, seaweeds also contain a high concentration of carbohydrates such as structural, storage, and functional polysaccharides, with values between 20% and 70%. However, they are not a good source of carbohydrates in terms of bioavailability ^[20] due to the high proportion of soluble dietary fiber between 55–70%.

The algae acquire from the marine environment, in which they live, a great wealth of mineral elements, being known for its high content of minerals between 8–40% of the dry weight of the seaweed (Table 3). They are worth highlighting the great abundance of essential minerals such as sodium, calcium, magnesium, potassium, chloride, sulfate, phosphorus, and micronutrients such as iodine, iron, zinc, copper, selenium, molybdenum, fluoride, manganese, boron, nickel, cobalt, etc. ^[16]. However, the mineral composition may vary depending on the taxonomic group, geographical, seasonal and physiological variations ^[30], and even with the type of processing and mineralization method applied ^[31]. Algae are a primary source of iodine, providing the daily iodine requirement (150 μg/day) ^[20]. Because of their high mineral content, algae can be used as a dietary supplement to help achieve the recommended daily amounts of some macro minerals and trace elements.

Algae, besides being an important source of minerals, are an excellent source of vitamins ^[32]. Algae, depending on their habitat, season, and species, vary in vitamin content, but almost all spend a lot of time exposed to direct sunlight in a watery environment. As a result, algae contain many forms of antioxidants, including vitamins and protective pigments. Seaweeds contain both water- and fat-soluble vitamins ^[33]^[34]. In this regard, algae are an excellent source of vitamins A, B1, B12, C, D, and E; riboflavin; niacin; pantothenic acid; and folic acid ^[32]. Water-soluble vitamins such as vitamin C are present in large amounts in laver (Porphyra umbilicalis), sea spaghetti (Himanthalia elongata), Crassiphycus changii (formerly Gracilaria changii) ^[35]^[36], and brown seaweed Ecklonia arborea (formerly Eisenia arborea) ^[37].

Algae also are a good source of B-group vitamins (particularly B1 and B12), as well as the lipophilic vitamin A (derived from β-carotene) and vitamin E (tocopherols) ^[38]^[39]. Finally, seaweed foods offer one of the few vegetarian alternatives for cobalamin (vitamin B12) in the diet. Cobalamin is not required or synthesized by higher plants ^[40], so fruits and vegetables are poor sources of vitamin B12, which explains why vitamin B12 deficiency is common among people following strict vegetarian or vegan diets ^[41]^[42]^[43].

Table 3. Mineral content in different algae (mg/100 g DW).

	Macro-Minerals					Micro-Minerals
Seaweed	Ca	K	Mg	Na	P	Fe	Mn	Zn	Cu	Ref.
Chlorophyta
Caulerpa lentillifera	1874.7	1142.7	1028.6	8917.5	-	21.37	-	3.51	0.11	^[26]
Ulva rigida	524.5	1561.0	2094.1	1595.0	210.0	283.0	1.60	0.60	0.50	^[44]
Rhodophyta
Chondrus crispus	420.0	3184.0	732.0	4270.0	-	3.97	1.32	7.14	<0.50	^[12]
Ellisolandia elongata (formerly Corallina mediterranea)	45,075.2	759.3	4977.4	2457.7	-	27.70	6.27	3.02	0.69	^[45]
Jania rubens	42,344.0	327.5	2986.6	2086.2	-	47.50	9.53	2.63	0.36	^[45]
Palmaria palmata	1000.0	2700.0	200.0	1100.0	500.0	31.56	3.59	2.85	0.56	^[46]
Porphyra umbilicalis	687.0	1407.0	283.3	1173.0	0.025	18.20	2.72	4.23	-	^[47]
Pyropia tenera (formerly Porphyra tenera)	390.0	3500.0	565.0	3627.0	-	10.30	2.72	2.21	<0.50	^[12]
Pterocladiella capillacea (formerly Pterocladia capillacea)	6105.0	1495.0	770.9	2949.5	-	22.70	3.33	4.21	0.43	^[45]
Phaeophyceae
Alaria esculenta	900.0	4400.0	700.0	3900.0	400.0	2.60	0.35	2.98	2.13	^[46]
Ascophyllum nodosum	984.7	3781.4	867.8	4575.7	-	13.34	1.96	-	-	^[16]
Bifurcaria bifurcata	996.4	9316.3	528.0	1836.8	169.5	-	-	-	-	^[16]
Fucus vesiculosus	938.0	4322.0	994.0	5469.0	-	4.20	5.50	3.71	<0.50	^[12]
Himanthalia elongata	909.0	6739.0	826.6	3700.0	0.015	1.81	4.09	3.77	-	^[47]
Laminaria digitata	1005.0	11,579.0	659.0	3818.0	-	3.29	<0.50	1.77	<0.50	^[12]
Undaria pinnatifida	931.0	8699.0	1181.0	7064.0	-	7.56	0.87	1.74	<0.50	^[12]

The protein content of algae varies greatly between large groups of algae (brown, red and green). In brown algae, the protein content is generally low (5–24% of dry weight), while red and green algae have a higher protein content (10–47% of dry weight) ^[48]. As with other nutritional components of algae, the content of proteins, peptides, and amino acids is influenced by various factors, especially seasonal variation ^[21]. For example, brown algae Saccharina and Laminaria displayed the maximum protein content during the months of February to May ^[21]. A similar variation has been found in red algae species, with a maximum in summer and a considerable reduction during winter ^[48]. In general, algae proteins are rich in glycine, arginine, alanine, and glutamic acid; they contain essential amino acids at levels comparable to the requirements indicated by FAO/WHO. Their limiting amino acids are lysine and cystine ^[20]^[32]. Other amino acids present in algae are taurine, laminin, kainoids, kainic and domoic acids, and some mycosporin-type amino acids ^[49]^[50]. Taurine, in humans, participates in many physiological processes such as immunomodulation, membrane stabilization, ocular development, and the nervous system ^[51]. In addition, kainic and domoic acids are involved in the regulation of neurophysiological processes ^[52].

On the other hand, some studies have shown that phycobiliproteins extracted from red algae (phycoerythrin) could be beneficial in the prevention or treatment of neurodegenerative diseases caused by oxidative stress (Alzheimer and Parkinson’s) due to their antioxidant effects ^[53]. The lectins found in Bryothamnion spp. (Rhodophyta) show an inhibitory effect on the growth of strains of Steptococcus spp.; therefore, they can be used as bactericidal compounds ^[54]. Among the peptides found in algae, those with 2–20 amino acids abound. They can be linear, cyclic, depsipetides, or peptides with one or more amide bonds replaced by ester-kahalalides- bonds, dipeptides (carnosine, almazole D), tripeptides (glutathione), pentapetides (galaximide), hexapeptides, oligopeptides, and phycobiliproteins ^[55]. These isolated peptides are characterized by having antioxidant, antitumor, antiviral, antimicrobial, antihypertensive, anticoagulatory, and immunostimulatory activities ^[56]. In particular, the kahalalides P and Q present in green algae possess cytotoxic action on the HL-60 cell line, while the kahalalide F, isolated from Bryopsis spp. (Chlorophyta), reduces the density of non-metastatic prostate tumor cells ^[52]. The most abundant amino acids are lectins, phycobiliproteins, agglutinins, and glycoproteins ^[50].

3. Bioactive Compounds in Algae

Apart from their nutritional components, algae contain bioactive compounds with high antioxidant capacity, such as carotenoids and polyphenols ^[5]^[57]^[58]^[59]^[60]^[61]^[62]. The natural pigments of algae have been studied finding antioxidant, anticancer, anti-inflammatory (mainly based on modulating macrophage function) activity, among others ^[63]. Among the natural algae pigments stands out fucoxanthin, a carotenoid that is available in different species of brown algae ^[64]. In this regard, several authors ^[65]^[66]^[67]^[68]^[69]^[70] have shown that fucoxanthin from different types of algae have an antioxidant, anticancer, anti-inflammatory, anti-obesity, neuroprotective, photoprotective, and osteoporosis preventive effects ^[62]^[65]^[66]^[67]^[68]^[69]^[70].

Polyphenols are a minority component of algae (Table 4). Green and red algae contain low concentrations of polyphenols (<1% dry weight) compared to brown algae ^[22]^[30] and can reach up to 14% dry weight in Ascophyllum and Fucus genera ^[21]. Phlorotannins are the most widely described polyphenols of brown algae, especially in species of the genus Ecklonia ^[21]^[61], and are formed from phloroglucinol (1,3,5-trihydroxybenzene) oligomeric structures ^[71]. Phlorotannins can be found at concentrations of 20–250 mg/g dry weight in Ascophyllum nodosum, Fucus vesiculosus, Sargassum spinuligerum, and Cystophora retroflexa ^[72]. In addition to phlorotannins, other polyphenols have been described, such as fucol and its derivatives, flavonoids, and derivatives such as catechin and epicatechin ^[21].

Table 4. Polyphenols content in different algae.

Seaweed	Total Polyphenols	Ref.
Chlorophyta
Ulva lactuca	2.86 ± 0.04 (mg GAE/100 g DW)	^[73]
Rhodophyta
Ellisolandia elongata (formerly Corallina mediterranea)	37 (mg GAE/100 g extract)	^[45]
Crassiphycus birdiae	1.06 ± 0.07 (mg GAE/100 g extract)	^[59]
Jania rubens	56 (mg GAE/100 g extract)	^[45]
Porphyra umbilicalis	5.53 (g GAE/100 g DW)	^[47]
Pterocladiella capillacea (formerly Pterocladia capillacea)	93 (mg GAE/100 g extract)	^[45]
Phaeophyceae
Alaria esculenta	2.80 ± 0.05 (mg GAE/100 g DW)	^[73]
Ascophyllum nodosum	0.96 ± 0.03 g PGE/100 g extract	^[74]
Bifurcaria bifurcata	1.99 ± 0.23 g PGE/100 g extract	^[74]
Fucus vesiculosus	1.15 ± 0.02 g PGE/100 g extract	^[74]
Halopteris scoparia	328.7 ± 2.87 (mg GAE/100 g DW)	^[75]
Himanthalia elongata	23.47 (g GAE/100 g DW)	^[47]
Saccharina latissima	11.1 mg GAE/g DW	^[46]
Turbinaria conoides	0.86 (mg GAE E/100 g DW)	^[57]
Undaria pinnatifida	4.46 (g GAE/100 g DW)	^[47]

DW–dry weight; GAE–gallic acid equivalents; PGE–Phloroglucinol equivalents.

The lipid algae content is low (1–5%), with neutral lipids and glycolipids being the most abundant. The proportion of essential fatty acids in algae is higher than in terrestrial plants, because they synthesize long chain polyunsaturated fatty acids, highlighting the eicosapentaenoic acid (EPA) and docosahexaenoic acid (DHA) that belong to the family of fatty acids ω-3 ^[76]. In general, red algae have high EPA, palmitic acid, oleic acid, and arachidonic acid contents compared to brown algae, which contain high concentrations of oleic acid, linoleic acid and α-linolenic acid but low EPA. Green algae have in greater quantity linoleic acid and α-linolenic, palmitic, oleic and DHA ^[77]^[78]. Both red and brown algae are a source of omega-3 and omega-6 fatty acids ^[30]^[79] Table 5 presents the proportion of EPA and DHA in algae and the relationship ω-6:ω-3.

Table 5. Lipid content in different algae.

Seaweed	Lipids g/100 g	EPA (%)	DHA (%)	Ref.
Chlorophyta
Caulerpa lentillifera	1.11 ± 0.05	0.86	-	^[26]
Codium fragile	1.5 ± 0.0	2.10 ± 0.00	-	^[39]
Ulva lactuca	1.27 ± 0.11	0.87 ± 0.16	0.8 ± 0.01	^[5]
Rhodophyta
Agarophyton chilense	1.3 ± 0.0	1.30 ± 0.01	-	^[39]
Porphyra/Pyropia spp. (China)	1.0 ± 0.2	10.4 ± 7.46	-	^[7]^[39]
Phaeophyceae
Ascophyllum nodosum	3.62 ± 0.17	7.24 ± 0.08	-	^[16]
Bifurcaria bifurcata	6.54 ± 0.27	4.09 ± 0.08	11.10 ± 1.13	^[16]
Durvillaea antarctica	0.8 ± 0.1	4.95 ± 0.11	1.66 ± 0.02	^[5]
Fucus vesiculosus	3.75 ± 0.20	9.94 ± 0.14	-	^[16]
Himanthalia elongata	<1.5	7.45	-	^[47]
Laminaria spp.	1.0 ± 0.3	16.2 ± 8.9	-	^[7]
Macrocystis pyrifera	0.7 ± 0.1	0.47 ± 0.01	-	^[39]
Sargassum fusiforme	1.4 ± 0.1	42.4 ± 11.9	-	^[7]
Undaria pinnatifida	4.5 ± 0.7	13.2 ± 0.66	-	^[7]

4. Biological Properties of Algae

The bioactive compounds present in seaweeds give them properties associated with the prevention and treatment of diseases (Figure 1), such as antidiabetic, antihypertensive, anti-inflammatory (based mainly on the modulation of macrophage function), antimicrobial, antitumor, antivirus, fat-lowering, and neuroprotective agents ^[63]^[80]^[81]. Primary and secondary metabolites can be also implicated in these applications. Primary metabolites are proteins, polysaccharides, and lipids involved in physiological functions. Among them, polysaccharides and fibers are the main compounds that display positive effects on chronic diseases such as cancer, cardiovascular diseases, diabetes, and obesity. On the other hand, secondary metabolites are minor molecules, such as phenolic compounds, halogenated compounds, sterols, terpenes, and small peptides, which are the result of stressful situations on seaweed tissues. Between them, exposure to ultraviolet radiation, changes in temperature and salinity, or environmental pollutants should be highlighted ^[82].

Figure 1. Biological properties of seaweeds.

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