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 Table of Contents  
ORIGINAL ARTICLE
Year : 2022  |  Volume : 7  |  Issue : 4  |  Page : 260-275

Evaluation of nutritional and functional properties of economically important seaweeds


Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh, India

Date of Submission02-May-2022
Date of Acceptance03-Aug-2022
Date of Web Publication21-Nov-2022

Correspondence Address:
Dr. K Suresh Kumar
Department of Botany, University of Allahabad, Prayagraj, Uttar Pradesh
India
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Source of Support: None, Conflict of Interest: None


DOI: 10.4103/jdras.jdras_56_22

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  Abstract 

BACKGROUND: Seaweeds or marine macroalgae are plant-like organisms occurring abundantly (either attached to rocks in the oceans or to other hard substrata in coastal areas). Being nutritionally rich in proteins, vitamins, fatty acids (FAs), and elements such as iodine, iron, and calcium, they are potential functional food ingredients. Their nutritional profile changes with climate and species. Lack of knowledge regarding their nutritional richness makes them less popularly used in our daily diet. This study investigates the nutritional composition and functional properties of six seaweeds for their utilization in the daily human diet. METHODS: Nutritional profiles of six seaweeds (five collected from India and one from South Korea) were evaluated in this study. Their protein content was estimated on the basis of the nitrogen value (N × 6.25). Mineral content was determined using inductively coupled plasma atomic mass spectroscopy. Extraction of FAs methyl esters (FAMEs) was conducted followed by gas chromatography–mass spectrometry (GC–MS). Vitamins were determined using high-performance liquid chromatography. Differential scanning calorimetric (DSC) analysis, thermogravimetric analysis (TGA), and Fourier transform infrared (FTIR) analysis of the dry seaweed samples were conducted. Functional properties [water-holding capacity (WHC), oil-holding capacity (OHC), and foaming capacity (FC)] of dried seaweed samples were determined using standard methods. RESULTS: The protein content of the studied seaweeds ranged from 7.940 to 36.190 g/100 g DW. Among the studied minerals, high Na content was observed in Enteromorpha compressa (i.e., 6.660 ± 0.013 mg/100 g) and high K in Kappaphycus alvarezii (5.590 ± 0.001 mg/100 g), respectively. FA profiling showed that Gracilaria sp. contained the highest saturated FAs. Maximum water-soluble vitamin, e.g., vitamin E (tocopherol) 0.643 mg/100 g contents, was seen in Caulerpa racemosa, whereas high ascorbic acid content was observed in E. compressa (2.975 mg/100 g). Riboflavin (B2) content of Ulva lactuca was 0.197 mg/100 g. FTIR, DSC, and TGA analyses were also conducted. WHC, OHC, and FC of the dried seaweeds revealed their applicability in food products. CONCLUSION: The nutritional and functional properties of the six seaweeds investigated suggest that they could be used for preparing functional food products. Promoting the use of seaweed as food and fodder could lead to enhancement of seaweed cultivation and harvesting, which in turn could also improve the socio-economic status of the coastal-dwellers.

Keywords: Biochemical properties, DSC, FTIR, functional properties, nutritional profiling, seaweeds, TGA


How to cite this article:
Kumari S, Singh K, Kushwaha P, Suresh Kumar K. Evaluation of nutritional and functional properties of economically important seaweeds. J Drug Res Ayurvedic Sci 2022;7:260-75

How to cite this URL:
Kumari S, Singh K, Kushwaha P, Suresh Kumar K. Evaluation of nutritional and functional properties of economically important seaweeds. J Drug Res Ayurvedic Sci [serial online] 2022 [cited 2022 Nov 30];7:260-75. Available from: http://www.jdrasccras.com/text.asp?2022/7/4/260/361578




  Introduction Top


Seaweeds (marine algae), as the name suggests, are large macroscopic algae that are generally autotrophic and grow in the sea (on the ocean floor, submerged under rocks, or attached to substrata near the coast). They are broadly classified into three groups: Phaeophyta, Chlorophyta, and Rhodophyta. Generally exploited for their polysaccharides (carrageenan, agar, and alginate), seaweeds are primarily used in industries as thickening agents in jellies, ice cream, sauces, etc. Seaweed cultivation has been taken up in several countries to cope with the phenomenal increase in demand for seaweeds worldwide.[1],[2] According to the Food and Agriculture Organization, out of the 23.8 million tons of seaweeds harvested globally, 38% are consumed by humans.[3],[4]

Besides performing vital ecological functions, seaweeds are nutritionally rich. They contain essential nutrients such as carbohydrates, proteins, amino acids, enzymes, fatty acids (FAs), pigments, essential minerals, micronutrients, as well as vitamins, making them suitable for utilization as food and fodder.[5],[6] In fact, they are often considered superior to other food resources like vegetables due to their unique protein, amino acids, fiber, mineral (especially sodium and iodine), vitamins, and FAs (eicosapentaenoic acid and docosahexaenoic acid of the omega (ω)-3 family and γ-linolenic acid) content.[7],[8],[9],[10],[11],[12],[13] Seaweeds fulfill the FAO/WHO-indicated prerequisite for essential amino acids levels. Some species of seaweeds are in high demand due to their low-calorie content and are rich in minerals, vitamins, and FAs, e.g. Undaria pinnatifida, Porphyra sp., Chondrus crispus.[8] Seaweeds also synthesize secondary metabolites such as terpenoids, oxylipins, phlorotannins, and volatile hydrocarbons. According to Colwell,[14] seaweeds also contain antibiotics, carotenoids, sterols, and several other fine chemicals. Nevertheless, the biochemical content of seaweeds varies with species, season, environmental and physiological factors, wave exposure; particularly, the mineral content varies with the method of processing and mineralization.[15],[16],[17]

Apart from being used in the food industries, seaweeds present a wide assortment of therapeutic applications. The medicinal values of seaweeds are recognized since ancient times. The Japanese and Chinese have been using seaweeds for the treatment of goiter and other cancers since 300 BC, whereas the Romans used them for treating burns, rashes, and wounds. Brown seaweeds have been traditionally used for treating thyroid goiter.[18] Dried or processed seaweeds were consumed as folk medicine against various ailments such as tuberculosis, rheumatism, colds, and influenza. Seaweeds have also been used for treating cough, asthma, hemorrhoids, boils, goiters, dysentery, stomach ailments, microbial infections, hypertension, and urinary diseases; they help reduce the incidence of tumors, ulcers, and headaches.[19] Reports also suggest that seaweeds provide protection against digestive disorders, hypertension, heart disease, allergy, cancers, diabetes, and oxidative stress.[20],[21] Phytochemicals such as sapononins, flavonoids, and alkaloids, obtained from Gelidium acerosa, are known to have medicinal value. Iodine rich seaweeds such as Asparagopsis toxiformis and Sarconema sp. help control goiter.[22] Among the seaweeds, polysaccharides and fucoidans are particularly fascinating as they exhibit biological activities (anti-proliferative, anti-viral, anti-thrombotic, anti-coagulant, anticancer, and anti-inflammatory).[23] Another seaweed polysaccharide “carrageenan” is used for ulcer therapy. The ω-3 and ω-6 polyunsaturated FA composition of seaweeds interestingly prevents cardiovascular diseases, osteoarthritis, and diabetes. Okai et al.[24] stated that apart from having antioxidant, anti-coagulant, anti-mutagenic, and anti-tumor activity, algae play an important role in the modification of lipid metabolism in human body. Extract of G. cartilagineum and Chondrus crispus is active against influenza B and mumps virus.[25] Nowadays, seaweeds have especially gained attention due to their bioactive compounds, such as antioxidants like polysaccharides, peptides, carotenoids, terpenes, alkaloids, and minerals[26],[27]; seaweed bioactive compounds have anti-inflammatory, anti-tumor, and antioxidant activities.[23] Seaweeds contain amino acids such as taurine, laminin, kainoids, kainic, and domoic acids and some mycosporin-type amino acids. Peñalver et al.[13] stated that taurine participates in many physiological processes such as ocular development, immunomodulation, membrane stabilization, and the nervous system in humans. In addition, kainic and domoic acids help regulate neurophysiological processes. Moreover, seaweeds are used for making cosmetics and pharmaceuticals.

Owing to their widespread occurrence, huge availability, macroscopic size, ease of processing, high species diversity,[28] as well as rich nutritional composition and health benefits, seaweeds hold a great potential as “wonder food” or “health wonders” of this millennium. They are “a universally sought product” in terms of “nutrition and health.” Incorporation of seaweeds in food, fodder, and food products could have health and nutritional benefits which need to be popularized in India. This manuscript highlights the nutritional composition and potential application of seaweeds.


  Materials and Methods Top


Seaweed samples U. lactuca, C. racemosa, Gracilaria dura, K. alvarezii, and E. compressa were collected from Port Okha (22o 28.65′N and 69o 04.01′E), Gujarat, Northwest coast of India. However, Porphyra sp. was procured from a commercial market in Wando Island, South Korea. The seaweeds were identified based on Jha et al.[29]

All the seaweed samples brought to the laboratory were thoroughly washed with tap water to remove adhering debris and attached epiphytes, followed by which they were washed with distilled water. The samples were shade-dried. These cleansed and dried seaweed samples were transferred to an oven (40oC, 24 h) until they were moisture-free and attained a constant weight. The moisture-free dried samples were crushed and sieved to obtain particles of the same size (0.5 mm); the powered seaweed samples were placed in air-tight closed jars at room temperature until further analysis.

Total protein content

The total protein content of seaweeds was determined by the method described by Kumar et al.[30] Concisely, the nitrogen content of each pulverized seaweed sample was determined using a CHN element analyzer, Euro Vector EA 3000. The percentage of total crude protein was calculated by multiplying the nitrogen content obtained by a factor of 6.25.

Analysis of minerals

Analysis of minerals was performed by inductively coupled plasma atomic mass spectroscopy (Perkin–Elmer, Optima 2000) by using the protocol outlined by Kumar et al.[31]

Fatty acid analysis

Determination of FAs was carried out using the extraction method of Levy et al.[32]; here, FA methyl esters (FAMEs) were determined using by gas chromatography–mass spectrometry (GC–MS) [Agilent: GC: (G3440A) 7890A]. In our study, MS-MS: 7000 Triple Quad GCMS was furnished with a mass spectrometry detector. Fat extraction was performed using the Soxhlet method.

Vitamin analysis

Seaweed powder was used for the determination of both fat-soluble and water-soluble vitamin samples according to the method of Syad et al.[33] Vitamin E, vitamin C, and niacin were determined by the high-performance liquid chromatography method (LC, Agilent, USA).[34],[35] Vitamins B1, B2, B3, B5, and B9 were analyzed spectrophotometrically according to the method of Bradbury and Singh.[36]

Differential scanning calorimetric (DSC) and thermogravimetric analysis (TGA)

DSC and TGA of each seaweed sample were performed according to Meng and Ma.[37] TGA was carried out using a Mettler Toledo TGA/SDTA system (Greifense, Switzerland).

Determination of Fourier transform infrared (FTIR) spectra of seaweeds

FTIR spectra of seaweeds were determined by using the method of Kumar et al.[30]

Determination of functional properties

The water-holding capacity (WHC) and oil-holding capacity (OHC)/fat-absorption capacity (FAC) of each seaweed sample were determined by using a slightly modified method of Zhang and Zhao.[38] The foaming capacity (FC) and stability of the algal biomass were determined using a modified method of Nath and Rao.[39]

Statistical analysis

Statistical analysis was carried out by one-way analysis of variance. Differences were considered to be statistically significant when P<0.05.


  Observations and Results Top


In this study, nutritional composition and functional properties of six economically important seaweeds were evaluated in view of their health benefits and application in the food industry. The seaweeds U. lactuca, C. racemosa, Porphyra sp., G. dura, K. alvarezii, and E. compressa had protein content of 14.480%, 24.570%, 36.190%, 14.290%, 7.940%, and 29.540% DW, respectively. Thus, the protein content ranged from 7.940% to 36.190% DW.

[Table 1] shows the mineral content of the seaweeds U. lactuca, C. racemosa, Porphyra sp., G. dura, K. alvarezii, and E. compressa studied; here, 17 minerals were analyzed. These seaweeds contained prodigious amount of macro-minerals (9.870 ± 0.034 to 13.780 ± 0.170 g/100 g) and trace elements (71.340 ± 6.090 to 327.67 ± 23.630 mg/100 g). The variation in the mineral content could be due to the changes in season, area of occurrence, species, etc. The highest total mineral content was seen in U. lactuca (13.780 ± 0.170 g/100 g), whereas least was recorded in C. racemosa (9.870 ± 0.034 g/100 g). The value of Na, K, Ca, Mg, and P contents of the six seaweeds ranged between 0.140 ± 0.00 and 6.66 ± 0.013 g/100 g. U. lactuca had high Na (6.320 ± 0.160 g/100 g DW) and low Hg contents (0.070 ± 0.030 mg/100 g), followed by C. racemosa that too had high Na (3.740 ± 0.009 g/100 g) and lowest content had Hg (0.040 ± 0.030 mg/100 g). Porphyra sp. had an Na content of 6.590 ± 0.013 g/100 g, whereas it had low Mo content (0.230 ± 0.010 mg/100 g). The relative amounts of bio-essential elements (Fe, Zn, Cu) occurred as Zn>Fe>Cu. The highest iron content was found in C. racemosa (100.220 ± 8.710 mg/100 g). The zinc content varied from 4.760 ± 0.020 to 46.890 ± 3.130 mg/100 g DW in all seaweeds studied. The mineral elements copper, cadmium, and chromium were found to range from 1.730 ± 0.030 to 99.880 ± 9.430 mg/100 g. [Table 2] suggests the amount daily intake of each seaweed based on the permissible daily doses for various toxic elements.[40],[41]
Table 1: Macro (g/100 g DW)-, micro-, and trace elements (mg/100 g DW) of studied seaweeds

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Table 2: Recommended dietary allowances of macronutrients, minerals, and trace elements of studied seaweeds

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The FA profiling of the six seaweeds showed that U. lactuca, C. racemosa, Porphyra sp., G. dura, K. alvarezii, and E. compressa contained 0.750%, 0.190%, 0.700%, 0.980%, 0.430%, and 0.230% total FA content, respectively, in which the FAs are expressed as g/100 g FAME/100 g total fat [Table 3]. The main saturated FAs (SFAs) found in U. lactuca, C. racemosa, Porphyra sp., G. dura, K. alvarezii, and E. compressa were lauric acid (C12:0), myristic acid (C14:0), palmitic acid (C16:0), heptadecanoic acid (C17:0), stearic acid (C18:0), arachidic acid (C20:0), behenic acid (C22:0), and lignoric acid (C24:0). Palmitic acid (C16:0) was the most dominant SFA in the seaweed samples analyzed [Table 3]. The amount of palmitic acid (C16:0) was highest in U. lactuca (0.305%), followed by G. dura (0.301%) and K. alvarezii (0.175%). The seaweeds studied had low levels of myristic acid (C14:0) (0.007–0.059%) and stearic acid (C18:0) (0.004–0.365%). In the case of monounsaturated FAs (MUFAs), methyl palmoitoleate (C16:1), oleic acid (C18:1), and methyl cis-11-eicosenoate (C20:1) and polyunsaturated FAs were detected in U. lactuca, Caulerpa sp., Porphyra sp., G. dura, K. alvarezii, and E. compressa. Further, oleic acid (C18:1) was the most dominant MUFA in the seaweeds and it ranged from 0.005% to 0.141%. Higher content of C18:1 was evident in G. dura (0.141%) when compared with U. lactuca (0.094%) and Porphyra sp. (0.049%). Oleic acid was also found in C. racemosa (0.005%) and K. alvarezii (0.007%). A small quantity of methyl palmoitoleate (C16:1) was present in U. lactuca (0.004 g/100 g), Caulerpa racemosa (0.002%), Porphyra sp. (0.001%), and G. dura (0.006%). In the case of polyunsaturated FAs, linoleic acid (C18:2) in the seaweed studied ranged from 0.007% to 0.164%. A small quantity of cis-11,14-eicosadienoic acid (C20:2) was also observed in Porphyra sp. (0.338%) in the present study. The total MUFA content of C. racemosa and K. alvarezii was similar, but these values were lower than the other seaweeds. The highest concentration of PUFA was found in Porphyra sp. (0.370%).
Table 3: Fatty acid composition

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[Table 4] provides the fat-soluble vitamin content, i.e., vitamin E (tocopherol) of the six seaweeds studied. K. alvarezii (0.7 mg/100 g) had the highest fat-soluble vitamin content, followed by C. racemosa (0.643 mg/100 g) and E. compressa (0.614 mg/100 g). However, Porphyra sp. and G. dura contained 0.581 and 0.530 mg/100 g vitamins. The water-soluble vitamin [viz., ascorbic acid, vitamin B1 (thiamine), vitamin B2 (riboflavin), vitamin B3 (niacin), and vitamin B5 (pantothenic acid)] contents of U. lactuca, C. racemosa, Porphyra sp., G. dura, K. alvarezii, and E. compressa are also shown in [Table 4]. Ascorbic acid values ranged from 0.817 to 2.975 mg/100 g; highest ascorbic acid was found in E. compressa 2.975 mg/100 g which was followed by G. dura and U. lactuca (2.437 and 1.261 mg/100 g, respectively). Petite vitamin B1 (thiamine) was found in U. lactuca (0.004 mg/100g), Porphyra sp. (0.005 mg/100 g), and G. dura (0.001 mg/100 g). Vitamin analyses revealed that G. dura had the highest content of vitamin B2 (Riboflavin) at 0.480 mg/100 g, followed by U. lactuca (0.197 mg/100 g) and E. compressa (0.071 mg/100 g). Highest vitamin B3 (niacin) was found in U. lactuca (0.033 mg/100 g), whereas the lowest value was seen in the case of E. compressa (0.013 mg/100 g). Less amount of vitamin B5 (pantothenic acid) was observed. U. lactuca and G. dura had similar pantothenic acid (0.008 mg/100 g), whereas C. racemosa and E. compressa showed a similar pantothenic acid (0.006 mg/100 g) content. However, the highest pantothenic acid was found in Porphyra sp. (0.028 mg/100 g).
Table 4: Vitamin content in seaweeds

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During DSC analysis, each seaweed sample was heated from 0 to 300oC at 10oC/min. DSC thermograms [Figure 1] of the seaweed samples (U. lactuca, C. racemosa, Porphyra sp., G. dura, K. alvarezii, and E. compressa) showed a characteristic endothermic peak indicating their respective glass transition temperatures (Tg) of 90.880oC, 61.830oC, 88.210oC, 111.420oC, 119.270oC, and 101.800oC. Due to the presence of carrageenan, G. dura showed an endothermic peak at 111.420oC. Thermograms of the seaweed powder of K. alvarezii showed characteristic endothermic peak and exothermic peak, indicating their respective glass transition temperatures (Tg) of 119.270oC and 217.360oC, respectively. Endothermic peak appeared due to the presence of carrageenan. K. alvarezii unveiled two observable endothermic peaks; the minor endothermic peak temperature (Tm) at about 108.520oC and the major one at 109.250oC (Tm).[30] The thermogram of U. lactuca showed a typical endothermic peak, indicating their respective glass transition temperatures (Tg). U. lactuca showed a Tg of 90.880oC.
Figure 1: DSC thermogram of (A) U. lactuca, (B) C. racemosa, (C) Porphyra sp., (D) G. dura, (E) K. alvarezii, and (F) E. compressa

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TGA for the seaweeds investigated is provided in the Supplementary section [Supplementary [Figure S1]] curves for U. lactuca, which indicates the initial weight loss of 17.190% by water evaporation at 80oC. The decomposition of U. rigida maximum 39.870% occurred in the temperature positioned at 310oC. The degradation of C. racemosa and Porphyra sp. took place in two stages: in the first stage, 10.920% and 10.080% weight loss of maximum biomass were recorded at 55oC and 60oC, respectively. During the second stage of degradation, 38.380% and 22.880% weight loss was observed at 310oC and 280oC, respectively. The total weight loss and the degradation of extracts occurred on a further increase in temperature. Similarly, TGA degradation of G. dura and E. compressa took place in two stages. In the initial stage, the weight loss by water evaporation was 1.650% and 11.580% at 110oC and 80oC, respectively. The second decomposition values at which the maximum weight loss occurred in case of G. dura and E. compressa were 50.780% and 35.280% at temperatures 310oC and 340oC, respectively. TGA shows that degradation of K. alvarezii also took place in two steps, wherein 11.250% weight loss of total biomass was recorded at 90oC which could be due to moisture content, and thereafter the second phase of degradation (41.770%) was observed with a maximum weight loss at 295oC.
Figure S1: Typical TGA thermogram of (A) U. lactuca, (B) C. racemosa, (C) Porphyra sp., (D) G. dura, (E) K. alvarezii, and (F) E. compressa

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The FTIR spectra [Figure 2] of the six seaweed samples were compared with standard peaks and studies. A broad band was seen between 3436.390 and 3424.890 cm−1; peaks were also observed at 2924.090–2922.640, 1728.220, and 1631.490–1632.700 cm−1 in our samples. IR spectra of G. dura displayed absorption bands at 1658.780, 1539.200, 1427.320, 1371.390, 1226.76, 1156.22, 1049.280, and 931.620 cm−1. In contrast, U. lactuca and C. racemosa showed bands at approximately 1420.850–1418.520 cm−1. In K. alvarezii, there were absorption bands at 2261.090 and 847.7 cm−1. An absorption band at 1027 cm−1was registered in U. lactuca, C. racemosa, and E. compressa; further, K. alvarezii showed an absorption band at 1036.98 cm−1. U. lactuca showed an absorption band near 619.370 cm−1.
Figure 2: FTIR spectrum of (A) U. lactuca, (B) C. racemosa, (C) Porphyra sp., (D) G. dura, (E) K. alvareziii, and (F) E. compressa

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[Figure 3] shows the WHCs of the seaweeds U. lactuca (6.440 ± 0.330 g water/g biomass), C. racemosa (6.120 ± 0.220 g water/g biomass), Porphyra sp. (6.970 ± 0.300 g water/g biomass), G. dura (9.150 ± 0.300 g water/g biomass), K. alvarezii (10.740 ± 0.100 g water/g biomass), and E. compressa (5.440 ± 0.560 g water/g biomass).
Figure 3: Water-holding capacity (WHC) of (A) U. lactuca, (B) C. racemosa, (C) Porphyra sp., (D) G. dura, (E) K. alvarezii, and (F) E. compressa. Values are expressed as mean ± standard deviation. The different superscript letters on columns are significantly different at P<0.05

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The OHCs of seaweeds for sunflower oil are shown in [Figure 4]. As shown, all the six seaweeds: U. lactuca (2.000 ± 0.060 g oil/g biomass), C. racemosa (2.540 ± 0.280 g oil/g biomass), Porphyra sp. (2.490 ± 0.230 g oil/g biomass), G. dura (2.530 ± 0.160 g oil/g biomass), K. alvarezii (1.670 ± 0.180 g oil/g biomass), and E. compressa (2.250 ± 0.060 g oil/g biomass), showed good OHC values.
Figure 4: Oil-holding capacity (OHC) of (A) U. lactuca, (B) C. racemosa, (C) Porphyra sp., (D) G. dura, (E) K. alvarezii, and (F) E. compressa. Values are expressed as mean ± standard deviation. The different superscript letters on columns are significantly different at P<0.05

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The foaming capacities [Figure 5] of the seaweeds U. lactuca (31.000 ± 3.600%), C. racemosa (25.000 ± 1.000%), Porphyra sp. (21.670 ± 1.520%), G. dura (30.330 ± 1.520%), K. alvarezii (35.000 ± 1.000%), and E. compressa (35.67 ± 3.000%) investigated herein were time-dependent. The lowest FC was recorded in Porphyra sp. (21.660 ± 1.520%) at pH 6.0 and the highest was found in E. compressa (35.670 ± 3.050%).
Figure 5: Foaming capacity and stability of (A) U. lactuca, (B) C. racemosa, (C) Porphyra sp., (D) G. dura, (E) K. alvarezii, and (F) E. compressa. Values are expressed as mean ± standard deviation. The different superscript letters on columns are significantly different at P<0.05

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  Discussion Top


Seaweeds encompass one of the most important natural marine resources. Out of the 20,000 seaweeds (marine macroalgae) occurring worldwide, barely 221 are commercially utilized; particularly, 145 species are used for food, whereas 110 are used for phycocolloid production.[44] Seaweeds are a good source of proteins, essential amino acids, minerals, vitamins (A, B1, B2, B9, B12, C, D, E, and K), essential minerals (calcium, iron, iodine, magnesium, phosphorus, potassium, zinc, copper, manganese, selenium, and fluoride), dietary fibers, and polyphenols (which have anti-inflammatory and antioxidant properties) and are therefore considered nutrient-rich food.[45] Although the seaweed industry is a promising and flourishing industry, utilization of seaweed as food supplement for its nutritional and health benefits is not prevalent in India.

In our investigation, the protein content of the seaweeds studied varied from 7.940 to 36.190% DW; the total protein content of seaweed is reported to vary with species and season.[46] The protein content of brown seaweed is reported to range between 3% and 15% DW,[47] whereas a combined range for red and green seaweeds is reported to be 10–47% DW.[48] Our value for protein content of U. lactuca (14.480% DW) was within the range reported by Balar et al.[49] (4.140–26.000% DW). U. rigida is reported have 17.800% DW protein.[50] The protein of C. racemosa (24.570% DW) obtained here was higher than that obtained by Gressler et al.[51] (12.880 ± 1.170% DW). Further, the protein content of K. alvarezii (7.940% DW) obtained in this study was lower than that of Kumar et al.[30] (18.160 ± 0.030%) and Rajasulochana et al.[52] (18.780% DW). Similarly, the protein contents of Porphyra sp. and G. dura obtained here were 36.190% and 14.290% DW, respectively, which were lower than the previously reported values (Porphyra sp. 42.990 ± 0.050 g/100 g DW[53] and G. dura 24.800% DW[54]). However, in the case of E. compressa (29.540% DW), we obtained higher protein content than a previous report (15.020%).[55] Overall, although all the studied seaweeds showed a high protein content, they varied based on the species. Changes in the total protein content observed in our study could be commensurate to the maturation of algal thallus, season, or environmental parameters. Several seaweed species possess significant protein content; especially red seaweeds contain higher protein levels (~50% DW). Pangestuti and Kim[56] demonstrate that seaweeds have a higher protein when compared with some conventional protein-rich foods. For example, high-protein vegetables such as soybeans have 35% DW protein, whereas protein levels of red seaweed P. tenera range from 28% to 47%; however, the red seaweed Gracilaria contains a low amount of protein (0.94–13.7%). The sea lettuce Ulva has a protein content ranging from 6% to 32%.[56] Nonetheless, the protein range obtained in our study (7.940–36.190% DW) shows that these seaweeds hold potential as a protein source in the food industry.

Seaweeds have strong biosorption and bioaccumulation abilities; they could possess 10–100 times higher mineral content than terrestrial vegetables.[57] In order to be utilized for human nutrition, edible seaweeds should be rich in several minerals such as sodium (Na), magnesium (Mg), phosphorous (P), potassium (K), iodine (I), iron (Fe), and zinc (Zn). Along with sodium and potassium, seaweeds are also rich in calcium and phosphorus, alongside with magnesium; in fact they surpass oranges, carrots, apples, and potatoes.[58] The ash content of seaweeds varies from species to species; this in turn could determine their mineral content. Circuncisão et al.[57] state that ash content of seaweeds could reach up to 40% DW, whereas that of spinach is only 20% DW. Seaweeds belonging to Phaeophyceae are reported to accumulate extraordinary iodine levels; iodine is well known to be an essential element for the maintenance of thyroid function and health. Thus consumption of seaweeds belonging to this group could be beneficial in handling iodine deficiency and could be added to iodized salts.[57] Several parameters such as pH, temperature, salinity, seasonal variation, maturity stage, seaweed species, sampling condition, and so on are known to influence the mineral content of seaweeds. In our study, the samples demonstrated high levels of macro-minerals and trace elements; however, each sample had an exclusive mineral content. Changes in season, area of occurrence, species, and so on have been known to influence the mineral content of seaweeds. All the six seaweeds investigated had high Na content compared with other minerals studied, which was obvious as they grew in the marine environment. Nevertheless, seaweeds often contain heavy metals (Cd, Cu, Hg, Pb, Zn). Although there is a defined permissible limit for the presence of these metals in seaweeds, this limit is known to vary in different countries. There is a fine line when it comes to these elements being essential, as crossing the limit would render them toxic. Our samples also contained bio-essential elements (Fe, Zn, Cu), apart from calcium; further, copper, cadmium, and chromium were also observed. Zinc amplifies the function of catalyst and also augments the structural and regulatory functions as well as stabilizes membranes, nucleic acids, and hormones.[42] Copper acts in various functions such as a cofactor in many enzymes, participating in blood clotting, and so on. Chromium regulates the various functions of insulin and takes part in lipid metabolism. Previous reports on C. racemosa show a lower zinc value of 3.410 ± 0.350 mg/100 g[43] when compared with our study. Apart from strengthening teeth structure and bone, calcium serves as a cofactor for cellular enzymes and proteins. Sodium and potassium, in contrast, act as excellent electrolyte balancers. Contrarily, elements such as As, Cd, Cr, Cu, Hg, Ni, Pb, and Zn are of immediate concern due to their potential toxicity to living organisms; therefore, it becomes essential to evaluate their content in the seaweed. Considering that it is essential to determine a permissible intake dose when we consider the food applicability of seaweed, the permissible and recommended intake of each seaweed species studied was calculated and a prescribed quantity has been stated. Although the mineral composition of the seaweeds investigated revealed their richness and suggests their utility as food supplements or in food products, detailed and repetitive studies of these seaweeds from various regions need to be undertaken.

Lipids chiefly provide energy; however, they also help maintain cell membrane integrity and hormone production. They are also essential to transport and absorb fat-soluble vitamins (A, D, E, and K). Although lipids are nutritionally essential for human health, it is essential to ensure a balanced intake. Seaweeds have emerged as an innovative feedstock when compared with terrestrial vegetation, with regard to FA. Rocha et al.[59] state that in addition to genetic characteristics from each alga, biotic and abiotic parameters influence the FA concentration and profile of seaweeds. Moreover, the life cycle of seaweed influences the FA content and characterization of algae. Seaweeds have essential unsaturated FAs (UFAs) that are crucial for human health. They particularly synthesize ω-3 and ω-6, polyunsaturated FAs (PUFAs), and highly unsaturated FAs (HUFAs), as well as MUFAs, which play vital roles in human metabolism (essential FAs or EFAs), being involved in cell growth and metabolic pathways, contrarily to SFA, which serve mainly as energy sources.[59] In our study, we observed that the amount of palmitic acid (C16:0) was highest in U. lactuca (0.305%), whereas G. dura (0.301%) and K. alvarezii (0.175%) also showed the presence of good amounts of the same; other reports also show the dominance of palmitic acid in U. lactuca and Porphyra sp.[60],[61],[62] Overall, the FA profiling of the six seaweeds ranged from 0.190% to 0.980%. The seaweeds contain ample saturated, unsaturated, and polyunsaturated FAs; they particularly contained a high total level of SFA than MUFA and PUFA.

Seaweeds have both water-soluble and fat-soluble vitamins, vitamin B-complex, provitamin A, vitamin C, and vitamin E; nevertheless, only few reports are available on the vitamin content of seaweeds and bioavailability of edible algae. The vitamin composition of seaweeds varies from species to species; it also varies with the stage of growth, geographic region, seasonal, salinity, seawater temperature, and light availability.[17],[42] In our study, K. alvarezii (0.7 mg/100 g) had the highest fat-soluble vitamin content. The reported riboflavin content of seaweed P. umbilicalisa (3.400 mg/100 g DW)[63] was different from that of Porphyra sp. (0.027 mg/100 g DW) investigated herein. Further, the vitamin B2 content of G. dura in our investigation (0.48 mg/100 g DW) was higher than the reported vitamin B2 content of G. corticata (0.050 mg/g).[64] Reports on the vitamin content of Gracilaria sp. are known to show varying values.[33],[65],[66] In our study, vitamin E content of 0.516 mg/100 g was obtained for U. lactuca, which is higher than that of Debbarama et al.[65] (0.06 mg%); they also reported the vitamin D2 and K1 content of U. lactuca to be 0.12 and 0.22,[65] respectively. Among the several studies that demonstrate nutritional benefits of seaweeds, a report on Undaria pinnatifida and Laminaria sp. shows high β-carotene content (i.e., 1.30 and 2.990 mg/100 g DW, respectively).[67] As seaweeds contain vital vitamins, consumption of seaweed in our daily diet could help meet the daily vitamin requirement of the human body.[60]

DSC is a valuable thermo-analytical technique that collects qualitative information of physical and chemical changes within a material in response to temperature. It is often used by industries that manufacture seaweed-based food products as the thermal data of seaweeds are given at appropriate temperature intervals; moreover, there is only a specific temperature range suitable for product preparation using seaweed, beyond which degradation occurs.[68] In our study, U. rigida showed the lower glass transition compared with the other seaweeds. The endothermic events show cumulative effects like exothermic and hydrogen bond breaking phenomenon such as aggregation of food proteins which was caused by the hydrophobic interactions.[69] The lower glass transition of U. rigida when compared with the other seaweeds could be due to inter-molecular and intra-molecular hydrogen bond, which is caused by the carboxylate and polysaccharide hydroxyl groups.[70]E. clathrata DSC thermogram is reported to show an endothermic peak of 95.500oC and an exothermic peak of 243.600oC[71]; however, in our investigation, a higher endothermic peak was obtained for E. compressa (where a glass transition was observed at 101.800oC). The reason for the low Tg value of E. compressa could be the variation in the occurrence of polysaccharides with hydroxyl groups. In our study, we observed that U. lactuca showed a Tg of 90.880oC, which was different from a previously reported glass transition value of U. rigida (78.100oC).[72]

TGA (a thermal analysis method) is one of the simplest methods for thermal analysis which would measure sample weight with increasing temperatures. It measures the changes in physical and chemical properties of seaweeds by increasing temperature as well as time. The weight loss of total biomass during the first stage ranges from 50oC to 100oC due to their moisture content.[30] In the second stage of TGA, the biomass degradation at higher temperatures causes maximum weight loss. The TGA of the six studied samples showed degradation taking place in two steps; however, the percentage weight loss of biomass varied based on the species in our study.

The FTIR technique identifies bioactive compounds in plants and algae. This qualitative method competently identifies functional groups and provides structural information about plants.[73] The broad band seen at 3436.390–3424.890 cm−1 is assigned to O–H and N–H stretching vibrations, which are due to polysaccharides and amino acids combined.[74] The peak at 2924.090–2922.640 cm−1 was due to the C–H asymmetric stretch on the saturated carbon atom, indicating the existence of the aliphatic groups.[75] In G. dura, the absorption peak at 1728.220 cm−1 was due to the C = O in carbonyl groups.[76] In G. dura, the absorption bands displayed at 1658.780, 1539.200, 1427.320, 1371.390, 1226.730, 1159.220, 1049.280, and 931.620 cm−1 corresponded to C = O and N = O of the ester and amide groups, C = C, C–O, OH stretch in lignin, symmetric C = O stretching, asymmetric -SO3 (S = O) stretching in sulfate esters, symmetric -SO3, CO and C–C vibrations in pyranose rings, and C–O in 3,6-anhydrogalactose.[72],[77],[78],[79],[80] Absorption peaks at 1631.490–1632.700 cm−1 were due to C = O and N–O asymmetric stretch that indicate the presence of an ester group.[75] Absorption band at 1036.98 cm−1 was assigned to C–H conformational vibration of the β-mannuronic acid residue.[79] In contrast, the bands at 1420.850–1418.520 cm−1 in U. lactuca and C. racemosa denoted C–O and O–H stretching bend vibrations in carboxylic acids.[75] In K. alvarezii, the absorption band at 1261.090 cm−1 was due to the carboxy group that was assigned to the C-O stretching.[77] An absorption band at 1027 cm−1 registered S = O stretching of the seaweed polysaccharides in the U. lactuca, C. racemosa, and E. compressa samples.[75] IR band at 1036.98 cm−1 was attributed to the mannuronic and gularonic units present in the alginate.[79] In K. alvarezii, the absorption band 847.7 cm−1 was assigned to C–H conformational vibration of the β-mannuronic acid residue.[79]U. lactuca shows C–S and C = S stretching vibrations in sulfide compounds (619.370 cm−1).[75] Overall, the IR analysis revealed the presence of various groups in the biochemical composition of the seaweeds. The amide, amino, hydroxyl, and ester groups in the IR spectrum were distinguishable due to the presence of polysaccharides, amino acids, proteins, and lipids.[81] These are known to influence metabolic process in humans and improve the immunity for the welfare of human health.[82] The presence of polysaccharides, glycoproteins, fucoidan, alginate, aliphatics, proteins, and amino acids evidenced in the samples herein indicated its nutritional richness and their applicability as health food.

Apart from biochemical analysis of the seaweed samples, they were also tested for few functional properties (that included evaluation of WHC, OHC, and foaming) to evaluate their applicability in the food and health industry.

Seaweeds are often used as functional ingredients in food; they help reduce calories, modify the viscosity, avoid syneresis, and help attain perfect texture of food products.[46] The high water absorption of seaweed biomass helps to reduce loss of moisture from packaged bakery products during processing and maintains the freshness and moist mouth-feel of baked food products.[83] As seen in [Figure 3], the WHCs of the seaweeds varied with species. The WHC of K. alvarezii obtained in our study (10.740 ± 0.100 g water/g biomass) was higher than that reported for K. alvarezii protein concentrate (2.220 ± 0.040 g water/g of PC).[30] WHCs for E. compressa (1.530 ± 0.070 g water/g PC), E. tubulosa (1.320 ± 0.110 g water/g PC), and E. linza (1.220 ± 0.060 g water/g PC)[84] have been previously reported. Another report on E. linza revealed a WHC of 5.410 ± 0.020 g/g DW[85] lower than our value for E. compressa (5.440 ± 0.560 g water/g biomass). We recorded a WHC of 9.150 ± 0.300 g water/g biomass for G. dura, whereas previous reports indicate WHCs of 4.030 ± 0.390 and 4.090 ± 0.280 g/g, respectively, for G. corticata and G. edulis at 25oC.[64] The WHC of U. lactuca was 6.440 ± 0.330 g water/g biomass, which was slightly higher than that reported for U. rigida (6.150 ± 0.080 g/g DW)[73]; nevertheless, the previously reported WHC for U. lactuca at 25oC is 7.500 g/g DW,[86] which is slightly higher than that found in our study. The WHC is a salient property of seaweeds in sticky foods, e.g., soups, custards, and baked products; high WHC implied that they could assimilate water (without breaking down proteins of seaweeds) and give body viscosity and stickiness to a food product. Based on our investigation, the six seaweeds demonstrated good WHC, which was an added advantage as they could find end application in preparation of food products.

The OHC of any compound could be attributed to a physical entrapment of oil by capillary action; it could be related to the non-polar side chains of proteins.[87] The OHC of a product depends on hydrophilicity, the total charge density, and the size of particles. OHC is an essential functional property of food products used to determine their applicability in formulated foods. High OHC of food ingredients allows formation of stable food emulsions[88] and better food products. The OHC of each of the six samples was distinct [Figure 4]. The OHC value of U. lactuca (2.000 ± 0.060 g oil/g biomass) was slightly lower than that reported for U. rigida (2.960 ± 0.130 g/g DW).[72] The FAC of K. alvarezii protein concentrate is reported to be 1.290 ± 0.200 g oil/g of protein,[30] which was nearly similar to our value (1.670 ± 0.180 g oil/g biomass). The OHC of E. compressa (2.250 ± 0.060 g oil/g biomass) was almost equivalent to the reported value of OHC of E. linza (2.52 ± 0.19 g/g DW) but differed from that of the reported values of E. tubulosa (2.140 ± 0.100 g/g DW) and E. compressa (1.970 ± 0.420 g/g DW).[85] The OHC value of 2.060 ± 0.240 g/g DW is reported in the case of Gracilaria sp.,[65] which was lower than our values for G. dura (2.530 ± 0.160 g oil/g biomass). OHC is essential in various food products such as salad dressing, cake making, sausages, and so on.[89] It is used to improve the viscous nature of food formulations.[30] The six seaweeds investigated herein demonstrated good OHC values. Interaction of water and oil with seaweeds is essential for the texture and taste of food products. It should be noted that the hydrophobicity of seaweed protein helps in the absorption of fats.[46]

The FC of E. compressa (35.670 ± 3.050%) in our study was higher than that reported for E. tubulosa (31.900 ± 2.700%) and E. linza (33.300 ± 5.700%) but lower than the FC value of E. compressa (55.000 ± 2.600%).[84] Our investigation on K. alvarezii (35.000 ± 1.000%) showed slightly lower FC when compared with a previous report that revealed 38.000 ± 2.000% FC for K. alvarezii.[30] The essential requirements of seaweed to become a good foaming agent are its ability to quickly adsorb at the air–water interface and to undergo rapid conformational changes at the interface during bubbling. The high FC largely depends on the protein-spreading ability, but the foaming stability is mainly affected by the degree of denatured protein.[90]

Overall, it could be said that just like other seaweeds that are nutritionally rich, i.e., sea vegetables that have tremendous health benefits, the seaweeds investigated herein were also nutritionally rich and contained polysaccharides, proteins, amino acids, lipids, FAs, fibers, minerals, vitamins, and so on that are unmatched. The very fact that seaweeds often have a higher nutritive value when compared with other terrestrially grown vegetables makes them suitable for consumption as health food. Currently, seaweeds are mainly used for the production of polysaccharides and also in few cosmetic and pharma industries; however, they need to be popularized for their nutritional, health, and medicinal values and incorporated in daily diet.

According to Kraan,[91] India with a coastline of 7500 km and a continental shelf of 372,424 km2 is home to 840 different species of seaweeds with a standing stock of 600,000 tones fresh weight. Several regions in states like Tamil Nadu and Gujarat, as well as areas in the vicinity of Batnagiri, Goa, Karawar, Mumbai, Varkala, Vishakapatnam, Vizhinjam, and in few other places like Chilika and Pulicat lakes, Andaman and Nicobar Islands, offer a hard substratum that is good for seaweed growth. Despite this rich seaweed diversity, there is little awareness regarding the use of seaweed as food for health and nutritional benefits in India. Seaweeds are plant-based and could be consumed by vegetarians as well as non-vegetarians; however, it is necessary to create an awakening regarding the health, medical, and nutritional benefits of seaweeds in the public domain especially in India. Incorporation of seaweeds in human diet is a low-cost natural alternative to supplement vitamins and minerals to the human diet and could benefit coastal-dwellers. Moreover, export of locally harvested or cultivated seaweeds for various applications could have socio-economic benefits.

Further, the use of seaweed as animal fodder or aquaculture feed is also feasible economic alternative; ensuring good fish and cattle in turn would ensure sustainable and safe products for human consumption. Lomartire et al.[45] reported that seaweeds like Ascophyllum nodosum (Phaeophyceae) and Laminaria digitata (Phaeophyceae) are already used to enrich animal diets in the UK and France, whereas in Iceland, Ascophyllum and Laminaria species already provide the main commercial ingredients used to feed land animals. A. nodosum extracts have phlorotannins and reduce  Escherichia More Details coli O157:H7; seaweed extracts are also known to reduce other pathogenic microorganisms such as  Salmonella More Details sp., Campylobacter species, and Clostridia in the gastrointestinal track of domestic animals.[45] Seaweeds could also provide a solution for iodine deficiency. A. nodosum-fed pigs are reported to have an increase in iodine concentration from 2.7 to 6.8.[45] A feeding strategy for producing iodine-enriched meat could be a good solution to incorporate iodine in the human diet, without overdosing or a need for a shift in eating pattern. In this context, seaweed extracts supplemented fish diet has been known to enhance the growth, physiological activity, lipid metabolism, disease resistance, stress response, and carcass quality of various fish species. For example, Saccharina latissima (Phaeophyceae) is reported to be a potential feed additive as its bioactive compounds ameliorate fish farming and also increase protective activity against oxidative stress in fish. Consuming seaweed-fed fish could be a healthy alternative of getting nutrients for human.


  Conclusion Top


The seaweeds studied were nutritionally rich and contained good amount of proteins, FAs, vitamins, and minerals contents; the macro- and micro-nutrients present in these seaweeds and their functional properties suggest their utility in various food products or as food. They could be extensively useful as a good source of nutrition that would help combat mineral or macronutrient deficiencies. Having specific functional properties, these seaweeds also facilitate processing and could serve as the basis for manufacturing tailor-made food products. India possesses a huge coastline with teeming seaweed diversity; however, we need to incorporate and popularize the use of seaweed as food for its nutritional and health benefits in India. It is necessary to also create an awareness regarding the utility of seaweeds as feed and fodder. Seaweed harvesting and cultivation in India need to be promoted to benefit the socio-economic status of the coastal-dwellers. On the contrary, export of local seaweeds would help enhance financial inflow to the nation.

Financial support and sponsorship

This study has been financially supported by UGC-BSR Startup grant New Delhi, India. The author Sushma Kumari is especially thankful to NFSC Fellowship for the financial support provided.

Conflicts of interest

The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper.





 
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