Journal of Applied Phycology

, Volume 21, Issue 1, pp 75–80

Nutrient content of tropical edible seaweeds, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum

Authors

  • Patricia Matanjun
    • School of Food Science and NutritionUniversiti Malaysia Sabah
    • Faculty of Food Science & TechnologyUniversiti Putra Malaysia
  • Noordin M. Mustapha
    • Faculty of Veterinary MedicineUniversiti Putra Malaysia
  • Kharidah Muhammad
    • Faculty of Food Science & TechnologyUniversiti Putra Malaysia
Article

DOI: 10.1007/s10811-008-9326-4

Cite this article as:
Matanjun, P., Mohamed, S., Mustapha, N.M. et al. J Appl Phycol (2009) 21: 75. doi:10.1007/s10811-008-9326-4

Abstract

The proximate composition, vitamin C, α-tocopherol, dietary fibers, minerals, fatty acid and amino acid profiles of three tropical edible seaweeds, Eucheuma cottonii (Rhodophyta), Caulerpa lentillifera (Chlorophyta) and Sargassum polycystum (Phaeophyta) were studied. The seaweeds were high in ash (37.15–46.19%) and dietary fibers (25.05–39.67%) and low in lipid content (0.29–1.11%) on dry weight (DW) basis. These seaweeds contained 12.01–15.53% macro-minerals (Na, K, Ca and Mg) and 7.53–71.53 mg.100 g−1 trace minerals (Fe, Zn, Cu, Se and I). The crude protein content of E. cottonii (9.76% DW) and C. lentillifera (10.41% DW) were higher than that of S. polycystum (5.4% DW), and protein chemical scores are between 20 and 67%. The PUFA content of E. cottonii was 51.55%, C. lentillifera 16.76% and S. polycystum 20.34%. Eicosapentaenoic acid (EPA), accounted for 24.98% of all fatty acids in E. cottonii. These seaweeds have significant vitamin C (∼35 mg.100 g−1) and α-tocopherol (5.85–11.29 mg.100 g−1) contents.

Keywords

SeaweedsNutrient compositionDietary fiberMineralsOmega-3 fatty acidsAmino acids

Introduction

The chemical composition of edible seaweeds from some regions of the world has been well documented, but no reports are available on the nutritive value of the tropical seaweeds of North Borneo. Climate and sea conditions may cause differences in nutrient composition of seaweeds (Burtin 2003; Darcy-Vrillon 1993). The recent increasing demand for seaweed products, as food, fodder, fertilizer and sources of medicinal drugs (Sánchez-Machado et al. 2004), justify this investigation on the nutritional composition of three of the most antioxidative tropical edible species namely, Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum from the Rhodophyta, Chlorophyta and Phaeophyta, respectively (Matanjun et al. 2008). This information is essential in the search for additional healthy food sources from the sea for use in human and animal nutrition.

Materials and methods

The three seaweeds were collected from the coastal areas of North Borneo, Malaysia. Eucheuma cottonii was harvested from Universiti Malaysia Sabah (UMS) farms in Bangi, Sabah (north coast of North Borneo), C. lentillifera from Semporna (east coast of North Borneo) and S. polycystum from Kota Kinabalu (west coast of North Borneo). Fresh seaweeds were thoroughly washed with distilled water, and their holdfasts and epiphytes removed, and then placed in a freezer (−20°C) immediately after collection. Dried ground samples were used for most of the analyses except for vitamin C and fatty acids composition where fresh samples were used. The ground samples were stored in air-tight plastic containers covered with aluminium foil and stored at−20°C for further analysis. Analyses were carried out in triplicate.

The moisture content (oven method at 105°C; AOAC, 934.01), crude protein (micro-Kjeldhal, N x 6.25; AOAC, 981.10), ash (550°C overnight; AOAC, 930.05), fat (Soxhlet extraction with diethyl ether; AOAC, 991.36), crude fiber (successive hydrolysis with 100°C 0.05 N H2SO4 and 0.05 N NaOH for 30 min each), and soluble and insoluble dietary fibers (enzymatic-gravimetric method; AOAC, 993.19, 991.42), were determined (AOAC 2000). Carbohydrate content was calculated by difference (James 1996). The vitamin C content of fresh seaweeds was determined using the 2,6-dichloroindophenol titrimetric method (AOAC, 967.21). α-Tocopherol was determined by HPLC (Sánchez-Machado et al. 2002), using methanol-acetonitrile (30:70 v/v) as the mobile phase, a flow rate 1.0 ml min−1, detection at 205 nm and 30°C.

Major mineral elements (Ca, Mg, Na, K) and trace elements (Fe, Zn, Cu and Se) were determined using a Perkin Elmer 5100 PC atomic absorption spectrophotometer equipped with a single hollow cathode lamp for each element and an air-acetylene burner (Rupérez 2002), against mineral elements standards (Merck, Germany). Iodine was determined using a spectrophotometric kinetic assay (Mahesh et al. 1992), based on measurement of iodide-catalyzed reduction of Ce(IV) to Ce(III) by As(III). The reaction was continuously monitored at 370 nm and the initial velocity for decrease in absorbance was plotted against iodine concentration.

Fatty acids were determined using a Fison 8000 gas chromatograph (30 m × 0.32 mm × 0.25 mm Supelco-Wax capillary column) and a Fison EL-980 flame ionization detector of their methyl esters (FAMEs), identified by the retention times compared with methyl-fatty acids standards (Merck, Germany) (Sánchez-Machado et al. 2004).

Amino acids were determined using HPLC (Sánchez-Machado et al. 2003) on PITC (phenyl isothiocyanate) derivatized samples, on an ODS2 reversed-phase column (25 cm × 4 cm i.d., 5 μm particle size) with UV detection at 254 nm. The mobile phase was a mixture of 0.14 M ammonium acetate buffer, pH 6.4, containing 0.05% triethylamine (A) and 60:40 (v/v) acetonitrile-water (B), at a flow rate of 1.1 mL min−1; the elution gradient (min:A%) was: 0:90, 8:90, 10:70, 12:70, 18:52, 20:0, 25:0, 28:90, 35:90. Protein quality was evaluated by determining the chemical score, i.e., the ratio of the amount of the limiting amino acid in a gram of seaweed protein to the amino acid in whole-egg (the protein, which has the highest net protein utilization value, biological value and protein efficiency ratio value) multiplied by 100 (Brody 1999).

All results are expressed as means±SD (n = 3). Significance difference at p < 0.05, was analyzed by one-way analysis of variance (ANOVA) followed by Duncan multiple range tests using SPSS system version 12.0 for Windows.

Results and discussion

Table 1 shows the nutrient contents of the seaweeds based on dry weight (DW) except for vitamin C content. The protein content of S. polycystum was the lowest (5.40%) compared to E. cottonii (9.76%) and C. lentillifera (10.41%), and were within the ranges of brown seaweeds (3–15% DW) and red and green seaweeds (10–47% DW) (Arasaki and Arasaki 1983; Darcy-Vrillon 1993; Mabeau and Fleurence 1993). The protein content of E. cottonii and C. lentillifera are comparable with that of high-protein plant foods such as soybean. Variations in the protein content of seaweeds can occur due to different species and season (Fleurence 1999; Galland-Irmouli et al. 1999).
Table 1

Nutrient composition of Eucheuma cottonii, Caulerpa lentillifera and Sargassum polycystum (% dry weight of sample)

Nutrient

E. cottonii

C. lentillifera

S. polycystum

Protein (%)

9.76 ± 1.33a

10.41 ± 0.26a

5.40 ± 0.07b

Lipid (%)

1.10 ± 0.05a

1.11 ± 0.05a

0.29 ± 0.01b

Ash (%)

46.19 ± 0.42a

37.15 ± 0.64c

42.40 ± 0.41b

Crude fiber (%)

5.91 ± 1.21b

1.91 ± 0c

8.47 ± 1.21a

Carbohydrate (%)

26.49 ± 3.01c

38.66 ± 0.96a

33.49 ± 1.70b

Moisture content (%)

10.55 ± 1.60a

10.76 ± 0.80a

9.95 ± 0.55 a

Soluble fiber (%)

18.25 ± 0.93a

17.21 ± 0.87a

5.57 ± 0.28b

Insoluble fiber (%)

6.80 ± 0.06c

15.78 ± 1.20b

34.10 ± 0.28a

Total dietary fiber (%)

25.05 ± 0.99

32.99 ± 2.07

39.67 ± 0.56

Vitamin C (mg 100 g−1 WW)

35.3 ± 0.01a

34.7 ± 0.02a

34.5 ± 0.01a

α-tocopherol (mg/100 g DW)

5.85 ± 0.27c

8.41 ± 0.12b

11.29 ± 0.61a

Na (mg/100 g mg 100 g−1 DW)

1771.84 ± 0.01b

8917.46 ± 0.00a

1362.13 ± 0.00c

K (mg.100 g−1 DW)

13,155.19 ± 1.14a

1142.68 ± 0.00c

8371.23 ± 0.01b

Ca (mg.100 g−1 DW)

329.69 ± 0.33c

1874.74 ± 0.20b

3792.06 ± 0.51a

Mg (mg.100 g−1 DW)

271.33 ± 0.20c

1028.62 ± 0.58a

487.81 ± 0.24b

Fe (mg.100 g−1 DW)

2.61 ± 0.00c

21.37 ± 0.00b

68.21 ± 0.03a

Zn (mg/100 g mg 100 g−1 DW)

4.30 ± 0.02a

3.51 ± 0.00b

2.15 ± 0.00c

Cu (mg.100 g−1 DW)

0.03 ± 0.00b

0.11 ± 0.00a

0.03 ± 0.00b

Se (mg.100 g−1 DW)

0.59 ± 0.00c

1.07 ± 0.00b

1.14 ± 0.03a

I (μg g−1 DW)

9.42 ± 0.12a

4.78 ± 0.59c

7.66 ± 0.10b

Na/K ratio

0.14

7.8

0.16

Total cations

15,535.58 ± 1.70a

12,989.56 ± 0.78c

14,084.76 ± 0.82b

Values are expressed as mean±standard deviation, n = 3

Values in the same row with different superscripts letters are significantly different (p < 0.05)

The total dietary fiber in S. polycystum was the highest (39.67%) followed by C. lentillifera (32.99%) and E. cottonii (25.05%). The total dietary fiber content are within the range of other seaweeds (Jiménez-Escrig and Sánchez-Muniz 2000; Mabeau and Fleurence 1993) and higher than most terrestrial plants. The soluble fiber in E. cottonii (18.25%) and C. lentillifera (17.21%) were significantly higher than S. polycystum (5.57%). Many soluble fibers have hypocholesterolemic and hypoglycemic effects, whereas insoluble fibers are mainly associated with a decrease in digestive tract transit time. Eucheuma cottonii (soluble fiber 18.25%) and C. lentillifera (soluble fiber 17.21%) appear to be a good potential functional food ingredient for lowering cholesterol and glycaemic index for prevention of metabolic syndromes.

The vitamin C content in all three seaweeds were not significantly different (p > 0.05). Sargassum polycystum (11.29 mg 100 g−1) has a higher α-tocopherol content than C. lentillifera (8.41 mg 100 g−1) and E. cottonii (5.85 mg 100 g−1). Vitamin E helps tp inhibit LDL oxidation and prostaglandin and tromboxan formation (Burtin 2003). Phaeophyte algae reportedly contain more α-tocopherol than rhodophytes and chlorophytes (Sánchez-Machado et al. 2002). Brown algae contain α, β and γ-tocopherols while the green and red algae only contain α-tocopherol (Burtin 2003). These seaweeds, especially the brown seaweeds, can be a natural source of vitamin C and α-tocopherol.

Eucheuma cottonii had the highest ash content (46.19%), followed by S. polycystum (42.40%) and C. lentillifera (37.15%). These seaweeds contained high amounts of macrominerals (12.01–15.53 mg 100 g−1) and trace elements (7.53–71.53 mg 100 g−1). The Na/K ratios were very low for E. cottonii and S. polycystum (0.14–0.16). Rupérez (2002) also reported low Na/K ratios, below 1.5 for the red and brown seaweeds studied. Intakes of high Na/K ratios have been related to the higher incidence of hypertension. Seaweeds can therefore help balance high Na/K ratio diets. In contrast, olives and sausages have Na/K ratios of 45.63 and 4.89, respectively (Ortega-Calvo et al. 1993). Eucheuma cottonii (9.42 μg g−1) had the highest iodine content followed by S. polycystum (7.66 μg g−1) and C. lentillifera (4.78 μg g−1). In comparison, the iodine content of terrestrial vegetables and fruits are approximately 0.02–0.88 μg g−1 (Mahesh et al. 1992). Ash was the most abundant component of dried seaweeds. The levels of ash and trace elements detected were within the ranges previously reported (Rupérez 2002; Mabeau and Fleurence 1993; Ortega-Calvo et al. 1993). The mineral content of seaweeds is higher than that of land plants (Ortega-Calvo et al. 1993).

The total lipid content in E. cottonii, C. lentillifera and S. polycystum were 1.10%, 1.11% and 0.29% DW, respectively, and were within the range for most seaweeds (1–3% DW) (Chapman and Chapman 1980). Thirty-three fatty acids were identified; the fatty acid composition of the different seaweeds varies considerably (Table 2). Eucheuma cottonii had a higher PUFA content (51.55%) than S. polycystum (20.34%) or C. lentillifera (16.76%). Consequently the saturated fatty acids in E. cottonii (25.17%) were lower than S. polycystum (51.30%) and C. lentillifera (46.41%).
Table 2

Fatty acid content (% of total fatty acid content) of E. cottonii, C. lentillifera and S. polycystum

Fatty acid

Seaweed (% of total fatty acid content)

Carbon no.

E. cottonii

C. lentillifera

S. polycystumm

Caprylic

C8:0

0.36

Capric

C10:0

0.17

0.16

0.36

Undecanoic

C11:0

3.67

0.85

Lauric

C12:0

0.88

0.13

3.62

Tridecanoic

C13:0

0.12

Myristic

C14:0

1.65

1.65

3.26

Myristoleic

C14:1

0.33

0.05

Pentadecanoic

C15:0

0.11

0.18

Palmitic

C16:0

15.10

33.78

37.97

Palmitoleic

C16:1

11.10

1.31

3.81

Heptadecanoic

C17:0

0.16

0.28

Cis-10-Heptadecanoic

C17:1

8.16

1.55

0.06

Stearic

C18:0

2.11

7.83

4.20

Elaidic

C18:1ω9

0.11

0.22

0.04

Oleic

C18:1ω9

3.44

32.49

24.21

Linolelaidic

C18:2ω6

1.44

0.09

0.05

Linoleic

C18:2ω6

1.15

7.64

8.44

γ-Linolenic

C18:3ω6

0.80

0.31

0.27

α-Linolenic

C18:3ω3

3.88

5.54

1.41

Arachidic

C20:0

0.21

0.47

0.40

Cis-11-Eicosenoic

C20:1ω9

0.29

0.17

0.12

Cis-11,14-Eicosadienoic

C20:2

0.07

0.22

Cis-11,14,17-Eicosatrienoic

C20:3ω3

16.87

1.15

6.38

Arachidonic

C20:4ω6

1.29

0.63

Cis-5,8,11,14,17-Eicosapentaenoic

C20:5ω3

24.98

0.86

1.71

Henocasanoic

C21:0

0.09

Behenic

C22:0

0.31

0.15

Erucic

C22:1ω9

0.20

0.27

0.08

Cis13,16-Docisadienoic

C22:2

0.86

0.95

1.10

Cis-4,7,10,13,16,19-Docosahexaenoic

C22:6ω3

0.13

Tricosanoic

C23:0

0.92

0.14

0.28

Lignoceric

C24:0

0.47

0.70

0.17

Nervonic

C24:1ω9

0.27

0.66

Saturated FAs

 

25.17 ± 0.38c

46.41 ± 0.56b

51.30 ± 0.51a

MUFAs

 

23.28 ± 0.47c

36.83 ± 0.55a

28.36 ± 0.48b

PUFAs

 

51.55 ± 0.57a

16.76 ± 0.27c

20.34 ± 0.43b

PUFAs ω6

 

4.68 ± 0.05c

8.04 ± 0.12b

9.40 ± 0.17a

PUFAs ω3

 

45.72 ± 0.59a

7.55 ± 0.09b

9.63 ± 0.15b

Ratio ω6/ω3

 

0.10

1.07

0.98

FA Fatty acid, MUFAs mono-unsaturated fatty acid, PUFA polyunsaturated fatty acid

Values are expressed as mean±standard deviation, n = 3

Values in the same row with different superscripts letters are significantly different (p < 0.05)

All three seaweeds contained the essential fatty acids linoleic acid (C18:2ω6) and linolenic acid (C18:3ω3), and the eicosanoid precursors arachidonic acid (C20:4ω6) (except C. lentillifera) and eicosapentaenoic acid (EPA) (C20:5ω3). The most abundant fatty acid in E. cottonii was the omega-3 fatty acid, EPA which accounted for 24.98% of all fatty acids. Sargassum polycystum contained a small quantity of docosahexaenoic acid. Palmitic (C16:0) and oleic acids (C18:1ω9) were the most abundant fatty acids in C. lentillifera and S. polycystum, and E. cottonii had the highest amount of omega-3 fatty acids (45.72%) compared to S. polycystum (9.63%) and C. lentillifera (7.55%).

Eucheuma cottonii contained a high level of C-20 PUFA as has been reported for several species of red algae (Fleurence et al. 1994; Khotimchenko et al. 2002). Both the green and brown seaweeds in this study had a high content of palmitic acid (C16:0) and oleic acid (C18:1ω9) but a low content of PUFA. The fatty acid composition of the Caulerpa is similar to those previously reported for green algae (Dembitsky et al. 1991). The composition of the Sargassum also agrees with the findings of Hamdy and Dawes (1988) and Herbreteau et al. (1997) on other species of Sargassum.

Eucheuma cottonii has a high amount of PUFAs especially omega-3 fatty acids (high levels of EPA) which is beneficial to health, thereby making it a healthy low-fat food, rich in omega-3 fatty acids. Omega-3 fatty acids help prevent the growth of atherosclerotic plaque and affect blood clotting, blood pressure and improve immune functions (Stone 1997). High dietary omega-6 PUFA decreases LDL cholesterol but may also decrease HDL cholesterol, which adversely affects heart disease risk (Dietschy 1998; Sánchez-Machado et al. 2004). WHO currently recommends that the ω6/ω3 ratio should not exceed 10 in the diet. These seaweeds have a low ω6/ω3 ratio (0.10 for E. cottonii and 1.06 for C. lentillifera) and may be of use for reducing the ω6/ω3 ratio. Dietary omega-3 PUFA can reduce heart disease risks, decrease low density lipoprotein (LDL) cholesterol but do not lower high density lipoprotein (HDL) cholesterol (Stone 1997). Although seaweeds are low in total lipids, their PUFAs content can be as high as those of terrestrial vegetables (Darcy-Vrillon 1993). The presence of these essential fatty acids in seaweeds allows future development in the search for new source of specific PUFA for nutrition and medicinal use. The differences in fatty acid composition between the species taxonomically and environmentally related (Herbreteau et al. 1997).

Amino acid analysis of E. cottonii, C. lentillifera and S. polycystum (Table 3) found 16 amino acids with reasonably resolved separations. The seaweeds contain all the essential amino acids in different proportions, except for tryptophan, which was destroyed during hydrolysis. Total amino acid content was highest in C. lentillifera followed by S. polycystum and E. cottonii. However, the essential amino acids in E. cottonii (60.59%) and S. polycystum (61.66%) were higher than in C. lentillifera (48.19%). The highest essential amino acid was phenylalanine in all the 3 species.
Table 3

Amino acid content of E. cottonii, C. lentillifera and S. polycystum

Amino acid

No. (mg g−1 reference protein)

Seaweed (mg g−1 dry weight)

E. cottonii

C. lentillifera

S. polycystum

Aspartic acid (Asp)

 

2.65 ± 0.15

8.33 ± 0.11

4.47 ± 0.87

Glutamic acid (Glu)

 

5.17 ± 0.13

13.47 ± 0.23

8.08 ± 1.08

Serine (Ser)

 

1.92 ± 0.04

5.49 ± 0.20

2.58 ± 0.16

Glycine (Gly)

 

2.27 ± 0.32

5.14 ± 0.03

3.19 ± 0.35

Histidine (His)

 

0.25 ± 0.10

1.44 ± 0.13

0.26 ± 0.11

Arginine (Arg)

 

2.60 ± 0.14

5.71 ± 0.22

2.88 ± 0.17

Threonine (Thr)

34

@2.09 ± 0.01

5.84 ± 0.22

2.60 ± 0.16

Alanine (Ala)

 

3.14 ± 0.11

6.88 ± 0.19

4.25 ± 0.15

Proline (Pro)

 

2.02 ± 0.09

4.29 ± 0.11

2.55 ± 0.14

Thyrosine (Tyr)

 

1.01 ± 0.12

3.33 ± 0.08

1.26 ± 0.06

Valine (Val)

35

@2.61 ± 0.07

6.18 ± 0.02

3.13 ± 0.14

Methionine (Met)

25

@0.83 ± 0.17

@1.58 ± 0.08

@1.25 ± 0.04

Isoleucine (Ile)

28

@2.41 ± 0.04

5.06 ± 0.12

2.94 ± 0.16

Leucine (Leu)

66

@3.37 ± 0.06

7.79 ± 0.19

4.67 ± 0.25

Phenylalanine (Phe)

63

19.07 ± 2.48

19.95 ± 1.41

30.42 ± 4.43

Lysine (Lys)

58

@1.45 ± 0.48

@1.22 ± 0.05

@2.11 ± 0.77

Chemical score (%)

 

25.6

20.2

67.4

Most limiting amino acid

 

lysine

lysine

lysine

Total amount

 

52.86 ± 3.37c

101.63 ± 2.92a

76.38 ± 2.31b

Essential amino acid (EAA)

 

32.07 ± 3.13b

48.98 ± 2.19a

47.13 ± 4.12a

EAA (%)

 

60.59 ± 1.36a

48.19 ± 0.77b

61.66 ± 4.73a

Protein (%)

 

9.76 ± 1.33a

10.41 ± 0.26a

5.40 ± 0.07b

Values are expressed as mean±standard deviation, n = 3

Values in the same row with different superscripts letters are significantly different (p < 0.05) \({\text{Chemical}}\;{\text{score}}\;\left( \% \right) = \frac{{\left( {{\text{mg}}\;{\text{limiting}}\;{\text{amino}}\;{\text{acid}}\;{\text{per}}\;{\text{g}}\;{\text{of}}\;{\text{test}}\;{\text{protein}}\; \times \;100} \right)}}{{\left( {{\text{mg}}\;{\text{limiting}}\;{\text{amino}}\;{\text{acid}}\;{\text{per}}\;{\text{g}}\;{\text{of}}\;{\text{reference}}\;{\text{protein}}} \right)}}\)

(No. based on FAO/WHO/UNU amino acid requirement pattern)

@limiting amino acids

The most limiting amino acid was lysine followed by methionine. Although the protein contents of the seaweeds are quite significant (5–10% DW) the protein chemical scores are relatively low at 20–67%, which is not unusual for plant proteins. Sargassum polycystum which had the lowest protein content (5.4% DW) had the highest chemical score of 67.4% which was better than casein (58%), oats (57%), rice (56%), soybeans (47%), wheat (43%) or peanuts (55%), but was slightly less than beef (69%) (Brody 1999). Generally, all three seaweeds had similar non-essential amino acid profiles. The high levels of aspartic and glutamine acid are responsible for the special flavor and taste of seaweeds (Mabeau et al. 1992). The total amount of amino acid of the green seaweed was significantly higher than the red and brown seaweeds, in contrast to the report by Wong and Cheung (2000) on subtropical red and green seaweeds. The levels of essential amino acids of all the three seaweeds were comparable to those of the FAO/WHO/UNU (1985) and FAO/WHO (1991) requirement pattern.

Acknowledgments

The authors thank Borneo Marine Research Institute at Universiti Malaysia Sabah, and Sabah Fisheries Department for supplying the seaweeds; Noorlilie Angkono and Mohd Azizani Rosli for assistance in mineral and trace element analysis. This study was funded by the Ministry of Science, Technology and Innovation of Malaysia.

Copyright information

© Springer Science+Business Media B.V. 2008