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Original article
Marine Biotechnology and Ecology Discipline, Central Salt and Marine Chemicals Research Institute, (CSIR) Bhavnagar 364 002, Gujarat, India
Laboratory of Biofunctional Chemistry, Graduate School of Fisheries Science, Hokkaido University, 3-1-1 Minato Cho, 041 8611 Hakodate, Japan
Department of Meat, Fish and Poultry Technology, Central Food Technological Research Institute (CSIR), 570 020 Mysore, India
a r t i c l e
i n f o
Article history:
Received 18 March 2014
Accepted 29 April 2014
Keywords:
Enteromorpha
Seaweed
Proximate
Mineral
Toxic limit
Fatty acids
Amino acids
a b s t r a c t
Studies on proximate, mineral, fatty and amino acid composition of edible Enteromorpha species,
viz. Enteromorpha compressa, Enteromorpha linza and Enteromorpha tubulosa, collected from the Northwest coast of India, revealed for species-dependent nutrient composition variation. The present study
showed a higher amount of sugar (51.05 1.22%), protein (19.09 0.91%) and lipid content (5.56 0.16%)
E. tubulosa. Amongst the seventeen elements analyzed (Ca, K, Mg, Na, P, As, Cd, Co, Cu, Fe, Hg, Mn, Mo,
Ni, Zn, Cr, Pb), all three species showed a higher amount of calcium content. E. compressa was obtained
with rich amount of macro-elements (11.42 0.017 g/100 g dry wt), while maximum micro- and traceelements (81.51 6.65 mg/100 g dry wt) were recorded in E. linza. Amino acid analysis revealed seven
out of the 10 essential amino acids were present either in excess or at-par with the reference proteins.
Moreover, all the three species studied possessed relatively high n-3 fatty acids; additionally they had
more unsaturated fatty acids than saturate ones, except in E. compressa. Therefore, based on the present
investigation, it could be stated that the three species studied could be used as food supplements to
improve the nutritive value in the omnivorous diet.
2014 Elsevier Masson SAS. All rights reserved.
1. Introduction
Seaweeds have been used directly or indirectly as human food
in Asian countries and are considered under-exploited resources
[1]. About 250 species have been commercially utilized worldwide,
about 150 species are favorably consumed as human food, while,
in western countries they form a source of polysaccharides (agar,
alginates, carrageenans) for food and pharmaceutical industry [2].
Seaweeds are good sources of nutritionally important PUFAs and
they contains a rich in minerals viz., micro- and macro-nutrients
and biochemical constituents like proteins, carbohydrates, vitamins, etc. necessary for human diets [3,4], therefore, they form
a promising food supplement. Amongst the seaweeds currently
Corresponding author. Present address at: Gangneung-Wonju National University, Department of Marine Science and Technology Gangneung, Gangwon- 210-702
Republic of Korea. Tel.: +82 10 64933082.
Co-corresponding author. Tel.: +91 821 2514840; fax: +91 821 2517233.
E-mail addresses: ganesh3081@gmail.com (K. Ganesan), bhasg3@yahoo.co.in
(N. Bhaskar).
1
Present address: Department of Environmental Marine Sciences, College of Science and Technology, Hanyang University, Ansan 426 791, Republic of Korea.
2
Presently: JSPS-Invitation Fellow at Graduate School of Fisheries Science,
Hokkaido University.
http://dx.doi.org/10.1016/j.bionut.2014.04.001
2210-5239/ 2014 Elsevier Masson SAS. All rights reserved.
consumed by humans (5% green, 62% brown and 33% red), Asia
countries ranks highest (mainly Japan, China and Korea) in consumption, and the demand has extended to North America, South
America and Europe [5]. Even the coastal dwellers of South India
extensively consume fresh and dried seaweeds such as Gracilaria
edulis, Ulva lactuca, Caulerpa racemosa, Eucheuma, Enteromorpha,
Porphyra and Hypnea. Depending on the type of species, they are
generally suitable for variety of dishes like Ulva jam, agar jelly,
salad, vegetable curry and porridge [6]. Seaweeds contains a are
good amount of protein, carbohydrates, polyunsaturated fatty acids
(PUFAs), amino acids, antioxidants, minerals, dietary bers, vitamins and protein concentrates [711].
The essential amino acids (EAA) contents of some species of Porphyra have been compared with those of soya and egg protein.
Many seaweed species possess high concentrations of arginine,
aspartic acid and glutamic acid [12] apart from being a source of
essential fatty acids such as eicosapentaenoic acid, C20:53 [13]
and 3 fatty acid C20:53 which are thought to reduce the risk of
heart disease, thrombosis and atherosclerosis [14].
The genus Enteromorpha popularly known as aonori in China,
Japan, USA, France and Chile has been used in the preparation of
variety of dishes including raw salads, soups, meals and condiments
[4]. Enteromorpha species comprises one of essential edible seaweeds in human diet [4], as it has been known to contain most
366
Table 1
Proximate composition of three Enteromorpha species viz. E. compressa, E. linza and
E. tubulosa.
Composition (%)
E. compressa
E. linza
Moisture
Ash
Total sugar
Crude ber
Lipid
Total protein
7.63 0.25
31.21 1.07a
44.08 0.11a
2.93 0.41a
3.56 0.12a
17.48 0.41a
7.14
28.33
50.01
7.14
4.10
12.5
E. tubulosa
0.37
4.51a
0.39b
0.37b
0.15a
1.26b
6.28
17.01
51.05
6.28
5.56
19.09
0.14
0.66b
1.22b
0.14b
0.11b
0.91a
Values are expressed as mean standard deviation. a, b, c: values with similar superscript in the same row are not signicantly different (P > 0.05)
E. compressa
E. linza
E. tubulosa
Ca
K
Mg
Na
P
Total (g/100 g)
4.76 0.002
1.38 0.003a
0.89 0.01a
2.75 0.001a
1.64 0.001a
11.42 0.017
5.12 0.21
0.23 0.01b
1.18 0.01b
0.52 0.04b
0.41 0.05b
7.46 0.32
5.07 0.01
0.27 0.001b
1.56 0.01b
0.72 0.001b
0.39 0.03b
8.01 0.052
As
Cd
Co
Cu
Fe
Hg
Mn
Mo
Ni
Zn
Cr
Pb
Total mg/100 g (D wt)
0.047 0.01a
0.59 0.01a
0.83 0.01a
12.7 0.15a
10.99 1.5a
0.28 0.1
1.71 0.07a
ND
0.58 0.01
7.29 0.04a
0.12 0.01
0.15 0.01
35.287 1.92
1.14 0.25b
8.64 0.13b
0.4 0.01b
13.15 0.14a
36.36 5.89b
0.37 0.04
6.44 0.03b
ND
0.59 0.01
14.12 0.13b
0.17 0.01
0.13 0.01
81.51 6.65
1.2 0.02b
9.25 0.02b
0.48 0.0b
6.7 0.01b
26.98 0.46c
0.21 0.01
4.69 0.017c
ND
0.51 0.01
7.12 0.06a
0.14 0.12
0.17 0.01
57.45 0.294
Values are expressed as mean standard deviation. ND: below the detection limit.
a, b, c: values with similar superscript in the same row are not signicantly different
(P > 0.05)
protein contents were recorded in E. tubulosa and E. linza respectively, while the protein content of E. compressa was 17.48 0.41%.
Though these protein values fell within the range of the red and
green edible seaweeds (1047%) reported by Fleurence [12] and,
they were higher than Ulva lactuca (7.06%) from northeast of Hong
Kong [26].
The lipid content of three species ranged from 3.56 0.12
to 5.56 0.11%, which was higher than lipid content of seaweeds reported for Osmundea pinnatida (4.3 6.38%) by Mabeau
and Fleurence [27] and Marshram et al. [28]. Highest crude
ber content (7.14 0.37%) was recorded in E. linza, followed
by E. tubulosa (6.28 0.14%) and E. compressa (2.93 0.41%); A
range of crude ber content in three species of Enteromorpha
(2.93 0.417.14 0.37%) was higher than the same reported for
Porphyra sp. (1.1 0.6%), Dumontia contorta (2.0 0.2%), Mastocarpus stellatus (1.8 0.5%) and Ulva lactuca (2.8 0.7%) [28]. The
mean lipid content value in these three species was found to be
E. compressa (3.56 0.12%), E. linza (4.10 0.15%) and E. tubulosa
(5.56 0.11%) which was comparable with other seaweeds and
higher than the levels reported for higher plants [21,27,29]. The
chemical nature and physicochemical properties of some common
seaweed dietary bers, such as alginates, carrageenans and agars,
are quite well known. However, most seaweed dietary bers, in
particular, the insoluble types and their physiological effects, have
still not received much attention [27].
The total macro-, micro- and trace-elements of three species
of Enteromorpha are shown in Table 2. Macro-elements (Na, K, Ca,
Mg and P) are expressed as g per 100 g dry wt, while other microand trace-elements as mg per 100 g dry wt. Macro- and microelement composition obtained for Entermorpha species were found
367
to vary signicantly. Ruprez [22] has mentioned that mineral content is bound to vary according to seaweed species, seasonal and
physiological factors. In this present study, amongst the seventeen elements analyzed, the amount of calcium content showed
higher in all three species. Lowest chromium values were recorded
in E. compressa and E. tubulosa, but E. linza showed least lead content. Higher amount of total macro-elements (Na + K + Ca + Mg,
as g/100 g dry wt) were obtained in E. compressa (9.78 0.20), followed by E. tubulosa (7.62 0.02) and E. linza (7.05 0.27). These
macro-mineral content were higher than the values reported for
edible land vegetables such as carrots 3.276, sweet corn 1.347,
green peas 1.452; potato 6.015; tomato 3.429 [24,30,31]. However, the macro-mineral in spinach (9.679) was higher than those
of E. tubulosa and E. linza.
Na/K ratios were lower than 3.0 in all the three seaweeds studied (1.992.67 g/100 g dry wt), which was indeed interesting and
benecial from the point of view of nutrition, since the intake of
sodium chloride in diet with a high Na/K ratio has been related to
the incidence of hypertension [31]. The present study indicates the
possibility of Enteromorpha species to be used as an ingredient in
food supplements to improve the nutritive value of the human diet.
The micro- and trace-elements (As, Cd, Co, Cu, Fe, Hg, Mn, Mo,
Ni, Zn, Cr, and Pb) were higher in E. linza (81.51 6.65 mg/100 g
d wt) followed by E. tubulosa (57.45 0.294 mg/100 g d wt) and
E. compressa (35.29 1.92 mg/100 g d wt). Selected micronutrients (Fe + Zn + Mn + Cu) in E. compressa, E. linza and E. tubulosa
(32.69 1.86, 70.07 8.05 and 45.49 0.54 mg/100 g d wt
respectively), were higher than that reported for sweet corn
(4.9 mg/100 g) as well as in edible seaweeds like Laminaria species
(5.1 mg/100 g d wt) [22], Monostroma oxyspermum (21.2 mg/100 g
d wt), Enteromorpha exuosa (11.8 mg/100 g d wt) Ulva faciata (11.2 mg/100 g d wt), Porphyra vietnamensis (21.3 mg/100 g
dry wt) [23], and also comparable with Porphyra vietnamensis
(45.5309 mg/100 g) from Indian coast [32]. Among the other
elements present in the seaweed were As, Cd, Cu, Hg, Pb, Cr and
Zn and their content was generally lower than the toxic limits of
several countries [30]. Based on quantity of the above elements
and keeping in mind their toxic limits, the daily-recommended
intake allowances were calculated for Enteromorpha species and
presented in the Table 3. It could therefore be recommended
to use not more than 14.29, 1.74, 1.62 g of E. compressa, E. linza
and E. tubulosa respectively. Nevertheless, these values denitely
indicate the possible use of Enteromorpha species as a food
supplements to improve the nutritive value of the human diet.
The fatty acid composition of E. compressa, E. linza and E. tubulosa
signicantly differed between the species as described in Table 4.
Specically, these three species had relatively high amounts of
n-3 fatty acids. Moreover, they also possessed more unsaturated
fatty acids than saturated fatty acid (SFA), except for E. compressa
that had marginally higher saturated fatty acid content. The SFAs
content of E. compressa signicantly differed from E. linza and
E. tubulosa, whereas, in case of E. linza and E. tubulosa no signicant differences in the content of SFAs were recorded. A similar
observation was obtained in case of the polyunsaturated fatty acids
(PUFAs) content, but the mono-unsaturated fatty acids (MUFAs)
Table 3
Daily-recommended dose of Enteromorpha species based on the toxic elements intake values.
Elements
Recommended daily
intake of E. linza (g/day)
Cd
Cr
Hg
As
Pb
50150
350
40
21
250
8.4725.42
291.67
14.29
44.68
166.67
< 1.74
205.88
10.81
1.84
192.31
< 1.62
250
19.05
1.75
147.11
368
Table 4
Fatty acid composition (%) of E. compressa, E. linza and E. tubulosa.
Fatty acid (wt%)
E. compressa
E. linza
E. tubulosa
12:0
14:0
16:0
17:0
18:0
20:0
22:0
16:1n-7
18:1n-9
18:1n-7
20:1n-9
22:1
18:2n-6
18:3n-6
20:2n-6
20:3n-6
20:4n-6
18:3n-3
18:4n-3
20:3n-3
20:5n-3
22:5n-3
SFA
MUFA
PUFA
n-6
n-3
Un-identied
0.10 0.01
0.91 0.05
44.64 1.34a
0.33 0.02
0.75 0.04
0.35 0.02
0.52 0.03
0.80 0.04
1.31 0.07
5.50 0.17a
0.12 0.01
0.21 0.01
5.79 0.29a
0.85 0.04
0.23 0.01
0.20 0.01
0.49 0.02
14.08 0.70
4.86 0.10a
0.10 0.01
0.54 0.03
1.190.06
47.60a
7.94a
28.33a
7.56
20.77
16.13
0.10 0.01
0.99 0.05
35.48 1.42b
0.52 0.03
0.52 0.03
0.27 0.01
0.55 0.03
0.77 0.04
1.12 0.06
4.83 0.34b
0.12 0.01
0.10 0.01
6.43 0.32b
0.87 0.04
0.18 0.01
0.34 0.02
0.60 0.03
15.13 1.06
9.28 0.56b
0.10 0.01
0.76 0.04
1.70 0.09
38.43b
6.94a
35.39b
8.42
26.97
19.24
0.10 0.01
0.80 0.04
34.80 0.70b
0.91 0.05
0.58 0.03
0.21 0.01
0.53 0.03
0.79 0.04
1.26 0.06
4.41 0.13b
0.10 0.01
9.61 0.48c
0.85 0.04
0.12 0.01
0.56 0.03
0.78 0.04
14.93 0.75
7.90 0.16c
0.10 0.01
0.52 0.03
1.10 0.06
37.93b
6.56a
36.47b
11.92
24.55
19.04
a, b, c: values with similar superscript in the same row are not signicantly different
(P > 0.05). SFA: saturated fatty acids; MUFA: mono-unsaturated fatty acids; PUFA:
polyunsaturated fatty acids.
the values reported for tropical marine macroalgae species [3]. All
the three species of Enteromorpha analyzed had considerable quantities of polyunsaturates including parinaric acid (18:4 n-3) as well
as gamma linolenic acid (18:3 n-3) apart from linoleic acid (18:2
n-6). Palmitic acid (16:0) has been reported to be the major saturated fatty acid in most of the tropical seaweeds [18] as it has been
conrmed in this report. As PUFA (n-3, n-6) has been reported to
offer several benecial affects to both humans as well as animals
[4,33]. In this context, the results of this study are indeed signicant.
Another signicant aspect of fatty acid composition of these three
species is the presence of considerable quantity of parinaric acid;
studies involving cancer cell lines reveal Parinaric acid (18:4 n-3) to
have anticancerous effects [34] Similarly, the occurrence of considerably higher quantity (> 14%) of 18:3 n-3 (gamma linnolenic acid)
in all the three species is signicant from the aquaculture nutrition point of view, because sh cannot synthesize PUFA but can
desaturate/elongate dietary 18:2 and 18:3 fatty acids [35].
Based on the results described in Table 5, it is evident that though
amino acids such as histidine followed by methionine and lysine
were low in these seaweeds. However, all the other amino acids
(7 out of the 10 essential amino acids) were either higher than or
equal to other reference proteins. The results are also clearly indicated that the studied seaweeds could be good source of aromatic
amino acids and leucine. Moreover, it is also evident that these
species studied could be used for supplementing essential amino
acids in food. The lysine to arginine ratio is responsible for expression of cholesterol lowering effects by dietary proteins [36]. Here,
the lysine to arginine ratio in E. compressa, E. linza and E. tubulosa
was 0.80, 0.87 and 0.81 respectively. This is extremely signicant
from the nutritional point of view as lower lysine to arginine ratio
in a protein could probably result in better hypocholesterolemic
effect [37]. This all the more emphasize on its potential application
in foods and food products that would provide cholesterol lowering
effects.
Minimum dietary requirements (as dry weight) for several sh
species suggest values of methionine, cysteine, lysine and arginine
to vary from 0.56 to1.35%, 0.54 to 0.74%, 1.2 to 2.1%, and 1.59 to
2.4% respectively [35]. The essential amino acid (EAA) composition
Table 5
Amino acid composition (g/100 g) of the three Enteromorpha species viz. E. compressa, E. linza and E. tubulosa.
Amino acids
Chemical scoresa
Test protein
Standard proteins
E-1
1.10
4.73
8.29
4.71
2.36
5.61
3.28
5.59
5.88
6.82
E-2
1.36
4.79
8.27
4.98
2.41
5.75
3.39
5.56
5.70
6.68
E-3
1.40
4.73
8.05
4.64
2.34
5.82
3.38
5.60
5.70
6.56
11.93
13.11
4.83
6.45
8.70
4.97
0.41
1.23
11.85
12.68
4.91
6.38
8.74
4.89
0.49
1.17
12.02
12.52
5.11
6.40
9.14
4.83
0.59
1.15
RP-1
2.00
4.00
7.00
5.50
3.50
4.29b
4.00
1.21
5.00
5.42
RP-2
2.10
2.50
3.30
5.70
3.10
6.50b
3.90
0.80
1.30
3.60
E. compressa
RP-3
2.20
2.70
4.30
5.20
2.40
3.70b
3.50
0.50
5.10
3.40
RP-1
0.55
1.18
1.18
0.86
0.67
2.07
1.40
1.18
1.26
RP-2
0.52
1.89
2.51
0.83
0.76
1.37
1.43
4.52
1.89
E. linza
RP-3
0.50
1.75
1.93
0.90
0.98
2.40
1.60
1.15
2.01
RP-1
0.68
1.20
1.18
0.91
0.69
2.13
1.39
1.14
1.23
E. tubulosa
RP-2
0.65
1.92
2.50
0.87
0.78
1.40
1.43
4.38
1.86
RP-3
0.62
1.77
1.92
0.96
1.00
2.47
1.59
1.12
1.97
RP-1
0.70
1.18
1.15
0.84
0.67
2.15
1.40
1.14
1.21
RP-2
0.67
1.89
2.44
0.81
0.75
1.42
1.44
4.39
1.82
RP-3
0.64
1.75
1.87
0.89
0.97
2.49
1.60
1.12
1.93
RP-1: essential amino acid composition of reference protein according to FAO/WHO 1985; RP-2: essential amino acid requirements of juvenile common carp according to
NRC, 1983; RP-3: essential amino acid requirements of marine penaeid shrimp (Penaeusmonodon) according to Millamena et al. [4044]; E-1: E. compressa; E-2: E. linza; E-3:
E. tubulosa.
a
Chemical scores with reference proteins as base as per Vidotti et al. [45].
b
Sum of tyrosine and phenyl alanine content.
of reference protein according to FAO/WHO 1985 [38] EAA requirements of juvenile common carp according to NRC, 1983 [39] and
EAA requirements of marine penaeid shrimp (Penaeus monodon)
according to Millamena et al. [4044] are given in the Table 5.
The chemical scores with reference protein are also presented in
Table 5 according to Vidotti et al. [45]. The results obtained herein
comply the demand of amino acid composition thereby suggesting the three species to be signicant from the point of view of
aquaculture nutrition. It is therefore concluded that all these three
Enteromorpha species were a good protein source thereby they
could be used in the human diet to supply adequate essential amino
acids moreover, they could also be incorporated into aquaculture
feed formulations.
4. Conclusion
The three Enteromorpha species viz. E. compressa, E. linza and
E. tubulosa, studied herein were rich in protein, lipids and minerals. Apart from having acceptable amounts of essential amino
acids, they also contained considerable quantities of n-3 fatty acids.
This projects their potential use in human diet as well as in aquaculture feed formulations. Especially, the lower lysine to arginine
ratio recorded herein for the proteins of Enteromorpha makes them
potential candidates in formulating health foods. It is absolutely
essential to point out the utility value of these species, which could
help in their proper utilization and also publicizing the probable use
of Enteromorpha species as a value added food supplement. Apart
from serving as a source of income, this would help to improve the
aesthetics of beaches and boost the tourism.
Disclosure of interest
The authors declare that they have no conicts of interest concerning this article.
Acknowledgements
Authors express their gratitude to Dr. P.K. Ghosh, Director, Central Salt and Marine Chemicals Research Institute (CSIR), Bhavnagar
for his encouragement and the facilities provided. Moreover, the
author K. Ganesan is especially thankful to Council of Scientic and
Industrial Research (CSIR), New Delhi for nancial assistance in the
form of Senior Research Fellowship.
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