Professional Documents
Culture Documents
The attached
copy is furnished to the author for internal non-commercial research
and education use, including for instruction at the authors institution
and sharing with colleagues.
Other uses, including reproduction and distribution, or selling or
licensing copies, or posting to personal, institutional or third party
websites are prohibited.
In most cases authors are permitted to post their version of the
article (e.g. in Word or Tex form) to their personal website or
institutional repository. Authors requiring further information
regarding Elseviers archiving and manuscript policies are
encouraged to visit:
http://www.elsevier.com/copyright
Food Chemistry
journal homepage: www.elsevier.com/locate/foodchem
a r t i c l e
i n f o
Article history:
Received 27 January 2009
Received in revised form 25 September
2009
Accepted 4 November 2009
Keywords:
Chlorophyta
Fatty acids
Lipids
n6/n3 ratio
Phaeophyta
PUFAs
Rhodophyta
Tropical macroalgae
a b s t r a c t
The lipid and fatty acid compositions of 27 tropical macroalgae belonging to the three phyla, Chlorophyta,
Phaeophyta and Rhodophyta, were studied from a nutritional and chemotaxonomic perspective. The lipid
content varied widely among the species and ranged from 0.57% to 3.5% on a dry weight basis (p 6 0.01).
Chlorophyta members showed higher C18PUFAs contents than did C20 PUFAs while for Rhodophyta the
trend was opposite. The Phaeophyta members displayed a prole of C18PUFAs similar to that of Chlorophyta and of C20PUFAs to that of Rhodophyta. Both Phaeophyta and Rhodophyta species were rich in
arachadonic acid (AA) and eicosopentaenoic acid (EPA) and Ulvales in docosahexaenoic acid (DHA) content. Most of the species studied had a nutritionally benecial n6/n3 ratio (0.615.15:1). Further, the
principal component analysis clearly segregated the three phyla by their FA composition and hierarchical
cluster analysis altogether classied them into six distinct groups, suggesting that FAs can be used as a
tool for chemotaxonomic studies.
2009 Elsevier Ltd. All rights reserved.
1. Introduction
Benthic marine macroalgae, commonly known as seaweeds,
are increasingly viewed as potential sources of bioactive compounds with immense pharmaceutical, biomedical and nutraceutical importance (Veena, Josephine, Preetha, & Varalakshmi,
2006). Many macroalgal species have been used as ingredients
in both medicinal and food preparations, traditionally, in different
regions across the world (Chandini, Ganesan, Suresh, & Bhaskar,
2008). In addition, some are common sources of phycocolloids
(gelling agents) of commercial value (Cardozo et al., 2007). There
are 250 macroalgal species which have been listed as commercially utilised worldwide, among which 150 are consumed as
human food (Barrow, 2007). They are also considered as low calorie foods with high contents of minerals, vitamins, proteins and
carbohydrates (Chandini et al., 2008). Although macroalgae have
been reported to have low lipid contents, their polyunsaturated
fatty acid (PUFA) contents are superior to those of the terrestrial
vegetables (Darcy-Vrillon, 1993). They are rich in C18 and C20
PUFAs with nutritional implications and are thus, studied
extensively for biotechnological, food, feed, cosmetic and pharmaceutical applications (Chandini et al., 2008). Long-chain n 3 PUFAs, such as EPA and DHA, have various benecial clinical and
* Corresponding authors. Tel.: +91 278 256 7352; fax: +91 278 257 0885/256
6970/256 7562.
E-mail address: bjha@csmcri.org (B. Jha).
0308-8146/$ - see front matter 2009 Elsevier Ltd. All rights reserved.
doi:10.1016/j.foodchem.2009.11.006
750
and temperature were 0.2 ll and 240 C and the split ratio was
1:30. The mass spectrometer operated in electron compact mode
with electron energy of 70 eV. Both the ion source temperature
and the interface temperature were set at 200 C. FAME peaks were
identied by comparison of their retention times with those of the
standard mixture (F.A.M.E. Mix C4-C24; Sigma) by GCMS Postrun
analysis and quantied by area normalisation.
A total of 27 different macroalgal species, belonging to the Chlorophyta, Phaeophyta and Rhodophyta, were collected during the
period January to April, 2008, from different locations of Diu and
Saurashtra, coast of Gujarat, India. Ulva tubulosa, U. linza, Ulva sp.,
and Kappaphycus alverzii were collected from Okha, Hypnea musciformis from Mithapur, Grateloupia indica and G. wattii from Diu,
Gracilaria debilis from Varvala, Ahnfeltia plicata and U. reticulata
from Kotuda and U. fasciata, U. rigida, Caulerpa racemosa, C. veravalnensis, Padina tetrastomatica, Spatoglossum asperii, Stoechospermum marginatum, Cystoseira indica, Sargassum tennerrimum, G.
dura, G. furgosonii, Amphiora anceps, Hypnea esperii, Sarconema liforme, Laurencia cruciata, L. papilosa and U. lactuca from Veraval. All
the algal samples were harvested manually from their respective
sites and then transported to the laboratory in wet tissue towels
in an ice box. They were then thoroughly cleaned to remove epiphytes and detritus attached to the fronds. The cleaned fronds
were dried at 60 C, in an oven, to constant weight to determine
their dry weight. For the lipid extraction and fatty acids analysis,
algal subsamples were shade-dried and stored at 40 C prior to
analysis.
Table 1
Total lipid contents of different tropical macroalgal species.
Algal species
1.
2.
3.
4.
5.
6.
7.
8.
9.
10.
11.
12.
13.
14.
15.
16.
17.
18.
19.
20.
21.
22.
23.
24.
25.
26.
27.
*
Chlorophyta
Ulvales
Ulva tubulosa
Ulva linza
Ulva fasciata
Ulva rigida
Ulva reticulata
Ulva lactuca
Ulva sp.
Bryopsidales
Caulerpa racemosa
Caulerpa veravalnensis
Phaeophyta
Dictyotales
Padina tetrastromatica
Spatoglossum asperum
Stoechospermum marginatum
Fucales
Cystoseira indica
Sargassum tenerrimum
Rhodophyta
Ahnfeltiales
Ahnfeltia plicata
Gracilariales
Gracilaria debilis
Gracilaria dura
Gracilaria furgosonii
Cryptonemiales
Grateloupia indica
Grateloupia wattii
Corallinales
Amphiora anceps
Gigartinales
Hypnea musciformis
Hypnea esperi
Kappaphycus alverzii
Sarconema liforme
Ceramiales
Laurencia cruciata
Laurencia papillosa
2.13 0.23c
2.10 0.10c
1.83 0.20cde
2.03 0.20c
2.00 0.20cd
1.27 0.11fgh
1.77 0.25fgh
2.64 0.20b
2.83 0.15b
2.07 0.30c
3.50 0.30a
3.36 0.49a
1.23 0.11c
2.03 0.35c
1.37 0.13efgh
1.23 0.15gh
1.10 0.20gh
0.57 0.05i
1.47 0.35efgh
1.43 0.32efgh
1.23 0.15gh
1.07 0.05gh
1.00 0.20h
1.50 0.30efg
1.47 0.05efgh
1.53 0.05def
1.73 0.11cdef
ah
751
Table 2
Fatty acid composition of different species of Chlorophyta given in means SD (% of total FAME) 5.
FAs
C12:0
C13:0
C14:0
C15:0
C16:0
C17:0
C18:0
C20:0**
C22:0
C24:0
C14:1
C15:1(n 5)
C16:1(n 7)
C17:1(n 7)
C18:1(n 9)trans
C18:1(n 9)
C20:1(n 9)
C22:1(n 9
C18:2(n 6)
C18:3(n 6)
C18:3(n 3)
C20:2(n 6)
C20:3(n 3)
C20:4(n 6)
C20:5(n 3)
C22:6(n 3)
P
SFA
P
MUFA
P
PUFA
P
C18PUFA
P
C20PUFA
n 6/n 3
U.I.B
1A
2
bc
0.24 0.11
0.03 0.02b
1.13 0.12c
0.54 0.18bc
49.2 2.79bc
0.25 0.09b
4.22 1.74ab
0.42 0.12b
0.27 0.07cd
n.d
0.03 0.02b
0.16 0.09a
2.05 0.42b
0.18 0.01b
n.d
18.6 1.99a
0.20 0.05bc
n.d
10.5 0.52bcd
2.24 0.89ab
1.02 0.31b
n.d
n.d
1.83 0.75c
2.37 0.80cd
4.77 0.90abcd
56.3 1.92bcd
21.1 1.87bc
22.7 3.66bcd
13.8 1.42bc
4.20 1.55d
1.83 0.27c
99.6 3.23bcd
3
ab
0.86 0.06
0.08 0.04b
2.79 0.14a
1.11 0.43a
40.9 .52d
0.17 0.19b
3.96 1.94ab
1.13 0.81a
0.60 0.31bcd
n.d
0.05 0.04b
0
3.27 1.21ab
0.24 0.20b
n.d
15.3 2.37ab
0.41 0.10a
n.d
11.4 0.43bc
1.61 0.44bcd
1.24 0.76ab
n.d
1.24 0.08a
3.92 1.38b
4.15 1.25c
5.51 2.14abc
51.7 3.59d
19.3 1.20c
29.1 4.54b
14.3 0.93ab
9.32 2.72c
1.42 0.18c
124 4.23ab
4
abc
0.56 0.12
0.06 0.01b
1.05 0.35c
0.45 .08bcd
52.9 1.23ab
0.27 0.04b
3.82 0.46ab
0.26 0.03b
0.92 0.11bc
n.d
0.07 0.04b
0
2.25 0.09b
0.15 0.05b
n.d
12.1 1.30b
0.11 0.01c
n.d
11.7 .31ab
2.08 0.30b
1.33 0.09ab
n.d
n.d
1.58 0.43c
2.39 0.39cd
6.05 1.29a
60.3 90abc
14.7 1.28d
25.1 23bc
15.1.36ab
3.97 0.80d
1.60 0.19c
103 2.83bc
5
a
1.05 0.03
0.08 0.01b
2.35 0.21ab
0.56 0.07b
48.2 0.38bc
0.20 0.01b
3.91 0.21ab
0.84 0.32ab
0.71 0.15bcd
n.d
0.13 0.01b
0.05 0.01b
3.60 0.12ab
0.15 0.03b
n.d
18.8 0.05a
0.03 0.002d
0.02 0.001a
8.88 0.10de
0.72 0.07d
1.54 0.04 ab
n.d
n.d
1.83 0.81c
0.89 0.29d
5.81 1.53ab
57.9 0.68abc
22.8 0.15abc
19.3 0.83cde
11.1 0.02d
2.72 0.56d
1.45 0.41c
93.8 5.31cd
6
ab
0.86 0.71
0.03 0.02b
2.61 0.60a
0.45 0.06bcd
52.3 3.07ab
0.27 0.09b
5.76 1.46a
0.41 0.31b
0.97 0.59b
n.d
0
0
4.44 1.73ab
0.18 0.10b
n.d
17.1 3.76a
n.d
n.d
7.60 1.76e
0.87 0.28cd
0.95 0.37b
n.d
n.d
0.85 0.49c
1.69 0.42d
2.79 1.27cde
63.7 2.15a
21.6 3.51bc
14.7 1.86e
9.43 2.00d
2.55 0.52d
1.84 0.70bc
70.9 5.33d
7
abc
0.67 0.22
0.28 0.02a
2.74 0.26a
1.05 0.12a
43.0 2.27cd
1.31 0.24a
3.27 0.40ab
0.50 0.12b
2.07 0.17a
n.d
n.d
n.d
5.77 0.38a
1.37 0.16a
n.d
17.8 0.99a
n.d
n.d
9.44 1.20cde
3.22 0.61a
2.25 1.61a
n.d
n.d
2.50 0.66bc
0.87 0.16d
2.15 0.44de
54.9 2.18cd
25.0 0.87ab
20.1 1.76cde
14.9 0.20ab
3.37 0.82d
3.03 1.16ab
87.5.5.76cd
8
bc
0.37 0.22
0.06 0.05b
1.76 0.25bc
0.50 0.19bc
50.1 0.67b
0.14 0.02b
2.60 0.40b
0.38 0.43b
1.16 0.42b
n.d
4.16 3.15a
0.08 0.05b
4.40 2.46ab
1.18 0.73a
n.d
16.3 1.75a
0.02 0.01d
n.d
9.72 0.47bcde
0.95 0.26cd
0.95 0.12b
n.d
n.d
0.98 0.82c
1.22 0.19d
3.21 1.11bcde
57.1 0.46bc
26.1 1.39a
16.8 1.35de
11.6 0.24cd
2.20 0.59d
2.21 0.32bc
76.3 5.40d
9
bc
0.38 0.12
0.03 0.02b
2.20 0.29ab
0.13 0.04cd
57.1 6.02a
0.10 0.01b
2.14 0.86b
0.03 0.01c
0.07 0.017d
n.d
0.04 0.02b
0
5.37 1.43a
0.11 0.21b
n.d
4.75 0.17c
0.36 0.09ab
0.04 0.02a
10.3 1.21bcd
0.66 0.06d
0.78 0.21b
1.06 0.17a
0.13 0.09c
4.03 1.02b
9.54 1.70a
0.81 0.50e
62.2 5.21ab
10.7 2.39d
27.2 4.58b
11.7 1.44cd
14.7 2.98b
1.44 012c
107 5.67bc
0.15 0.02c
0.03 0.02b
1.67 0.27bc
0.04 0.002d
51.2 0.86ab
0.12 0.04b
1.75 0.54b
0.05 0.03c
0.02 0.01e
n.d
0.03 .001b
0
2.62 0.35b
0.08 0.008b
n.d
2.20 0.40c
0.04 0.006d
n.d
13.7 .64a
1.85 0.17bc
0.79 0.42b
1.14 0.06a
0.46 0.05b
14.6 0.18a
6.64 0.53b
1.08 0.20de
55.0 .08cd
4.97 0.10e
40.0 1.13a
16.3 1.06a
22.8 0.64a
3.49 0.11a
142 2.96a
n.d.: Undetectable; ad Values in a row without a common superscript are signicantly different at P < 0.01.
**
Values in a row without a common superscript are signicantly different at P < 0.05.
A
Numbers designate algal species given in Table 1.
B
U.I. (unsaturation index) was calculated by multiplying the percentage of each fatty acid by the number of double bonds followed by summing up these contributions
(Poerschmann, Spijkerman, & Langer, 2004).
752
Table 3
Fatty acid compositions of different species of Phaeophyta given in means SD (% of total FAME).
FAs
A
C12:0
C13:0A
C14:0
C15:0
C16:0
C17:0
C18:0A
C20:0A
C22:0
C24:0
C14:1
C15:1(n 5)**
C16:1(n 7)
C17:1(n 7)A
C18:1(n 9) transB
C18:1(n 9)
C20:1(n 9)
C22:1(n 9
C18:2(n 6)
C18:3(n 6)
C18:3(n 3)
C20:2(n 6)
C20:3(n 3)
C20:4(n 6)
C20:5(n 3)B
C22:6(n 3)
P
SFA
P
MUFA
P
PUFA
P
C18PUFA
P
C20PUFA
n 6/n 3
U.I.C
10B
11
12
13
14
0.11 0.06
0.03 0.02
7.29 0.57bc
0.48 0.06b
35.9 2.36a
0.11 0.02b
2.44 1.30
0.21 0.03
0.04 0.01b
n.d
0.02 0.01c
0.03 0.01b
5.87 0.49ab
0.16 0.03
1.38 0.69a
6.51 0.09a
n.d
n.d
7.92 0.47ab
2.18 0.20b
1.96 0.06c
0.57 0.12b
1.07 0.83a
21.4 1.58b
3.51 0.17c
0.78 0.45a
46.6 2.38a
14.0 0.94ab
39.4 1.49b
12.1 0.71bc
26.6 1.27b
4.46 0.81a
155 5.50 b
0.11 0.012
0.01 0.008
9.25 0.49b
0.45 0.02 b
24.5 1.03b
0.15 0.02b
1.10 0.30
0.35 0.09
0.06 0.02b
0.08 0.01b
0.11 0.004ab
0.04 0.02b
6.86 0.42a
0.25 0.02
0.20 0.09b
6.84 0.59a
0.13 0.10d
n.d
5.96 0.37c
2.67 0.25a
5.54 0.44b
0.58 0.30b
0.42 0.30a
22.7 0.97b
11.7 0.63a
0.05 0.01b
36.0 1.12b
14.4 0.86a
49.6 1.98a
14.2 0.86ab
35.4 2.11a
1.81 0.10b
203 3.06a
0.16 0.12
0.04 0.01
21.8 2.00a
0.72 0.07a
22.3 3.55b
0.28 0.03a
0.74 0.09
0.24 0.13
0.05 0.01b
0.02 0.03b
0.07 0.01bc
0.05 0.04b
1.33 0.11c
0.26 0.02
0.65 0.14b
6.64 0.50a
0.19 0.03c
0.04 0.01c
3.54 0.33d
1.46 0.06c
9.95 0.31a
0.36 0.05b
0.15 0.01b
21.0 1.21b
7.76 5.05ab
0.29 0.007a
46.3 5.54a
9.24 0.60c
44.4 6.10b
15.0 0.34a
29.2 6.11b
1.52 0.35b
176 3.56ab
0.13 0.06
0.04 0.06
3.89 1.43d
0.38 0.07 b
34.4 5.90a
0.16 0.02b
1.24 0.35
0.24 0.04
0.33 0.13a
n.d
0.15 0.05a
0.24 0.19a
4.82 0.27b
0.18 0.03
0.53 0.25b
3.98 2.01b
1.57 0.08a
0.31 0.03b
6.45 1.15bc
0.49 0.06d
0.84 0.11d
n.d
0.06 0.01b
31.9 2.91a
7.28 0.43bc
0.47 0.11a
40.9 4.39ab
11.7 2.29abc
47.5 2.71a
7.77 1.31d
39.2 3.42a
4.49 0.02a
195 4.21ab
0.35 0.15
n.d
4.81 0.49cd
0.31 0.13 b
33.8 2.60a
0.14 0.06b
0.87 0.50
0.19 0.01
0.29 0.14a
0.28 0.13a
n.d
n.d
4.83 0.68b
0.22 0.10
0.53 0.06b
4.00 0.12b
0.67 0.25b
0.54 0.03a
8.53 0.87a
0.83 0.09d
0.96 0.06d
1.31 0.11a
1.07 0.41a
29.7 2.31a
5.83 0.27bc
n.d
41.0 3.06ab
10.8 0.77bc
48.2 3.10a
10.3 1.02c
37.9 2.87a
5.15 0.37a
187 4.47ab
n.d.: Undetectable; ad Values in a row without a common superscript are signicantly different at P < 0.01.
**
Values in a row without a common superscript are signicantly different at P < 0.05.
A
Values in a row are non-signicant.
B
Numbers designate algal species given in Table 1.
C
U.I. (unsaturation index) was calculated by multiplying the percentage of each fatty acid by the number of double bonds followed by summing up these contributions
(Poerschmann, Spijkerman, & Langer, 2004).
values reported earlier for the same species. The U. lactuca from the
Chile coast also had a DHA content up to 0.8% of TFA while it was
absent in the same and other members of Ulvales from the Bohai
Sea (Li et al., 2002) and California (Khotimchenko et al., 2002).
The members of the Bryopsidales, namely C. racemosa and C.
veravalensis, also exhibited higher SFA contents (55.062.2% TFA),
(p 6 0.01) like Ulvales but registered low oleic acid, 2.24.75%
TFA, and higher PUFA contents, 27.240% TFA (p 6 0.01). Khotimchenko (1995) also described Caulerpa species with low C18 MUFA
contents. The C20 PUFA content in Caulerpa species ranged from
14.7% to 22.8% of TFA while Ulva species had a 35 times lower
content of C20 PUFA than C18 PUFA. In keeping with earlier reports, Caulerpa spp. in the present study had higher PUFA. However, Matanjun, Mohamed, Mustapha, and Muhammad (2008),
while studying C. lentilllifera, reported lower PUFA contents and described a typical FA prole of Cholorophyta with higher C18 PUFA
contents, oleic acid and low C20 PUFAs. The observed variations in
PUFA content in the present study could be attributed to the interspecic differences.
The n6/n3 ratio in the Cholorophyta members in the present
study ranged from 1.42:1 in U. linza to 3.49:1 in C. veravalensis.
The unsaturated index varied from 70.9 to 124, indicating a lower
degree of total unsaturation than in Rhodophyta and Phaeophyta
members (p 6 0.01).
3.2.2. Phaeophyta
The FA composition of 5 Phaeophyta members belonging to the
orders Dictyotales and Fucales is given in Table 3. Despite the
Table 4
Fatty ccid compositions of different species of Rhodophyta given in means SD (% of total FAME).
15B
16
17
18
19
20
21
22
0.59 0.39ab
0.07 0.07c
2.67 1.03bcd
0.63 0.31bc
26.7 2.40f
0.32 0.22abcd
2.86 0.99bcd
0.40 0.29
0.20 0.20b
n.d
0.15 0.04b
0.07 0.03c
6.42 0.42bcd
0.36 0.39a
0.95 0.21fg
1.23 0.82ab
0.02 0.01d
3.70 0.46bcd
0.80 0.06abc
34.4 1.41def
0.07 0.02d
2.46 0.11bcd
0.76 0.45
0.05 0.04 b
n.d
n.d
n.d
1.25 0.25e
0.06 0.02b
1.64 0.01def
0.10 0.01c
n.d
1.94 0.11cd
0.40 0.21c
27.8 1.52f
0.20 0.02abcd
2.57 0.07bcd
0.18 0.18
n.d
n.d
n.d
n.d
1.36 0.25e
n.d
1.42 0.12efg
0.16 0.03c
n.d
2.58 0.30bcd
0.53 0.07bc
52.7 2.22a
0.11 0.03cd
2.17 0.13bcd
0.22 0.08
0.12 0.03 b
n.d
n.d
n.d
0.99 0.25e
0.21 0.07a
2.49 0.27bc
0.85 0.61ab
0.26 0.08a
1.98 1.25cd
0.37 0.19c
26.4 2.78f
0.12 0.01cd
2.50 0.45bcd
0.36 0.28
0.21 0.10 b
n.d
0.11 0.08b
n.d
0.74 0.33e
0.14 0.05b
1.54 0.02def
0.90 0.78ab
n.d
4.28 2.01bc
0.51 0.28bc
43.4 6.71bc
0.25 0.09abcd
4.29 1.10ab
0.58 0.88
0.15 0.21b
n.d
n.d
n.d
2.09 0.40e
n.d
1.54 0.40def
0.85 0.43ab
0.20 0.04abc
4.83 0.80bc
1.49 0.98a
48.9 3.59ab
0.37 0.14a
5.80 0.65a
0.85 0.62
0.56 0.23a
n.d
0.48 0.42a
0.43 0.29a
3.07 0.53cd
0.29 0.08a
2.94 0.43ab
0.92 0.13ab
1.40 0.29a
0.21 0.15ab
0.17 0.08abc
9.93 3.12a
10.6 1.89a
ab
1.21 0.26
1.29 0.39ab
ab
50.4 6.85
49.9 .79ab
0.29 0.01abcd 0.36 0.06a
abc
4.08 1.49
4.26 1.23ab
0.63 0.60
0.32 0.31
b
0.17 0.06
0.34 0.29ab
n.d
n.d
0.15 0.11b
0.19 0.11b
0.23 0.01bc
0.23 0.13bc
3.39 0.84cd
3.22 1.99cd
0.59 0.40a
0.55 0.24a
a
3.41 0.52
2.71 0.20abc
1.62 0.26cd
0.20 0.23
0.24 0.20bc
1.41 0.46c
0.29 0.25bc
0.94 0.31bc
n.d
0.07 0.01b
34.1 5.53c
18.1 2.12bcd
1.56 0.90a
34.5 5.17fg
9.93 0.91cde
55.6 5.79abc
2.64 0.92c
52.3 7.61ab
1.78 0.16c
250 1.01ab
2.43 0.002bcd
0.07 0.003
0.06 0.002d
1.18 1.06c
0.17 0.05c
2.51 0.75a
0.46 0.37a
n.d
46.8 1.60b
0.21 0.06g
n.d
43.5 0.77ef
5.51 0.26ef
51.0 0.58bc
3.86 1.76bc
47.4 1.82b
18.8 5.46b
205 3.07cd
1.36 0.18d
n.d
n.d
2.24 0.47bc
n.d
1.90 0.25ab
n.d
n.d
58.3 0.53a
0.32 0.06g
n.d
33.2 1.13g
4.14 0.46f
62.7 1.22a
4.13 0.71bc
58.6 0.58a
27.7 3.91a
249 3.66abc
3.75 0.20ab
n.d
n.d
3.23 1.10bc
0.31 0.12abc
1.43 0.34abc
0.85 0.36a
n.d
28.0 1.81cd
0.39 0.14g
n.d
58.6 2.42bc
7.43 0.52def
34.0 0.27ef
4.97 1.03b
29.2 1.41de
18.7 5.89b
135 1.14fgh
2.58 0.95bcd
n.d
n.d
1.80 0.51bc
0.63 0.08a
1.79 0.74ab
n.d
n.d
21.1 2.03ef
37.0 4.49a
n.d
33.0 4.54g
5.10 1.35ef
61.9 5.87a
4.23 0.78bc
58.2 5.81a
0.61 0.06c
286 5.91a
3.21 0.47bc
n.d
n.d
1.32 0.97c
0.51 0.26ab
1.23 0.87abc
n.d
n.d
14.8 2.73efg
21.4 2.47bc
n.d
54.4 1.99cd
6.84 0.69ef
38.8 2.14de
3.05 1.97bc
36.1 0.51cd
0.74 0.21c
181 3.77de
1.45 0.35cd
5.38 0.20a
0.20 0.09
0.15 0.07
a
0.55 0.12
0.31 0.01b
a
10.1 2.23
2.47 0.71bc
n.d
0.39 0.21abc
0.61 0.62bc
1.29 0.86abc
0.87 0.74a
n.d
0.57 0.41a
n.d
ghi
9.54 0.18
6.70 4.06hi
4.97 0.20f
7.14 3.0ef
n.d
0.96 0.57b
63.9 2.26ab
67.9 .46a
9.41 0.65cdef 13.3 0 .46bc
26.7 1.63fg
18.9 8.73g
10.8 2.02a
4.16 1.34bc
f
16.0 2.12
13.8 7.00f
c
3.37 0.40
1.03 0.08c
97.5 2.47gh
91.3 4.11h
23
5.55 1.67a
0.48 0.60
n.d
2.05 0.43bc
0.44 0.23abc
1.16 1.03bc
n.d
n.d
6.14 1.47i
8.60 2.31ef
0.75 0.47bc
68.6 6.24a
12.7 1.33bcd
18.7 4.92g
3.65 1.09bc
14.8 3.78f
0.83 0.11c
93.6 4.63h
24
25
LC
27
0.51 0.46ab
0.03 0.01d
3.71 0.62bcd
0.68 0.14bc
36.3 0.92cde
0.21 0.17abcd
5.41 2.27a
0.30 0.34
0.05 0.04 b
n.d
0.14 0.04b
n.d
19.8 6.19a
0.10 0.07b
1.31 0.43fg
0.17 0.13c
0.09 0.02bc
0.98 0.31d
0.33 0.08c
30.6 4.07ef
0.07 0.01d
1.61 0.27d
0.07 0.03
0.07 0.03 b
0.06 0.01 b
n.d
n.d
6.60 0.45bc
0.10 0.02 b
0.92 0.19g
0.36 0.16b
0.07 0.04c
5.33 0.47b
0.69 0.28bc
38.8 1.89cd
0.13 0.09cd
1.11 0.81d
0.13 0.01
0.11 0.04 b
0.13 0.05a
0.22 0.06a
0.11 0.02c
10.0 0.69b
0.15 0.01b
2.05 0.07cde
0.11 0.01c
n.d
4.87 1.24bc
0.34 0.03c
37.8 1.02cde
0.14 0.04bcd
1.86 0.96cd
0.12 0.05
0.10 0.02 b
n.d
n.d
n.d
2.25 0.41d
0.05 0.01b
2.14 0.48cd
4.23 2.00ab
0.15 0.01
0.11 0.06cd
1.14 0.56c
0.18 0.01c
1.50 0.37abc
n.d
n.d
13.2 4.57gh
11.1 5.29e
n.d
47.2 1.96de
25.8 8.56a
27.0 9.53fg
2.83 0.26c
24.2 9.47ef
1.28 048c
141 4.05efg
1.21 0.13d
0.05 0.02
n.d
1.59 0.11c
0.22 0.04bc
0.62 0.04bc
n.d
n.d
42.6 4.38b
12.1 0.68de
n.d
34.1 4.81g
8.85 0.36cdef
57.1 5.17abc
2.43 0.11c
54.7 5.07ab
3.48 0.15c
246 1.27abc
3.26 0.27bc
0.06 0.02
0.16 0.08cd
4.01 0.33b
0.32 0.02abc
0.21 0.01c
0.48 0.32a
n.d
14.7 1.31fg
17.2 1.61cd
0.27 0.19c
46.9 1.24de
16.0 1.04b
37.2 2.27def
4.54 0.33bc
32.4 2.60de
1.10 0.05c
173 5.64def
3.00 0.23bcd
n.d
n.d
2.72 1.49bc
0.31 0.01abc
n.d
n.d
n.d
21.4 0.67de
22.8 0.72b
n.d
45.4 0.39de
7.44 0.08def
47.2 1.37cd
3.02 1.49bc
44.2 1.28bc
1.07 0.09c
213 4.89bcd
FAs
C12:0
C13:0
C14:0
C15:0
C16:0
C17:0
C18:0
C20:0A
C22:0
C24:0
C14:1
C15:1(n 5)
C16:1(n 7)
C17:1(n 7)
C18:1(n 9)
trans
C18:1(n 9)
C20:1(n n 9)A
C22:1(n-9)
C18:2(n 6)
C18:3(n 6)
C18:3(n 3)
C20:2(n 6)
C20:3(n 3)
C20:4(n 6)
C20:5(n 3)
C22:6(n 3)
P
SFA
P
MUFA
P
PUFA
P
C18PUFA
P
C20PUFA
n 6/n 3
U.I.C
n.d.: Not detected; ai Values in a row without a common superscript are signicantly different (P < 0.01).
A
Values in a row are non-signicant.
B
Numbers designate algal species given in Table 1.
C
U.I. (unsaturation index) was calculated by multiplying the percentage of each fatty acid by the number of double bonds, followed by summing up these contributions (Poerschmann, Spijkerman, & Langer, 2004).
753
754
cantly lower contents of AA (0.63%) and EPA (1.71%) of TFA for Sargassum polycystum. A similar lower AA (1021%) and EPA (1%) of
TFA has also been reported for Sargassum kjellmanianum and Sargassum thunbergii collected from Bohai Sea (Li et al., 2002). However, Cystoseira indica had slightly lower PUFA content, with
47.5% of TFA, as compared to C. osmundacea, with 54% of TFA from
the Pacic coast (Khotimchenko et al., 2002). Stoechospermum marginatum was found to have an exceptionally high myristic acid
(C14:0) content with 21.8% of TFA (p 6 0.01), which might be a
characteristic of the genus and also such high content was not
found in any other algal species in our study.
3.2.3. Rhodophyta
Totally, 13 red algal species, belonging to the orders Ahnfeltiales, Gracilariales, Cryptonemiales, Corallinales, Gigartinales and
Ceramiales, were investigated (Table 4). Their overall FA compositions had the distinct pattern of Rhodophyta (Jamieson & Reid,
1972) with relatively higher levels of palmitic acid, oleic acid, AA
and EPA. These FAs together accounted for 6586.6% of TFA
(p 6 0.01) whereas C18 PUFAs were present as minor components,
ranging from 2.64% to 4.54% of TFA, except in Amphiora anceps, in
which C18 PUFA content was 10.8% TFA. The present ndings are in
accordance with earlier studies where C20 PUFAs (AA and EPA)
were recorded as the dominant fraction of FA in red algae (Dawezynski et al., 2007; Khotimchenko et al., 2002; Khotimchenko &
Gusarova, 2004; Li et al., 2002; Sanchez-Machado et al., 2004).
From the comparative data analysis of PUFAs, the members of
the Rhodophyta can be divided into three groups. The rst group
included A. plicata, G. debilis, G. dura, G. furgosonii, A. anceps and
S. liforme, in which the content of n 6 PUFAs was higher than that
of the n 3 PUFAs, with n6/n3 ratio ranging from 1.77:1 in A. plicata
to 27.7:1 in G. dura and AA > EPA. The Grateloupia (G. indica and G.
wattii) was included in the second group where n3 PUFAs were
higher than n 6 PUFAs, with n6/n3 ratio ranging from 0.61:1 to
0.74:1 and EPA > AA. The third group included Hypnea sp. (H. musciformis and H. esperi), K. alverzii and Laurencia sp. (L. cruciata and L.
papillosa) in which the contents of n 6 and n 3 PUFAs were nearly
same with n6/n3 ratio being close to 1 and the contents of AA and
EPA were also more or less equal. DHA was absent in most of the
red algal species studied, except in A. plicata, H. musciformis, H.
esperi and L. cruciata, in which it ranged from 0.27% of TFA in L. cruciata to 1.56% in A. plicata (p 6 0.01). The unsaturation index (U.I.)
ranged from 91.3 to 286, indicating a higher degree of unsaturation
and in conformity with the fact that U.I. increases with increase in
the content of AA (C20:4, n 6) and EPA (C20:5, n 3) (Colombo
et al., 2006).
The overall results of this study showed that the palmitic acid
(C16:0) appeared to be the most abundant FA, irrespective of species. Its content was signicantly higher in Chlorophyta (40.9
52.9% TFA), followed by Phaeophyta and Rhodophyta. Palmitoleic
acid and oleic acid were the major MUFAs of the three groups studied and ranged from 4.97% to 26.1% of TFA for Chlorophyta, 9.24
14.4% for Phaeophyta and 4.1413.3% for Rhodophyta members.
The contents of PUFAs were noticeably higher within most of the algal species examined when compared with earlier studies carried
out with related species. Furthermore, most of the species examined contained approximately 90% TFA as long-chain fatty acids
(C15C24). Surprisingly, the short-chain fatty acids (C4C10) were
not detected. This may be attributed to such low amounts in the
seaweeds that they were beyond the detection limit. The fatty acids
with C11C14 carbon chains were generally low and varied between 1.87% of TFA in C. veravalnensis and 12.5% of TFA in H. esperi.
Fig. 1. Principal component analysis of 27 macroalgal species, indexed from 1 to 27 according to Table 1; bi-plot (score/loading plot) of 19 fatty acids with rst two principal
components.
the axis 1 were palmitic, stearic, DHA, LA, oleic, docosanoic, AA and
EPA, while, along the axis 2, were ALA, tetradecanoic, myristic,
pentadecanoic, elaidic and GLA. Although these percentages were
low, the analysis provided a global statistical distinction between
three groups. Axis 1 separated Group 1 from the other two groups
and included the orders Ulvales and Bryopsidales belonging to
Chlorophyta. All the species of Ulvales showed close similarity
and were positively correlated, with palmitic, stearic, DHA, LA
and oleic acid, except U. lactuca, due to higher contributions of
GLA, heptadecanoic, 10-heptadecenoic and docosanoic acid. At
the same time Caulerpa spp. were also distinct, due to higher loadings of AA and EPA. Group 2 included the two orders of Phaeophyta
(Dictyotales and Fucales) but higher contributions of tetradecanoic
acid and ALA made S. marginatum an outlier. Group 3, that included
755
Fig. 2. Principal component analysis of 27 macroalgal species, indexed from 1 to 27 according to Table 1; bi-plot (score/loading plot) of PUFAs with rst two principal
components.
756
Fig. 4. Principal component and hierarchic analysis of 27 macroalgae, indexed from 1 to 27 according to Table 1. Six groups were evidenced by the hierarchic analysis.
PCA analysis of the PUFA data matrix (LA, GLA, ALA, AA, EPA and
DHA) for evaluating their distribution in macroalgae explained 68%
of the variability, PC147%; PC221% (Fig. 2). The result showed
higher amounts of LA in all the Chlorophyta species while DHA
was exceptionally higher in Ulva spp., which is essential for visual
and neurological development of infants. Gracilaria spp. (G. dura
and G. debilis) and S. liforme had higher loadings for AA and Grateloupia spp., Laurencia spp. and A. plicata for EPA. Both these FAs
are precursors of prostaglandins, thromboxanes and other eicosanoids, which inuence inammation processes and immune reactions (Calder & Grimble, 2002).
A dendrogram was obtained by Ward hierarchical clustering,
using squared Euclidean distance (Ward, 1963) for 27 macroalgal
species described by the rst 9 principal components with eigenvalues >1 (Kaisers rule) (Fig. 3). Ward linkage is an agglomerative
clustering algorithm which starts with n singleton clusters (each
consisting of one element of the data set) and merges two clusters
on the basis of a similarity measure. Six different clusters were obtained, whereby all the species of the same family were grouped
together, except U. lactuca, which formed a separate group. In fact,
the present study revealed that FA trends remained conserved up
to orders except for Gigartinales whereas Hypneaceae and Solieriaceae were grouped separately. Similar clustering is also shown in
a two dimensional plot where the separation of individual clusters
is more illustrative (Fig. 4).
4. Conclusion
Although macroalgae showed low lipid contents (<4 g 100 g 1
DW), their PUFA contents are equivalent or even higher than those
of terrestrial vegetables. The availability of important PUFAs, such
as LA, ALA, GLA, AA, EPA and DHA, with proven biomedical and
nutraceutical applications, indicates their potential utilisation in
preparation of low fat foods. Statistical analysis exhibited that FA
signatures can be used to unravel chemotaxonomic relationships
among macroalgal species.
Acknowledgements
The nancial support received from CSIR (NWP-018) is gratefully acknowledged. The rst author (PK) gratefully acknowledges
the CSIR, New Delhi for awarding the Junior Research Fellowship
(JRF). The second (MK) and third (VG) authors also express their
gratitude to the Department of Biotechnology, New Delhi and
Department of Science and Technology, New Delhi, for their
fellowships.
References
Barrow, C. J. (2007). Marine by-products as functional food ingredients. Food
Technology International, 15. Available from www.foodtech-international.com.
Bhaskar, N., & Miyashita, K. (2005). Lipid composition of Padina tetrastomatica
(Dictyotales, Phaeophyta), brown seaweed of the west coast of India. Indian
Journal of Fisheries, 52, 263268.
Bhaskar, N., Hosokawa, M., & Miyashita, K. (2004). Comparative evaluation of fatty
acid composition of different Sargassum (Fucales, Phaeophyta) species
harvested from temperate and tropical waters. Journal of Aquatic Product
Technology, 3, 5370.
Bhosale, R. A., Velankar, D. A., & Chaugule, B. B. (2008). Fatty acid composition of the
cold water-inhabiting freshwater red alga Sirodoita kylin. Journal of Applied
Phycology, 21, 99102.
Bligh, E. G., & Dyer, W. J. (1959). A rapid method of total lipid extraction and
purication. Canadian Journal of Biochemistry and Biophysiology, 37(8), 911915.
Calder, P. C., & Grimble, R. F. (2002). Polyunsaturated fatty acids, inammation and
immunity. Journal of Clinical Nutrition, 56(Suppl. 3), 1419.
Cardozo, K. H. M., Guaratini, T., Barros, M. P., Falcao, V. R., Tonon, A. P., Lopes, N. P.,
et al. (2007). Metabolites from algae with economical impact. Comparative
Biochemistry and Physiology, Part C, 146, 6078.
Carreau, J. P., & Dubacq, J. P. (1978). Adaptation of macroscale method to the
microscale for fatty acid methyl transesterication of biological lipid extracts.
Journal of Chromatography, 151, 384390.
Chandini, S. K., Ganesan, P., Suresh, P. V., & Bhaskar, N. (2008). Seaweeds as source of
nutritionally benecial compounds A review. Journal of Food Science and
Technology, 45(1), 113.
Colombo, M. L., Rise, P., Giavarini, F., Sngelis, L. De., Galli, C., & Bolis, C. L. (2006).
Macroalgae as sources of polyunsaturated fatty acids. Plant Foods for Human
Nutrition, 61, 6772.
Critchely, A. T., Ohno, M., & Largo, D. B. (2006). World seaweed resources: An
authoritative reference system (in DVD format). Berkshire, UK: ETI Information
Services Ltd.. 25 pp..
Darcy-Vrillon, B. (1993). Nutritional aspects of the developing use of marine
macroalgae for the human food industry. International Journal of Food Science
and Nutrition, 44, 2335.
Dawezynski, C., Schubert, R., & Jahreis, G. (2007). Amino acids, fatty acids and
dietary bre in edible seaweed products. Food Chemistry, 103, 891899.
Ginzberg, A., Cohen, M., Sod-Moriah, U. A., Shany, S., Rosentrauch, A., & Arad, S. M.
(2000). Chickens fed with biomass of the red microalga Porphyridium sp. have
reduced blood cholesterol level and modied fatty acid composition in egg yolk.
Journal of Applied Phycology, 2, 325330.
Herbreteau, F., Coiffard, L. J. M., Derrien, A., & De Roeck-Holtzhauer, Y. (1997). The
fatty acid composition of ve species of macroalgae. Botanica Marina, 40, 2527.
Jamieson, G. R., & Reid, E. H. (1972). The component fatty acids of some marine algal
lipids. Phytochemistry, 11(4), 14231432.
757
Poerschmann, J., Spijkerman, E., & Langer, U. (2004). Fatty acid patterns in
Chlamydomonas sp. as a marker for nutritional regimes and temperature
under extremely acidic conditions. Microbial Ecology, 48, 7889.
Rodriguez, C., Acosta, C., Badia, P., Cejas, J. R., Santamaria, F. J., & Lorenzo, A. (2004).
Assessment of lipid and essential fatty acids requirements of black seabream
(Spondyliosoma cantharus) by comparison of lipid composition in muscle and
liver of wild and captive adult sh. Comparative Biochemistry and Physiology,
139(B), 619629.
Sanchez-Machado, D. I., Lopez-Cervantes, J., Lopez-Hernandez, J., & Paseiro-Losada,
P. (2004). Fatty acids, total lipid, protein and ash contents of processesd edible
seaweeds. Food Chemistry, 85, 439444.
Temina, M., Rezankovab, H., Rezankac, T., & Dembitsky, V. M. (2007). Diversity of
the fatty acids of the Nostoc species and their statistical analysis. Microbiological
Research, 162, 308321.
Veena, C. K., Josephine, A., Preetha, S. P., & Varalakshmi, P. (2006). Benecial role of
sulfated polysaccharides from edible seaweed Fucus vesiculosus in experimental
hyperoxaluria. Food Chemistry, 100, 15521559.
Visentainer, J. V., Noffs, M. D. A., Carvalho, P. O., de Almeida, V. V., de Oliveira, C. C., &
de Souza, N. E. (2007). Lipid content and fatty acid composition of marine sh
species from the south coast of Brazil. Journal of American Oil Chemists Society,
84, 543547.
Ward, J. H. (1963). Hierarchical grouping to optimize an objective function. Journal
of the American Statistical Association, 58, 236244.