Fatty Acid Composition of Twelve Algae from Japanese Waters
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1 Fatty Acid Composition of Twelve Algae from Japanese Waters Toru TAKAGI, Masahiko ASAHI, and Yutaka ITABASHI Department of Chemistry, Faculty of Fisheries, Hokkaido University (Minato-cho, Hakodate, Hokkaido) Open-tubular gas chromatographic analysis was carried out on fatty acids from the total lipids from each of 3 species of the Chlorophyta (I), and Rhodophyta (II), and 6 speices of Phaeophyta (III). The specific features of polyenoic acids in each class were relatively high percentages of 16:3 (n-3) (2.2 `7.8%) and 16:4 (n-3) (16.2 `17.7%) in I, 20:4 (n-6) (60%) or 20:5 (n-3) (51%) in II, and one or more of 18:3 (n-3), 18:4 (n-3), 20:4 (n-6), and 20:5 (n-3) in III. The percentage of 20:4 (n-6) in total lipids from Garcilaria verrucosa was noticeably as high as 60% of the total acids, and 91% of the total polyenoic acids. The algae belong to II are expected to be the source for 20:4 (n-6) and 20:5 (n-3). The 18:1 (n-7)/18:1 (n-9) ratios were generally high in I, and extremely low in III. 1 Introduction Although a number of studies have been carried out on the fatty acid compositions of marine algae as described in the reviews1),2), the detailed compositions obtained by opentubular gas-liquid chromatography (GLC) have been reported only in small number of papers3) `5). In this study, composition of fatty acids from the total lipids from the samples of 12 species of marine algae was obtained by the analysis with open-tubular GLC. The alga samples were obtained in Japanese waters, and most of them are employed for the edible purposes. The samples used in the previous studies for opentubular GLC analysis were obtained from the Atlantic coast3),5) and Australian waters4). The detailed fatty acid compositions of algal lipids presented by this paper are important in order to allow fatty acids to be used directly in food chain studies, e.g. the studies on the sea urchin lipids6). The data may be also useful to identify distinguishing taxonomic features. 2 Experimental 2 E1 Materials The species of algae studied and the contents of total lipids and fatty acids are listed in Table-1. A sample No.2 was obtained from the Ise Bay in Mie prefecture. Dried products of algae, sample No.6 and 7, were obtained at a grocery store. Other samples were collected from an intertidal zone at Hakodate. The species of them were identified by members of the laboratory of marine botany of our faculty. 2 E2 Extraction and Methanolysis of Lipids After washing of algae in distilled water, the algae were cutted fine and extracted by the method of Bligh and Dyer7). The dried algae were ground to powder with an electric mill and extracted by the same method. Total lipids were saponified by refluxing with 1M KOH/ ethanol for 1h, and the unsaponifiables were extracted with ether. Following acidification with dilute HCl, fatty acids were recovered by n- hexane extraction and were converted to methyl esters by heating in a sealed tube at 100 Ž for 15min with 7% BF3-MeOH. A nitrogen atmosphere was maintained at all times. 2 E3 Open-Tubular GLC and AgNO3-TLC Open-tubular GLC of the methyl esters was carried out with a Shimadzu GC-6 A and GC- 7 A (Shimadzu Seisakusho, Kyoto) equipped with a flame-ionization detector. The glass wall-coated open-tubular column used were 60 m in length and 0.28mm i.d., coated with Silar 12
2 Table-1 Species of algae and contents of total lipids and fatty acids. a) Percentages to wet weight except 2, 9, and 10 (percentages of dry weight). b) Percentages to total lipids. 5 CP. The carrier gas was N2 or H2 (flow rate about 0.5ml/min). The column temperature was 160 Ž, and the detector and injector were 230 Ž. Peak area percentages and retention data were obtained with Shimadzu integrator E1 A and R1 A. The detailed conditions for GLC were described in the previous paper8). The component of each peak on the gas chromatogram was identified as shown in Table -2 on the basis of agreement of the retention data with those of the reference specimen, methyl esters of sea urchin fatty acid6),9). The log plot procedure and systematic separation factor procedures10) were used concurrently for the identification. The separation of fatty acid methyl esters based on the degree of unsaturation was carried out by preparative argentation thin-layer chromatography (AgNO3-TLC) on silver nitrateimpregnated layers of Silica Gel G by developing with n-hexane/ether, 95:5 or 90:10. The fractions of methyl esters of alga fatty acids separated by their degrees of unsaturation with AgNO3-TLC were also used for identification and to verify that specific peaks in GLC of total esters were single components with one or more cis olefinic bonds. 3 Result and Discussion 3 E1 Major Fatty Acid Components The fatty acid components of alga lipids detected by GLC are shown in Table-2, The major components, those percentages to the total acids are above 3% in one or more acid samples in each class, were 16:0, 18:1 (n-7) (cis-7-octadecenoic acid), 16:3 (n-3) (all-cis- 7, 10, 13-hexadecatrienoic acid), 16:4 (n-3), 18: 2 (n-6), 18:3 (n-3), 18:4 (n-3), 20:5 (n-3), and 22:5 (n-3) in Chlorophyta, 14:0, 16:0, 16:1 (n-7), 18:1 (n-9), 18:2 (n-6), 18:3 (n- 3), 18:3 (n-4), 20:4 (n-6), and 20:5 (n-3) in Phaeophyta, and 14:0, 16:0, trans-16:1 (n- 13), 18:1 (n-9) and (n-7), 20:4 (n-6), and 20:5 (n-3) in Rhodophyta. The total contents of the major components were higher than 90 % in each sample, except sample No.2 (88%) in Table-2. The proportion of minor components were generally higher in Chlorophyta (9 `12%) than in Phaeophyta (5 `9%) and Rhodophyta (6 `10%). The major components described above almost agreed with those reported as the major fatty acid components of algal lipids in the previous papers3) `5),8),11). In most of marine lipids, 20:1 and 22:1 are major fatty acid components12) `14), but they have been reported as the minor acids but not major acids in marine algal lipids3) `5),8),11). The results shown in Table-2 also supports this specific features. The ordinary polyenoic fatty acids in marine lipids, 22:6 (n-3) are minor or trace components, or unable to be found in marine algal lipids3) `5),8),11). The similar fact was observed in this study. It is attributable to the decarboxylation of 22:6 (n-3) to polyene hydrocarbon, e.g. all-cis-3, 6, 9, 12, 15, 18-21:6 hydrocarbon15), or inactive biosynthesis of 22: 6 (n-3) acid. 3 E2 Saturated Fatty Acids 13
3 Table-2 Fatty acid composition of marine alga lipids. a) Tentatively identified by comparison of the retention data3) `5). The percentages of 14:0 in the total fatty acids of Chlorophyta lipids were below 3% in all samples., while they were relatively higher percentages such as 4 `10% in those of Phaeophyta and Rhodophyta lipids. This specific feature of Chlorophyta lipids are valid in the data of the previous papers1) `5), though high percentages of 14:0 were reported for fatty acids of Cladophora: 9.76% for C. fascicularis and 3.7 `6.2% for C. rupestris, exceptionally. The percentages of 16:0 were relatively lower in the lipids of Chlorophyta, and they varied in very wide range upto 55% in Rhodophyta and upto 39% in Phaeophyta. The sample No. 11 (G. furcata) showed significantly high 16: 0 percentage 55% and high saturated acid percentage 63%. The highest percentages of these which have been reported are 41.7% for 16:0 and 47.6% for total saturated acids in fatty acids of Ptilota serrata3). 14
4 3 E3 Monounsaturated fatty acids The occurrence of cis-vaccenic acid [18:1 (n-7)] in the algae have hitherto been reported in the previous paper1),2). In this study, it was found in the fatty acids from the lipids of Chlorophyta and Rhodophyta in relatively high level. It is noticeable that the 18:1 (n-7)/18:1 (n-9) ratios were significantly high in the fatty acids from 2 species of Chlorophyta, and 1 species of Rhodophyta. The ratios increased in the order, Phaeophyta, Fig.-1 Gas chromatogram of fatty acid methyl esters on green alga Ulva pertusa. Rhodophyta and Chlorophyta on the whole. This relation are valid in the data reported in the previous papers1),2). The percentages of total monoenoic acids were below 30% in all samples used in this study, and most of the samples used in the previous studies1) `5). In the marine lipids, the total percentages of monoenoic acids generally varied in a more wide range12) ` 14). 3 E4 Polyunsaturated Fatty Acids The proportion of each polyunsaturated fatty acid in the algal lipids are shown in Fig. Fig.-2 Gas chromatogram of fatty acid methyl esters of brown alga Heterochordaria abietina. -1 to 3. The most remarkable feature of Chlorophyta fatty acids was relatively high percentages of 16:3 (n-3) (2.2 ` 7.8%) and 16:4 (n-3) (16.2 ` 17.7%) as shown in Table-2 and Fig.-1. The percentages of these fatty acids were below 0.5% in the samples of other classes. The high percentages of 16:4 (n-3) have been already reported for the fatty acids from Chlorophyta in the previous papers3) `5). The high percentages of 16:3 (n-3) (7.8%) in the acids from the sample No.3 Fig.-3 Gas chromatogram of fatty acid methyl esters of red alga Gloiopeltis furcata. 15
5 was noticeable in this study, since the highest percentage reported was 5.3% in the fatty acids from the total lipids from Enteromorpha intestinalis lipids5). The percentages of 16:3 (n-3), 16:4 (n-3), 18:3 (n-3), and 18:4 (n-3) in the acids from Rhodophyta lipids were below 1%, and the chief polyenoic acids in the lipids were 20:4 (n-6) or 20:5 (n-3) as shown in Table-2 and Fig.-3. In the previous papers1) `5), 20:4 (n-6) or/and 20:5 (n-3) have been reported to be predominant polyenoic acids1) `5). The high percentages of 20:4 (n-6) 60.3% in the acids from the sample No.12 was striking, since the highest percentages reported for 20:4 (n-6) in the acids from Centroceras claratum in Rhodophyta4). Fatty acids from Phaeophyta contained 18:3 (n-3), 18:4 (n-3), 20:4 (n-6), and 20:5 (n-3) as major polyenoic acids as shown in Table-2 and Fig.-2. The results agreed with the specific features of the polyenoic acids in Phaeophyta lipids reported in the previous papers1) `5). 3 E5 Importance of Fatty Acids in Algal Lipids The lipids from the algae have possibility as the resource of some polyenoic acids. The algae belong to Rhodophyta are expected to be original materials for 20:4 (n-6) and 20:5 (n-3), and the algae belong to Chlorophyta for 16:4 (n-3), 18:4 (n-3) and 16:3 (n-3), respectively. In the sample No.12, 20:4 (n-6) were 83% to the total unsaturated acids, and 91% to the total polyenoic acids. It can be an excellent source for 20:4 (n-6). However, it is a very difficult problem to get the alga samples which contain fatty acids of similar compositions through all seasons, because the lipid composition changes in the wide range depending the various factors such as temperature, characteristics and intensity of light, the levels of minerals, nitrogen compounds, and others in the medium, and the period in the life cycle of algae1),16). The investigation on these influence of the factors and the screening of the fatty acid composition of the natural and cultivated algae obtained from the various origins must be necessary to get the algae containing the desired fatty acids in abundance. (Received July 11, 1985) References 1) P. Pohl and F. Zurheide, gmarine Algae in Pharmaceutical Science (ed. H.A. Hoppe, T. Levring, and Y. Tanaka) h Walter de Gruyter, Berlin (1979) p ) J.D. Weete, gchemistry and Biochemistry of Natural Waxes (ed. P.E. Kolattukudy) h Elsvier, Amsterdam, p ) R.G. Ackman and J. McLachlan, Proc. N.S. Inst. Sci., 28, 47 (1977). 4) R.B. Johns, P.D. Nichols, and G.J. Perry, Phytochemistry, 18, 799 (1979). 5) G.R. Jamieson and E.H. Reid, Phytochemistry 11, 1423 (1972). 6) T. Takagi, C.A. Eaton, and R.G. Ackman, Can. J. Fish. Aquat. Sci., 37, 195 (1982). 7) E.G. Bligh and W.J. Dyer, Can. J. Biochem. Physiol., 37, 51 (1959). 8) Y. Itabashi and T. Takagi, Yukagaku, 29, 855 (1980). 9) T. Takagi, M. Kaneniwa, and Y. Itabashi, Bull. Fac. Fish. Hokkaido Univ., 33, 263 (1984). 10) R.G. Ackman, gmethods in Enzymology Vol. 14 (ed. J.M. Lowenstein) h, Academic Press, New York (1969) p ) T. Takagi and T. Aoyama, Bull. Fac. Fish. Hokkaido Univ., 35, 50 (1984)., 12) R.G. Ackman, gfish Lipids. Part 1 h, in Advances in Fish Sciences and Technology (ed. J.J. Connell) h Fishing News Books, Garnham, Surrey, England (1980) p ) R.G. Ackman, gfatty Acid Compositions of Fish Oils h, in Nutritional Evaluation of Long Chain Fatty Acids in Fish Oil (ed. S.M. Barlow and M.E. Stansby) h, Academic Press, New York (1982) p ) J.R. Sargent, gthe Structure, Metabolism and Function of Lipids in Marine Organisms, in Biochem. Biophys. Perspectives in Marine Biology, Vol.3 (ed. D.C. Mallins and J.R. Sargent) h, Academic Press, New York (1976) p ) W.W. Yougblood, M. Blumer, R.L. Guillard and J. Fiore, Marine Biology, 8, 190 (1971). 16) W.D.P. Stewart, galgal Physiology and Biochemistry h, Blackwell Sci. Pub. London (1983) p. 15 and 236.
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