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Lipids and Fatty Acids of Sea Hares Aplysia Kurodai and Aplysia Juliana

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Lipids and Fatty Acids of Sea Hares Aplysia Kurodai and Aplysia Juliana Journal of Oleo Science Copyright ©2019 by Japan Oil Chemists’ Society doi : 10.5650/jos.ess19137 J. Oleo Sci. 68, (12) 1199-1213 (2019) Lipids and Fatty Acids of Sea Hares Aplysia kurodai and Aplysia juliana: High Levels of Icosapentaenoic and n-3 Docosapentaenoic Acids Hiroaki Saito1, 2＊ and Hisashi Ioka1† 1 SA Lipid Laboratory, 2-1-12, Koyanagi, Aomori 030-0915, JAPAN 2 Japan Inspection Institute of Fats and Oils, 1-8-2, Shinobashi, Koto-ku, Tokyo 135-0007, JAPAN † Present address, Shimane Prefectural Fisheries Technology Center, Hamada 697-0051, Shimane, JAPAN Abstract: The lipid and fatty acid compositions of two species of gastropods, Aplysia kurodai and Aplysia juliana (collected from shallow sea water), were examined to assess their lipid profiles, health benefits, and the trophic relationships between herbivorous gastropods and their diets. The primary polyunsaturated fatty acids (PUFAs) found in the neutral lipids of all gastropod organs consisted of four shorter chain n-3 PUFAs: linolenic acid (LN, 18:3n-3), icosatetraenoic acid (ITA, 20:4n-3), icosapentaenoic acid (EPA, 20:5n- 3), and docosapentaenoic acid (DPA, 22:5n-3). The PUFAs found in polar lipids were various n-3 and n-6 PUFAs: arachidonic acid (ARA, 20:4n-6), adrenic acid (docosatetraenoic acid, DTA, 22:4n-6), icosapentaenoic acid (EPA, 20:5n-3), and docosapentaenoic acid (DPA, 22:5n-3) in addition to trace levels of docosahexaenoic acid (DHA, 22:6n-3). Various n-3 and n-6 PUFAs (18:2n-6, 20:2n-6, 18:3n-6, 20:3n-6, 18:3n-3, 18:4n-3, 20:3n-3, n-3 ITA, and 22:3n-6,9,15) comprised the biosynthetic profiles of A. kurodai and A. juliana. Both Aplysia species have traditionally been eaten as local foods in Japan, and the high levels of n-3 (EPA and n-3 DPA) and n-6 (ARA and DTA) PUFAs indicate that they are a healthful addition to a human’s diet. Key words: arachidonic acid, docosapentaenoic acid, docosatetraenoic acid, herbivore, icosapentaenoic acid, icosatetraenoic acid, marine gastropod, marine lipid, marine-grazing food chain, polyunsaturated fatty acids 1 Introduction dae8）; clams, Veneridae9－12）; and mussels, Mytilidae11, 13））. Many studies have identified the importance of n-3 long- In contrast, relatively little information is available re- chain polyunsaturated fatty acids（LC-PUFAs）, such as garding the fatty acid composition of other mollusk species; icosapentaenoic acid（EPA, 20:5n-3）and docosahexaenoic only a few reports on the lipid and the fatty acid composi- acid（DHA, 22:6n-3）, which provide health benefits1）. tions of Gastropoda have been pubished（nudibranch: Recent studies have also proposed the beneficial health sphingolipids of Aplysia kurodai14）; Chromodoris sp. and effects of docosapentaenoic acid（n-3 DPA, 22:5n-3）, which Phyllidia coelestis15）; Dendrodoris nigra16）; Aeolidiella is involved in platelet aggregation inhibition and endothelial Abbreviations: ARA, arachidonic acid; CAEP, ceramide ami- 2） cell migration . Searching for sources of these compounds noethyl phosphonate; DMA, dimethylacetals; DMOX, 4,4-di- is an area of active interest. Although DHA sources, such methyloxazoline; DHA, docosahexaenoic acid; DPA, docosa- as tuna and krill oils, are already known throughout the pentaenoic acid; DTA, docosatetraenoic acid (adrenic acid); world3）, a high-quality source of other n-3 LC-PUFAs（EPA EPA (IPA), icosapentaenoic acid; ITA, icosatetraenoic acid; and n-3 DPA）has not been discovered. It is well established GC-MS, gas chromatography-mass spectroscopy; LC, long- that many high-trophic-level marine animals accumulate chain; LN, linolenic acid; MUFA, monounsaturated fatty acids; NMI(D), non-methylene interrupted (dienoic acids); NMR, nu- LC-PUFAs3, 4）. Some commercially important bivalves Bi- （ clear magnetic resonance; PC, phosphatidylcholine; PCA, prin- valvia）, such as oysters and mussels, have been investigat- cipal component analysis; PE, phosphatidylethanolamine; ed in detail to determine their fat and lipid profiles（oysters, PUFA, polyunsaturated fatty acids; TAG, triacylglycerols; TFA, Ostreidae5, 6）; pearl oysters, Pteriidae7）; scallops, Pectini- total fatty acids. ＊Correspondence to: Hiroaki Saito, SA Lipid Laboratory, 2-1-12, Koyanagi, Aomori 030-0915, JAPAN E-mail: [email protected] Accepted September 25, 2019 (received for review May 22, 2019) Journal of Oleo Science ISSN 1345-8957 print / ISSN 1347-3352 online http://www.jstage.jst.go.jp/browse/jos/ http://mc.manusriptcentral.com/jjocs 1199 H. Saito and H. Ioka stephanieae17）; limpet18）; vent snail, Provaniidae19）; muscular tissues, gonads, digestive glands, and other common periwinkle, Littorinidae20）; abalones, Haliotidae21, 22）; viscera; in addition, the stomach contents were analyzed and turban shell, Turbo cornutus23））. （Table 1）. The muscular tissues included the foot, mantle, The herbivorous gastropod, the sea hare（genus Aplysia, tail, parapodia, rhinophore, and other muscular tissues. Aplysiidae, Anaspidea, Heterobranchia）, grazes on small Aplysia spp. are hermaphrodites, therefore, the gonad macroalgae in the tidal and subtidal zones of tropical and were separated into ovaries and testis. Each sample was temperate regions. Near Japan, two Aplysia species, homogenized in a mixture of chloroform and methanol（2:1, Aplysia kurodai Baba（the Northwestern Pacific）and vol/vol）, and a portion of the homogenized sample was ex- Aplysia juliana Quoy & Gainard（cosmopolitan, circum- tracted according to the Folch procedure27）. The Folch ex- tropical in all warm seas）, inhabit the sea surrounding the traction was performed as follows: 10 g of sample tissue Japanese archipelago24, 25）. In some coastal areas of Japan, was homogenized in 60 mL of methanol, 55 mL of chloro- Aplysia species are traditional, local foods that are consid- form was added, and the mixture was homogenized again. ered healthy and medicinal. Although the ecological func- The mixture was filtered, and the residual precipitate was tions of these species have been well documented24, 25）, the washed three times with 5 mL of chloroform（filtrate 1: ap- fatty acid and lipid profiles have yet to be rigorously eluci- proximately 120 mL）. The residue was homogenized with dated（however, sphingolipids have been studied14, 26））; in 55 mL of chloroform and washed with 5 mL of chloroform particular, a detailed analysis of their PUFAs is lacking. To （filtrate 2: approximately 60 mL）. Then, 0.8％ of brine（35 clarify the health benefits and lipid physiologies of A. mL）was added to the combined filtrate（1 and 2）at a final kurodai and A. juliana, the present study presents an ratio of 8:4:3 chloroform/methanol/brine in a separatory analysis of the lipid and fatty acid compositions of these funnel. After allowing to stand for 3 h, the chloroform layer two species. was collected and dried over anhydrous sodium sulfate; after evaporation, the crude lipids were stored in an argon atmosphere. The crude lipids of the organs of A. kurodai and A. juliana were separated on silicic acid columns 2 Materials and Methods （Merck and Co. Ltd., Kieselgel 60, 70-230 mesh）, and a 2.1 Materials quantitative analysis of the lipid constituents was per- The samples of A. kurodai（9 individuals, 502.1±118.0 formed via gravimetric analysis of each collected fraction12）. g）and A. juliana（13 individuals, 336.4±33.1 g）were col- lected from the sea off the Japanese coast of Honshu Island 2.3 NMR spectroscopy and the determination of lipid （34°54’N; 132°04’E, in Hamada City, Sea of Japan）. classes Spectra were recorded on a GSX-270 NMR spectrometer 2.2 Lipid extraction and analysis of lipid classes （JEOL Co. Ltd., Tokyo, Japan）in a pulsed Fourier trans- All samples of A. kurodai and A. juliana were dissect- form mode at 270 MHz in a deuterochloroform solution ed, and the organs were divided into 4 groups: foot and using tetramethylsilane as the internal standard28）. Table 1 The lipid contents and lipid classes of the two Aplysia species. 1200 J. Oleo Sci. 68, (12) 1199-1213 (2019) Lipids and Fatty Acids of Sea Hares Aplysia spp. 2.4 Preparation of methyl esters and gas-liquid chroma- with Shimadzu Model C-R3A（Shimadzu Seisakusho Co. tography analysis Ltd.）and HP ChemStation System（A. 06 revision, Yokoga- The individual components of the TAG, PE and PC frac- wa HP Co. Ltd.）electronic integrators. tions were converted into fatty acid methyl esters by direct transesterification with methanol and 1％ concentrated 2.5 Preparation of 4,4-dimethyloxazoline（DMOX）deriva- hydrochloric acid under reflux for 1.5 h12）. The methyl tives and their analysis by gas chromatography - esters were purified using silica gel column chromatogra- mass spectrometry（GC-MS） phy via elution with n-hexane/diethyl ether（10/1, v/v）. DMOX derivatives were prepared by adding excess The compositions of the fatty acid methyl esters were 2-amino-2-methylpropanol to a small amount of the fatty determined by gas-liquid chromatography. Analysis was acid methyl esters（for example, 30 mg of fatty acid methyl performed on a Shimadzu GC-8A（Shimadzu Seisakusho esters and 1 mL of 2-amino-2-methylpropanol）in a test Co. Ltd., Kyoto, Japan）and an HP-6890（Hewlett Packard tube in an argon atmosphere. The mixture was heated at Co., Yokogawa Electric Corporation, Tokyo, Japan）gas 180℃ for 18 h. The reaction mixture was cooled, poured chromatograph equipped with an Omegawax-250 fused onto saturated brine, and extracted with n-hexane. Tripli- silica capillary column（30 m×0.25 mm i.d.; 0.25 µm film, cate extractions with n-hexane were perfomed; the ex- Supelco Japan Co. Ltd., Tokyo, Japan）. The temperatures tracts were washed with saturated brine and dried over an- of the injector and the column were held at 230℃ and hydrous sodium sulfate. The solvent was removed under 215℃, respectively, and the split ratio was 1:76（FID detec- reduced pressure, and the samples were again dissolved in tor at 240℃）.
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