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Fatty acid characteristics in two symbiont-bearing mussels from deep-sea hydrothermal vents of the south-western Pacific

Published online by Cambridge University Press:  06 October 2009

Vincent Pranal ,
Aline Fiala-Medioni  and
Jean Guezennec
Vincent Pranal
Affiliation:
Observatoire Océanologique ARAGO, Université Pierre et Marie Curie, CNRS URA 117, BP 44, 66651 Banyuls-Sur-Mer Cedex, France.
Aline Fiala-Medioni
Affiliation:
Observatoire Océanologique ARAGO, Université Pierre et Marie Curie, CNRS URA 117, BP 44, 66651 Banyuls-Sur-Mer Cedex, France.
Jean Guezennec
Affiliation:
IFREMER Centre de Brest, DRO/EP/LBMH, BP 70-29280 Plouzané, France
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Abstract

Two bacteria-bearing mussels, Bathymodiolus brevior and B. elongatus, collected at five deep-sea hydrothermal sites from Lau and Fiji back arc basins (south-west Pacific), were analysed for polar and neutral lipids using gas-liquid chromatography mass spectroscopy (GLC-MS). The respective fatty acid distributions found in gills and mantles were compared to data from a Mediterranean littoral filter-feeding mussel, Mytilus galloprovincialis. The main characteristic common to the gills of the two vent mussels was the high level of (n-7) monounsaturated phospholipid fatty acids, which are supposed to originate from sulphur-oxidizing symbionts. Using palmitoleic, 16:1 (n-7), and vaccenic, 18:1 (n-7), phospholipid fatty acids as bacterial markers, endobacterial biomass was estimated to account for 2–10% of the vent mussel gill volume. Vent mussel tissues were poor in plant-derived polyunsaturated fatty acids, indicating the limited importance of the photosynthesis based material in the metabolism of these hydrothermal vent bivalves. It is suggested that some compounds, such as nonmethylene-interrupted dienoic fatty acids and specific trienoic fatty acids originating from elongation and desaturation of oleic and palmitoleic acids, respectively, were synthesized in order to substitute exogenous plant-derived polyunsaturated fatty acids considered as essential in marine invertebrates. The high level of neutral lipids in vent mussel gills suggests that these compounds are used as a major energy storage material. The neutral lipid/phospholipid ratio in gills emphasized the preponderance of the endosymbionts in vent mussel nutrition. Using this ratio as an index of the physiological state, the symbiosis patterns in different hydrothermal fields were compared.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 77 , Issue 2 , May 1997 , pp. 473 - 492
Copyright
Copyright © Marine Biological Association of the United Kingdom 1997

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References

REFERENCES

Ackman, R.G., 1982. Fatty acid metabolism of bivalves. In Biochemical and physiological approaches to shellfishes nutrition. Proceedings of the second international conference on aquaculture nutrition (ed. Pruder, G.D. et al. ), pp. 358–376. Baton Rouge: Louisiana State University Press.Google Scholar
Ackman, R.G. & Hooper, S.N., 1973. Non-methylene-interrupted fatty acids in lipids of shallow-water marine invertebrates: a comparison of two molluscs (Littorina littorea and Lunatia triseriata) with the sand shrimp (Crangon septemspinosus). Comparative Biochemistry and Physiology, 46B, 153–165.Google Scholar
Bayne, B.L., Widdows, J. & Thompson, R.J., 1976. Physiological integrations. In Marine mussels, their ecology and physiology (ed. Bayne, B.L.), pp. 261–292. Cambridge University Press.Google Scholar
Belkin, S., Nelson, D.C. & Jannash, H. W., 1986. Symbiotic assimilation of C02 in two hydrothermal vent animals, the mussel Bathymodiolus thermophilus and the tube worm Riftia pachyptila. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 170, 110–121.CrossRefGoogle Scholar
Ben-Mlih, F., Marty, J.C. & Fiala-Médioni, A., 1992. Fatty acid composition in deep hydrothermal vent symbiotic bivalves. Journal ofLipid Research, 33, 1797–1806.Google ScholarPubMed
Berg, C.J. Jr, Krzynowek, J., Alatalo, P. & Wiggin, K., 1985. Sterol and fatty acid composition of the clam, Codakia orbicularis, with chemoautotrophic symbionts. Lipids, 20, 116–120.CrossRefGoogle ScholarPubMed
Bishop, D.G., 1976. Lipids and lipid metabolism. In Comparative animal nutrition. Vol. 1. Carbohydrates, lipids and accessory growth factors (ed. Rechcigl, M. and Washington, D.C.), pp. 74–98. Basel: S. Karger.Google Scholar
Bligh, E.G. & Dyer, W.J., 1959. A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology, 37, 911–917.CrossRefGoogle ScholarPubMed
Bowman, J.P., Skerratt, J.H., Nichols, P.D. & Sly, L.I., 1991. Phospholipid fatty acid and lipopolysaccharid fatty acid signature lipids in methane-utilizing bacteria. Federation of European Microbiological Societies, Microbiological Ecology, 85, 15–22.CrossRefGoogle Scholar
Bradshaw, S.A., O'Hara, S.C.M., Corner, E.D.S. & Eglinton, G., 1991. Effects on dietary lipids of marine bivalve Scrobicidaria plana feeding in different modes. Journal of the Marine Biological Association of the United Kingdom, 71, 635–653.CrossRefGoogle Scholar
Cavanaugh, C.M., 1983. Symbiotic chemoautotrophic bacteria in marine invertebrates from sulphide-rich habitats. Nature, London, 302, 58–61.CrossRefGoogle Scholar
Cavanaugh, C.M., Wirsen, CO. & Jannash, H.W., 1992. Evidence for methylotrophic symbionts in a hydrothermal vent mussel (Bivalvia: Mytilidae) from the Mid-Atlantic Ridge. Applied and Environmental Microbiology, 58, 3799–3803.CrossRefGoogle Scholar
Chevaldonné, P., Desbruyères, D. & Le Haitre, M., 1991. Time-series of temperatures from three deep-sea hydrothermal vent sites. Deep-Sea Research, 38, 1417–1430.CrossRefGoogle Scholar
Childress, J.J. & Fisher, C.R., 1992. The biology of hydrothermal vent animals physiology, biochemistry and autotrophic symbiosis. Oceanography and Marine Biology. Annual Review. London, 30, 337–441.Google Scholar
Chu, F.-L.E. & Webb, K.L., 1984. Polyunsaturated and neutral lipids in developing larvae of the oyster, Crassostrea virginica. Lipids, 19, 815–820.CrossRefGoogle Scholar
Conway, N. & Capuzzo, J.McD., 1990. The use of biochemical indicators in the study of trophic interactions in animal-bacteria symbiosis: Solemya velum, a case study. In Trophic relationships in the marine environment. Proceedings of the 24th European Marine Biology Symposium (ed. Barnes, M. and Gibson, R.N.), pp. 553–564. Aberdeen University Press.Google Scholar
Conway, N. & Capuzzo, J.McD., 1991. Incorporation and utilization of bacterial lipids in the Solemya velum symbiosis. Marine Biology, 108, 277–291.CrossRefGoogle Scholar
Conway, N., Howes, B.L., Capuzzo, J.McD., Turner, R.D. & Cavanaugh, C.M., 1992. Characterization and site description of Solemya borealis (Bivalvia; Solemyidae), another bivalve-bacteria symbiosis. Marine Biology, 112, 601–613.CrossRefGoogle Scholar
Delaunay, F., Marty, Y., Moal, J. & Samain, J.F., 1993. The effect of monospecific algal diets on growth and fatty acid composition of Pecten maximus (L.) larvae. Journal of Experimental Marine Biology and Ecology, 173, 163–179.CrossRefGoogle Scholar
De Moreno, J.E.A., Pollero, R.J., Moreno, V.J. & Brenner, R.R., 1980. Lipids and fatty acids of the mussel (Mytilus platensis d'Orbigny) from South Atlantic waters. Journal of Experimental Marine Biology and Ecology, 48, 263–276.CrossRefGoogle Scholar
Desbruyères, D., Alayse-Danet, A.M. & Otha, S., and the scientific parties of Biolau and Starmer cruises, 1994. Deep-sea hydrothermal communities in south-western Pacific back-arc basins (the North-Fiji and Lau Basins): composition, microdistribution and food-web. North Fiji Basin: STARMER French-Japanese program (ed. J.-M. Auzende and T. Urabe). Marine Geology, 116, 227–242.CrossRefGoogle Scholar
De Zwaan, A., 1983. Carbohydrate catabolism in bivalves. In The Mollusca. Vol. 1. Metabolic biochemistry and molecular biomechanics (ed. Hochachka, P.W.), pp. 138–176. New York: Academic Press.Google Scholar
De Zwaan, A. & Van Marrewijk, W.J. A., 1973. Intracellular localization of pyruvate carboxylase, phosphoenolpyruvate carboxykinase and ‘malic enzyme’ and the absence of glyoxylate cycle enzymes in the sea mussel (Mytilus edulis L.). Comparative Biochemistry and Physiology, 44B, 1057–1066.Google Scholar
Distel, D.L., 1989. Detection, identification and phylogenic analysis of endosymbiotic bacteria using ribosomal RNA sequences. In Fourth International Colloquium on Endocytobiology and Symbiosis (ed. Nardon, P. et al. ), pp. 339–342.Villeurbanne, France: INRA.Google Scholar
Distel, D.L. & Felbeck, H., 1988. Pathways of inorganic carbon fixation in the endosymbioticbearing lucinid clam Lucinoma xquizonata. Part 1. Purification and characterization of the endosymbiotic bacteria. Journal of Experimental Zoology, 247, 1–10.CrossRefGoogle Scholar
Essex, J. W., Hann, M.M. & Richards, W.G., 1994. Molecular dynamics simulation of a hydrated phopholipid bilayer. Philosophical Transactions of the Royal Society, 344, 239–260.Google Scholar
Fang, J., Comet, P.A., Brooks, J.M. & Wade, T.L., 1993. Nonmethylene-interrupted fatty acids of hydrocarbon seep mussels: occurrence and signification. Comparative Biochemistry and Physiology, 104B, 287–291.Google Scholar
Fiala-Médioni, A. & Felbeck, H., 1990. Autotrophic process in invertebrate nutrition: bacterial symbiosis in bivalve molluscs. In Animal nutrition and transport processes. Vol 1. Nutrition in wild and domestic animals (ed. Mellinger, J.), pp. 49–69. Basel: S. Karger.Google Scholar
Findlay, R.H., Trexler, M.B., Guckert, J.B. & White, D.C., 1990. Laboratory study of disturbance in marine sediments: response of a microbial community. Marine Ecology Progress Series, 62, 121–133.CrossRefGoogle Scholar
Fisher, C.R., Brooks, J.M., Vodenichar, J. S., Zandee, J.M., Childress, J.J. & Burke, R.A., 1993. The co-occurrence of methanotrophic and chemoautotrophic sulphur-oxidizing bacterial symbionts in a deep-sea mussel. Marine Ecology, 14, 277–289.CrossRefGoogle Scholar
Fouquet, Y. et al. ,, 1991. Hydrothermal activity and metallogenesis in the Lau back-arc basin. Nature, London, 349, 778–781.CrossRefGoogle Scholar
Fullarton, J.G., Dando, P.R., Sargent, J.R., Southward, A.J. & Southward, E.C., 1995. Fatty acids of hydrothermal vent Ridgeia piscesae and inshore bivalves containing symbiotic bacteria. Journal of the Marine Biological Association of the United Kingdom, 75, 455–68.CrossRefGoogle Scholar
Gabbott, P.A. & Peek, K., 1991. Cellular biochemistry of the mantle tissue of the mussel Mytilus edulis L. Aquaculture, 94, 165–176.CrossRefGoogle Scholar
Gallager, S.M. & Mann, R., 1986. Individual variability in lipid content of bivalve larvae quantified histochemically by absorption photometry. Journal of Plankton Research, 8, 927–937.CrossRefGoogle Scholar
Gallager, S.M., Mann, R. & Sasaki, G.L., 1986. Lipid as an index of growth and viability in three species of bivalve larvae. Aquaculture, 56, 81–103.CrossRefGoogle Scholar
Gehron, M.J. & White, D.C., 1982. Quantitative determination of the nutritional status of detrital microbiota and the grazing fauna by triglycérides and glycerol analysis. Journal of Experimental Marine Biology and Ecology, 64, 145–158.CrossRefGoogle Scholar
Giere, O., Conway, N., Gastrock, G. & Schmidt, C., 1991. Regulation of gutless annelid ecology by endosymbiotic bacteria. Marine Ecology Progress Series, 68, 287–299.CrossRefGoogle Scholar
Guckert, J.B., Antworth, C.P., Nichols, P.D. & White, D.C., 1985. Phospholipid, ester-linked fatty acid profiles as reproducible assays for changes in prokaryotic community structure of estuarine sediments. Federation of European Microbiological Societies, Microbiological Ecology, 31, 147–158.CrossRefGoogle Scholar
Guckert, J.B., Ringelberg, D.B., White, D.C., Hanson, R.S. & Bratina, B.J., 1991. Membrane fatty acids as phenotypic markers in the polyphasic taxonomy of methylotrophs within the Proteobacteria. journal of General and Applied Microbiology, 137, 2631–2641.CrossRefGoogle ScholarPubMed
Guezennec, J., 1991. Influence of cathodic protection of mild steel on the growth of sulphate-reducing bacteria at 35∘C in marine sediments. Biofouling, 3, 339–348.CrossRefGoogle Scholar
Gurr, M.I. & James, A.T., ed., 1980. Lipid biochemistry: an introduction, 3rd ed. London: Chapman & Hall.CrossRefGoogle Scholar
Hily, A., Le Pennée, M., Prieur, D. & Fiala-Médioni, A., 1986. Anatomie et structure du tractus digestif d'un mytilidae des sources hydrothermales profondes de la ride du pacifique oriental. Cahiers de Biologie Marine, 27, 235–241.Google Scholar
Hopkins, C.C.E., Sargent, J.R. & Nilssen, E.M., 1993. Total lipid content, and lipid and fatty acid composition of the deep-water prawn Pandalus borealis from Balsfjord, northern Norway: growth and feeding relationships. Marine Ecology Progress Series, 96, 217–228.CrossRefGoogle Scholar
Ishibashi, J., Grimaud, D., Nojiri, Y., Auzende, J.M. & Urabe, T., 1994. Fluctuation of chemical composition of the phase-separated hydrothermal fluid from the North Fiji Basin Ridge. Marine Geology, 116, 215–226.CrossRefGoogle Scholar
Johns, R.B., Nichols, P.D. & Perry, G.J., 1980. Fatty acid components of nine species of molluscs of the littoral zone from Australian waters. Comparative Biochemistry and Physiology, 65B, 207–214.Google Scholar
Jørgensen, C.B., 1990. Bivalves filter feeding: hydrodynamics, bioenergetics, physiology and ecology (ed. Jørgensen, C.B.). Denmark: Olsen & Olsen.Google Scholar
Joseph, J.D., 1982. Lipid composition of marine and estuarine invertebrates. Part II. Mollusca. Progress in Eipid Research, 22, 109–153.CrossRefGoogle Scholar
Kanazawa, A., Teshima, S. & Ono, K., 1979. Relationship between essential fatty acid requirements of aquatic animals and the capacity for bioconversion of linolenic acid to highly unsaturated fatty acids. Comparative Biochemistry and Physiology, 63B, 295–298.Google Scholar
Klingensmith, J.S., 1982. Distribution of nonmethylene-interrupted dienoic fatty acids in polar lipids and triglycerols of selected tissues of the hardshell clam (Mercenaria mercenaria). Lipids, 17, 976–981.CrossRefGoogle Scholar
Langdon, C.J. & Waldock, M.J., 1981. The effect of algal and artificial diets on the growth and fatty acid composition of Crassostrea gigas spat. Journal of the Marine Biological Association of the United Kingdom, 61, 431–448.CrossRefGoogle Scholar
Lehninger, A.L., 1981. Biochimie: Flammarion médecine sciences (ed. , Flammarion). Paris: Worth Publishers.Google Scholar
Le Pennec, M. & Prieur, D., 1984. Observations sur la nutrition d'un Mytilidae d’un site hydrothermal actif de la dorsale du Pacifique oriental. Comptes Rendus de l'Académie des Sciences. Paris, Série III, 298, 493–498.Google Scholar
Levine, D.M. & Sulkin, S.D., 1984. Nutritional significance of long-chain polyunsaturated fatty acids to the zoeal development of the brachyuran crab, Eurypanopeus depressus (Smith). Journal of Experimental Marine Biology and Ecology, 81, 211–223.CrossRefGoogle Scholar
MacCaffrey, M.A., Farrington, J.W. & Repeta, D., 1989. Geochemical implications of the lipid composition of Thioploca spp. from the Peru upwelling region 15°S. Organic Geochemistry, 14, 61–68.CrossRefGoogle Scholar
Manusco, C.A., Franzmann, H.R., Burton, P.D. & Nichols, P.D., 1990. Microbial community structure and biomass estimates of a methanogenic antartic lake ecosystem as determined by phospholipid analyses. Microbial Ecology, 19, 73–95.Google Scholar
Morse, D.E., Duncan, H., Hooker, N. & Morse, A., 1977. Hydrogen peroxide induces spawning in mollusks with activation of prostaglandin endoperoxide synthetase. Science, New York, 196, 298–300.CrossRefGoogle ScholarPubMed
Nichols, P.D., Volkman, J.K. & Everitt, D.A., 1989. Occurrence of cis-6-hexadecanoic acid and other unusual monounsaturated fatty acids in the lipids of oceanic particulate matter. Oceanologica Ada, 4, 393–403.Google Scholar
Pacey, A.A. & Bentley, M.G., 1992. The fatty acid 8, 11, 14-eicosatrienoic acid induces spawning in the male lugworm Arenicola marina. Journal of Experimental Biology, 173, 165–179.CrossRefGoogle Scholar
Page, H.M., Fiala-Médioni, A., Fisher, C.R. & Childress, J.J., 1991. Experimental evidence for filter-feeding by the hydrothermal vent mussel, Bathymodiolus thermophilus. Deep-Sea Research, 38, 1455–1461.CrossRefGoogle Scholar
Parkes, R.J. & Taylor, J., 1983. The relationship between fatty acid distributions and bacterial respiratory types in contemporary marine sediments. Estuarine, Coastal and Shelf Science, 16, 173–189.CrossRefGoogle Scholar
Powell, M.A. & Somero, G.N., 1986. Adaptation to sulfide by hydrothermal vent animals: sites and mechanisms of detoxification and metabolism. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 171, 274–290.CrossRefGoogle Scholar
Pranal, V., 1995. Marqueurs et caractéristiques biochimiques des associations symbiotiques mollusques-bactéries chimiosynthétiques. Phd thesis, Université Pierre et Marie Curie (Paris 6), Paris, France.Google Scholar
Pranal, V., Fiala-Médioni, A. & Colomines, J.C., 1995. Amino acid and related compound composition in two symbiotic mytilid species from hydrothermal vents. Marine Ecology Progress Series, 119, 155–166.CrossRefGoogle Scholar
Rajendran, N., Matsuda, O., Imamura, N. & Urushigawa, Y., 1992. Determination of microbial biomass and its community structure from the distribution of phospholipid ester-linked fatty acids in sediments of Hiroshima Bay and its adjacent Bays. Estuarine, Coastal and Shelf Science, 34, 501–514.CrossRefGoogle Scholar
Rajendran, N., Matsuda, O., Urushigawa, Y. & Simidu, U., 1994. Characterization of microbial community structure in the surface sediment of Osaka Bay, Japan, by phospholipid fatty acid analysis. Applied and Environmental Microbiology, 60, 248–257.CrossRefGoogle ScholarPubMed
Rajendran, N., Suwa, Y. & Urushigawa, Y., 1993. Distribution of phospholipid ester-linked fatty acid biomarkers for bacteria in the sediment of Ise Bay, Japan. Marine Chemistry, 42, 39–56.CrossRefGoogle Scholar
Ringelberg, D.B. et al. , 1989. Validation of signature polar lipid fatty acid biomarkers for alkaneutilizing bacteria in soils and subsurface aquifer materials. Federation of European Microbiological Societies, Microbiological Ecology, 62, 39–50.CrossRefGoogle Scholar
Sargent, J.R., Bell, M. V., Henderson, R.J. & Tocher, D.R., 1990. Polyunsaturated fatty acids in the marine and terrestrial food webs. In Animal nutrition and transport processes. Part I. Nutrition in wild and domestic animals, vol. 5 (ed. Mellinger, J.), pp. 11–23. Basel: S. Karger.Google Scholar
Sargent, J.R., Parkes, R.J., Mueller-Harvey, I. & Henderson, R.J., 1987. Lipid biomarkers in marine ecology. In Microbes in the sea (ed. Sleigh, M.A.), pp. 119–138. Chichester: E. Horwood.Google Scholar
Schoffeniels, E. & Moonen, G., 1993. La membrane plasmique. In Physiologie des régulations (ed. Masson, ), pp. 39–43. Paris: Masson.Google Scholar
Shaw, N., 1974. Lipid composition as a guide to the classification of bacteria. Advances in Applied Microbiology, 17, 63–108.CrossRefGoogle Scholar
Thompson, P.A. & Harrison, P.J., 1992. Effects of monospecific algal diets of varying biochemical composition on the growth and survival of Pacific oyster (Crassostrea gigas) larvae. Marine Biology, 113, 645–654.CrossRefGoogle Scholar
Turunen, S. & Pekkarinen, M., 1990. Fatty acid profile of the digestive gland and mantle in the bivalve Macoma balthica. Comparative Biochemistry and Physiology, 97B, 269–273.Google Scholar
Urabe, T. et al. , 1991. Yokosuka 91 Cruise with Shinkai 6500 in the North Fiji Basin, leg 1. Starmer Cruise Report, 7, 128–130.Google Scholar
Von Cosel, R., Métivier, B. & Hashimoto, J., 1994. Three new species of Bathymodiolus (Bivalvia: Mytilidae) from hydrothermal vents in the Lau Basin and the North Fiji Basin, Western Pacific, and the Snake Pit area, Mid-Atlantic Ridge. Veliger, 37, 374–392.Google Scholar
Voogt, P.A., 1983. Lipids: their distribution and metabolism. In The Mollusca, vol. 1 (ed. Hochachka, P.W.), pp. 329–371. NewYork: Academic press.Google Scholar
Wakeham, S.G. & Canuel, E.A., 1988. Organic geochemistry of particulate matter in the eastern tropical North Pacific Ocean: implications for particle dynamics. journal of Marine Research, 46, 183–213.CrossRefGoogle Scholar
Waldock, M.J. & Holland, D.L., 1984. Fatty acid metabolism in young oysters, Crassostrea gigas, polyunsaturated fatty acids. Lipids, 19, 332–336.CrossRefGoogle Scholar
Watanabe, T., Kitajima, C. & Fujita, S., 1983. Nutritional value of live organisms used in Japan for mass propagation of fish: a review. Aquaculture, 34, 115–143.CrossRefGoogle Scholar
White, D.C., 1988. Validation of quantitative analysis for microbial biomass, community structure, and metabolic activity. Archivfiir Hydrobiologie. Ergebrisse der Limnogie, 31, 1–18.Google Scholar
White, D.C., Bobbie, R.J., Morrison, S.J., Oosterhof, D.K., Taylor, C.W. & Meeter, D.A., 1977. Determination of microbial activity of estuarine detritus by relative rates of lipid biosynthesis. Limnology and Oceanography, 22, 1089–1099.CrossRefGoogle Scholar
Whyte, J.N.C., 1988. Fatty acid profiles from direct methanolysis of lipids in tissue of cultured species. Aquaculture, 75, 193–203.CrossRefGoogle Scholar
Whyte, J.N.C., Bourne, N. & Hodgson, C.A., 1989. Influence of algal diets on biochemical composition and energy reserves in Patinopecten yessoensis (Jay) larvae. Aquaculture, 78, 333–347.CrossRefGoogle Scholar
Zandee, D.I., Kluytmans, J.H., Zuburg, H. & Pieters, H., 1980. Seasonal variations in biochemical composition of Mytilus edulis with reference to energy metabolism and gametogenesis. Netherlands journal of Sea Research, 14, 1–29.CrossRefGoogle Scholar
Zhukova, N.V., 1986. Biosynthesis of non-methylene-interrupted dienoic acids from C14-acetate in molluscs. Biochemistry et Biophysic Ada, 878, 131–133.Google Scholar
Zhukova, N.V., 1991. The pathway of the biosynthesis of non-methylene interrupted dienoic fatty acids in molluscs. Comparative Biochemistry and Physiology, 100B, 801–804.Google Scholar
Zhukova, N.V., Kharlamenko, V.I., Svetashev, V.I. & Rodionov, I.A., 1992. Fatty acids as markers of bacterial symbionts of marine bivalve molluscs. journal of Experimental Marine Biology and Ecology, 162, 253–263.CrossRefGoogle Scholar