Hostname: page-component-586b7cd67f-2plfb Total loading time: 0 Render date: 2024-11-22T21:25:06.091Z Has data issue: false hasContentIssue false

Fatty Acids of Hydrothermal Vent Ridgeia Piscesae and Inshore Bivalves Containing Symbiotic Bacteria

Published online by Cambridge University Press:  11 May 2009

J. Gregor Fullarton
Affiliation:
NERC Unit of Aquatic Biochemistry, Department of Biological & Molecular Sciences, University of Stirling, Stirling, FK9 4LA.
Paul R. Dando
Affiliation:
Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB.
John R. Sargent
Affiliation:
NERC Unit of Aquatic Biochemistry, Department of Biological & Molecular Sciences, University of Stirling, Stirling, FK9 4LA.
Alan J. Southwards
Affiliation:
Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB. Department of Biology, University of Victoria, Victoria, British Columbia, Canada, V8W 2Y.
Eve C. Southward
Affiliation:
Marine Biological Association, Citadel Hill, Plymouth, PL1 2PB.

Extract

Ridgeia piscesae from a hydrothermal vent and lucinid and thyasirid bivalves from inshore Canadian and UK waters, known to contain sulphur-oxidizing symbiotic bacteria, had lipids rich in 16:0,16:l(n-7) and 18:l(n-7) fatty acids in both bacteria-rich trophosome or gill tissue and in tissues without symbiotic bacteria. The results are consistent with the animals deriving these fatty acids from their sulphur-oxidizing symbionts. Ridgeia piscesae, Lucinoma annulata, Parvilucina tenuisculpta, Lucinoma borealis and Myrtea spinifera also contained substantial amounts of the non-methylene-interrupted dienoic fatty acids 20:2δ5,13 and 22:2δ7,15. It is proposed that these fatty acids are produced by chain elongation and δ5 desaturation in animal tissues of 18:l(n-7) produced by the bacterial symbionts. Thyasira flexuosa did not contain 20:2δ5,13 or 22:2δ7,15 but instead contained 18:l(n-ll) and 20:l(n-13) which were not present in the other species analysed. It is proposed that 18:l(n-ll) and 20:l(n-13) arise from the δ9 desaturation of 20:0 and 22:0, respectively, followed by chain shortening of the mono-unsaturated fatty acid products of δ9 desaturation. It is considered that 20:2δ5,13 and 22:2δ7,15 are formed in the animals in response to a relative excess of 16:0, 16:l(n-7) and 18:l(n-7), accompanied by a relative deficiency of (n-3) and (n-6) polyunsaturated fatty acids. The results are discussed in relation to the lipid nutrition of marine invertebrates containing bacterial symbionts.

Type
Research Article
Copyright
Copyright © Marine Biological Association of the United Kingdom 1995

Access options

Get access to the full version of this content by using one of the access options below. (Log in options will check for institutional or personal access. Content may require purchase if you do not have access.)

References

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, 153165.Google Scholar
Ackman, R.G., Epstein, S. & Kelleher, M., 1974. A comparison of lipids and fatty acids of the ocean quahaug, Arctica islandica, from Nova Scotia and New Brunswick. Journal of the Fisheries Research Board of Canada, 31,18031811.CrossRefGoogle Scholar
Bell, M.V. & Sargent, J.R., 1985. Fatty acid analyses of phosphoglycerides from tissues of the clam Chlamys islandica (Miiller) and the starfish Ctenodiscus crispatus (Retzius) from Balsfjorden, northern Norway. Journal of Experimental Marine Biology and Ecology, 87,31—40.CrossRefGoogle Scholar
Ben-Mlih, F., Marty, J.-C. & Fiala-Medioni, A., 1992. Fatty acid composition in deep hydrothermal vent symbiotic bivalves. Journal ofLipid Research, 33,17971806.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, 20,116120.CrossRefGoogle ScholarPubMed
Cavanaugh, C.M., Levering, P.R., Maki, J.S., Mitchell, R. & Lidstrom, M.E., 1987. Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature, London, 325, 346348.CrossRefGoogle Scholar
Childress, J.J. & Fisher, C.R., 1992. The biology of hydrothermal vent animals: physiology, biochemistry and autotrophic symbioses. Oceanography and Marine Biology. Annual Review. London, 30,337441.Google Scholar
Childress, J.J., Fisher, C.R., Brooks, J.M., Kennicutt, M.C. Ii, Bidigare, R. & Anderson, A.E., 1986. A methanotrophic marine molluscan (Bivalvia, Mytilidae) symbiosis: mussels fuelled by gas. Science, New York, 233, 13061308.CrossRefGoogle Scholar
Christie, W.W., Brechany, E.Y. & Stefanov, K., 1988. Silver ion high-performance chromatography and gas chromatography - mass spectroscopy in the analysis of complex fatty acid mixtures. Chemistry and Physics of Lipids, 46, 127135.CrossRefGoogle Scholar
Conway, N. & Capuzzo, J.McD., 1991. Incorporation and utilization of bacterial lipids in the Solemya velum symbiosis. Marine Biology, 108, 277291.CrossRefGoogle Scholar
Dando, P.R. & Spiro, B., 1993. Varying nutritional dependence of the thyasirid bivalves Thyasira sarsi and T. equalis on chemoautotrophic symbiotic bacteria, demonstrated by isotope ratios of tissue carbon and shell carbonate. Marine Ecology Progress Series, 92,151158.CrossRefGoogle Scholar
Dando, P.R., Southward, A.J. & Southward, E.C., 1986. Chemoautotrophic symbionts in the gills of the bivalve mollusc Lucinoma borealis and the sediment chemistry of its habitat. Proceedings of the Royal Society B, 227, 227247.Google Scholar
Delong, E.F. & Yayanos, A.A., 1986. Biochemical function and ecological significance of novel bacterial lipids in deep-sea prokaryotes. Applied and Environmental Microbiology, 51, 730737.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, 263276.CrossRefGoogle Scholar
Didomenico, D.A. & Iverson, R.L., 1977. Uptake of glycolic acid by a marine bivalve. Journal of Experimental Marine Biology and Ecology, 28, 243254.CrossRefGoogle Scholar
Fisher, C.R., 1990. Chemoautotrophic and methanotrophic symbioses in marine invertebrates. Critical Reviews in Aquatic Sciences, 2, 399436.Google Scholar
Folch, J., Lees, M. & Sloane-Stanley, G.H., 1957. A simple method for the isolation and purification of total lipids from animal tissues. Journal of Biological Chemistry, 226, 497509.CrossRefGoogle ScholarPubMed
Fullarton, J.G., Wood, A.P. & Sargent, J.R., 1995. Fatty acid composition of lipids from sulphuroxidizing and methylotrophic bacteria from thyasirid and lucinid bivalves. Journal of the Marine Biological Association of the United Kingdom, 75, 445454.CrossRefGoogle Scholar
Gage, J., 1972. A preliminary survey of the benthic macrofauna and sediments in Lochs Etive and Creran, sea-lochs along the west coast of Scotland. Journal of the Marine Biological Association of the United Kingdom, 52, 237276.CrossRefGoogle Scholar
Henderson, R.J., Millar, R.-M., Sargent, J.R. & Jostensen, J.-P., 1993. Trans monoenoic acid and polyunsaturated fatty acids in phospholipids of a Vibrio species of bacterium in relation to growth conditions. Lipids, 28, 389396.CrossRefGoogle ScholarPubMed
Hoist, H. & Zebe, E., 1984. Absorption of volatile fatty acids from ambient water by the lugworm Arenicola marina. Marine Biology, 80, 125130.Google Scholar
Johns, R.B. & Perry, G.J., 1977. Lipids of the marine bacterium Flexibacter polymorphus. Archives of Microbiology, 114, 267271.CrossRefGoogle Scholar
Jones, M.L. & Gardiner, S.L., 1989. On the early development of the vestimentiferan tube worm Ridgeia sp. and observations on the nervous system and trophosome of Ridgeia sp. and Riftia pachyptila. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 177, 254276.CrossRefGoogle Scholar
Joseph, J.D., 1982. Lipid composition of marine and estuarine invertebrates. Part II. Mollusca. Progress in Lipid Research, 21, 109153.CrossRefGoogle ScholarPubMed
Neuringer, M., Anderson, G.J. & Connor, W.E., 1988. The essentiality of n-3 fatty acids for the development and function of the retina and brain. Annual Review of Nutrition, 8, 517541.CrossRefGoogle ScholarPubMed
Sargent, J.R., Bell, J.G., Bell, M.V., Henderson, R.J. & Tocher, D.R., 1993. The metabolism of phospholipids and polyunsaturated fatty acids in fish. In Aquaculture: fundamental and applied aspects (ed. B., Lahlou and P., Vitiello). Washington, DC: American Geophysical Union. [Coastal and Estuarine Studies, 43,103–124.]Google Scholar
Sargent, J.R., Falk-Petersen, I.-B. & Calder, A.G., 1983. Fatty acid compositions of neutral glycerides from the ovaries of the asteroids Ctenodiscus crispatus, Asterias lincki and Pteraster militaris from Balsfjorden, northern Norway. Marine Biology, 72,257264.CrossRefGoogle Scholar
Sargent, J.R., Henderson, R.J. & Tocher, D.R., 1989. The lipids. In Fish nutrition 2nd ed. (ed. J.R., Halver), pp. 154219. Academic Press.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. M.A., Sleigh), pp. 119138. Chichester: Ellis Horwood.Google Scholar
Schmaljohann, R. & Fliigel, H.J., 1987. Methane-oxidizing bacteria in Pogonophora. Sarsia, 72, 9198.CrossRefGoogle Scholar
Southward, A.J., 1989. Animal communities fuelled by chemosynthesis: life at hydrothermal vents, cold seeps and in reducing sediments. Journal of Zoology, 217, 705709.CrossRefGoogle Scholar
Southward, A.J. & Southward, E.C., 1980. The significance of dissolved organic compounds in the nutrition of Siboglinum ekmani and other small species of Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 60, 10051034.CrossRefGoogle Scholar
Southward, E.C., 1987. Contribution of symbiotic chemoautotrophs to the nutrition of benthic invertebrates. In Microbes in the sea (ed. M.A., Sleigh), pp. 83118. Chichester: Ellis Horwood.Google Scholar
Southward, E.C., 1988. Development of the gut and segmentation of newly settled stages of Ridgeia (Vestimentifera): implications for the relationships between Vestimentifera and Pogonophora. Journal of the Marine Biological Association of the United Kingdom, 68, 465487.CrossRefGoogle Scholar
Southward, E.C. & Southward, A.J., 1991. Virus-like particles in bacteria symbiotic in bivalve gills. Journal of the Marine Biological Association of the United Kingdom, 71, 3745.CrossRefGoogle Scholar
Spiro, B., Greenwood, P.B., Southward, A.J. & Dando, P.R., 1986. 13C/12C ratio in marine invertebrates from reducing sediments: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Marine Ecology Progress Series, 28, 233240.CrossRefGoogle Scholar
Testerman, J.K., 1972. Accumulation of free fatty acids from sea water by marine invertebrates. Biological Bulletin. Marine Biological Laboratory, Woods Hole, 142, 160177.CrossRefGoogle ScholarPubMed
Thomas, J.D., Sterry, P.R. & Patience, R.L., 1984. Uptake and assimilation of short chain carboxylic acids by Biomphalaria glabrata (Say), the freshwater pulmonate snail host of Schistosoma mansoni (Sambon). Proceedings of the Royal Society of London B, 222, 447476.Google Scholar
Wright, S.H., 1988. Nutrient transport across the integument of marine invertebrates. Advances in Comparative and Environmental Physiology, 2, 173217.CrossRefGoogle 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, 253263.CrossRefGoogle Scholar