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Incorporation and utilization of bacterial lipids in theSolemya velum symbiosis

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Abstract

We undertook a detailed analysis of the lipid composition ofSolemya velum (Say), a bivalve containing endosymbiotic chemoautotrophic bacteria, in order to determine the presence of lipid biomarkers of endosymbiont activity. The symbiont-free clamMya arenaria (L.) and the sulfur-oxidizing bacteriumThiomicrospira crunogena (Jannasch et al.) were analyzed for comparative purposes. Theδ 13C ratios of the fatty acids and sterols were also measured to elucidate potential carbon sources for the lipids of each bivalve species. Both fatty acid and sterol composition differed markedly between the two bivalves. The lipids ofS. velum were characterized by large amounts of 18: 1ω7 (cis-vaccenic acid), 16:0, and 16 : 1ω7 fatty acids, and low concentrations of the highly unsaturated plant-derived fatty acids characteristic of most marine bivalves. Cholest-5-en-3β-ol (cholesterol) accounted for greater than 95% of the sterols inS. velum. In contrast,M. arenaria had fatty acid and sterol compositions similar to typical marine bivalves and was characterized by large amounts of the highly unsaturated fatty acids 20 : 5ω3 and 22 : 6ω3 and a variety of plant-derived sterols. The fatty acids ofT. crunogena were similar to those ofS. velum and were dominated by 18:1ω7, 16:0 and 16:1ω7 fatty acids. Thecis-vaccenic acid found inS. velum is almost certainly symbiontderived and serves as a potential biomarker for symbiontlipid incorporation by the host. The high concentrations ofcis-vaccenic acid (up to 35% of the total fatty acid content) in both symbiont-containing and symbiont-free tissues ofS. velum demonstrate the importance of the endosymbionts in the lipid metabolism of this bivalve. The presence ofcis-vaccenic acid in all the major lipid classes ofS. velum demonstrates both incorporation and utilization of this compound. Theδ 13C ratios of the fatty acids and sterols ofS. velum were significantly lighter (−38.4 to −45.3‰) than those ofM. arenaria (−23.8 to − 24.2‰) and were similar to the values found for the fatty acids ofT. crunogena (−45‰); this suggests that the lipids ofS. velum are either derived directly from the endosymbionts or are synthesized using endosymbiontderived carbon.

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Literature cited

  • Anderson, A. E., Childress, J. J., Favuzzi, J. A. (1987). Net uptake of CO2 driven by sulphide and thiosulphate oxidation in the bacterial symbiont-containing clamSolemya reidi. J. exp. Biol. 133: 1–31

    Google Scholar 

  • Bobbie, R. J., White, D. C. (1980). Characterization of benthic microbial community structure by high-resolution gas chromatography of fatty acid methyl esters. Appl envirl. Microbiol. 39: 1212–1222

    Google Scholar 

  • Cavanaugh, C. M. (1983). Symbiosis of chemoautotrophic bacteria and marine invertebrates from sulphide-rich habitats. Nature, Lond. 302: 58–61

    Google Scholar 

  • Cavanaugh, C. M. (1985). Symbiosis of chemoautotrophic bacteria and marine invertebrates. Ph.D. Thesis, Harvard University

  • Cavanaugh, C. M., Abbott, M. S., Veenhuis, M. (1988). Immunochemical localization of ribulose-1,5-biphosphate carboxylase in the symbiont-containing gills ofSolemya velum (Bivalvia: Mollusca). Proc. natn. Acad. Sci. USA 85: 7786–7789

    Google Scholar 

  • Conway, N. (1990). The nutritional role of endosymbiotic bacteria in animal-bacteria symbioses:Solemya velum, a case study. MIT/WHOI Ph.D. thesis

  • Conway, N., McDowell Capuzzo, J. (1990). The use of biochemical indicators in the study of trophic interactions in animal-bacteria symbioses:Solemya velum, a case study. In: Barnes, M., Gibson, R. N. (eds.) Trophic relationships in the marine environment. Proc. 24th Eur. mar. biol. Symp. Aberdeen University Press, Aberdeen, p. 553–564

    Google Scholar 

  • Conway, N., McDowell Capuzzo, J., Fry, B. (1989). The role of endosymbiotic bacteria in the nutrition ofSolemya velum: Evidence from a stable isotope analysis of endosymbionts and host. Limnol. Oceanogr. 34: 149–155

    Google Scholar 

  • DeBurgh, M. E., Juniper, S. K., Singla, C. L. (1989). Bacterial symbiosis in Northeast Pacific Vestimentifera: a TEM study. Mar. Biol 101: 97–105

    Google Scholar 

  • Degens, E. T. (1969). Biogeochemistry of stable carbon isotopes. In: Eglinton, E., Murphy, M. J. T. (eds.) Organic geochemistry. Springer-Verlag, Berlin, p. 304–329

    Google Scholar 

  • DeLong, E. F., Yayanos, A. A. (1986). Biochemical function and ecological significance of novel bacterial lipids in deep-sea procaryotes. Appl. envirl Microbiol. 51: 730–737

    Google Scholar 

  • Fagerland, U. H. M., Idler, D. R. (1960). Marine sterols. VI. Sterol biosynthesis in molluscs and echinoderms. Can. J. Biochem. Physiol. 38: 997–1002

    Google Scholar 

  • Farrington, J. W., Davis, A. C., Sulanowski, J., McCaffrey, M. A., Clifford, C. H., Dickenson, P., Volkman, J. K. (1988). Biogeochemistry of lipids in surface sediments of the Peru upwelling area — 15°S. In: Mattivelli, L., Novelli, L. (eds.) Advances in organic geochemistry 1987. Org. Geochem. 13: 607–617

    Google Scholar 

  • Felbeck, H. (1983). Sulfide oxidation and carbon fixation by the gutless clamSolemya reidi: an animal-bacteria symbiosis. J. comp. Physiol. 152: 3–11

    Google Scholar 

  • Felbeck, H., Childress, J. J., Somero, G. N. (1981). Calvin-Benson cycle and sulfide oxidation enzymes in animals from sulfide-rich habitats. Nature, Lond. 293: 291–293

    Google Scholar 

  • Fiala-Médioni, A. (1984). Ultrastructural evidence of abundance of intracellular symbiotic bacteria in the gills of bivalve molluscs of deep hydrothermal vents. Cr. Lebd. Séanc. Acad. Sci., Paris (Ser. III) 298: 487–492

    Google Scholar 

  • Fiala-Médioni, A., Alayse, A. M., Cahet, G. (1986). Evidence of in situ uptake and incorporation of bicarbonate and amino acids by a hydrothermal vent mussel. J. exp. mar. Biol. Ecol. 96: 191–198

    Google Scholar 

  • Fiala-Médioni, A., LePennec, M. (1987). Trophic structural adaptations in relation to the bacterial association of bivalve molluscs from hydrothermal vents and subduction zones. Symbiosis 4: 63–74

    Google Scholar 

  • Fulco, A. J. (1983). Fatty acid metabolism in bacteria. Prog. Lipid Res. 22: 133–160

    Google Scholar 

  • Gagosian, R. B. (1975). Sterols in the western North Atlantic Ocean. Geochim. Cosmochim. Acta 39: 1443–1454

    Google Scholar 

  • Gardner, D., Riley, J. P. (1972). The component fatty acids of the lipids of some species of marine and freshwater molluscs. J. mar. biol. Ass. U.K. 52: 827–838

    Google Scholar 

  • Giere, O., Conway, N. M., Gastrock, G., Schmidt, C. (1991). ‘Regulation’ of gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68: 287–299

    Google Scholar 

  • Giere, O., Felbeck, H., Dawson, R., Liebezeit, G. (1984). The gutless marine oligochaetePhallodrilus leukodermatus Giere, a tubificid of structural, ecological and physiological significance. Hydrobiologica 115: 83–89

    Google Scholar 

  • Gillan, F. T., Johns, R. B. (1986). Chemical markers for marine bacteria: Fatty acids and pigments. In: Johns, R. B. (ed.) Biological markers in the sedimentary environment. Elsevier, Amsterdam, p. 291–309

    Google Scholar 

  • Gillan, F. T., Stoilov, I. L., Thompson, J. E., Hogg, R. W., Wilkinson, C. R., Djerassi, C. (1988). Fatty acids as biological markers for bacterial symbionts in sponges. Lipids 23: 1139–1145

    Google Scholar 

  • Goad, L. J. (1976). The steroids of marine algae and invertebrate animals. In: Malins, D. C., Sargent, J. R. (eds.) Biochemical and biophysical perspectives in marine biology, vol. 3. Academic Press, New York, p. 213–318

    Google Scholar 

  • Goldfine, H. (1972). Comparative aspects of bacterial lipids. Adv. microb. Physiol. 8: 1–58

    Google Scholar 

  • Guarnieri, M., Johnson, R. M. (1970). The essential fatty acids. Adv. Lipid Res 8: 115–174

    Google Scholar 

  • Hazel, J. R., Sellner, P. A. (1979). The regulation of membrane lipid composition in thermally acclimated poikilotherms. In: Gilles, R. (ed.) Animals and environmental fitness. Physiological and biochemical aspects of adaptation and ecology. Proc. 1st Conf. Eur. Soc. Comp. Physiol. Biochem. Pergamon Press, New York, p. 541–559

    Google Scholar 

  • Idler, D. R., Wiseman, P. (1971). Sterols of Molluscs. Int. J. Biochem. 2: 516

    Google Scholar 

  • Jannasch, H. W., Wirsen, C. O., Nelson, D. C., Robertson, L. A. (1985).Thiomicrospira crunogena sp. nov., a colorless, sulfuroxidizing bacterium from a deep-sea hydrothermal vent. Int. J. system Bact. 35: 422–424

    Google Scholar 

  • Johns, R. B., Perry, G. J. (1977). Lipids of the marine bacteriumFlexibacter polymorphus. Archs Microbiol. 114: 267–271

    Google Scholar 

  • Joseph, J. D. (1982). Lipid composition of marine and estuarine invertebrates. Part II: Mollusca. Prog. Lipid Res. 22: 109–153

    Google Scholar 

  • Katayama-Fujimura, Y., Tsuzaki, N., Kuraishi, H. (1982). Ubiquinone, fatty acid and DNA base composition determination as a guide to the taxonomy of the genus Thiobacillus. J. gen. Microbiol. 128: 1599–1611

    Google Scholar 

  • Kokko, W. C. M. C., Epstein, S., Look, S. A., Rau, G., Fenical, W., Djerassi, C. (1984). Culture studies and an application of13C/12C isotope ratio mass spectrometry. J. biol. Chem. 259: 8168–8173

    Google Scholar 

  • McCaffrey, M. A., Farrington, J. W., Repeta, D. J. (1989). Geochemical implications of the lipid composition ofThioploca sp. from the Peru upwelling region — 15°S. Org. Geochem. 14: 61–68

    Google Scholar 

  • Monson, K. D., Hayes, J. M. (1982). Carbon isotope fractionation in the biosynthesis of bacterial fatty acids. Ozonolysis of unsaturated fatty acids as a means of determining the intramolecular distribution of carbon isotopes. Geochim. Cosmochim. Acta. 46: 139–149

    Google Scholar 

  • Moreno, J., Pollero, A. E., Moreno, V. J., Brenner, R. R. (1980). Lipids and fatty acids of the mussel (Mytilus platensis d'Orbigny) from South Atlantic Waters. J. exp. mar. Biol. Ecol. 48: 263–276

    Google Scholar 

  • Okuyama, H., Yamada, K., Kameyama, Y., Ikezawa, H., Akamatzu, Y., Nojima, S. (1977). Regulation of membrane lipid synthesis inEscherichia coli after shifts in temperature. Biochem. 16: 2668–2673

    Google Scholar 

  • Ourisson, G., Albrecht, P., Rohmer, M. (1979). The hopanoids. Palaeochemistry and biochemistry of a group of natural products. Pure appl. Chem. 51: 709–729

    Google Scholar 

  • Parkes, R. J., Taylor, J. (1983). The relationship between fatty acid distributions and bacterial respiratory types in contemporary marine sediments. Estuar. cstl mar. Sci. 16: 173–189

    Google Scholar 

  • Perry, G. J., Volkman, J. K., Johns, R. B, Bavor, H. J. Jr. (1979). Fatty acids of bacterial origin in contemporary marine sediments. Geochim. Cosmochim. Acta 43: 1715–1725

    Google Scholar 

  • Phillips, N. W. (1984). The role of different microbes and substrates as potential suppliers of specific, essential nutrients to marine detritivores. Bull. mar. Sci. 35: 283–298

    Google Scholar 

  • Piretti, M. V., Pistore, R., Pagliuca, G. (1989). Uptake and utilization of lipid constituents dispersed in culture water by the bivalve molluscScapharca inaequivalvis (Bruguiere). Comp. Biochem. Physiol. 92B: 755–758

    Google Scholar 

  • Piretti, M. V., Tioli, F., Pagliuca, G. (1987). Investigation of the seasonal variations of sterol and fatty acid constituents in the bivalve molluscsVenus gallina andScapharca inaequivalvis (Bruguiére). Comp. Biochem. Physiol. 88B: 1201–1208

    Google Scholar 

  • Prahl, F. G., Meuhlhausen, L. A. (1989). Lipid biomarkers as geochemical tools for paleoceanographic study. Berger, W. H., Smetacek, V. S., Wefer, G. (eds.) Productivity of the ocean: present and past. T. Wiley and Sons limited, New York, p. 271–289

    Google Scholar 

  • Rau, G. H. (1985).13C/12C and15N/14N in hydrothermal vent organisms: ecological and biogeochemical implications. Bull. biol. Soc. Wash. 6: 243–247

    Google Scholar 

  • Ruby, E. G., Jannasch, H. W., Deuser, W. G. (1987). Fractionation of stable carbon isotopes during chemoautotrophic growth of sulfur-oxidizing bacteria. Appl. envirl. Microbiol. 53: 1940–1943

    Google Scholar 

  • Southward, A. J., Southward, E. C., Dando, P. R., Rau, G. H., Fehlbeck, H., Flugel, H. (1981). Bacterial symbionts and low13C/12C ratios in tissues of Pogonophora suggest unusual nutrition and metabolism. Nature, Lond. 293: 616–620

    Google Scholar 

  • Teshima, S.-I., Kanazawa, A. (1974). Biosynthesis of sterols in abalone,Haliotis gurneri, and mussel,Mytilus edulis. Comp. Biochem. Physiol 47B: 555–561

    Google Scholar 

  • Teshima, S.-I., Patterson, S. W. (1981). Sterol biosynthesis in the oysterCrassostrea virginica. Lipids 16: 234–239

    Google Scholar 

  • Volkman, J. K. (1986). A review of sterol markers for marine and terrigenous organic matter. Org. Geochem 9: 83–99

    Google Scholar 

  • Volkman, J. K., Johns, R. B., Gillan, F. T., Perry, G. J., Bavor, H. J. Jr (1980). Microbial lipids of an intertidal sediment. Fatty acids and hydrocarbons. Geochem. Cosmochim. Acta 44: 1133–1143

    Google Scholar 

  • Voogt, P. A. (1975). Investigations of the capacity of synthesizingβ-sterols in Mollusca. XII. Biosynthesis and composition of sterols in some bivalves (Anisomyasia). Comp. Biochem. Physiol. 50B: 499–504

    Google Scholar 

  • Voogt, P. A. (1972). Lipid and sterol components and metabolism in Mollusca. In: Florkin, M., Sheer, B. T. (eds.) Chemical zoology, Vol. 7. Academic Press, London and New York, p. 245

    Google Scholar 

  • Wada, M., Fukunaga, N., Sasaki, S. (1989). Mechanism of biosynthesis of unsaturated fatty acids inPseudomonas sp. strain E-3, a psychotrophic bacterium. J. Bacteriol. 171: 4267–4271

    Google Scholar 

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  1. Biology Department, Woods Hole Oceanographic Institution, 02543, Woods Hole, Massachusetts, USA

    N. Conway & J. McDowell Capuzzo

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Communicated by J. Grassle, Woods Hole

Woods Hole Oceanographic Institution Contribution No. 7356

Please address all correspondence and reprint requests to Dr Conway at her present address: Department of Biological Sciences, University of Pittsburgh, Pennsylvania 15260, USA

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Conway, N., McDowell Capuzzo, J. Incorporation and utilization of bacterial lipids in theSolemya velum symbiosis. Mar. Biol. 108, 277–291 (1991). https://doi.org/10.1007/BF01344343

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