Marine Biology

, Volume 108, Issue 2, pp 277–291

Incorporation and utilization of bacterial lipids in theSolemya velum symbiosis

  • N. Conway
  • J. McDowell Capuzzo
Article

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. Theδ13C 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. Theδ13C 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

  1. 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: 1–31Google Scholar
  2. 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: 1212–1222Google Scholar
  3. Cavanaugh, C. M. (1983). Symbiosis of chemoautotrophic bacteria and marine invertebrates from sulphide-rich habitats. Nature, Lond. 302: 58–61Google Scholar
  4. Cavanaugh, C. M. (1985). Symbiosis of chemoautotrophic bacteria and marine invertebrates. Ph.D. Thesis, Harvard UniversityGoogle Scholar
  5. 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: 7786–7789Google Scholar
  6. Conway, N. (1990). The nutritional role of endosymbiotic bacteria in animal-bacteria symbioses:Solemya velum, a case study. MIT/WHOI Ph.D. thesisGoogle Scholar
  7. 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. 553–564Google Scholar
  8. 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: 149–155Google Scholar
  9. DeBurgh, M. E., Juniper, S. K., Singla, C. L. (1989). Bacterial symbiosis in Northeast Pacific Vestimentifera: a TEM study. Mar. Biol 101: 97–105Google Scholar
  10. Degens, E. T. (1969). Biogeochemistry of stable carbon isotopes. In: Eglinton, E., Murphy, M. J. T. (eds.) Organic geochemistry. Springer-Verlag, Berlin, p. 304–329Google Scholar
  11. DeLong, E. F., Yayanos, A. A. (1986). Biochemical function and ecological significance of novel bacterial lipids in deep-sea procaryotes. Appl. envirl Microbiol. 51: 730–737Google Scholar
  12. Fagerland, U. H. M., Idler, D. R. (1960). Marine sterols. VI. Sterol biosynthesis in molluscs and echinoderms. Can. J. Biochem. Physiol. 38: 997–1002Google Scholar
  13. 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: 607–617Google Scholar
  14. Felbeck, H. (1983). Sulfide oxidation and carbon fixation by the gutless clamSolemya reidi: an animal-bacteria symbiosis. J. comp. Physiol. 152: 3–11Google Scholar
  15. 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: 291–293Google Scholar
  16. 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: 487–492Google Scholar
  17. 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: 191–198Google Scholar
  18. 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: 63–74Google Scholar
  19. Fulco, A. J. (1983). Fatty acid metabolism in bacteria. Prog. Lipid Res. 22: 133–160Google Scholar
  20. Gagosian, R. B. (1975). Sterols in the western North Atlantic Ocean. Geochim. Cosmochim. Acta 39: 1443–1454Google Scholar
  21. 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: 827–838Google Scholar
  22. Giere, O., Conway, N. M., Gastrock, G., Schmidt, C. (1991). ‘Regulation’ of gutless annelid ecology by endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 68: 287–299Google Scholar
  23. 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: 83–89Google Scholar
  24. 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. 291–309Google Scholar
  25. 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: 1139–1145Google Scholar
  26. 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. 213–318Google Scholar
  27. Goldfine, H. (1972). Comparative aspects of bacterial lipids. Adv. microb. Physiol. 8: 1–58Google Scholar
  28. Guarnieri, M., Johnson, R. M. (1970). The essential fatty acids. Adv. Lipid Res 8: 115–174Google Scholar
  29. 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. 541–559Google Scholar
  30. Idler, D. R., Wiseman, P. (1971). Sterols of Molluscs. Int. J. Biochem. 2: 516Google Scholar
  31. 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: 422–424Google Scholar
  32. Johns, R. B., Perry, G. J. (1977). Lipids of the marine bacteriumFlexibacter polymorphus. Archs Microbiol. 114: 267–271Google Scholar
  33. Joseph, J. D. (1982). Lipid composition of marine and estuarine invertebrates. Part II: Mollusca. Prog. Lipid Res. 22: 109–153Google Scholar
  34. 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: 1599–1611Google Scholar
  35. 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: 8168–8173Google Scholar
  36. 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: 61–68Google Scholar
  37. 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: 139–149Google Scholar
  38. 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: 263–276Google Scholar
  39. 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: 2668–2673Google Scholar
  40. Ourisson, G., Albrecht, P., Rohmer, M. (1979). The hopanoids. Palaeochemistry and biochemistry of a group of natural products. Pure appl. Chem. 51: 709–729Google Scholar
  41. 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: 173–189Google Scholar
  42. 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: 1715–1725Google Scholar
  43. 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: 283–298Google Scholar
  44. 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: 755–758Google Scholar
  45. 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: 1201–1208Google Scholar
  46. 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. 271–289Google Scholar
  47. Rau, G. H. (1985).13C/12C and15N/14N in hydrothermal vent organisms: ecological and biogeochemical implications. Bull. biol. Soc. Wash. 6: 243–247Google Scholar
  48. 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: 1940–1943Google Scholar
  49. 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: 616–620Google Scholar
  50. Teshima, S.-I., Kanazawa, A. (1974). Biosynthesis of sterols in abalone,Haliotis gurneri, and mussel,Mytilus edulis. Comp. Biochem. Physiol 47B: 555–561Google Scholar
  51. Teshima, S.-I., Patterson, S. W. (1981). Sterol biosynthesis in the oysterCrassostrea virginica. Lipids 16: 234–239Google Scholar
  52. Volkman, J. K. (1986). A review of sterol markers for marine and terrigenous organic matter. Org. Geochem 9: 83–99Google Scholar
  53. 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: 1133–1143Google Scholar
  54. 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: 499–504Google Scholar
  55. 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. 245Google Scholar
  56. 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: 4267–4271Google Scholar

Copyright information

© Springer-Verlag 1991

Authors and Affiliations

  • N. Conway
    • 1
  • J. McDowell Capuzzo
    • 1
  1. 1.Biology DepartmentWoods Hole Oceanographic InstitutionWoods HoleUSA

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