Marine Biology

, Volume 101, Issue 3, pp 305–312 | Cite as

Chemoautotrophic symbionts and translocation of fixed carbon from bacteria to host tissues in the littoral bivalve Loripes lucinalis (Lucinidae)

  • A. Herry
  • M. Diouris
  • M. Le Pennec
Article

Abstract

Specimens of Loripes lucinalis (Lucinidae) living in reducing sediments were collected near a sewage outfall at low tide on the Moulin Blanc beach, Brest, France, from January to March 1987. Electron microscope studies revealed numerous Gram-negative-type bacteria in the gill cells. Ribulosebiphosphate carboxylase, a diagnostic enzyme of the Calvin-Benson cycle of CO2-fixation was measured only in the gill extracts. Various tissues of L. lucinalis were examined for activity of APS reductase, (EC 1.8.99.2), ATP sulphurylase (EC 2.7.7.4) and rhodanese (EC 2.8.1.1), enzymes involved in sulphide oxidation. APS reductase was only found in symbiont-containing tissues, i.e., gills. These enzymatic studies characterise the symbionts as chemoautotrophic sulphide-oxidizing bacteria. Histoautoradiography demonstrated that part of the carbon dioxide fixed by symbiotic bacteria in the gills is translocated to symbiont-free tissues of the bivalve. The ultrastructure of the gill is detailed and a nomenclature based on established and new terminology is proposed to describe the various cellular types comprising the gill filament.

Keywords

Sewage Beach Bivalve Fixed Carbon Sulphide Oxidation 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Allen, J. A. (1958). On the basic form and adaptations to habitat in the Lucinacea (Eulamellibranchia). Phil. Trans. R. Soc. (Ser. B) 241:421–484Google Scholar
  2. Atkins, D. (1938). On the ciliary mechanisms and interrelationships of lamellibranchs. Part V. Note on gills of Amussium pleuronectes L. Q. Jl microsc. Sci. 80:321–329Google Scholar
  3. Berg, J. B., Alatalo, P. (1984). Potential of chemosynthesis on molluscan mariculture. Aquaculture, Amsterdam 39:165–179Google Scholar
  4. Cavanaugh, C. M. (1983). Symbiotic chemoautotrophic bacteria in marine invertebrates frome sulfide-rich habitats. Nature, Lond. 302:58–61Google Scholar
  5. Cavanaugh, C. M. (1985). Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Bull. biol. Soc. Wash. 1985 (6):373–388Google Scholar
  6. Cavanaugh, C. M., Gardiner, S. L., Jones, M. L., Jannasch, H. E. Warterbury, J. B. (1981). Prokaryotic cells in the hydrothermal vent tube worm Riftia pachyptila Jones: possible chemoautotrophic symbionts. Science, N.Y. 213:340–342Google Scholar
  7. Dando, P. R., Southward, A. J. (1986). Chemoautotrophy in bivalve molluscs of the genus Thyasira. J. mar. biol. Ass. U.K. 66: 915–929Google Scholar
  8. 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. Proc. R. Soc. (Ser. B) 227:227–247Google Scholar
  9. Dando, P. R., Southward, A. J., Southward, E. C., Terwilliger, N. B., Terwilliger, R. C. (1985). Sulphur oxidising bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Mar. Ecol. Prog. Ser. 23:85–98Google Scholar
  10. Diouris, M., Moraga, D., Le Pennec, M., Herry, A., Donval, A. (1988). Chimioautotrophie et nutrition chez les Lucinacea, bivalves littoraux de milieux réducteurs. I — Activités enzymatiques des bactéries chemoautotrophes associées aux branchies de Lucinacea (mollusques bivalves). Haliotis, Paris 18:195–205Google Scholar
  11. Distel, D. L., Felbeck, H. (1987). Endosymbiosis in the lucinid clams Lucinoma aequizonata, Lucinoma annulata and Lucina floridana: a reexamination of the functional morphology of the gills as bacteria-bearing organs. Mar. Biol. 96:79–86Google Scholar
  12. Donval, A., Le Pennec, M., Herry, A., Diouris, M., Moraga, D. (1988). Les caractéristiques du tube digestif d'un bivalve symbiotique, Thyasira flexuosa (Thyasiridae). Haliotis, Paris 18: 159–169Google Scholar
  13. Felbeck, H. (1981). Chemoautotrophic potential of the hydrothermal vent tube worm Riftia pachyptila Jones (Vestimentifera). Science, N.Y. 213:336–338Google Scholar
  14. Felbeck, H., Childress, J. J., Somero, G. N. (1981). Calvin-Benson cycle and sulphide oxidation enzymes in animals from sulphide-rich habitats. Nature, Lond. 293:291–293Google Scholar
  15. Felbeck, H., Childress, J. J., Somero, G. N. (1983a). Biochemical interactions between molluscs and their algal and bacterial symbionts. In: P. W. Hochachka (ed.). The Mollusca. Vol. 2. Academic Press, New York, p. 331–358Google Scholar
  16. Felbeck, H., Liebezeit, G., Dawson, R., Giere, O. (1983b). CO2 fixation in tissues of marine oligochaetes (Phallodrilus leukodermatus and P. planus) containing symbiotic, chemoautotrophic bacteria. Mar. Biol. 75:187–191Google Scholar
  17. Fiala-Médiona, A. (1984). Mise en évidence par microscopie électronique à transmission de l'abondance de bactéries symbiotiques dans la branchie de mollusques bivalves de sources hydrothermales profondes. C.r. hebd. Séanc. Acad. Sci., Paris 298 (17): 487–492Google Scholar
  18. Fiala-Médioni, A., Métivier, C., Herry, A., Le Pennec, M. (1986). Ultrastructure of the gill of the hydrothermal-vent mytilid Bathymodiolus sp. Mar. Biol. 93:65–72Google Scholar
  19. Fisher, C. R., Childress, J. J. (1986). Translocation of fixed carbon from symbiotic bacteria to host tissues in the gutless bivalve Solemya reidi. Mar. Biol. 93:59–68Google Scholar
  20. Fisher, M. R., Hand, S. C. (1984). Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biol. Bull. mar. biol. Lab., Woods Hole 167:445–459Google Scholar
  21. Giere, O. (1981). The gutless marine oligochaete Phallodrilus leukodermatus. Structural studies on an aberrant tubificid associated with bacteria. Mar. Ecol. Prog. Ser. 5:353–357Google Scholar
  22. Giere, O. (1985). Structure and position of bacterial endosymbionts in the gill filaments of Lucinidae from Bermuda (Mollusca, Bivalvia). Zoomorphologie 105:296–301Google Scholar
  23. Herry, A., Le Pennec, M. (1987). Endosymbiotic bacteria in the gills of the littoral bivalve molluscs Thyasira flexuosa (Thyasiridae) and Lucinella divaricata (Lucinidae). Sumbioses 4:25–36Google Scholar
  24. Kelly, D. P. (1982). Biochemistry of the chemolithotrophic oxidation of inorganic sulphur. Phil. Trans. S. Soc. (Ser. B) 298: 429–602Google Scholar
  25. Le Pennec, M., Diouris, M., Herry, A. (1988a). Endocytosis and lysis of bacteria in gill epithelium of Bathymodiolus thermophilus, Thyasira flexuosa and Lucinella divaricata (bivalve, molluscs). J. Shellfish Res. 7:489–493Google Scholar
  26. Le Pennec, M., Herry, A., Diouris, M., Moraga, D., Donval, A. (1987). Chemoautotrophie bactérienne chez le mollusque bivalve littoral Lucinella divaricata (Linne). C.r. hebd. Séanc. Acad. Sci., Paris 305:1–5Google Scholar
  27. Le Pennec, M., Herry, A., Diouris, M., Moraga, D., Donval, A. (1988b). Chimioautotrophie et nutrition chez les Lucinacea, bivalves littoraux de milieux réducteurs. II — Charactéristiques morphologiques des bactéries symbiotiques et modifications structurales adaptatives des branchies de l'hôte. Haliotis, Paris 18:207–217Google Scholar
  28. Le Pennec, M., Hily, A. (1984). Anatomie, structure et ultrastructure de la branchie d'un Mytilidae des sites hydrothermaux du Pacifique oriental. Oceanol. Acta 7:517–523Google Scholar
  29. Owen, G. (1978). Classification of the bivalve gill. Phil. Trans. R. Soc. (Ser. B) 284:377–385Google Scholar
  30. Rau, G. H. (1981). Hydrothermal vent clam and tube worm 13C/12C: further evidence of nonphotosynthetic food sources. Science, N.Y. 213:338–340Google Scholar
  31. Reid, R. G. B. (1980). Aspects of the biology of a gutless species of Solemya (Bivalvia: Protobranchia). Cam. J. Zool. 58:386–393Google Scholar
  32. Reid, R. G. B., Bernard, F. R. (1980). Gutless bivalves. Science, N.Y. 208:609–610Google Scholar
  33. Reid, R. G. B., Brand, D. G. (1986). Sulfide-oxidizing symbiosis in lucinaceans: implications for bivalve evolution. Veliger 29:3–24Google Scholar
  34. Schweimanns, M., Felbeck, H. (1985). Significance of the occurrence of chemoautotrophic bacterial endosymbionts in lucinid clams from Bermuda. Mar. Ecol. Prog. Ser. 24:113–120Google Scholar
  35. Southward, A. J., Southward, E. C., Dando, P. R., Rau, G. H., Felbeck, H., Flügel, H. (1981). Bacterial symbionts and low 13C/12C ratios in tissues of Pogonophora indicate unusual nutrition and metabolism. Nature, Lond. 293:616–620Google Scholar
  36. Southward, E. C. (1982). Bacterial symbionts in Pogonophora. J. mar. biol. Ass. U.K. 62:889–906Google Scholar
  37. Southward, E. C. (1986). Gill symbionts in thyasirids and other bivalve molluscs. J. mar. biol. Ass. U.K. 66:889–914Google Scholar
  38. Southward, E. C. (1987). Contribution of symbiotic chemoautotrophs to the nutrition of benthic invertebrates. In: Sleigh M. A. (ed.) Ellis Horwood series in marine science. Microbes in the sea. New York, p. 83–118Google Scholar
  39. Spiro, B., Greenwood, P. B., Southward, A. J. Dando, P. R. (1986). 13C/12C ratios in marine invertebrates from reducing sediment: confirmation of nutritional importance of chemoautotrophic endosymbiotic bacteria. Mar. Ecol. Prog. Ser. 28:233–240Google Scholar
  40. Spurr, A. R. (1969). A low-viscosity epoxy-resin embedding medium for electron microscopy. J. Ultrastruc. Res. 26:31–43Google Scholar

Copyright information

© Springer-Verlag 1989

Authors and Affiliations

  • A. Herry
    • 1
  • M. Diouris
    • 2
  • M. Le Pennec
    • 1
  1. 1.Faculté des SciencesLaboratoire de ZoologieBrest CédexFrance
  2. 2.Faculté des SciencesLaboratoire de Physiologie VégétaleBrest CédexFrance

Personalised recommendations