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

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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.

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Literature cited

  • Allen, J. A. (1958). On the basic form and adaptations to habitat in the Lucinacea (Eulamellibranchia). Phil. Trans. R. Soc. (Ser. B) 241:421–484

    Google Scholar 

  • Atkins, D. (1938). On the ciliary mechanisms and interrelationships of lamellibranchs. Part V. Note on gills of Amussium pleuronectes L. Q. Jl microsc. Sci. 80:321–329

    Google Scholar 

  • Berg, J. B., Alatalo, P. (1984). Potential of chemosynthesis on molluscan mariculture. Aquaculture, Amsterdam 39:165–179

    Google Scholar 

  • Cavanaugh, C. M. (1983). Symbiotic chemoautotrophic bacteria in marine invertebrates frome sulfide-rich habitats. Nature, Lond. 302:58–61

    Google Scholar 

  • Cavanaugh, C. M. (1985). Symbioses of chemoautotrophic bacteria and marine invertebrates from hydrothermal vents and reducing sediments. Bull. biol. Soc. Wash. 1985 (6):373–388

    Google Scholar 

  • 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. 213:340–342

    Google Scholar 

  • Dando, P. R., Southward, A. J. (1986). Chemoautotrophy in bivalve molluscs of the genus Thyasira. J. mar. biol. Ass. U.K. 66: 915–929

    Google 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. Proc. R. Soc. (Ser. B) 227:227–247

    Google Scholar 

  • 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. 23:85–98

    Google Scholar 

  • 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 18:195–205

    Google Scholar 

  • 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. 96:79–86

    Google Scholar 

  • 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: 159–169

    Google Scholar 

  • Felbeck, H. (1981). Chemoautotrophic potential of the hydrothermal vent tube worm Riftia pachyptila Jones (Vestimentifera). Science, N.Y. 213:336–338

    Google Scholar 

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

    Google Scholar 

  • 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. 331–358

    Google Scholar 

  • 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. 75:187–191

    Google Scholar 

  • 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): 487–492

    Google Scholar 

  • Fiala-Médioni, A., Métivier, C., Herry, A., Le Pennec, M. (1986). Ultrastructure of the gill of the hydrothermal-vent mytilid Bathymodiolus sp. Mar. Biol. 93:65–72

    Google Scholar 

  • 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. 93:59–68

    Google Scholar 

  • Fisher, M. R., Hand, S. C. (1984). Chemoautotrophic symbionts in the bivalve Lucina floridana from seagrass beds. Biol. Bull. mar. biol. Lab., Woods Hole 167:445–459

    Google Scholar 

  • Giere, O. (1981). The gutless marine oligochaete Phallodrilus leukodermatus. Structural studies on an aberrant tubificid associated with bacteria. Mar. Ecol. Prog. Ser. 5:353–357

    Google Scholar 

  • Giere, O. (1985). Structure and position of bacterial endosymbionts in the gill filaments of Lucinidae from Bermuda (Mollusca, Bivalvia). Zoomorphologie 105:296–301

    Google Scholar 

  • Herry, A., Le Pennec, M. (1987). Endosymbiotic bacteria in the gills of the littoral bivalve molluscs Thyasira flexuosa (Thyasiridae) and Lucinella divaricata (Lucinidae). Sumbioses 4:25–36

    Google Scholar 

  • Kelly, D. P. (1982). Biochemistry of the chemolithotrophic oxidation of inorganic sulphur. Phil. Trans. S. Soc. (Ser. B) 298: 429–602

    Google Scholar 

  • 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. 7:489–493

    Google Scholar 

  • 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 305:1–5

    Google Scholar 

  • 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 18:207–217

    Google Scholar 

  • Le Pennec, M., Hily, A. (1984). Anatomie, structure et ultrastructure de la branchie d'un Mytilidae des sites hydrothermaux du Pacifique oriental. Oceanol. Acta 7:517–523

    Google Scholar 

  • Owen, G. (1978). Classification of the bivalve gill. Phil. Trans. R. Soc. (Ser. B) 284:377–385

    Google Scholar 

  • Rau, G. H. (1981). Hydrothermal vent clam and tube worm 13C/12C: further evidence of nonphotosynthetic food sources. Science, N.Y. 213:338–340

    Google Scholar 

  • Reid, R. G. B. (1980). Aspects of the biology of a gutless species of Solemya (Bivalvia: Protobranchia). Cam. J. Zool. 58:386–393

    Google Scholar 

  • Reid, R. G. B., Bernard, F. R. (1980). Gutless bivalves. Science, N.Y. 208:609–610

    Google Scholar 

  • Reid, R. G. B., Brand, D. G. (1986). Sulfide-oxidizing symbiosis in lucinaceans: implications for bivalve evolution. Veliger 29:3–24

    Google Scholar 

  • Schweimanns, M., Felbeck, H. (1985). Significance of the occurrence of chemoautotrophic bacterial endosymbionts in lucinid clams from Bermuda. Mar. Ecol. Prog. Ser. 24:113–120

    Google Scholar 

  • 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. 293:616–620

    Google Scholar 

  • Southward, E. C. (1982). Bacterial symbionts in Pogonophora. J. mar. biol. Ass. U.K. 62:889–906

    Google Scholar 

  • Southward, E. C. (1986). Gill symbionts in thyasirids and other bivalve molluscs. J. mar. biol. Ass. U.K. 66:889–914

    Google Scholar 

  • 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. 83–118

  • 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. 28:233–240

    Google Scholar 

  • Spurr, A. R. (1969). A low-viscosity epoxy-resin embedding medium for electron microscopy. J. Ultrastruc. Res. 26:31–43

    Google Scholar 

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Communicated by J. M. Pérès, Marseille

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Herry, A., Diouris, M. & Le Pennec, M. Chemoautotrophic symbionts and translocation of fixed carbon from bacteria to host tissues in the littoral bivalve Loripes lucinalis (Lucinidae). Marine Biology 101, 305–312 (1989). https://doi.org/10.1007/BF00428126

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