Skip to main content

Advertisement

SpringerLink
Log in

Contrasting effects of sulfide and thiosulfate on symbiotic CO2-assimilation of Phallodrilus leukodermatus (Annelida)

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Experiments were conducted in order to specify the reductants responsible for the carbon dioxide fixation of the symbiotic sulfur bacteria in the gutless marine oligochaete Phallodrilus leukodermatus (Annelida) from shallow calcareous sediments in Bermuda. Carbon dioxide-uptake rates were suppressed by S= and stimulated by S2O3 =. Individuals which hosted bacteria containing reserve energy substances maintained a high short-term CO2-uptake activity, while bacteria in worm homogenates and in worms treated with an antibiotic (Baypen) did not show any significant metabolic activity. Absolute uptake rates in P. leukodermatus were usually considerably higher than those reported for other animals harbouring prokaryotic sulfuroxidizing symbionts. Utilization of thiosulfate rather than sulfide is compatible with the preferred occurrence of the worms around the redox discontinuity layer and has been confirmed in other “thiobiotic” animals. Sulfur stored in the symbiotic bacteria appears to be oxidized to sulfate and be excreted when the worms are held under energy-limited conditions. The data emphasize the complexity of the possible metabolic pathways involved in the oxidation of reduced-sulfur compounds by bacterial symbionts in marine invertebrates.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

Literature cited

  • Almgren, T., Hagström, A. (1974). The oxidation rate of sulfide in seawater. Wat. Res. 8: 395–400

    Google Scholar 

  • Belkin, S., Nelson, D. C., Jannasch, H. W. (1986). Symbiotic assimilation of CO2 in two hydrothermal vent animals, the mussel Bathymodiolus thermophilus and the tube worm Riftia pachyptila. Biol. Bull. mar. biol. Lab., Woods Hole 170: 110–121

    Google Scholar 

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

    Google Scholar 

  • Cavanaugh, C. M., Levering, P. R., Maki, J. S., Mitchell, R., Lidstrom, M. E. (1987). Symbiosis of methylotrophic bacteria and deep-sea mussels. Nature, Lond. 325: 346–348

    Google Scholar 

  • Childress, J. J., Fisher, C. R., Brooks, J. M., Kennicutt, II, M. C., Bidigare, R., Anderson, A. E. (1986). A methanotrophic marine mollusean (Bivalvia, Mytilidae) symbiosis: mussels fueled by gas. Science, N.Y. 233: 1306–1308

    Google Scholar 

  • Childress, J. J., Mickel, T. J. (1982). Oxygen and sulfide consumption rates of the vent clam Calyptogena pacifica. Mar. Biol. Lett. 3: 73–80

    Google Scholar 

  • Cuhel, R. L., Taylor, C. D., Jannasch, H. W. (1981). Assimilatory sulfur metabolism in marine microorganisms: characteristics and regulations of sulfate transport in Pseudomonas halodurans and Altermonas luteo-violaceus. J. Bact. 147: 340–349

    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., Barrett, R. L. (1986). Possible energy sources for chemoautotrophic prokaryotes symbiotic with invertebrates from a Norwegian fjord. Ophelia 26: 135–150

    Google Scholar 

  • Dando, P. R., Southward, A. J., Southward, E. C., Terwilliger, N. B., Terwilliger, R. C. (1985). Sulphur-oxidizing bacteria and haemoglobin in gills of the bivalve mollusc Myrtea spinifera. Mar. Ecol. Prog. Ser. 23: 85–98

    Google Scholar 

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

    Google Scholar 

  • Felbeck, H., Liebezeit, G., Dawson, R., Giere, O. (1983). CO2 fixation in tissues of marine oligochaetes (Phallodrilus leukodermatus and P. planus) containing symbiotic, chemoautotrophic bacteria. Mar. Biol. 75: 187–191

    Google Scholar 

  • Fenchel, T. (1969). The ecology of marine microbenthos. IV. Structure and function of the benthic ecosystem, its chemical and physical factors and the microfauna communities with special reference to the ciliate Protozoa. Ophelia 6: 1–182

    Google Scholar 

  • Fenchel, T. M., Riedl, R. J. (1970). The sulfide system: a new biotic community underneath the oxidized layer of marine sand bottoms. Mar. Biol. 7: 255–268

    Google Scholar 

  • Giere, O. (1985). The gutless marine tubificid Phallodrilus planus, a flattened oligochaete with symbiotic bacteria. Results from morphological and ecological studies. Zoologica Scr. 14: 279–286

    Google Scholar 

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

    Google Scholar 

  • Giere, O., Langheld, C. (1987). Structural organisation, transfer and biological fate of endosymbiotic bacteria in gutless oligochaetes. Mar. Biol. 93: 641–650

    Google Scholar 

  • Giere, O., Liebezeit, G., Dawson, R. (1982). Habitat conditions and distribution pattern of the gutless oligochaete Phallodrilus leukodermatus. Mar. Ecol. Prog. Ser. 8: 291–299

    Google Scholar 

  • Hammen, C. S. (1966). Carbon dioxide fixation in marine invertebrates. V. Rate and pathway in the oyster. Comp. Biochem. Physiol. 17: 289–296

    Google Scholar 

  • Howarth, R. W., Giblin, A., Gale, J., Peterson, B. J., Luther, III, G. W. (1983). Reduced sulfur compounds in the pore waters of a New England salt marsh. Ecol. Bull., Stockholm 35: 135–152

    Google Scholar 

  • Howarth, R. W., Teal, J. M. (1980). Energy flow in a salt marsh ecosystem: the role of reduced inorganic sulfur compounds. Am. Nat. 116: 862–872

    Google Scholar 

  • Jannasch, H. W., Wirsen, C. O. (1985). The biochemical versatility of chemosynthetic bacteria at deep-sea hydrothermal vents. Bull. biol. Soc. Wash. 6: 325–334

    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 

  • Jørgensen, B. B. (1982). Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. Phil. Trans. R. Soc. Lond. (Ser. B) 298: 543–561

    Google Scholar 

  • Jones, M. L. (ed.) (1985). Hydrothermal vents of the eastern Pacific: An overview. Bull. biol. Soc. Wash. 6: 1–545

    Google Scholar 

  • Kelly, D. P. (1982). Biochemistry of the chemolithotrophic oxidation of inorganic sulfur. Phil. Trans. R. Soc. Lond. (Ser. B) 298: 499–528

    Google Scholar 

  • Morris, B., Barnes, J., Brown, F., Markham, J. (1977). The Bermuda marine environment. A report of the Bermuda inshore waters investigations 1976–1977. Spec. Publs Bermuda biol. Stn Res. 15: 1–120

    Google Scholar 

  • Powell, M. A., Somero, G. N. (1986). Adaptations to sulfide by hydrothermal vent animals: sites and mechanism of detoxification and metabolism. Biol. Bull. mar. biol. Lab., Woods Hole 171: 274–290

    Google Scholar 

  • Schmaljohann, R., Flügel, H. J. (1987). Methane-oxidizing bacteria in Pogonophora. Sarsia 72: 91–98

    Google Scholar 

  • Slepecky, R. A., Law, J. H. (1961). A rapid spectrophotometric assay of α-, β-unsaturated acid and β-hydroxy acid. Analyt. Chem. 32: 1697–1699

    Google Scholar 

  • Southward, A. J., Southward, E. C., Dando, P. R., Barrett, R. L., Ling, R. (1986). Chemoautotrophic function of bacterial symbionts in small Pogonophora. J. mar. biol. Ass. U.K. 66: 415–437

    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 

  • Steudel, R. (1985). Neue Entwicklungen in der Chemie des Schwefels und des Selens. Nova Acta Leopoldina 59 (264): 231–246

    Google Scholar 

  • Steudel, R., Holdt, G., Göbel, T., Hazeu, W. (1987). Chromatographische Trennung höherer Polythionate SnO6 2- (n=3...22) und deren Nachweis in Kulturen von Thiobacillus ferrooxidans; molekulare Zusammensetzung bakterieller Schwefelausscheidungen. Angew. Chem. 99: 143–146

    Google Scholar 

  • Steudel, R., Holdt, G., Nagorka, R. (1986). On the autoxidation of aqueous sodium polysulfide. Z. Naturf. (Sect. B) 41: 1519–1522

    Google Scholar 

  • Tabatabai, M. A. (1974). A rapid method for determination of sulfate in water samples. Envir. Lett. 7: 237–243

    Google Scholar 

  • Tuttle, J. H. (1985). The role of sulfur-oxidizing bacteria at deepsea hydrothermal vents. Bull. biol. Soc. Wash. 6: 335–344

    Google Scholar 

  • Tuttle, J. H., Jannasch, H. W. (1977). Thiosulfate stimulation of microbial dark assimilation of carbon dioxide in shallow marine environments. Microb. Ecol. 4: 9–25

    Google Scholar 

  • Tuttle, J. H., Wirsen, C. O., Jannasch, H. W. (1983). Microbial activities in the emitted hydrothermal waters of the Galápagos Rift vents. Mar. Biol. 73: 293–299

    Google Scholar 

  • Vetter, R. D., Wells, M. E., Kurtsman, A. L., Somero, G. N. (1987). Sulfide detoxification by the hydrothermal vent crab Bythograea thermydron and other decapod crustaceans. Physiol. Zoöl. 60: 121–137

    Google Scholar 

Download references

Author information

Authors and Affiliations

  1. Zoologisches Institut und Museum, Universität Hamburg, Martin-Luther-King Platz 3, D-2000, Hamburg 13, FRG

    O. Giere & C. Schmidt

  2. Woods Hole Oceanographic Institution, 02543, Woods Hole, Massachusetts, USA

    C. O. Wirsen & H. W. Jannasch

Authors
  1. O. Giere
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. C. O. Wirsen
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. C. Schmidt
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. H. W. Jannasch
    View author publications

    You can also search for this author in PubMed Google Scholar

Additional information

Communicated by O. Kinne, Oldendorf/Luhe

Rights and permissions

Reprints and permissions

About this article

Cite this article

Giere, O., Wirsen, C.O., Schmidt, C. et al. Contrasting effects of sulfide and thiosulfate on symbiotic CO2-assimilation of Phallodrilus leukodermatus (Annelida). Mar. Biol. 97, 413–419 (1988). https://doi.org/10.1007/BF00397771

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00397771

Keywords

Search

Navigation