Marine Biology

, Volume 106, Issue 1, pp 129–137 | Cite as

Metabolic studies on thiobiotic free-living nematodes and their symbiotic microorganisms

  • F. Schiemer
  • R. Novak
  • J. Ott


The marine, free-living Stilbonematinae (Nematoda: Desmodoridae) are remarkable for the ectosymbiotic, prokaryotic microorganisms that populate their entire body surface. These nematodes occur in sulfidic sediments in the microoxic zone just above the sulfide maximum. Several facts point to a chemolithotrophic, sulfide oxidizing nature of the microorganisms. The oxygen uptake of three species was measured with and without their microbial coat using Cartesian and Gradient Diver microrespirometry in February 1989 at Carrie Bow Cay (Belize Barrier Reef). Symbiont-free stilbonematids exhibited constant and uniform oxygen uptake rates over several hours; rates which are significantly lower than those of oxyphilic nematodes. Freshly extracted stilbonematids, with intact bacterial coats, consumed significantly more oxygen than symbiont-free worms in the first 3 h of measurement. While the rates of aposymbiotic worms were more or less constant over time, the rates of symbiont-carrying worms exhibited a conspicuous drop during prolonged respiration. InStilbonema sp., symbiont carrying individuals kept under oxygenated conditions for more than 12 h had a respiration rate similar to those of aposymbiotic specimens. When such worms were re-incubated in sulfide-enriched seawater the respiration rate was significantly elevated. The possibility of “recharging” the oxygenated symbiosis system via sulfide-uptake is seen as an indication that storage of reduced sulfur compounds, or reserve substances synthetized in the presence of sulfide, play a decisive role in the metabolisms of the symbiotic bacteria. Migration of nematodes between sulfidic and oxidized sediment-layers are, most likely, the key to understanding the success of this nematode-bacteria symbiosis.


Sulfide Oxygen Uptake Oxygen Uptake Rate Symbiotic Bacterium Symbiosis System 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

Literature cited

  1. Boaden, P. (1974). Three new thiobiotic gastrotrichs. Cah. Biol. mar. 15: 367–378Google Scholar
  2. Boaden, P. (1975). Anaerobiosis, meiofauna and early metazoan evolution. Zool. Scr. 4: 21–24Google Scholar
  3. Childress, J. J., Mickel, T. J. (1982). Oxygen and sulfide consumption rates of the vent clamCalyptogenia pacifica. Mar. Biol. Lett. 3: 73–79Google Scholar
  4. Dando, P. R., Southward, A. J., Southward, E. C. (1986). Chemoautotrophic symbionts in the gills of the bivalve molluscLucinoma borealis and the sediment chemistry of its habitat. Proc. R. Soc. (Ser. B) 227: 227–247Google Scholar
  5. Fenchel, T., Finlay, B. J. (1989).Kentrophoros: A mouthless ciliate with a symbiotic kitchen garden. Ophelia 30: 75–93Google Scholar
  6. Giere, O., Wirsen, C. O., Schmidt, C., Jannasch, H. W. (1988). Contrasting effects of sulfide and thiosulfate on symbiotic CO2-assimilation ofPhallodrilus leukodermatus (Annelida). Mar. Biol. 97: 413–419CrossRefGoogle Scholar
  7. Hamburger, K. (1981). A gradient diver for measurement of respiration in individual organisms from the micro- and meiofauna. Mar. Biol. 61: 179–183CrossRefGoogle Scholar
  8. Hammen, C. S., Osborne, P. J. (1959). Carbon dioxide fixation in marine invertebrates: a survey of major phyla. Science, N. Y. 130: 1409–1410Google Scholar
  9. Jannasch, H. W., Wirsen, C. O. (1985). The biochemical versatility of chemosynthetic bacteria at deep-sea hydrothermal vents. Bull. biol. Soc. Wash. 6: 325–334Google Scholar
  10. Jensen, P. (1986). Nematode fauna in the sulphide-rich brine seep and adjacent bottoms of the East Flower Garden, NW Gulf of Mexico. Mar. Biol. 92: 489–502CrossRefGoogle Scholar
  11. Jensen, P. (1987a). Feeding ecology of free-living aquatic nematodes. Mar. Ecol. Prog. Ser. 35: 187–196Google Scholar
  12. Jensen, P. (1987b). Differences in microhabitat, abundance, biomass and body size between oxybiotic and thiobiotic freeliving marine nematodes. Oecologia 71: 564–567CrossRefGoogle Scholar
  13. Kelly, P. D. (1982). Biochemistry of the chemolithotrophic oxidation of inorganic sulphur. Phil. Trans. R. Soc. (Ser. B) 298: 473–497Google Scholar
  14. Klekowski, R. Z. (1971). Cartesian diver respirometry for aquatic animals. Polskie Archwm. Hydrobiol. 18: 93–114Google Scholar
  15. Klekowski, R. Z., Schiemer, F., Duncan, A. (1980). Ampulla gradient diver microrespirometry. Ekol. Pol. 28 (4): 675–683Google Scholar
  16. Kuenen, J. G., Beudeker, R. F. (1982). Microbiology of thiobacilli and other sulphur oxidizing autotrophs, mixotrophs and heterotrophs. Phil. Trans. R. Soc. (Ser. B) 298: 473–497Google Scholar
  17. Lasserre, P. (1976). Metabolic activities of benthic microfauna and meiofauna: recent advances and review of suitable methods of analysis. In: Mac Cave, I. N. (ed.) The benthic boundary layer. Plenum, New York, p. 95–142Google Scholar
  18. Lovlie, A., Zeuthen, E. (1962). The gradient diver — a recording instrument for gasometric micro-analysis. Compt. Rend. Trav. Lab. Carlsberg 32(31): 512–534Google Scholar
  19. Nexø, B. A., Hamburger, K., Zeuthen, E. (1972). Simplified microgasometry with gradient divers. Compt. Rend. Trav. Lab. Carlsberg 39(4): 33–63Google Scholar
  20. Ott, J. A. (1972). Determination of fauna boundaries of nematodes in an intertidal sand flat. Int. Revue ges. Hydrobiol. 57(4): 645–663Google Scholar
  21. Ott, J. A., Novak, R. (1989). Living at an interface: Meiofauna at the oxygen/sulfide boundary of marine sediments. In: Ryland, J. S., Tyler, P. A. (eds.). Reproduction, genetics and distribution of marine organisms. Olsen & Olsen, Fredensborg, p. 415–422Google Scholar
  22. Ott, J. A., Rieger, G., Rieger, R., Enderes, F. (1982). New mouthless interstitial worms from the sulfide system: symbiosis with prokaryotes. Pubbl. Staz. zool. Napoli (I: Mar. Ecol.) 3(4): 313–333Google Scholar
  23. Ott, J. A., Schiemer, F. (1973). Respiration and anaerobiosis of free living nematodes from marine and limnic sediments. Neth. J. Sea Res. 7: 233–243CrossRefGoogle Scholar
  24. Powell, E. N., Crenshaw, M. A., Rieger, R. M. (1979). Adaptation to sulfide in the meiofauna of the sulfide system. I.35S-sulfide accumulation and the presence of a sulfide detoxification system. J. exp. mar. Biol. Ecol. 37: 57–76CrossRefGoogle Scholar
  25. Riemann, F., Schrage, M. (1988). Carbon dioxide as an attractant for the free-living marine nematodeAdoncholaimus thalassophygas. Mar. Biol. 98: 81–95CrossRefGoogle Scholar
  26. Schiemer, F. (1987). Nematoda. In: Pandian, T. J., Vernberg, F. J. (eds.). Animal energetics, Vol. 1. Academic Press, New York, p. 185–215Google Scholar
  27. Schiemer, F., Duncan, A. (1974). The oxygen consumption of a freshwater benthic nematodeTobrilus gracilis (Bastian). Oecologia 15: 212–216CrossRefGoogle Scholar
  28. Southward, E. C. (1986). Gill symbionts in thyasirids and other bivalve mollusca. J. mar. biol. Ass. U.K. 66: 889–914Google Scholar
  29. Steudel, R. (1989). On the nature of the “elemental sulfur” (S°) produced by sulfur-oxidizing bacteria — a model for S° globules. In: Schlegel, H. G., Bowien, B. (eds.). Biology of autotrophic bacteria. Science Tech. Publ., Madison, p. 193–217Google Scholar
  30. Vetter, R. D. (1985). Elemental sulfur in the gills of three species of clams containing chemoautotrophic symbiotic bacteria: a possible inorganic energy storage compound. Mar. Biol. 88: 33–42CrossRefGoogle Scholar
  31. Wieser, W. (1959). Eine ungewöhnliche Assoziation zwischen Blaualgen und freilebenden marinen Nematoden. Österr. bot. Zeitschr. 106: 81–87CrossRefGoogle Scholar
  32. Wieser, W. (1960). Benthic studies in Buzzards Bay II. The meiofauna. Limnol. Oceanogr. 5: 121–137Google Scholar
  33. Wieser, W. (1975). Meiofauna as a tool in the study of sediment heterogeneity: ecophysiological aspects. A review. Cah. Biol. Mar. 16: 647–670Google Scholar
  34. Wieser, W., Ott, J. A., Schiemer, F., Gnaiger, E. (1974). An ecophysiological study of some meiofauna species inhabiting a sandy beach at Bermuda. Mar. Biol. 26: 248–253CrossRefGoogle Scholar
  35. Zeuthen, E. (1950). Cartesian diver microrespirometer. Biol. Bull. mar. biol. Lab., Woods Hole 48(2): 139–143Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • F. Schiemer
    • 1
  • R. Novak
    • 1
  • J. Ott
    • 1
  1. 1.Institute of ZoologyUniversity of ViennaViennaAustria

Personalised recommendations