Hydrobiologia

, Volume 222, Issue 1, pp 1–12 | Cite as

Histological studies on Halicryptus spinulosus (Priapulida) with regard to environmental hydrogen sulfide resistance

  • Rolf Oeschger
  • Hans Heinrich Janssen
Article

Abstract

The priapulid Halicryptus spinulosus has an outstanding resistance to anoxia and hydrogen sulfide, which enables the animal to survive in deteriorating environments. Whole-body staining procedures, as well as light and scanning electron microscopy were used to study structures and mechanisms possibly involved in sulfide detoxification.

The cuticle of the trunk is covered by a coat of mucus and bacteria. Within this coat considerable amounts of finely dispersed iron are precipitated, probably as a Fe2+-compound. It is suggested that the iron functions as a rechargeable buffer against hydrogen sulfide, protecting both the bacteria and the priapulid host. Although this chemical shield may not alone account for long-term protection, it allows the animal to gain time for metabolic adaptations.

Key words

histology iron hydrogen sulfide Halicryptus spinulosus 

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References

  1. Apel, W., 1885. Beitrag zur Anatomic and Histologic des Priapulus caudatus (Lam.) and des Halicryptus spinulosus (v. Sieb.). Z. wiss. Zool. 42: 459–528.Google Scholar
  2. Back, H. & F. Prosi, 1985. Distribution of inorganic cations in Limnodrilus udekemianus (Oligochaeta, Tubificidae) using laser induced microprobe mass analysis, with special emphasis on heavy metals. Micron. Mirosc. Acta 16: 145–150.Google Scholar
  3. Bagarinao, T. & R. D. Vetter, 1989. Sulfide tolerance and detoxification in shallow-water marine fishes. Mar. Biol. 103: 291–302.Google Scholar
  4. Barnes, R. D., 1974. Invertebrate Zoology. 3rd edn. Saunders, Philadelphia etc.Google Scholar
  5. Bernárt, I., 1981. Eisenstoffwechsel. G. Fischer Verlag, Stuttgart, New York.Google Scholar
  6. Boeck, P., 1984. Der Semidünnschnitt. J. F. Bergmann Verlag München.Google Scholar
  7. Brock, T. D., S. W. Smith & M. T. Madigan, 1984. Biology of microorganisms. 4th edn., Prentice Hall, New Jersey.Google Scholar
  8. Cavanaugh, C. M., 1983. Symbiotic chemoautotrophic bacteria in sulfide-habitat marine invertebrates. Nature 302: 59–61.Google Scholar
  9. Cavanaugh, C. M., S. L. Gardiner, M. L. Jones, H. W. Jannasch & J. B. Waterbury, 1981. Prokaryotic cells in the hydrothermal vent tube worm, Riftia pachyptila Jones: Possible chemoautotrophic symbionts. Science 213: 340–342.Google Scholar
  10. Cheng, K. J., R. T. Irvin & J. W. Costerton, 1981. Autochthonous and pathogenic colonization of animal tissues by bacteria. Can. J. Microbiol. 27: 461–490.PubMedGoogle Scholar
  11. Chia, F.-S. & R. M. Warwick, 1969. Assimilation of labelled glucose from seawater by marine nematodes. Nature 224: 720–721.Google Scholar
  12. Daniels, L., N. Belay, B. S. Rajagopal & P. J. Welmer, 1987. Bacterial methanogenesis and growth from CO2 with elemental iron as the sole source of electrons. Science 237: 509–511.Google Scholar
  13. Felbeck, H., 1983. Sulfide oxidation and carbon fixation by the gutless clam Solemya reidi: An animal-bacteria symbiosis. J. Comp. Physiol. 152: 3–11.Google Scholar
  14. Fischer, E. & I. Horváth, 1977. Cytochemical studies on the cuticle and epidermis of Tubifex tubifex Müll. with special regard to the localization of polysaccharides, heavy metals and the DAB-reactivity. Histochemistry 54: 259–271.PubMedGoogle Scholar
  15. Fleming, T. P. & K. S. Richards, 1982. Uptake and surface adsorption of zinc by the freshwater tubificid oligochaete Tubifex tubifex. Comp. Biochem. Physiol. 71C: 69–75.Google Scholar
  16. Frank, L. & D. Massaro, 1980. Oxygen toxicity. Am. J. Med. 69: 117–126.PubMedGoogle Scholar
  17. Gibbs, P. E., G. W. Bryan & K. P. Ryan, 1981. Copper accumulation by the Polychaete Melinna palmata: an antipredation mechanism? J. mar. Biol. Ass. U.K. 61: 707–722.Google Scholar
  18. Giere, O., B. Rhode & N. Dubilier, 1988. Structural peculiarities of the body wall of Tubificoides benedii (Oligochaeta) and possible relations to its life in sulphidic sediments. Zoomorphology 108: 29–39.Google Scholar
  19. Halliwell, B. & J. M. C. Gutteridge, 1985. Free radicals in biology and medicine. Clarendon Press, Oxford.Google Scholar
  20. Holland, N. D. & K. H. Nealson, 1978. The fine structure of the Echinoderm cuticle and the subcuticular bacteria of Echinoderms. Acta zool. (Storch.) 59: 169–185.Google Scholar
  21. Janssen, H. H., 1989. Heavy metal analysis in earthworms from an abandoned mining area. Zool. Anz. 222: 335–360.Google Scholar
  22. Janssen, H. H. & U. Ertelt-Janssen, 1983. Cytochemical demonstration of cadmium and iron in experimental Mytilus edulis. Mikroskopie (Wien) 40: 329–340.Google Scholar
  23. Land, J. van der, 1970. Systematics, zoogeography, and ecology of the Priapulida. Zool. Verh. Leiden 112: 1–118.Google Scholar
  24. Lojda, Z., R. Gorsrau & T. H. Schiebler, 1976. Enzymhistochemische Methoden. Springer Verlag, Berlin.Google Scholar
  25. Millero, F., 1986. The thermodynamics and kinetics of the hydrogen sulfide system in natural waters. Mar. Chem. 18: 121–147.Google Scholar
  26. Morill, A. C., E. N. Powell, R. R. Bidigare & J. M. Shick, 1988. Adaptations to life in the sulfide system: a comparison of oxygen detoxifying enzymes in thiobiotic and oxybiotic meiofauna (and freshwater planarians). J. Comp. Physiol. B 158: 335–344.Google Scholar
  27. National Research Council, Committee on Medical and Biological Effects of Environmental Pollutants, Subcommittee on Hydrogen Sulfide, 1979. Hydrogen sulfide, University Park Press, Baltimore.Google Scholar
  28. Oeschger, R., 1990. Long-term anaerobiosis in sublittoral marine invertebrates from the Western Baltic Sea: Halicryptus spinulosus (Priapulida), Astarte borealis and Arctica islandica (Bivalvia). Mar. Ecol. Prog. Ser. 59: 133–143.Google Scholar
  29. Oeschger, R. & R. Schmaljohann, 1988. Association of various types of epibacteria with Halicryptus spinulosus (Priapulida). Mar. Ecol. Progr. Ser. 48: 285–293.Google Scholar
  30. Oeschger, R. & H. Theede, 1988. Use of biochemical features of macrobenthic species as indicators of long-term oxygen deficiency. Kiefer Meeresforsch., Sonderh. 6: 99–110.Google Scholar
  31. Owen, G., 1965. Observations on the stomach and digestive diverticula of the Lamellibranchiata. II. The nuculidae. Quart. J. Microscop. Sci. 97: 541–567.Google Scholar
  32. Owen, G., 1973. The fine structure and histochemistry of the digestive diverticula of the protobranchiate bivalve Nucula sulcata. Phil. Trans. R. Soc., Lond. 183 (B): 249–264.Google Scholar
  33. Pearse, A. G. E., 1960. Histochemistry. Theoretical and applied. 2nd edn. London, Churchill.Google Scholar
  34. Powell, M. A. & A. J. Arp, 1989. Hydrogen sulfide oxidation by abundant nonhemoglobin heme compounds in marine invertebrates from sulfide-rich habitats. J. exp. Zool. 249: 121–132.Google Scholar
  35. Reinheimer, G., 1981. Mikrobiologie der Gewässer. G. Fischer Verlag, Stuttgart.Google Scholar
  36. Riemann, F. & M. Schrage, 1988. Carbon dioxide as an attractant for the free-living marine nematode Adoncholaimus thalassophygas. Mar. Biol. 98: 81–85.Google Scholar
  37. Rosenberg, L., 1971. Chemical Basis for the histological use of Safranin O in the study of articular cartilage. J. Bone Joint Surgery 53A: 69–82.Google Scholar
  38. Schreiber, A., V. Storch, M. Powilleit & R. P. Higgins, 1991. The blood of Halicryptus spinulosus (Priapulida). Can. J. Zool.: in press.Google Scholar
  39. Southward, A. J. & E. C. Southward, 1968. On a wholeanimal method for the histochemical localization of enzymes under field conditions. J. mar. biol. Ass. U.K. 48: 323–334.Google Scholar
  40. Storch, V., 1991. Priapulida. In: Harrison, F. H. (ed.) Microscopic anatomy of invertebrates, Vol. IV. Liss, New York: in press.Google Scholar
  41. Storch, V., R. P. Higgins, Morse, 1989. Internal anatomy of Meiopriapulus fijiensis (Priapulida). Trans. am. Microsc. Soc. 108: 245–261.Google Scholar
  42. Theede, H., A. Ponat, K. Hiroki & C. Schlieper, 1969. Studies on the resistance of marine bottom invertebrates to oxygen deficiency and hydrogen sulphide. Mar. Biol. 2: 325–337.Google Scholar
  43. 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: 33–42.Google Scholar
  44. Weber, R. E., R. Fange & K. Krogh Rasmussen, 1979. Respiratory significance of priapulid hemerythrin. Mar. Biol. Let. 1: 87–97.Google Scholar
  45. Whitten, B. K. & C. J. Goodnight, 1966. Strontium-89 and calcium-45 accumulation in an aquatic oligochaete. Am. Soc. Zool. 6: 508.Google Scholar

Copyright information

© Kluwer Academic Publishers 1991

Authors and Affiliations

  • Rolf Oeschger
    • 1
  • Hans Heinrich Janssen
    • 2
  1. 1.MeereszoologieUniversität BremenBremerhavenGermany
  2. 2.Alfred-Wegener-Institut für Polar- and MeeresforschungBremerhavenGermany

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