Skip to main content
Log in

Sulfide tolerance and detoxification in shallow-water marine fishes

  • Published:
Marine Biology Aims and scope Submit manuscript

Abstract

Hydrogen sulfide is a potent inhibitor of aerobic respiration. Sulfide is produced in sediments, and many species of fish live in association with the bottom. Tolerance tests, enzyme assays, and chromatography of sulfur compounds in thirteen species of shallow-water marine fishes (collected in San Diego, California, USA in 1987–1988) indicate adaptations to sulfide that vary with habitat and lifestyle. Tidal-marsh inhabitants, like Gillichthys mirabilis and Fundulus parvipinnis, have higher tolerance to sulfide (96 h LC50 at 525 to 700 μM) relative to outer-bay and open-coast inhabitants (surviving <12 h at much lower concentrations). The cytochrome c oxidase of all species shows high activity and susceptibility to sulfide poisoning, with 50% inhibition at 30 to 500 nM in various tissues. The two marsh species are able to survive at sulfide concentrations already inhibitory to their cytochrome c oxidase and fatal to other species. All species detoxify sulfide by oxidizing it to thiosulfate. All have sulfide-oxidizing activity in the blood, spleen, kidney, liver and gills, which correlates significantly with heme content. Thiosulfate appears in the tissues of sulfide-exposed fish and builds up to high concentrations (up to 2 mM) with stronger and longer exposure. Unexposed fish contain little or no thiosulfate. Sulfide is barely detectable in the tissues, even in high-sulfide exposure tests. We suggest that fish blood, in having high sulfide-oxidizing activity and no cytochrome c oxidase, can act as a short-term first line of defense against sulfide, and thus minimize the amount that reaches the vital organs. The results of this study indicate that sulfide is a significant environmental factor influencing the ecological distribution of marine fishes.

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

Access this article

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

Instant access to the full article PDF.

Similar content being viewed by others

Literature cited

  • Adelman, I. R., Smith, L. L., Jr. (1970). Effect of hydrogen sulfide on northern pike eggs and sac fry. Trans. Am. Fish. Soc. 99: 501–509

    Google Scholar 

  • Adelman, I. R., Smith, L. L., Jr. (1972). Toxicity of hydrogen sulfide to goldfish (Carassius auratus) as influenced by temperature, oxygen and bioassay techniques. J. Fish. Res. Bd Can., 29: 1309–1317

    Google Scholar 

  • Arp, A. J., Childress, J. J., Vetter, R. D. (1987). The sulpide-binding protein in the blood of the vestimentiferan tube-worm, Riftia pachyptila, is the extracellular hemoglobin. J. exp. Biol. 128: 139–158

    Google Scholar 

  • Baird, R., Wilson, D., Milliken, D. (1973). Observations of Bregmaceros nectabanus Whitley in the anoxic, sulfurous water of the Cariaco Trench. Deep-Sea Res. 20: 503–504

    Google Scholar 

  • Baxter, C. F., Van Reen, R. (1958). The oxidation of sulfide to thiosulfate by metallo-protein complexes and by ferritin. Biochim. biophys. Acta 28: 573–578

    Google Scholar 

  • Berner, R. (1963). Electrode studies of hydrogen sulfide in marine sediments. Geochim. cosmochim. Acta 27: 563–575

    Google Scholar 

  • Bonn, E. W., Follis, B. J. (1967). Effects of hydrogen sulfide on channel catfish (Ictalurus punctatus). Trans. Am. Fish. Soc. 96: 31–37

    Google Scholar 

  • Broderius, S. J., Smith, L. L., Jr. (1976). Effect of hydrogen sulfide on fish and invertebrates. Part II. Hydrogen sulfide determination and relationship between pH and sulfide toxicity. Ecol. Res. Ser. (U.S. Environmental Protection Agency, Duluth, Minn.) Ref. 600/3-76-062b: 1–109

  • Cline, J. D. (1969). Spectrophotometric determination of hydrogen sulfide in natural waters. Limnol. Oceanogr. 14: 454–458

    Google Scholar 

  • Colby, P. J., Smith, L. L., Jr. (1967). Survival of walleye eggs and fry on paper fiber sludge deposits in Rainy River, Minnesota. Trans. Am. Fish. Soc. 96: 278–296

    Google Scholar 

  • Courtois, L. A. (1976). Respiratory responses of Gillichthys mirabilis to changes in temperature, dissolved oxygen and salinity. Comp. Biochem. Physiol. 53A: 7–14

    Google Scholar 

  • Fahey, R. C., Newton, G. L. (1987). Determination of low-molecular-weight thiols using monobromobimane fluorescent labeling and high-performance liquid chromatography Meth. Enzym. 143: 83–96

    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 

  • Greaney, G. S., Place, A. R., Cashon, R. E., Smith, G., Powers, D. A. (1980). Time course of changes in enzyme activities and blood respiratory properties of killifish during long-term acclimation to hypoxia. Physiol. Zoöl. 53: 136–144

    Google Scholar 

  • Hand, S. C., Somero, G. N. (1983). Energy metabolism pathways by hydrothermal vent animals: adaptations to a food-rich and sulfide-rich deep-sea environment. Biol. Bull. mar. biol. Lab., Woods Hole 165: 167–181

    Google Scholar 

  • Hartree, E. F. (1972). Determination of protein: a modification of the Lowry method that gives a linear photometric response. Analyt. Biochem. 48: 422–427

    Google Scholar 

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

    Google Scholar 

  • Luther, G. W. III, Church, T. M., Scudlark, J. R., Cosman, M. (1986). Inorganic and organic sulfur cycling in salt-marsh pore waters. Science, N. Y. 232: 746–749

    Google Scholar 

  • Meister, A., Anderson, M. E. (1983). Glutathione. A. Rev. Biochem. 52: 711–760

    Google Scholar 

  • National Research Council (Division of Medical Science, Subcommittee on Hydrogen Sulfide), (1979). Hydrogen sulfide. University Park Press, Baltimore

    Google Scholar 

  • Patel, S., Spencer, C. (1963). The oxidation of sulfide by the haem compounds from the blood of Arenicola marina. J. mar. biol. Ass. U.K. 43: 167–175

    Google Scholar 

  • Powell, M. A., Arp, A. J. (1989). Hydrogen sulfide oxidation by abundant non-hemoglobin heme compounds in marine invertebrates from sulfide-rich habitats. J. exp. Zool. 249: 121–132

    Google Scholar 

  • Powell, E. N., Crenshaw, M. A., Reiger, R. M. (1979). Adaptations to sulfide in the meiofauna of the sulfide system. I. 35S accumulation and the presence of a sulfide detoxification system. J. exp. mar. Biol. Ecol. 37: 57–76

    Google Scholar 

  • Powell, E. N., Crenshaw, M. A., Reiger, R. M. (1980). Adaptations to sulfide in the sulfide-system meiofauna. Endproducts of sulfide detoxification in three turbellarians and a gastrotrich. Mar. Ecol. Prog. Ser. 2: 169–177

    Google Scholar 

  • Powell, M. A., Somero, G. N. (1985). Sulfide oxidation oceurs in the animal tissue of the gutless clam, Solemya reidi. Biol. Bull. mar. biol. Lab. Woods Hole 169: 164–181

    Google Scholar 

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

    Google Scholar 

  • Reynolds, F. A., Haines, T. A. (1980). Effects of chronic exposure to hydrogen sulfide on newly hatched brown trout Salmo trutta L. Envir. Pollut. (Ser. A) 22: 11–17

    Google Scholar 

  • Smith, L., Kruszyna, H., Smith, R. P. (1977). The effect of methemoglobin on the inhibition of cytochrome c oxidase by cyanide, sulfide or azide. Biochem. Pharmac. 26: 2247–2250

    Google Scholar 

  • Smith, L. L., Jr., Oseid, D. M. (1974). Effect of hydrogen sulfide on development and survival of eight freshwater fish species. In: Blaxter, J. H. S. (ed.) Early life history of fishes. Springer-Verlag, New York, p. 417–430

    Google Scholar 

  • Smith, L. L., Jr., Oseid, D. M., Kimball, G. L., El-Kandelgy, S. (1976a) Toxicity of hydrogen sulfide to various life history stages of bluegill (Lepomis macrochirus Rafinesque). Trans. Am. Fish Soc. 105: 442–449

    Google Scholar 

  • Smith, L. L., Jr., Oseid, D. M., Olson, L. E. (1976b). Acute and chronic toxicity of hydrogen sulfide to the fathead minnow (Pimephales promelas). Envir. Sci. Technol. 10: 565–568

    Google Scholar 

  • Smith, R. P., Abbanat, R. A. (1966). Protective effect of oxidized glutathione in acute sulfide poisoning. Toxic. appl. Pharmac. 9: 209–217

    Google Scholar 

  • Smith, R. P., Gosselin, R. E. (1964). The influence of methemoglobinemia on the lethality of some toxic anions. II. Sulfide. Toxic. appl. Pharmac. 6: 584–592

    Google Scholar 

  • Smith, R. P., Gosselin, R. E. (1966). On the mechanism of sulfide inactivation by methemoglobin. Toxic. appl. Pharmac. 8: 159–172

    Google Scholar 

  • Sörbo, B. (1958). On the formation of thiosulfate from inorganic sulfide by liver tissue and heme compounds. Biochim. biophys. Acta 27: 324–329

    Google Scholar 

  • Theede, H., Ponat, A., Hiroki, K., Schlieper, C. (1969). Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulfide. Mar. Biol. 2: 325–337

    Google Scholar 

  • Torrans, E. L., Clemens, H. P. (1982). Physiological and biochemical effects of acute exposure of fish to hydrogen sulfide. Comp. Biochem. Physiol. 71C: 183–190

    Google Scholar 

  • Vetter, R. D., Hodson, R. E. (1982). Use of adenylate concentrations and adenylate energy charge as indicators of hypoxic stress in estuarine fish. Can. J. Fish. aquat. Sciences 39: 535–541

    Google Scholar 

  • Vetter, R. D., Matrai, P. A., Javor, B., O'Brien, J. (1989). Reduced sulfur compounds in the marine environment: analysis by HPLC. Symp. Ser. Am. chem. Soc. 393: 243–261

    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 

  • Wharfe, J. (1977). The intertidal sediment habitats of the Lower Medway estuary in Kent. Envir. Pollut. 13: 79–91

    Google Scholar 

  • Zar, J. H. (1984). Biostatistical analysis. 2nd ed. Prentice-Hall, New Jersey

    Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Additional information

Communicated by M. G. Hadfield, Honolulu

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bagarinao, T., Vetter, R.D. Sulfide tolerance and detoxification in shallow-water marine fishes. Mar. Biol. 103, 291–302 (1989). https://doi.org/10.1007/BF00397262

Download citation

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/BF00397262

Keywords

Navigation