Skip to main content Accessibility help

Sulphide Metabolism in Thalassinidean Crustacea

  • A.R. Johns (a1), A.C. Taylor (a1), R.J.A. Atkinson (a2) and M.K. Grieshaber (a3)


Sulphide occurs widely in marine sediments and is highly toxic to most organisms. Its principal poisoning effect occurs at extremely low concentrations and is the result of inhibition of mitochondrial cytochrome c oxidase. Mud-shrimps (Crustacea: Thalassinidea), construct burrows in sublittoral muddy sediments. The sediment in which they burrow is markedly reduced and conditions within the burrow are usually hypoxic and hypercapnic. Field measurements indicate that the shrimps may be exposed to potentially toxic levels of sulphide in the burrow water (range 0–206 μM, N=37). Laboratory experiments carried out on Calocaris macandreae, Callianassa subterranea and Jaxea nocturna have shown that these species have a high tolerance of sulphide. An oxygen dependent detoxification mechanism exists to defend cytochrome c oxidase from sulphide poisoning. The main detoxification product of this mechanism is thiosulphate which accumulates rapidly even during brief exposures to low concentrations of sulphide. Sulphite also appears as a secondary detoxification product. Aerobic metabolism can be maintained even under severe hypoxia and toxic sulphide conditions. The mud-shrimps switch to anaerobiosis when the detoxification mechanism is saturated. These data indicate that mud-shrimps are physiologically adapted to tolerate elevated levels of sulphide that they may encounter in their natural habitat.



Hide All
Anderson, A.E., Childress, J.J. & Favuzzi, J.A., 1987. Net uptake of CO2 driven by sulphide and thiosulphate oxidation in the bacterial symbiont-containing clam Solemya reidi. Journal of Experimental Biology, 133, 131.
Anderson, A.E., Felbeck, H. & Childress, J.J., 1990. Aerobic metabolism is maintained in animal tissue during rapid sulfide oxidation in the symbiont-containing clam Solemya reidi. Journal of Experimental Zoology, 256, 130134.
Anderson, S.J., 1989. Physiological ecology of the mud-burrowing shrimp Calocaris macandreae. PhD thesis, University of Glasgow.
Anderson, S.J., Atkinson, R.J.A. & Taylor, A.C., 1991. Behavioural and respiratory adaptations of the mud-burrowing shrimp Calocaris macandreae Bell (Thalassinidea: Crustacea) to the burrow environment. Ophelia, 34, 143156.
Arp, A.J., Hansen, B.M. & Julian, D., 1992. Burrow environment and coelomic fluid characteristics of the echiuran worm Urechis caupo from populations at three sites in northern California. Marine Biology, 113, 613623.
Astall, C., 1993. Comparative physiological ecology of some burrowing mud-shrimps (Crustacea, Decapoda, Thalassinidea). PhD thesis, University of Glasgow.
Astall, C.M., Taylor, A.C. & Atkinson, R.J.A., 1996. Notes On Some Branchial Isopods Parasitic On Upogebiid Mud-Shrimps (Decapoda: Thalassinidea). Journal of the Marine Biological Association of the United Kingdom, 76, 821824.
Atkinson, R.J.A., 1987. The burrowing megafaunal communities of the upper arms of Loch Sween. Peterborough: Nature Conservancy Council.
Atkinson, R.J.A & Taylor, A.C., 1988. Physiological ecology of burrowing decapods. Symposia of the Zoological Society of London, 59, 201226.
Bagarinao, T., 1992. Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquatic Toxicology, 24, 2162.
Bagarinao, T. & Vetter, R.D., 1990. Oxidative detoxification of sulphide by mitochondria of the California killifish Fundulus parvipinnis and the speckled sanddab Citharichthys stigmaeus. Journal of Comparative Physiology, 160B, 519527.
Beauchamp, R.O. Jr, Bus, J.S., Popp, J.A., Boreiko, C.J. & Andjelkovich, D.A., 1984. A critical review of the literature on hydrogen sulphide toxicology. CRC Critical Reviews in Toxicology, 13, 2597.
Chen, C., Rabourdin, B. & Hammen, C.S., 1987. The effect of hydrogen sulfide on the metabolism of Solemya velum and enzymes of sulfide oxidation in gill tissue. Comparative Biochemistry and Physiology, 88B, 949952.
Chen, K.Y. & Morris, J.C., 1972. Kinetics of oxidation of aqueous sulfide by O2. Environmental Science and Technology, 6, 529537.
Childress, J.J. & Mickel, T.J., 1982. Oxygen and sulfide consumption rates of the vent clam Calytogena pacifica. Marine Biology Letters, 3, 7379.
Cline, J.D., 1969. Spectrophotometric determination of hydrogen sulphide in natural waters. Limnology and Oceanography, 14, 454458.
Cline, J.D. & Richards, F.A., 1969. Oxygenation of hydrogen sulfide in seawater at constant salinity, temperature, and pH. Environmental Science and Technology, 3, 838843.
Dworschak, P.C., 1983. The biology of Upogebia pusilla (Petagna) (Decapoda, Thalassinidea). I. The burrows. Marine Ecology. Pubblicazioni della Stazione Zoologica di Napoli I, 4, 1943.
Eaton, R.A. & Arp, A.J., 1993. Aerobic respiration during sulfide exposure in the marine echiuran worm Urechis caupo. Physiological Zoology, 66, 119.
Engel, P. & Jones, P.B., 1978. Causes and elimination of erratic blanks in enzymatic metabolite assays involving the use of NAD+ in alkaline buffers: improved conditions for assay of L-glutamate and L-lactate and other metabolites. Analytical Biochemistry, 88, 475—484.
Evans, C.L., 1967. The toxicity of hydrogen sulphide and other sulphides. Quarterly Journal of Experimental Physiology, 52, 231248.
Fahey, R.C., Newton, G.L., Dorian, R. & Kosower, E.M., 1981. Analysis of biological thiols: quantitative determination of thiols at the picomole level based upon derivatization with monobromobimanes and separation by cation-exchange chromatography. Analytical Biochemistry, 111, 357365.
Felder, D.L., 1979. Respiratory adaptations of the estuarine mud-shrimp, Callianassa jamaicense (Schmitt, 1935) (Crustacea, Decapoda, Thalassinidea). Biological Bulletin. Marine Biological Laboratory, Woods Hole, 157, 125137.
Felder, D.L. & Rodrigues, S., 1993. Reexamination of the ghost shrimp Lepidophthalmus louisianensis (Schmitt, 1953) from the northern Gulf of Mexico and comparison to L. siribola, new species, from Brazil (Decapoda: Thalassinidea: Callianassidae). Journal of Crustacean Biology, 13, 357376.
Fenchel, T.M. & Reidl, R.J., 1970. The sulfide system: a new biotic community underneath the oxidised layer of marine sand bottoms. Marine Biology, 7, 255268.
Forster, S. & Graf, G., 1992. Continuously measured changes in redox potential influenced by oxygen penetrating from burrows of Callianassa subterranea. Hydrobiologia, 235/236, 527532.
Forster, S. & Graf, G., 1995. Impact of irrigation on oxygen flux into the sediment: intermittent pumping by Callianassa subterranea and ‘piston-pumping’ by Lanice conchilega. Marine Biology, 123, 335346.
Gilboa-Garber, N., 1971. Direct spectrophotometric determination of inorganic sulfide in biological materials and in other complex mixtures. Analytical Biochemistry, 43, 129133.
Goldhaber, M.B. & Kaplan, I.R. 1975. Apparent dissociation constants of hydrogen sulphide in chloride solutions. Marine Chemistry, 3, 83104.
Gorodezky, L.A. & Childress, J.J., 1994. Effects of sulfide exposure history and hemolymph thiosulphate on oxygen-consumption rates and regulation in the hydrothermal vent crab Bythograea thermydron. Marine Biology, 120, 123131.
Gutman, I. & Wahlefeld, A.W., 1974. L-(+)-lactate. Determination with lactate dehydrogenase and NAD+. In Methods in enzymatic analysis (ed. H.U., Bergmeyer), pp. 14641468. New York: Academic Press.
Hagerman, L. & Vismann, B., 1993. Anaerobic metabolism, hypoxia and hydrogen sulphide in the brackish water isopod Saduria entomon (L.). Ophelia, 38, 111.
Hagerman, L. & Vismann, B., 1995. Anaerobic metabolism in the shrimp Crangon crangon exposed to hypoxia, anoxia and hydrogen sulfide. Marine Biology, 123, 235240.
Ingvorsen, K. & Jørgensen, B.B., 1979. Combined measurement of oxygen and sulfide in water samples. Limnology and Oceanography, 24, 390393.
Jorgensen, B.B., 1982. Ecology of the bacteria of the sulphur cycle with special reference to anoxic-oxic interface environments. Philosophical Transactions of the Royal Society B, 298, 548560.
Jorgensen, B.B., 1988. Ecology of the sulfur cycle: oxidative pathways in sediments. In The nitrogen and sulphur cycles (ed. J.A., Cole), pp. 3163. Cambridge University Press.
Jergensen, B.B. & Fenchel, T., 1974. The sulfur cycle of a marine sediment model system. Marine Biology, 24, 189201.
Manning, R.B., 1975. Two methods for collecting decapods in shallow water. Crustaceana, 29, 317319.
Meadows, P.S., Deans, E.A. & Anderson, J.G., 1981. Responses of Corophium volutator to sediment sulphide. Journal of the Marine Biological Association of the United Kingdom, 61, 739748.
National Research Council, 1979. Hydrogen sulfide. Baltimore, USA: University Park Press.
Newton, G.L., Donain, R.D. & Fahey, R.C., 1981. Analysis of biological thiols: derivatization with monobromobimane and separation by reverse phase highperformance liquid chromatography. Biochimica et Biophysica Acta, 114, 383387.
Nicholls, P., 1975. The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts on reduced alpha-peak. Biochimica et Biophysica Acta, 396, 2435.
Nickell, L.A., 1992. Deep bioturbation in organically enriched sediments. PhD thesis, University of London.
Nickell, L.A. & Atkinson, R.J.A., 1995. Functional morphology of burrows and trophic modes of three thalassinidean shrimp species, and a new approach to the classification of thalassinidean burrow morphology. Marine Ecology Progress Series, 128, 181197.
O'brien, J. & Vetter, R.D., 1990. Production of thiosulphate during sulphide oxidation by mitochondria of the symbiont-containing bivalve Solemya reidi. Journal of Experimental Biology, 149, 133148.
Oeschger, R. & Vetter, R.D., 1992. Sulphide detoxification and tolerance in Halicryptus spinulosus (Priapulida): a multiple strategy. Marine Ecology Progress Series, 86, 167179.
Oeschger, R. & Vismann, B., 1994. Sulphide tolerance in Heteromastus filiformis (Polychaeta): mitochondrial adaptations. Ophelia, 40, 147158.
Ott, J., Novak, R., Schiemer, F., Hentschel, U., Nebelsick, M. & Polz, M., 1991. Tackling the sulfide gradient: a novel strategy involving marine nematodes and chemoautotrophic ectosymbionts. Marine Ecology. Pubblicazioni della Stazione Zoologica di Napoli 1, 12, 261279.
Paterson, B.D. & Thome, M.J., 1995. Measurements of oxygen uptake, heart and gill bailer rates of the callianassid burrowing shrimp Trypaea australiensis Dana and its responses to low oxygen tensions. Journal of Experimental Marine Biology and Ecology, 194, 3952.
Polz, M.F., Felbeck, H., Novak, R., Nebelsick, M. & Ott, J.A., 1992. Chemoautotrophic, sulfuroxidizing symbiotic bacteria on marine nematodes: morphological and biochemical characterisation. Microbial Ecology, 24, 313329.
Powell, M.A. & Somero, G.N., 1986. Hydrogen sulfide oxidation is coupled to oxidative phosphorylation in mitochondria of Solemya reidi. Science, New York, 233, 563566.
Revsbech, N.P. & Ward, D.M., 1983. Oxygen microelectrode that is insensitive to medium chemical composition: use in an acid microbial mat dominated by Cyanidium caldarium. Applied and Environmental Microbiology, 45, 755759.
Steffensen, J.F., 1989. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry, 6, 4959.
Somero, G.N., Childress, J.J. & Anderson, A.E., 1989. Transport, metabolism, and detoxification of hydrogen sulfide in animals from sulfide-rich marine environments. I. General introduction: problems and opportunities facing animals living in high-sulfide environments. Reviews of Aquatic Sciences, 1, 591614.
Southward, E.C., 1994. Hot vents, deep seeps and black mud: symbiosis in sulphur and methane based ecosystems, pp. 136. Isle of man: Port Erin Laboratory Centenary Publication.
Spurr, A.R., 1969. A low viscosity epoxy embedding resin for electron microscopy. journal of Ultrastructural Research, 26, 3143.
Suchanek, T.H., 1983. Control of seagrass communities and sediment distribution by Callianassa (Crustacea, Thalassinidea) bioturbation. Journal of Marine Research, 41, 281298.
Theede, H., 1973. Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates. Netherlands Journal of Sea Research, 7, 244252.
Theede, H., Ponat, A., Hiroki, K. & Schlieper, C., 1969. Studies on the resistance of marine bottom invertebrates to oxygen-deficiency and hydrogen sulphide. Marine Biology, 2, 325337.
Thiermann, F., Niemeyer, A.S. & Giere, O., 1996. Variations in the sulfide regime and the distribution of macrofauna in an intertidal flat in the North Sea. Helgoländer Meeresuntersuchungen, 50, 87104.
Thompson, R.K. & Pritchard, A. W., 1969. Respiratory adaptations of two burrowing crustaceans, Callianassa californiensis and Upogebia pugettensis (Decapoda, Thalassinidea). Biological Bulletin. Marine Biology Laboratory, Woods Hole, 136, 274287.
Tunnicliffe, V., 1991. The biology of the hydrothermal vents: ecology and evolution. Oceanography and Marine Biology. Annual Review. London, 29, 319–107.
Vaugelas, J.V. De, 1990. Ecologie des callianasses (Crustacea, Decapoda, Thalassinidea) et milieu récifal Indo-Pacifique. Conséquences du remaniement sédimentaire sur la distribution des matieres humique, des métaux trace et des radionucléides. Doctorat d'Habilitation a Diriger des Recherches, Université de Nice.
Vetter, R.D., Matrai, P. A., Javor, B. & O'brien, J., 1989. Reduced sulfur compounds in the marine environment: analysis by high-performance liquid chromatography. In Biogenic sulfur in the environment (ed. E.S., Saltzman and W.J., Cooper). Washington, DC: American Chemical Society. [ACS Symposium Series no. 393.]
Vetter, R.D., Powell, M.A. & Somero, G.N., 1991. Metazoan adaptations to hydrogen sulphide. In Metazoan life without oxygen (ed. C., Bryant), pp. 109128. London: Chapman & Hall.
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. Physiological Zoology, 60, 121137.
Vismann, B., 1991a. Sulfide tolerance: physiological mechanisms and ecological implications. Ophelia, 34, 127.
Vismann, B., 1991b. Physiology of sulfide in the isopod Saduria (Mesidotea) entomon. Marine Ecology Progress Series, 76, 283293.
Völkel, S. & Grieshaber, M.K., 1992. Mechanisms of sulphide tolerance in the peanut worm, Sipnnculus nudus (Sipunculidae) and in the lugworm, Arenicola marina (Polychaeta). Journal of Comparative Physiology, 162B, 469477.
Völkel, S. & Grieshaber, M.K., 1994. Oxygen dependent sulfide detoxification in the lugworm Arenicola marina. Marine Biology, 118, 137147.
Völkel, S. & Grieshaber, M.K., 1995. Sulfide tolerance in marine invertebrates. Advances in Comparative and Environmental Physiology, 22, 233257.
Völkel, S. & Grieshaber, M.K., 1996. Mitochondrial sulphide oxidation in Arenicola marina. Evidence for alternative electron pathways. European Journal of Biochemistry, 235, 231237.
Völkel, S., Hauschild, K. & Grieshaber, M.K., 1995. Sulfide stress and tolerance in the lugworm Arenicola marina during low tide. Marine Ecology Progress Series, 122, 205215.
Waslenchuk, D.G., Matson, E. A., Zajac, R.N., Dobbs, F.C. & Tramontano, J.M., 1983. Geochemistry of burrow waters vented by a bioturbating shrimp in Bermudian sediments. Marine Biology, 72, 219225.

Sulphide Metabolism in Thalassinidean Crustacea

  • A.R. Johns (a1), A.C. Taylor (a1), R.J.A. Atkinson (a2) and M.K. Grieshaber (a3)


Full text views

Total number of HTML views: 0
Total number of PDF views: 0 *
Loading metrics...

Abstract views

Total abstract views: 0 *
Loading metrics...

* Views captured on Cambridge Core between <date>. This data will be updated every 24 hours.

Usage data cannot currently be displayed