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Sulphide Metabolism in Thalassinidean Crustacea

Published online by Cambridge University Press:  11 May 2009

A.R. Johns ,
A.C. Taylor ,
R.J.A. Atkinson  and
M.K. Grieshaber
A.R. Johns
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, Scotland, G12 8QQ
A.C. Taylor
Affiliation:
Institute of Biomedical and Life Sciences, University of Glasgow, Glasgow, Scotland, G12 8QQ
R.J.A. Atkinson
Affiliation:
University Marine Biological Station, Millport, Isle of Cumbrae, Scotland, KA28 OEG
M.K. Grieshaber
Affiliation:
Institut für Zoophysiologie, Heinrich-Heine-Universität, Düsseldorf, Germany
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Extract

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.

Type
Research Article
Information
Journal of the Marine Biological Association of the United Kingdom , Volume 77 , Issue 1 , February 1997 , pp. 127 - 144
Copyright
Copyright © Marine Biological Association of the United Kingdom 1997

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References

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, 1–31.Google Scholar
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, 130–134.CrossRefGoogle Scholar
Anderson, S.J., 1989. Physiological ecology of the mud-burrowing shrimp Calocaris macandreae. PhD thesis, University of Glasgow.Google Scholar
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, 143–156.CrossRefGoogle Scholar
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, 613–623.CrossRefGoogle Scholar
Astall, C., 1993. Comparative physiological ecology of some burrowing mud-shrimps (Crustacea, Decapoda, Thalassinidea). PhD thesis, University of Glasgow.Google Scholar
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, 821–824.CrossRefGoogle Scholar
Atkinson, R.J.A., 1987. The burrowing megafaunal communities of the upper arms of Loch Sween. Peterborough: Nature Conservancy Council.Google Scholar
Atkinson, R.J.A & Taylor, A.C., 1988. Physiological ecology of burrowing decapods. Symposia of the Zoological Society of London, 59, 201–226.Google Scholar
Bagarinao, T., 1992. Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms. Aquatic Toxicology, 24, 21–62.CrossRefGoogle Scholar
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, 519–527.Google Scholar
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, 25–97.CrossRefGoogle Scholar
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, 949–952.Google Scholar
Chen, K.Y. & Morris, J.C., 1972. Kinetics of oxidation of aqueous sulfide by O2. Environmental Science and Technology, 6, 529–537.CrossRefGoogle Scholar
Childress, J.J. & Mickel, T.J., 1982. Oxygen and sulfide consumption rates of the vent clam Calytogena pacifica. Marine Biology Letters, 3, 73–79.Google Scholar
Cline, J.D., 1969. Spectrophotometric determination of hydrogen sulphide in natural waters. Limnology and Oceanography, 14, 454–458.CrossRefGoogle Scholar
Cline, J.D. & Richards, F.A., 1969. Oxygenation of hydrogen sulfide in seawater at constant salinity, temperature, and pH. Environmental Science and Technology, 3, 838–843.CrossRefGoogle Scholar
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, 19–43.CrossRefGoogle Scholar
Eaton, R.A. & Arp, A.J., 1993. Aerobic respiration during sulfide exposure in the marine echiuran worm Urechis caupo. Physiological Zoology, 66, 1–19.CrossRefGoogle Scholar
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.CrossRefGoogle ScholarPubMed
Evans, C.L., 1967. The toxicity of hydrogen sulphide and other sulphides. Quarterly Journal of Experimental Physiology, 52, 231–248.CrossRefGoogle ScholarPubMed
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, 357–365.CrossRefGoogle ScholarPubMed
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, 125–137.CrossRefGoogle Scholar
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, 357–376.Google Scholar
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, 255–268.CrossRefGoogle Scholar
Forster, S. & Graf, G., 1992. Continuously measured changes in redox potential influenced by oxygen penetrating from burrows of Callianassa subterranea. Hydrobiologia, 235/236, 527–532.CrossRefGoogle Scholar
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, 335–346.CrossRefGoogle Scholar
Gilboa-Garber, N., 1971. Direct spectrophotometric determination of inorganic sulfide in biological materials and in other complex mixtures. Analytical Biochemistry, 43, 129–133.Google Scholar
Goldhaber, M.B. & Kaplan, I.R. 1975. Apparent dissociation constants of hydrogen sulphide in chloride solutions. Marine Chemistry, 3, 83–104.CrossRefGoogle Scholar
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, 123–131.CrossRefGoogle Scholar
Gutman, I. & Wahlefeld, A.W., 1974. L-(+)-lactate. Determination with lactate dehydrogenase and NAD+. In Methods in enzymatic analysis (ed. H.U., Bergmeyer), pp. 1464–1468. New York: Academic Press.Google Scholar
Hagerman, L. & Vismann, B., 1993. Anaerobic metabolism, hypoxia and hydrogen sulphide in the brackish water isopod Saduria entomon (L.). Ophelia, 38, 1–11.CrossRefGoogle Scholar
Hagerman, L. & Vismann, B., 1995. Anaerobic metabolism in the shrimp Crangon crangon exposed to hypoxia, anoxia and hydrogen sulfide. Marine Biology, 123, 235–240.Google Scholar
Ingvorsen, K. & Jørgensen, B.B., 1979. Combined measurement of oxygen and sulfide in water samples. Limnology and Oceanography, 24, 390–393.CrossRefGoogle Scholar
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, 548–560.Google ScholarPubMed
Jorgensen, B.B., 1988. Ecology of the sulfur cycle: oxidative pathways in sediments. In The nitrogen and sulphur cycles (ed. J.A., Cole), pp. 31–63. Cambridge University Press.Google Scholar
Jergensen, B.B. & Fenchel, T., 1974. The sulfur cycle of a marine sediment model system. Marine Biology, 24, 189–201.CrossRefGoogle Scholar
Manning, R.B., 1975. Two methods for collecting decapods in shallow water. Crustaceana, 29, 317–319.CrossRefGoogle Scholar
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, 739–748.CrossRefGoogle Scholar
National Research Council, 1979. Hydrogen sulfide. Baltimore, USA: University Park Press.Google Scholar
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, 383–387.Google Scholar
Nicholls, P., 1975. The effect of sulphide on cytochrome aa3. Isosteric and allosteric shifts on reduced alpha-peak. Biochimica et Biophysica Acta, 396, 24–35.CrossRefGoogle ScholarPubMed
Nickell, L.A., 1992. Deep bioturbation in organically enriched sediments. PhD thesis, University of London.Google Scholar
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, 181–197.Google Scholar
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, 133–148.CrossRefGoogle ScholarPubMed
Oeschger, R. & Vetter, R.D., 1992. Sulphide detoxification and tolerance in Halicryptus spinulosus (Priapulida): a multiple strategy. Marine Ecology Progress Series, 86, 167–179.CrossRefGoogle Scholar
Oeschger, R. & Vismann, B., 1994. Sulphide tolerance in Heteromastus filiformis (Polychaeta): mitochondrial adaptations. Ophelia, 40, 147–158.Google Scholar
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, 261–279.Google Scholar
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, 39–52.Google Scholar
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, 313–329.CrossRefGoogle Scholar
Powell, M.A. & Somero, G.N., 1986. Hydrogen sulfide oxidation is coupled to oxidative phosphorylation in mitochondria of Solemya reidi. Science, New York, 233, 563–566.CrossRefGoogle ScholarPubMed
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, 755–759.CrossRefGoogle Scholar
Steffensen, J.F., 1989. Some errors in respirometry of aquatic breathers: how to avoid and correct for them. Fish Physiology and Biochemistry, 6, 49–59.CrossRefGoogle Scholar
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, 591–614.Google Scholar
Southward, E.C., 1994. Hot vents, deep seeps and black mud: symbiosis in sulphur and methane based ecosystems, pp. 1–36. Isle of man: Port Erin Laboratory Centenary Publication.Google Scholar
Spurr, A.R., 1969. A low viscosity epoxy embedding resin for electron microscopy. journal of Ultrastructural Research, 26, 31–43.Google Scholar
Suchanek, T.H., 1983. Control of seagrass communities and sediment distribution by Callianassa (Crustacea, Thalassinidea) bioturbation. Journal of Marine Research, 41, 281–298.Google Scholar
Theede, H., 1973. Comparative studies on the influence of oxygen deficiency and hydrogen sulphide on marine bottom invertebrates. Netherlands Journal of Sea Research, 7, 244–252.CrossRefGoogle Scholar
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, 325–337.CrossRefGoogle Scholar
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, 87–104.CrossRefGoogle Scholar
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, 274–287.CrossRefGoogle Scholar
Tunnicliffe, V., 1991. The biology of the hydrothermal vents: ecology and evolution. Oceanography and Marine Biology. Annual Review. London, 29, 319–107.Google Scholar
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.Google Scholar
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.]Google Scholar
Vetter, R.D., Powell, M.A. & Somero, G.N., 1991. Metazoan adaptations to hydrogen sulphide. In Metazoan life without oxygen (ed. C., Bryant), pp. 109–128. London: Chapman & Hall.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. Physiological Zoology, 60, 121–137.CrossRefGoogle Scholar
Vismann, B., 1991a. Sulfide tolerance: physiological mechanisms and ecological implications. Ophelia, 34, 1–27.CrossRefGoogle Scholar
Vismann, B., 1991b. Physiology of sulfide in the isopod Saduria (Mesidotea) entomon. Marine Ecology Progress Series, 76, 283–293.Google Scholar
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, 469–477.Google Scholar
Völkel, S. & Grieshaber, M.K., 1994. Oxygen dependent sulfide detoxification in the lugworm Arenicola marina. Marine Biology, 118, 137–147.Google Scholar
Völkel, S. & Grieshaber, M.K., 1995. Sulfide tolerance in marine invertebrates. Advances in Comparative and Environmental Physiology, 22, 233–257.CrossRefGoogle Scholar
Völkel, S. & Grieshaber, M.K., 1996. Mitochondrial sulphide oxidation in Arenicola marina. Evidence for alternative electron pathways. European Journal of Biochemistry, 235, 231–237.CrossRefGoogle ScholarPubMed
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, 205–215.CrossRefGoogle Scholar
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, 219–225.CrossRefGoogle Scholar