Skip to main content
Log in

Hydrogen Sulfide in the Physiological Processes of Jawless Cyclostomes and Jawed Fishes

  • ORIGINAL PAPERS
  • Published:
Russian Journal of Marine Biology Aims and scope Submit manuscript

Abstract

This review summarizes data on the involvement of hydrogen sulfide as an active signal molecule in the physiological processes of jawless cyclostomes and jawed fishes, which are the most ancient members of vertebrates, and its interaction with the hypoxia factor in an aquatic habitat. The characteristics of the adaptation of jawed fishes to an increased level of hydrogen sulfide are discussed.

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

REFERENCES

  1. Abe, K. and Kimura, H., The possible role of hydrogen sulfide as an endogenous neuromodulator, J. Neurosci., 1996, vol. 16, pp. 1066–1071.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  2. Affonso, E.G., Polez, V.L.P., Correa, C.F., et al., Metabolic and blood responses of Hoplosternum littorale (Siluriformes, Callichthyidae) exposed to acute hydrogen sulfide, in Proc. International Congress on the Biology of Fish “Fish Response to Toxic Environments”, Baltimore, Md.: Towson Univ., 1998, pp. 153–167.

  3. Affonso, E.G., Polez, V.L.P., Correa, C.F., et al., Blood parameters and metabolites in the teleost fish Colossoma macropomum exposed to sulfide or hypoxia, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol., 2002, vol. 133, pp. 375–382.

    CAS  Google Scholar 

  4. Affonso, E.G. and Rantin, F.T., Respiratory responses of the air-breathing fish Hoplosternum littorale to hypoxia and hydrogen sulfide, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol., 2005, vol. 141, pp. 275–280.

    CAS  Google Scholar 

  5. Bagarinao, T., Sulfide as an environmental factor and toxicant: tolerance and adaptations in aquatic organisms, Aquat. Toxicol., 1992, vol. 24, pp. 21–62.

    Article  CAS  Google Scholar 

  6. Bagarinao, T. and Vetter, R.D., Sulfide tolerance and detoxification in shallow-water marine fishes, Mar. Biol., 1989, vol. 103, pp. 291–302.

    Article  CAS  Google Scholar 

  7. Bagarinao, T. and Vetter, R.D., Oxidative detoxification of sulfide by mitochondria of the California killifish Fundulus parvipinnis and the speckled sanddab Citharichthys stigmaeus, J. Comp. Physiol., B, 1990, vol. 160, pp. 519–527.

    Article  CAS  Google Scholar 

  8. Bagarinao, T. and Vetter, R.D., Sulfide-hemoglobin interactions in the sulfide-tolerant salt marsh resident, the California killifish Fundulus parvipinnis, J. Comp. Physiol., B, 1992, vol. 162, pp. 614–624.

    Article  CAS  Google Scholar 

  9. Bagarinao, T. and Vetter, R.D., Sulphide tolerance and adaptation in the California killifish, Fundulus parvipinnis, a salt marsh resident, J. Fish Biol., 1993, vol. 42, pp. 729–748.

    Article  CAS  Google Scholar 

  10. Brauner, C.J., Ballantyne, C.L., Randall, D.J., and Val, A.L., Air breathing in the armoured catfish (Hoplosternum littorale) as an adaptation to hypoxic, acidic, and hydrogen sulphide rich waters, Can. J. Zool., 1995, vol. 73, pp. 739–744.

    Article  Google Scholar 

  11. Buckler, K.J., Effects of exogenous hydrogen sulphide on calcium signalling, background (TASK) K channel activity and mitochondrial function in chemoreceptor cells, Pflügers Arch., 2012, vol. 463, pp. 743–754.

  12. Buckler, K.J. and Vaughan-Jones, R.D., Effects of mitochondrial uncouplers on intracellular calcium, pH and membrane potential in rat carotid body type I cells, J. Physiol., 1998, vol. 513, pp. 819–833.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Chen, K. and Morris, J., Kinetics of oxidation of aqueous sulfide by O2, Environ. Sci. Technol., 1972, vol. 6, pp. 529–537.

    Article  CAS  Google Scholar 

  14. Cooper, C.E. and Brown, G.C., The inhibition of mitochondrial cytochrome oxidase by the gases carbon monoxide, nitric oxide, hydrogen cyanide and hydrogen sulfide: chemical mechanism and physiological significance, J. Bioenerg. Biomembr., 2008, vol. 40, pp. 533–539.

    Article  CAS  PubMed  Google Scholar 

  15. Dombkowski, R.A., Russell, M.J., and Olson, K.R., Hydrogen sulfide as an endogenous regulator of vascular smooth muscle tone in trout, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2004, vol. 286, pp. R678–R685.

    CAS  Google Scholar 

  16. Dombkowski, R.A., Russell, M.J., Schulman, A.A., et al., Vertebrate phylogeny of hydrogen sulfide vasoactivity, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2005, vol. 288, pp. R243–R252.

    Article  CAS  Google Scholar 

  17. Dorman, D.C., Moulin, F.J.M., McManus, B.E., et al., Cytochrome oxidase inhibition induced by acute hydrogen sulfide inhalation: correlation with tissue sulfide concentrations in the rat brain, liver, lung, and nasal epithelium, Toxicol. Sci., 2002, vol. 65, pp. 18–25.

    Article  CAS  PubMed  Google Scholar 

  18. Forgan, L.G. and Forster, M.E., Oxygen consumption, ventilation frequency and cytochrome c oxidase activity in blue cod (Parapercis colias) exposed to hydrogen sulphide or isoeugenol, Comp. Biochem. Physiol., Part C: Toxicol. Pharmacol., 2010, vol. 151, no. 1, pp. 57–65.

    Google Scholar 

  19. Gilmour, K.M. and Perry, S.F., Branchial chemoreceptor regulation of cardiorespiratory function, Fish Physiol., 2007, vol. 25, pp. 97–151.

    Article  Google Scholar 

  20. Grieshaber, M.K. and Völkel, S., Animal adaptations for tolerance and exploitation of poisonous sulfide, Annu. Rev. Physiol., 1998, vol. 60, pp. 33–53.

    Article  CAS  PubMed  Google Scholar 

  21. Guidotti, T.L., Hydrogen sulphide, Occup. Med., 1996, vol. 46, pp. 367–371.

    Article  CAS  Google Scholar 

  22. Hildebrandt, T.M. and Grieshaber, M.K., Three enzymatic activities catalyze the oxidation of sulfide to thiosulfate in mammalian and invertebrate mitochondria, FEBS J., 2008, vol. 275, pp. 3352–3361.

    Article  CAS  PubMed  Google Scholar 

  23. Hosoki, R., Matsuki, N., and Kimura, H., The possible role of hydrogen sulfide as an endogenous smooth muscle relaxant in synergy with nitric oxide, Biochem. Biophys. Res. Commun., 1997, vol. 237, no. 3, pp. 527–531.

    Article  CAS  PubMed  Google Scholar 

  24. Jonz, M.G., Oxygen sensing, in The Physiology of Fishes, Boca Raton, Fla.: CRC Press, 2013, pp. 149–174.

    Google Scholar 

  25. Jonz, M.G., Buck, L.T., Perry, S.F., et al., Sensing and surviving hypoxia in vertebrates, Ann. N. Y. Acad. Sci., 2016, vol. 1365, pp. 43–58.

    Article  CAS  PubMed  Google Scholar 

  26. Jonz, M.G., Fearon, I.M., and Nurse, C.A., Neuroepithelial oxygen chemoreceptors of the zebrafish gill, J. Physiol., 2004, vol. 560, pp. 737–752.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Kamoun, P., Endogenous production of hydrogen sulfide in mammals, Amino Acids, 2004, vol. 26, pp. 243–254.

    Article  CAS  PubMed  Google Scholar 

  28. Kimura, H., Metabolic turnover of hydrogen sulfide, Front. Physiol., 2012, vol. 3, pp. 1–3.

    Article  CAS  Google Scholar 

  29. Kimura, H., Hydrogen sulfide and polysulfides as signaling molecules, Proc. Jpn. Acad., Ser. B, 2015, vol. 91, no. 4, pp. 131–159.

    CAS  Google Scholar 

  30. Marino, M.T., Urquhart, M.R., Sperry, M.L., et al., Pharmacokinetics and kinetic-dynamic modelling of aminophenones as methaemoglobin formers, J. Pharm. Pharmacol., 1997, vol. 49, pp. 282–287.

    Article  CAS  PubMed  Google Scholar 

  31. Milsom, W.K. and Burleson, M.L., Peripheral arterial chemoreceptors and the evolution of the carotid body, Respir. Physiol. Neurobiol., 2007, vol. 157, pp. 4–11.

    Article  CAS  PubMed  Google Scholar 

  32. Olson, K.R., Vascular actions of hydrogen sulfide in nonmammalian vertebrates, Antioxid. Redox Signaling, 2005, vol. 7, nos. 5–6, pp. 804–812.

    Article  CAS  Google Scholar 

  33. Olson, K.R., Hydrogen sulfide and oxygen sensing: Implications in cardiorespiratory control, J. Exp. Biol., 2008, vol. 211, pp. 2727–2734.

    Article  CAS  PubMed  Google Scholar 

  34. Olson, K.R., Is hydrogen sulfide a circulating “gasotransmitter” in vertebrate blood?, Biochim. Biophys. Acta, 2009, vol. 1787, pp. 856–863.

    Article  CAS  PubMed  Google Scholar 

  35. Olson, K.R., Mitochondrial adaptations to utilize hydrogen sulfide for energy and signaling, J. Comp. Physiol., B, 2012, vol. 182, pp. 881–897.

    Article  CAS  Google Scholar 

  36. Olson, K.R., Hydrogen sulfide as an oxygen sensor, Clin. Chem. Lab. Med., 2013, vol. 51, no. 3, pp. 623–632.

    Article  CAS  PubMed  Google Scholar 

  37. Olson, K.R., Russell, M.J., and Forster, M.E., Hypoxic vasoconstriction of cyclostome systemic vessels: the antecedent of hypoxic pulmonary vasoconstriction?, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2001, vol. 280, pp. R198–R206.

    CAS  Google Scholar 

  38. Olson, K.R., Dombkowski, R.A., Russell, M.J., et al., Hydrogen sulfide as an oxygen sensor/transducer in vertebrate hypoxic vasoconstriction and hypoxic vasodilation, J. Exp. Biol., 2006, vol. 209, pp. 4011–4023.

    Article  CAS  PubMed  Google Scholar 

  39. Olson, K.R., Forgan, L.G., Dombkowski, R.A., et al., Oxygen dependency of hydrogen sulfide-mediated vasoconstriction in cyclostome aortas, J. Exp. Biol., 2008, vol. 211, pp. 2205–2213.

    Article  CAS  PubMed  Google Scholar 

  40. Olson, K.R., Healy, M.J., Qin, Z., et al., Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2008, vol. 295, no. 2, pp. R669–R680.

    CAS  Google Scholar 

  41. Olson, K.R., Donald, J.A., Dombkowski, R.A., and Perry, S.F., Evolutionary and comparative aspects of nitric oxide, carbon monoxide and hydrogen sulfide, Respir. Physiol. Neurobiol., 2012, vol. 184, pp. 117–129.

    Article  CAS  PubMed  Google Scholar 

  42. Olson, K.R., Gao, Y., Arif, F., et al., Metabolism of hydrogen sulfide (H2S) and production of reactive sulfur species (RSS) by superoxide dismutase, Redox Biol., 2018, vol. 15, pp. 74–85.

    Article  CAS  PubMed  Google Scholar 

  43. Perry, S.F., Kumai, Y., Porteus, C.S., et al., An emerging role for gasotransmitters in the control of breathing and ionic regulation in fish, J. Comp. Physiol., B, 2016, vol. 186, no. 2, pp. 145–159.

    Article  CAS  Google Scholar 

  44. Perry, S.F., McNeill, B., Elia, E., et al., Hydrogen sulfide stimulates catecholamine secretion in rainbow trout (Oncorhynchus mykiss), Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2009, vol. 296, pp. R133–R140.

    CAS  Google Scholar 

  45. Perry, S.F. and Tzaneva, V., The sensing of respiratory gases in fish: Mechanisms and signalling pathways, Respir. Physiol. Neurobiol., 2016, vol. 224, pp. 71–79.

    Article  CAS  PubMed  Google Scholar 

  46. Porteus, C.S., Abdallah, S.J., Pollack, J., et al., The role of hydrogen sulphide in the control of breathing in hypoxic zebrafish (Danio rerio), J. Physiol., 2014, vol. 592, pp. 3075–3088.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Prabhakar, N.R., Sensing hypoxia: physiology, genetics and epigenetics, J. Physiol., 2013, vol. 591, pp. 2245–2257.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  48. Reid, S.G. and Perry, S.F., Peripheral O2 chemoreceptors mediate humoral catecholamine secretion from fish chromaffin cells, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2003, vol. 284, pp. R990–R999.

    CAS  Google Scholar 

  49. Riesch, R., Plath, M., and Schlupp, I., Toxic hydrogen sulfide and dark caves: life-history adaptations in a livebearing fish (Poecilia mexicana, Poeciliidae), Ecology, 2010, vol. 91, no. 5, pp. 1494–1505.

    Article  PubMed  Google Scholar 

  50. Skovgaard, N. and Olson, K.R., Hydrogen sulfide mediates vasoconstriction through a production of mitochondrial ROS in trout gill, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 2012, vol. 303, pp. R487–R494.

    CAS  Google Scholar 

  51. Smith, L., Kruszyna, H., and Smith, R.P., The effect of methemoglobin on the inhibition of cytochrome c oxidase by cyanide, sulphide or azide, Biochem. Pharmacol., 1977, vol. 26, pp. 2247–2250.

    Article  CAS  PubMed  Google Scholar 

  52. Smith, M.P., Russell, M.J., Wincko, J.T., et al., Effects of hypoxia on isolated vessels and perfused gills of rainbow trout, Comp. Biochem. Physiol., Part A: Mol. Integr. Physiol., 2001, vol. 130, no. 1, pp. 171–181.

    Article  CAS  Google Scholar 

  53. Sundin, L., Responses of the branchial circulation to hypoxia in the Atlantic cod, Gadus morhua, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 1995, vol. 268, pp. R771–R778.

    Article  CAS  Google Scholar 

  54. Sundin, L. and Nilsson, G.E., Neurochemical mechanisms behind gill microcirculatory responses to hypoxia in trout: in vivo microscopy study, Am. J. Physiol.: Regul., Integr. Comp. Physiol., 1997, vol. 272, pp. R576–R585.

    Article  CAS  Google Scholar 

  55. Telezhkin, V., Brazier, S.P., Cayzac, S.H., et al., Mechanism of inhibition by hydrogen sulfide of native and recombinant BKCa channels, Respir. Physiol. Neurobiol., 2010, vol. 172, no. 3, pp. 169–178.

    Article  CAS  PubMed  Google Scholar 

  56. Tobler, M., DeWitt, T.J., Schlupp, I., et al., Toxic hydrogen sulfide and dark caves: phenotypic and genetic divergence across two abiotic environmental gradients in Poecelia mexicana, Evolution, 2008, vol. 62, pp. 2643–2649.

    Article  PubMed  Google Scholar 

  57. Tobler, M., Palacios, M., Chapman, L.J., et al., Evolution in extreme environments: replicated phenotypic differentiation in livebearing fish inhabiting sulfidic springs, Evolution, 2011, vol. 65, no. 8, pp. 2213–2228.

    Article  PubMed  Google Scholar 

  58. Torrans, E.L. and Clemens, H.P., Physiological and biochemical effects of acute exposure of fish to hydrogen sulfide, Comp. Biochem. Physiol., C: Comp. Pharmacol., 1982, vol. 71, no. 2, pp. 183–190.

    Article  CAS  Google Scholar 

  59. Völkel, S. and Berenbrink, M., Sulphaemoglobin formation in fish: a comparison between the haemoglobin of sulphide-sensitive rainbow trout (Oncorhynchus mykiss) and of the sulphide-tolerant common carp (Cyprinus carpio), J. Exp. Biol., 2000, vol. 203, pp. 1047–1058.

  60. Völkel, S., Berenbrink, M., Heisler, N., et al., Effects of sulfide on K+ flux pathways in red blood cells of crucian carp and rainbow trout, Fish Physiol. Biochem., 2001, vol. 24, pp. 213–233.

  61. Wang, R., Two’s company, three’s crowd: can H2S be the third endogenous gaseous transmitter?, FASEB J., 2002, vol. 16, pp. 1792–1798.

    Article  CAS  PubMed  Google Scholar 

  62. Wang, R., Physiological implications of hydrogen sulfide: a whiff exploration that blossomed, Physiol. Rev., 2012, vol. 92, pp. 791–896.

    Article  CAS  PubMed  Google Scholar 

  63. Wu, B., Teng, H., Yang, G., et al., Hydrogen sulfide inhibits the translational expression of hypoxia-inducible factor-1α, Br. J. Pharmacol., 2012, vol. 167, pp. 1492–1505.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Zhao, W., Ndisang, J.F., and Wang, R., Modulation of endogenous production of H2S in rat tissues, Can. J. Physiol. Pharmacol., 2003, vol. 81, no. 9, pp. 848–853.

    Article  CAS  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to E. E. Kolesnikova.

Additional information

Translated by E. Shvetsov

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Kolesnikova, E.E. Hydrogen Sulfide in the Physiological Processes of Jawless Cyclostomes and Jawed Fishes. Russ J Mar Biol 45, 163–173 (2019). https://doi.org/10.1134/S1063074019030076

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1134/S1063074019030076

Keywords:

Navigation