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COMPARATIVE AND EVOLUTIONARY PHYSIOLOGY

Hydrogen sulfide as an oxygen sensor in trout gill chemoreceptors

¹Indiana University School of Medicine South Bend, South Bend, Indiana; ²Department of Biology, University of Ottawa, Ottawa, Ontario; and ³Department of Biology, Lakehead University, Ontario, Canada

Submitted 5 November 2007 ; accepted in final form 17 June 2008

O₂ chemoreceptors elicit cardiorespiratory reflexes in all vertebrates, but consensus on O₂-sensing signal transduction mechanism(s) is lacking. We recently proposed that hydrogen sulfide (H₂S) metabolism is involved in O₂ sensing in vascular smooth muscle. Here, we examined the possibility that H₂S is an O₂ sensor in trout chemoreceptors where the first pair of gills is a primary site of aquatic O₂ sensing and the homolog of the mammalian carotid body. Intrabuccal injection of H₂S in unanesthetized trout produced a dose-dependent bradycardia and increased ventilatory frequency and amplitude similar to the hypoxic response. Removal of the first, but not second, pair of gills significantly inhibited H₂S-mediated bradycardia, consistent with the loss of aquatic chemoreceptors. mRNA for H₂S-synthesizing enzymes, cystathionine β-synthase and cystathionine -lyase, was present in branchial tissue. Homogenized gills produced H₂S enzymatically, and H₂S production was inhibited by O₂, whereas mitochondrial H₂S consumption was O₂ dependent. Ambient hypoxia did not affect plasma H₂S in unanesthetized trout, but produced a PO₂-dependent increase in a sulfide moiety suggestive of increased H₂S production. In isolated zebrafish neuroepithelial cells, the putative chemoreceptive cells of fish, both hypoxia and H₂S, produced a similar 10-mV depolarization. These studies are consistent with H₂S involvement in O₂ sensing/signal transduction pathway(s) in chemoreceptive cells, as previously demonstrated in vascular smooth muscle. This novel mechanism, whereby H₂S concentration ([H₂S]) is governed by the balance between constitutive production and oxidation, tightly couples tissue [H₂S] to PO₂ and may provide an exquisitely sensitive, yet simple, O₂ sensor in a variety of tissues.

hydrogen sulfide concentration

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