Hydrogen Sulfide as an Oxygen Sensor in Trout Chemoreceptors

Abstract

Oxygen (O2) sensing chemoreceptors elicit cardiorespiratory reflexes in all vertebrates but the oxygen sensing‐signal transduction mechanism(s) is unknown. Here we examined the possibility that H2S is an O2 sensor in rainbow trout where the first pair of gill arches is a primary site of chemoreception and the homolog of the mammalian carotid body. In unanesthetized trout, ambient hypoxia produced a PO2‐dependent increase in plasma [H2S] indicative of inverse coupling of PO2 and H2S. mRNA for the H2S synthesizing enzymes CBS and CSE was present in gill tissue and gills produced H2S enzymatically. Intrabuccal injection of H2S in unanesthetized trout produced a dose‐dependent bradycardia and increased ventilatory frequency and amplitude similar to hypoxia. Removal of the first but not second gill arches inhibited H2S‐mediated bradycardia, consistent with the hypothesized loss of aquatic chemoreceptor function. In isolated zebrafish neuroepithelial cells, the putative chemoreceptive cells of fish, hypoxia and H2S produced a similar ~10 mV depolarization. This suggests that H2S is involved in the O2 sensing/signal transduction pathway in chemoreceptive cells as it is in vascular smooth muscle. This mechanism, whereby [H2S] is governed by the balance between constitutive production and oxidation, tightly couples tissue [H2S] to PO2 and may provide an exquisitely sensitive O2 sensor in a variety of tissues. Support: NSF IOS 0641436 & NSERC