Heat flux, oxygen flux, and mitochondrial redox state as a function of oxygen availability and ciliary activity in excised gills of Mytilus edulis.

Abstract

The ciliated gill of bivalve molluscs is situated at an interface between animal and environment. Cilia propel water past the gills to deliver oxygen and nutrition to the animal. Ciliary activity is driven by dynein ATPases and requires a continual supply of ATP at a rate sufficient to match the rate of ATP hydrolysis. Control of the balance between ATP supply and demand in the ciliated gill, and how this balance may be altered by environmental stresses, is unknown. In this pilot study, metabolic flux of excised gills from the marine mussel Mytilus edulis was examined in response to oxygen availability and to serotonin-stimulated ciliary activity. Heat flux and oxygen flux were measured simultaneously with calorespirometry. In parallel experiments, the redox state of mitochondrial cytochromes was determined with in vivo spectrophotometry. Above 4 kPa pO2, heat flux was supported by aerobic metabolism. Anoxic heat flux was less than 5% of aerobic heat flux. Heat and oxygen fluxes nearly doubled in gills in the presence of 10 microM serotonin; however, half-maximal pO2 for heat and oxygen fluxes and for reduction of mitochondrial cytochromes remained unchanged from control levels. In gills having inactive cilia in half-strength seawater, half-maximal pO2 for heat and oxygen fluxes and for cytochrome reduction nearly doubled compared with valves in full-strength seawater. These data indicate that limitation to oxygen delivery imposed by boundary layers may be reduced when ciliary beat frequency is elevated, leading to enhanced oxygen flux to intracellular mitochondrial which matches the increased energy demand by the cilia.