DOELLER, Jeannette E.*; KRAUS, David W.: Mussel Gill Mitochondria Oxidize Sulfide in the Absence of Oxygen

Geukensia demissa, the ribbed mussel, inhabits marine sulfidic sediments. Ciliated gills form the interface between animal and environment, encountering millimolar concentrations of sulfide along with low oxygen. Gill energy metabolism has been described as chemolithoheterotrophic, indicating that energy but not reduced carbon (animals live amidst decaying organic matter) is produced via the oxidation of inorganic substrate. In this case, sulfide is oxidized and resulting electrons are fed into the mitochondrial electron transport chain perhaps at cytochrome c for the production of ATP, with ATP/oxygen and oxygen/sulfide ratios of one. This process may be influenced by several factors. Products of sulfide oxidation, for example, a major one being thiosulfate, may serve to feedback-inhibit carbon substrate oxidation in intact cells. Another factor may be oxygen. Oxygen consumption in intact gills is sensitive to oxygen, with conformity beginning about 19 torr pO2. Gill sulfide oxidation, measured directly with a polarographic sulfide sensor, also shows conformity to pO2. However, in the absence of oxygen, sulfide oxidation in isolated gill mitochondria continues for a brief time, showing saturation kinetics. This pattern can be simulated in mitochondria exposed to cyanide to inhibit cytochrome c oxidase and SHAM to inhibit a putative alternative oxidase. We propose that electrons from gill sulfide oxidation travel ultimately to cytochrome c oxidase under normoxic conditions, to alternative oxidase under conditions that inhibit cytochrome c oxidase, and to an unknown electron acceptor under conditions that inhibit both terminal oxiases. This unknown electron acceptor may serve to store electrons for delivery under more conducive conditions to supply the animal with energy.