Chemolithoheterotrophy in a metazoan tissue: thiosulfate production matches ATP demand in ciliated mussel gills

The ribbed mussel Geukensia demissa inhabits sulfide-rich coastal sediments with a distribution that suggests a preference for exposure to sulfide. Although sulfide is a respiratory poison, it is also a potent reductant. Geukensia demissa gill mitochondria can use sulfide as a respiratory substrate for ATP production, and the gills of this species exhibit sulfide-supported oxygen consumption that matches the energy demand of ciliary beating. Here, we demonstrate (i) that the major product of G. demissa gill sulfide oxidation is thiosulfate and (ii) that the rate of sulfide oxidation also matches the cellular energy demand, resulting in a ratio near unity of oxygen consumed to sulfide oxidized at both low and high ciliary beat frequencies. A value for this ratio of unity is consistent with electrons from sulfide oxidation entering the mitochondrial electron transport chain. In the gills of the blue mussel Mytilus edulis from sulfide-free conditions, this ratio is 3-5 times higher, indicating an uncoupling of oxygen consumption from sulfide oxidation. Whereas M. edulis gills exhibit anaerobic metabolism during sulfide exposure, G. demissa gills do not, indicating a difference in sulfide tolerance between the two mussel species.