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. Al though sulfide is a respiratory poison, it is also a potent reductant. Geuk ensia 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 gin sulfide oxida tion is thiosulfate and (ii) that the rate of sulfide oxidation also matche s the cellular energy demand, resulting in a ratio near unity of oxygen con sumed to sulfide oxidized at both low and high ciliary beat frequencies. A value for this ratio of unity is consistent with electrons from sulfide oxi dation 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 sulf ide oxidation. Whereas M. edulis gills exhibit anaerobic metabolism during sulfide exposure, G. demissa gills do not, indicating a difference in sulfi de tolerance between the two mussel species.