Chemolithoheterotrophy in a metazoan tissue: sulfide supports cellular work in ciliated mussel gills

Hydrogen sulfide, a common constituent of marine intertidal sediments, is both a potent toxin of aerobic cellular respiration and an electron-rich molecule used by some prokaryotic organisms as a source of energy. In ciliated gills from Geukensia demissa, a marine mussel from sulfide-rich sediments, sulfide oxidation supports cellular work. Evidence for this comes from measurements of ciliary beat frequency (fCB) as a measure of ATP turnover rate, the rate of gill oxygen consumption ( m_dot O2) as a measure of ATP production rate, and mitochondrial cytochrome redox state as an indicator of the path of electron flow. Results from experiments performed in the presence and absence of the mitochondrial complex III inhibitor antimycin A to limit endogenous carbon substrate oxidation showed that exposure to sulfide stimulated oxygen consumption and ciliary beating, with cytochrome c being the dominant reduced species. These results, along with the resultant fCB/ m_dot O2 ratio, are qualitatively and quantitatively consistent with the hypothesis that electrons from sulfide oxidation support mitochondrial ATP production. We propose that Geukensia demissa gills use sulfide as a respiratory substrate when given the choice and thus function metabolically as facultative chemolithoheterotrophs. Similar conclusions could not be drawn for the ciliated gills from Mytilus edulis, a marine mussel from aerated habitats, or for the ciliated lungs from the phylogenetically distinct leopard frog Rana pipiens.