Sulfide consumption by mussel gill mitochondria is not strictly tied to oxygen reduction: measurements using a novel polarographic sulfide sensor

Some organisms that survive in environments rich in hydrogen sulfide possess specific metabolic pathways for sulfide oxidation and subsequent use of reducing equivalents in oxidative phosphorylation, a process called chemolithoheterotrophy. This process is dependent on ambient oxygen partial pressure and environmental sulfide exposure. To define accurately the kinetics of sulfide metabolism and its dependence on cellular conditions, we have developed a polarographic sulfide sensor (PSS) to measure sulfide concentrations directly and continuously under physiological conditions. The ribbed mussel Geukensia demissa, an inhabitant of sulfide-rich coastal sediments, consumes sulfide in a chemolithoheterotrophic metabolic strategy. Gill mitochondria use sulfide as respiratory substrate for ATP production, and sulfide consumption is sufficiently rapid and so kinetically complex that only continuous real-time detection captures these events. Under normoxic conditions, oxygen and sulfide consumption are matched. Under hypoxic to anoxic conditions, however, sulfide consumption continues without commensurate oxygen consumption, and these results can be duplicated at higher oxygen conditions by selective blockade of terminal oxidases. These metabolic capabilities depend on prior environmental sulfide exposure, which suggests substantial mitochondrial metabolic plasticity. The recent finding that endogenous sulfide is a critical cell signaling molecule in all organisms suggests that the metabolic pathways that tightly control cellular sulfide levels are widespread. Sensors that accurately report sulfide concentrations under physiologically relevant conditions are valuable tools with which to explore the expanding role of sulfide in biological systems.