Compatible osmolytes modulate mitochondrial function in a marine osmoconformer Crassostrea gigas (Thunberg, 1793)

Abstract

Salinity is an important environmental factor affecting physiology of marine organisms. Osmoconformers such as marine mollusks maintain metabolic function despite changes of the osmolarity and composition of the cytosol during salinity shifts. Currently, metabolic responses to the salinity-induced changes of the intracellular milieu are not well understood. We studied the effects of osmolarity (450 vs. 900 mOsm) and compatible osmolytes (70–590 mM of taurine or betaine) on isolated gill mitochondria of a marine osmoconformer, the Pacific oyster Crassostrea gigas. Physiological concentrations of taurine enhanced mitochondrial ATP synthesis and electron transport system (ETS) capacity, increased mitochondrial coupling and stimulated the forward flux through the Complex I. Notably, the stimulatory effects of taurine were more pronounced at 900 mOsm compared to 450 mOsm. In contrast, betaine proportionally increased the rates of the mitochondrial proton leak, oxidative phosphorylation and ETS flux (with no net effect on the mitochondrial coupling) and suppressed the activity of cytochrome c oxidase in oyster mitochondria. However, the effective concentration of betaine (590 mM) was higher than typically found in bivalves, and thus betaine is not likely to affect oyster mitochondria under the physiological conditions in vivo. Our findings indicate that taurine may support the mitochondrial bioenergetics during hyperosmotic stress in oysters. Compatibility of taurine with the metabolic functions and its beneficial effects on mitochondria may have contributed to its broad distribution as an osmolyte in marine osmoconformers and might explain the earlier reports of the positive effects of taurine supplementation on energy metabolism of other organisms, including mammals.