Osmotolerance reflected in mitochondrial respiration of Mytilus populations from three different habitat salinities

Mussels from the Mytilus edulis species complex experience a salinity gradient from the North Sea into the Baltic Proper ranging from 32 to 5. As osmoconformers, they adjust their internal osmolarity to match that of their surroundings, which presents a significant challenge to the metabolic machinery, including their mitochondria. We hypothesized that the osmotic optima for the mitochondrial function of mussels matches the prevailing habitat salinity and is accompanied by a population specific metabolite profile. To test this hypothesis, mussels from three populations along the salinity gradient were assessed. We found a population specific shift in the optimal osmolarities for maximal mitochondrial respiration capacity that mirrored the populations' habitat salinity. So, mitochondria from North Sea mussels reached their highest capacity at higher osmotic concentrations than their Baltic Sea congeners. Additionally, Baltic Sea populations appear to have traded off an adaptation to low salinities for a narrower mitochondrial tolerance range resulting in a more specialized mitochondrial phenotype, while North Sea populations have mitochondria with a more general functioning phenotype. The local adaptation to a low salinity habitat was supported by the analysis of gill tissue metabolites via LC-MS/MS. Abundances of metabolites involved in energy generation, osmotic homeostasis or the urea cycle were similar between North Sea and southern Baltic Sea mussels, while northern Baltic Sea mussels seem to follow a different metabolic strategy, which may allow them to inhabit very low salinities. Thus, northern Baltic Sea mussels have adapted to low salinities on a mitochondrial and metabolic level.