Interactive effects of pH and metals on mitochondrial functions of intertidal bivalves Crassostrea virginica and Mercenaria mercenaria

• Interactive effects of trace metals Cd and Cu and pH were studied in mitochondria of clams and oysters.
• Mitochondrial respiration and membrane potential of bivalves were robust to pH variation (6.6–7.8).
• Elevated levels of Cd and Cu inhibited mitochondrial respiration in the pH-dependent manner but did not affect the membrane potential.
• Negative effects of Cd and Cd on mitochondrial respiration were alleviated at low pH (7.0 and below).
• Moderate acidosis may protect molluscan mitochondria from metal toxicity.

Intertidal bivalves experience broad fluctuations of environmental temperature, pH and oxygen content which could change their intracellular pH. They are also exposed to trace metals such as cadmium (Cd) and copper (Cu) that accumulate in their tissues and may negatively affect mitochondrial functions and bioenergetics. We determined the interactive effects of pH and trace metals (25 μM Cd or Cu) on mitochondrial functions (including respiration and membrane potentials in both ADP-stimulated (state 3) and resting (state 4) states) of two common marine bivalves, the hard clams (Mercenaria mercenaria) and eastern oysters (Crassostrea virginica). In the absence of the trace metals, mitochondrial functions of C. virginica and M. mercenaria were insensitive to pH in a broad physiologically relevant range (6.6–7.8). Mitochondrial respiration was generally suppressed by 25 μM Cd or Cu (with the stronger effects observed for ADP-stimulated compared to the resting respiration) while the mitochondrial membrane potential was unaffected. pH modulated the effects of Cu and Cd on mitochondrial respiration of the bivalves. In oysters, Cu suppressed ADP-stimulated mitochondrial respiration at high and low pH values (6.6 and 7.8, respectively), but had no effect in the intermediate pH range (7.0–7.4). In clams, the negative effect of Cu on ADP-stimulated respiration was only observed at extremely high pH (7.8). A decrease in pH was also protective against Cd in mitochondria of clams and oysters. In clams, 25 μM Cd suppressed ADP-stimulated respiration at all pH; however, at low pH (6.6–7.0) this suppression was paralleled by a decrease in the rates of proton leak thereby effectively restoring mitochondrial coupling. In oysters, the inhibitory effects of Cd on ADP-stimulated respiration were fully abolished at low pH (6.6–7.0). This indicates that moderate acidosis (such as occurs during exposure to air, extreme salinities or elevated CO2 levels in the intertidal zone) may have a beneficial side-effect of protecting mitochondria of clams and oysters against the toxic effects of trace metals in polluted estuaries.