Inefficient lactate dehydrogenases of deep-sea fishes

Abstract

The respiratory rates of deep-sea animals are extremely low. Deep-sea fishes may consume oxygen at rates only 5–10% those characteristic of shallow-water species1–4. These low metabolic rates are probably an adaptation to the presumed scarcity of food in deeper water4. The biochemical basis of this metabolic adaptation is a low level of enzyme activity in the skeletal muscle (but not the heart or brain), mainly because of the low enzyme concentrations in that tissue5. We report here, however, that a second source of reduced enzyme activity contributes to the low metabolic rate. For muscle-type (M4) lactate dehydrogenases (LDH, EC 1.1.1.27, NAD+ :lactate oxidoreductase), the enzymes of deep-sea fishes have significantly higher activation free energy (ΔG*) and enthalpy (ΔH*) characteristics than the homologous enzymes of cold-adapted, shallow-water fishes. Because of these higher energy barriers to catalysis, pyruvate is reduced to lactate at approximately 60% of the rate observed with LDHs of shallow-water fishes. Thus, in terms of rate of function per enzyme molecule, deep-sea fishes would be at a disadvantage in shallow waters because of their relatively poor capacity for muscle glycolysis. Such enzymatic factors may help determine the upper distributions of deep-sea species, much as the relatively large pressure insensltivities of LDHs of these deep-sea fishes6,7 may enable them to tolerate high and variable pressures. We suggest that the low catalytic efficiencies of high-pressure-adapted LDHs are concomitant with their low sensitivities to pressure.