Metabolic cold adaptation in the lugworm Arenicola marina: comparison of a North Sea and a White Sea population

Mitochondrial mechanisms, which may define and adjust an organism’s thermal tolerance window to the environmental temperature regime, were studied in 2 intertidal populations of the polychaete worm Arenicola marina (L.) from the North Sea (boreal) and the White Sea (subpolar). Adaptation to lower mean annual temperatures in the subpolar White Sea population (4 vs 10°C in the North Sea) was reflected in a 2.4 times higher mitochondrial volume density in their muscle tissue. In White Sea worms acclimated to 6°C, a 10 times higher cytochrome c-oxidase (CytOx) activity was seen and the activation energy (Ea) for the oxidation of cytochrome c was reduced compared to boreal specimens acclimated to 11°C. Moreover, mitochondria from White Sea lugworms were characterised by a 2.7 times higher succinate oxidation rate and reduced Ea under mitochondrial State 3 (phosphorylating) respiration at low temperatures, as well as a higher activity of NADP-dependent isocitrate dehydrogenase (IDH) compared to North Sea worms, even when acclimated to the same temperature of 11°C. All these patterns reflect an overall rise in the capacity of aerobic energy production with cold adaptation. This explains the downward shift in the low critical temperature (Tc), beyond which anaerobic metabolism set in. However, the higher mitochondrial density is likely to have induced the rise in standard metabolic rate seen in the White Sea lugworms, causing a concomitant shift in the high Tc to a lower value. An increase in the Ea for the decarboxylation of isocitrate in White Sea specimens may help to minimise the increase in the standard metabolic rate induced by their higher mitochondrial density and capacity, at the expense of a higher thermal sensitivity of metabolism at higher temperatures.