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

Abstract

Mitochondrial mechanisms, which may define and adjust the thermal tolerance window to the environmental temperature regime, were studied in two intertidal populations of the polychaete worm Arenicola marina from the North Sea (boreal) and the White Sea (subpolar).Adaptation to lower mean annual temperatures in White Sea animals (4 versus 10 °C) is reflected by a 2.4 times higher mitochondrial volume density in the muscle tissue of subpolar animals. In White Sea worms acclimated to 6 °C a 10 times higher cytochrome c-oxidase (CYTOX) activity is seen and the value of activation energy (Ea) for the oxidation of cytochrome c is reduced compared with boreal specimens acclimated to 11 °C. Moreover, mitochondria from White Sea lugworms are characterised by a 2.7 times higher succinate oxidation rate in state 3 respiration, a reduced Ea-value for mitochondrial state 3 respiration at low temperatures, as well as a higher activity of NADP dependent isocitrate dehydrogenase (IDH) compared to North Sea animals, even when acclimated to the same temperature of 11 °C. All of these patterns reflect an overall rise in the capacity of aerobic energy production with cold adaptation. This explains the downward shift of the low critical temperature, beyond which anaerobic metabolism sets in. However, the higher mitochondrial density is likely to induce the rise in standard metabolic rate seen in White Sea lugworms, thereby causing a concomitant shift of the high Tc to a lower value. An increase in the Ea value for the decarboxylation of isocitrate in White Sea specimens may help to minimize the increment in standard metabolic rate induced by the higher mitochondrial density and capacity, at the expense of a higher thermal sensitivity of metabolism in the warm.Key Words: Cold adaptation, Mitochondria, Aerobic capacity, Critical temperature, Arenicola marina