Physiological adaptation of an Antarctic Na+/K+-ATPase to the cold

Abstract

SUMMARYBecause enzymatic activity is strongly suppressed by the cold, polar poikilotherms face significant adaptive challenges. For example, at 0°C the catalytic activity of a typical enzyme from a temperate organism is reduced by more than 90%. Enzymes embedded in the plasma membrane, such as the Na + /K + -ATPase, may be even more susceptible to the cold because of thermal effects on the lipid bilayer. Accordingly, adaptive changes in response to the cold may include adjustments to the enzyme or the surrounding lipid environment, or synergistic changes to both. To assess the contribution of the enzyme itself, we cloned orthologous Na + /K + -ATPase -subunits from an Antarctic (Pareledone sp.; -1.8°C) and a temperate octopus (Octopus bimaculatus; ~18°C), and compared their turnover rates and temperature sensitivities in a heterologous expression system. The primary sequences of the two pumps were found to be highly similar (97% identity), with most differences being conservative changes involving hydrophobic residues. The physiology of the pumps was studied using an electrophysiological approach in intact Xenopus oocytes. The voltage dependence of the pumps was equivalent. However, at room temperature the maximum turnover rate of the Antarctic pump was found to be 25% higher than that of the temperate pump. In addition, the Antarctic pump exhibited a lower temperature sensitivity, leading to significantly higher relative activity at lower temperatures. Orthologous Na + /K + pumps were then isolated from two tropical and two Arctic octopus. The temperature sensitivities of these pumps closely matched those of the temperate and Antarctic pumps, respectively. Thus, reduced thermal sensitivity appears to be a common mechanism driving cold adaptation in the Na + /K + -ATPase. Supplementary material available online at

Energy landscape of the reactions governing the Na + deeply occluded state of the Na + /K + -ATPase in the giant axon of the Humboldt squid

“…From the data in Fig. 2, we estimated ΔH ‡ to be approximately 24 kcal∕mol, which corresponds to a Q 10 of approximately 4.3, similar to previous reports (31)(32)(33). The value of the transition entropy, ΔS ‡ ¼ 89.8 − R ln A, necessarily requires a knowledge of the factor A, which for large molecules in aqueous solutions is largely unknown.…”

Temperature compensation of aerobic capacity and performance in the Antarctic pteropod,Clione antarctica, compared to its northern congener,C. limacina

“…It may also be that CS in the polar pteropod has an increased catalytic capacity. It has been reported that some enzymes from Antarctic ectotherms are more efficient than those of warmer species (Kawall et al, 2002;Galarza-Muñoz et al, 2011). Therefore, the 4-fold difference in CS enzymatic activity between C. limacina and C. antarctica may be a result of both quantitative and qualitative changes to the enzyme.…”

“…However, investigations in Antarctic animals have been hampered by the lack of an appropriate comparative system in warmer waters (Weinstein and Somero, 1998). To date, most comparative studies on temperature adaptation have focused on the Notothenioidae (Crockett and Sidell, 1990;Weinstein and Somero, 1998;Hardewig et al, 1999), an abundant group of fishes that is highly endemic to the Southern Ocean, and some benthic invertebrates Morley et al, 2009;Galarza-Muñoz et al, 2011). Although the studies uncovered substantial evidence of temperature adaptation, the models they used focused on sluggish, bottom-dwelling species with little need to up-regulate aerobic capacity (Peck, 2002).…”

Parallel ionoregulatory adjustments underlie phenotypic plasticity and evolution ofDrosophilacold tolerance

“…Reductions in enzyme thermal sensitivity are often associated with adaptation to low temperatures (Somero, 2004;Dong and Somero, 2009;Galarza-Muñoz et al, 2011;Garrett and Rosenthal, 2012). For example, polar and temperate octopus species have Na + /K + -ATPase α-subunits that differ in thermal sensitivity; at temperatures greater than 25°C the maximal rate of Na + /K + -ATPase does not differ between polar and temperate octopuses, but that of polar octopuses is 4-fold higher at 10°C (Galarza-Muñoz et al, 2011). Thus, cold tolerance may also be improved in Drosophila through similar reductions in the thermal sensitivity of Na…”