Abstract
Fish of the suborder Notothenioidei have successfully radiated into the Southern Ocean and today comprise the dominant fish sub-order in Antarctic waters in terms of biomass and species abundance. During evolution in the cold and stable Antarctic climate, the Antarctic lineage of notothenioids developed several unique physiological adaptations, which make them extremely vulnerable to the rapid warming of Antarctic waters currently observed. Only recently, a further phenomenon exclusive to notothenioid fish was reported: the translocation of the mitochondrial gene encoding the NADH Dehydrogenase subunit 6 (ND6), an indispensable part of complex I in the mitochondrial electron transport system.This study investigated the potential physiological consequences of ND6 translocation for the function and thermal sensitivity of the electron transport system in isolated liver mitochondria of the two nototheniid species Notothenia coriiceps and Notothenia rossii, with special attention to the contributions of complex I (NADH DH) and complex II (Succinate DH) to oxidative phosphorylation. Furthermore, enzymatic activities of NADH∶Cytochrome c Oxidoreductase and Cytochrome C Oxidase were measured in membrane-enriched tissue extracts.During acute thermal challenge (0–15°C), capacities of mitochondrial respiration and enzymatic function in the liver could only be increased until 9°C. Mitochondrial complex I (NADH Dehydrogenase) was fully functional but displayed a higher thermal sensitivity than the other complexes of the electron transport system, which may specifically result from its unique amino acid composition, revealing a lower degree of stability in notothenioids in general. We interpret the translocation of ND6 as functionally neutral but the change in amino acid sequence as adaptive and supportive of cold stenothermy in Antarctic nototheniids. From these findings, an enhanced sensitivity to ocean warming can be deduced for Antarctic notothenioid fish.
Highlights
Antarctic marine life is broadly associated with successful metabolic adaptation to a cold environment, where low temperature and higher oxygen solubility in water are strong selective factors and are paralleled by a specialisation of animals to limited thermal windows [1]
3.1 Animal parameters At the time of sampling, fish of both species were of the same size and weight range, but displayed different hepatosomatic indices of 2.2260.33% (N. coriiceps) and 1.5760.06% (N. rossii), respectively
4.7 Conclusions In the light of the translocation of the NADH Dehydrogenase subunit 6 (ND6) gene, we focused our interest on the performance and capacity of the individual mitochondrial complexes I and II
Summary
Antarctic marine life is broadly associated with successful metabolic adaptation to a cold environment, where low temperature and higher oxygen solubility in water are strong selective factors and are paralleled by a specialisation of animals to limited thermal windows [1]. Fish living in this environment are considered highly stenothermal, and their adaptations have been verified at the molecular, cellular, tissue, and organismal hierarchical organisation levels [2,3,4,5]. Studies of energy allocation in isolated cells of Antarctic notothenioids have suggested that within a thermal range of about 21uC to 12uC, thermal tolerance limits are defined at whole organism level, e.g. by capacity limitations of the circulatory system rather than by a general failure of cellular energy metabolism [24,25]
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