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Thermal sensitivity of cellular energy budgets in some Antarctic fish hepatocytes

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Abstract

Oxygen demand elicited by the main cellular energy consumers was examined in isolated hepatocytes of sub-Antarctic (Lepidonotothen larseni) and high-Antarctic notothenioids (Trematomus eulepidotus, Trematomus pennellii, Trematomus lepidorhinus, Trematomus bernacchii, Artedidraco orianae) and in a zoarcid (Pachycara brachycephalum) fish with respect to the role of cellular metabolism in co-defining thermal tolerance. The relative proportions of energy allocated to protein and RNA/DNA synthesis, ion regulation and ATP synthesis were quantified between 0°C and 15°C by analysis of inhibitor sensitive cellular respiration. In all the investigated species, protein synthesis constituted 25–37%, RNA synthesis 24–35%, Na+/K+-ATPase 40–45% and mitochondrial ATP synthesis 57–65% of total respiration. The sub-Antarctic nototheniid L. larseni displayed lower cellular protein synthesis rates but somewhat higher active ion regulation activities than its high-Antarctic confamilials, as is typical for more eurythermal species. Assumed thermal optima were mirrored in minimized overall cellular energy demand. In the sub-Antarctic L. larseni and P. brachycephalum, minima of oxygen consumption were located between 3°C and 6°C, indicating elevated energy turnover below and above these temperatures. In contrast, the high-Antarctic species displayed progressively rising respiration rates during warming with a cellular energetic minimum at 0°C. The sub-Antarctic nototheniid and the zoarcid showed signs of cold-eurythermy and appear to live close to their lower limit of thermal tolerance, while high-Antarctic notothenioids show high degrees of energetic efficiency at 0°C. All cellular preparations maintained energy budgets over a wide thermal range, supporting the recent concept that thermal limits are set by oxygen and associated energy limitations at the whole organism level.

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Acknowledgements

The authors would like to thank E-M. Brodte, K. Mintenbeck, N. Koschnick, C. Bock, R. Knust and the crew of RV Polarstern cruise ANT XXI-2 for their valuable and excellent help in catch, identification, maintenance and preparation of the fish species used in this study, and T. Brey for his helpful comments on the statistics.

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Correspondence to F. C. Mark.

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Mark, F.C., Hirse, T. & Pörtner, H.O. Thermal sensitivity of cellular energy budgets in some Antarctic fish hepatocytes. Polar Biol 28, 805–814 (2005). https://doi.org/10.1007/s00300-005-0018-0

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