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Metabolic and regulatory responses involved in cold acclimation in Atlantic killifish, Fundulus heteroclitus

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Abstract

Ectotherms often respond to prolonged cold exposure by increasing mitochondrial capacity via elevated mitochondrial volume density [V V(mit,f)]. In fish, higher V V(mit,f) is typically associated with increased expression of nuclear respiratory factor 1 (Nrf1), a transcription factor that induces expression of nuclear-encoded respiratory genes. To examine if nrf1 expression or the expression of other genes that regulate mitochondrial biogenesis contribute to changes in whole-organism metabolic rate during cold acclimation, we examined the time course of changes in the expression of these genes and in metabolic rate in Atlantic killifish, Fundulus heteroclitus. Cold acclimation rapidly decreased metabolic rate, but increased the expression of nrf1 more gradually, with a time course that depended on how rapidly the fish were transitioned to low temperature. Cold-induced nrf1 expression was not associated with increases in biochemical indicators of mitochondrial respiratory capacity, suggesting that cold-induced mitochondrial biogenesis may occur without increases in oxidative capacity in this species. These observations imply that changes in nrf1 expression and metabolic rate due to cold acclimation occur through different physiological mechanisms, and that increases in V V(mit,f) are likely not directly related to changes in metabolic rate with cold acclimation in this species. However, nrf1 expression differed between northern and southern killifish subspecies regardless of acclimation temperature, consistent with observed differences in metabolic rate and V V(mit,f) at 5 °C between these subspecies. Taken together, these results reveal substantial complexity in the regulation of V V(mit,f) and mitochondrial capacity with temperature in fish and the relationship of these parameters to metabolic rate.

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Acknowledgments

This work was supported by a Natural Sciences and Engineering Research Council of Canada (NSERC) Discovery Grant to PMS, NSERC Canada Graduate Scholarships to DJC and TMH, and an NSERC Undergraduate Student Research Award to KGC.

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Correspondence to Timothy M. Healy.

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All procedures performed in this study were in accordance with an approved University of British Columbia animal care Protocol: A11-0372.

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Communicated by G. Heldmaier.

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Healy, T.M., Chung, D.J., Crowther, K.G. et al. Metabolic and regulatory responses involved in cold acclimation in Atlantic killifish, Fundulus heteroclitus . J Comp Physiol B 187, 463–475 (2017). https://doi.org/10.1007/s00360-016-1042-9

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