Regulation of mitochondrial metabolism during hibernation by reversible suppression of electron transport system enzymes

Abstract

Small hibernators cycle between periods of torpor, with body temperature (T b) approximately 5 °C, and interbout euthermia (IBE), where T b is approximately 37 °C. During entrance into a torpor bout liver mitochondrial respiration is rapidly suppressed by 70 % relative to IBE. We compared activities of electron transport system (ETS) complexes in intact liver mitochondria isolated from 13-lined ground squirrels (Ictidomys tridecemlineatus) sampled during torpor and IBE to investigate potential sites of this reversible metabolic suppression. Flux through complexes I–IV and II–IV was suppressed by 40 and 60 %, respectively, in torpor, while flux through complexes III–IV and IV did not differ between torpor and IBE. We also measured maximal enzyme activity of ETS enzymes in homogenized isolated mitochondria and whole liver tissue. In isolated mitochondria, activities of complexes I and II were significantly lower in torpor relative to IBE, but complexes III, IV, and V did not differ. In liver tissue, only activity of complex II was suppressed during torpor relative to IBE. Despite the significant differences in both ETS flux and maximal activity, the protein content of complexes I and II did not differ between torpor and IBE. These results suggest that the rapid, reversible suppression of mitochondrial metabolism is due to regulatory changes, perhaps by post-translational modification during entrance into a torpor bout, and not changes in ETS protein content.

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Acknowledgments

We thank Alvin Iverson and staff at the Carman Area Research Center (University of Manitoba) for assistance in trapping animals, and Manitoba Conservation for permission to trap animals. We thank Amanda MacCannell and Natalie Po for their assistance with surgeries and general animal care. We thank Allison McDonald for the use of her Oroboros-2K for the duration of this study, and we thank Dr. Timothy Regnault for assistance with MitoProfile immunoblots. This study was supported financially by a Discovery Grant to JFS from the Natural Sciences and Engineering Research Council (Grant Number RGPIN-2014-04860) and Queen Elizabeth II Graduate Scholarships in Science and Technology to KEM and SVM.

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Correspondence to Katherine E. Mathers.

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Communicated by H.V. Carey.

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Mathers, K.E., McFarlane, S.V., Zhao, L. et al. Regulation of mitochondrial metabolism during hibernation by reversible suppression of electron transport system enzymes. J Comp Physiol B 187, 227–234 (2017). https://doi.org/10.1007/s00360-016-1022-0

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Keywords

  • Mitochondria
  • Oxidative phosphorylation
  • Metabolic suppression
  • Mitochondrial respiration