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Copper Alters the Effect of Temperature on Mitochondrial Bioenergetics in Rainbow Trout, Oncorhynchus mykiss

Archives of Environmental Contamination and Toxicology volume 66, pages 430–440 (2014)Cite this article

Abstract

We investigated the interaction of temperature and copper (Cu) on mitochondrial bioenergetics to gain insight into how temperature fluctuations imposed by natural phenomena or anthropogenic activities would modulate the effects of Cu on cellular energy homeostasis. Mitochondria were isolated from rainbow trout livers and, in the first set of experiments, exposed to Cu (0–2.5 mM) at 5, 11, and 25 °C with measurement of mitochondrial complex II (mtCII)-driven respiration. In the second set of experiments, unenergized mitochondria were incubated for 30 or 60 min with lower concentrations (0–160 μM) of Cu to measure the effects on mtCII enzyme activity. Whereas maximal (state 3) respiration was inhibited by high Cu exposure, low Cu doses stimulated and high Cu doses inhibited resting (state 4) and 4ol (proton leak) respirations. High temperature alone increased mitochondrial respiration in all states. The Q10 values for state 3, state 4, and proton leak respirations suggested active processes with state 4 respiration and proton leak exhibiting greater thermal sensitivity than state 3 respiration. The differential thermal sensitivity of resting relative to phosphorylating mitochondrial state led to uncoupling and limitation of mitochondrial oxidative capacity at both high temperature and doses of Cu. Moreover, exposure to high Cu caused loss of thermal dependence of the mitochondrial bioenergetics culminating in Q10 values well below unity and decreased activation energies (E a) for both maximal and resting respiration rates. In addition, mtCII activity was increased by low and decreased by high doses of Cu indicating that direct effects on this enzyme contribute to Cu-induced mitochondrial dysfunction. Taken together, it appears that the substrate oxidation (electron transport chain and tricarboxylic acid cycle) and proton leak subsystems are targets of the deleterious effects of Cu and increased temperature on mitochondrial bioenergetics. However, mitochondrial effects of Cu and temperature may not be easily distinguished because they are generally qualitatively similar.

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Acknowledgments

This study was supported by Discovery Grants (C. K., D. S., and M. F.) from the Natural Sciences and Engineering Research Council (NSERC) of Canada and Novartis Animal Health Research Chair on Fish Health. R. S. was supported by a Pathology and Microbiology Scholarship, and M. M. was supported by NSERC Undergraduate Student Research Award. We are grateful to Nicole MacDonald for technical support and John Burka for reading and editing an early version of the manuscript.

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  1. Department of Biomedical Sciences, Atlantic Veterinary College, University of Prince Edward Island, 550 University Ave., Charlottetown, PE, C1A 4P3, Canada

    Ravinder Sappal, Michelle MacDougald, Don Stevens & Collins Kamunde

  2. Department of Pathology and Microbiology, Atlantic Veterinary College, University of Prince Edward Island, Charlottetown, PE, C1A 4P3, Canada

    Ravinder Sappal & Mark D. Fast

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  1. Ravinder Sappal
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  2. Michelle MacDougald
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Correspondence to Collins Kamunde.

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Sappal, R., MacDougald, M., Stevens, D. et al. Copper Alters the Effect of Temperature on Mitochondrial Bioenergetics in Rainbow Trout, Oncorhynchus mykiss . Arch Environ Contam Toxicol 66, 430–440 (2014). https://doi.org/10.1007/s00244-013-9985-2

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Keywords

  • Respiration
  • Rainbow Trout
  • Mitochondrial Respiration
  • Thermal Sensitivity
  • Proton Leak