Comparison of Mitochondrial Reactive Oxygen Species Production of Ectothermic and Endothermic Fish Muscle

Abstract

Recently we demonstrated that the capacity of isolated muscle mitochondria to produce reactive oxygen species, measured as H2O2 efflux, is temperature-sensitive in isolated muscle mitochondria of ectothermic fish and the rat, a representative endothermic mammal. However, at physiological temperatures (15° and 37°C for the fish and rat, respectively), the fraction of total mitochondrial electron flux that generated H2O2, the fractional electron leak (FEL), was far lower in the rat than in fish. Those results suggested that the elevated body temperatures associated with endothermy may lead to a compensatory decrease in mitochondrial ROS production relative to respiratory capacity. To test this hypothesis we compare slow twitch (red) muscle mitochondria from the endothermic Pacific bluefin tuna (Thunnus orientalis) with mitochondria from three ectothermic fishes [rainbow trout (Oncorhynchus mykiss), common carp (Cyprinus carpio), and the lake sturgeon (Acipenser fulvescens)] and the rat. At a common assay temperature (25°C) rates of mitochondrial respiration and H2O2 efflux were similar in tuna and the other fishes. The thermal sensitivity of fish mitochondria was similar irrespective of ectothermy or endothermy. Comparing tuna to the rat at a common temperature, respiration rates were similar, or lower depending on mitochondrial substrates. FEL was not different across fish species at a common assay temperature (25°C) but was markedly higher in fishes than in rat. Overall, endothermy and warming of Pacific Bluefin tuna red muscle may increase the potential for ROS production by muscle mitochondria but the evolution of endothermy in this species is not necessarily associated with a compensatory reduction of ROS production relative to the respiratory capacity of mitochondria.

Mitochondrial Costs of Being Hot: Effects of Acute Thermal Change on Liver Bioenergetics in Toads (Bufo bufo)

“…The data presented here show that the rapid increase in temperature induces higher mitochondrial rates of oxygen consumption, ATP synthesis, and H 2 O 2 production. These results are in accordance with the acute temperature effects on oxidative phosphorylation activity and ROS production reported in several ectothermic species (Cassuto, 1971;Abele et al, 2002;Heise et al, 2003;Paital and Chainy, 2014;Chung and Schulte, 2015;Wiens et al, 2017). However, high temperatures also decrease the mitochondrial coupling efficiency (ATP/O).…”

“…The H 2 O 2 generation in toad liver mitochondria is also positively correlated to the rates of oxygen consumption, with these two mitochondrial fluxes increasing as temperature increases. The increase of H 2 O 2 production along with respiratory activity in response to an acute rise in temperature has been widely reported in mitochondria from ectothermic species (Abele et al, 2002;Heise et al, 2003;Paital and Chainy, 2014;Chung and Schulte, 2015;Wiens et al, 2017). In the present study, we used succinate, a FADH 2 -linked substrate, which drives ROS production which is critically sensitive to proton-motive force (Korshunov et al, 1997;Miwa et al, 2003;Keller et al, 2004).…”

“…Thus, a key reason for focusing on mitochondrial functioning is its importance in supplying energy and regulating the oxidative balance that are involved in many life history traits and trade-offs (Monaghan et al, 2009;Seebacher et al, 2010;Salin et al, 2015;Schulte, 2015). Mitochondrial oxidative phosphorylation and ROS generation are known to be directly influenced by temperature (Cassuto, 1971;Abele et al, 2002;Heise et al, 2003;Chamberlin, 2004;Paital and Chainy, 2014;Chung and Schulte, 2015;Wiens et al, 2017), generating similar shapes of performance curves with those of many biochemical and physiological processes (Pörtner et al, 2007;Schulte, 2015). Performance increases as temperatures rise, followed by a plateau when the processes reach thermal optimum, followed by a steep decline at higher temperatures (Pörtner et al, 2007;Schulte, 2015).…”

High Temperature, pH, and Hypoxia Cause Oxidative Stress and Impair the Spermatic Performance of the Amazon Fish Colossoma macropomum

“…Studies have shown that temperature increases potentially induce oxidative stress in different fish tissues ( Wiens et al, 2017 ), including sperm cells, as presented in this paper with the increase in antioxidant enzymes, contributing to the increase in lipid peroxidation levels, as shown by Dadras et al (2016) when evaluating the sperm of C. carpio , identifying that the lipid peroxidation in these cells is temperature sensitive. Lipids are probably used as a source of energy by sperm to increase motility duration ( Baeza et al, 2015 ) that plays an important role in fertilization capacity ( Gholami et al, 2011 ).…”

Comparing Electron Leak in Vertebrate Muscle Mitochondria

“…The substrate cocktail added is indicated in each panel and in all cases additions was 5 mM except rotenone (4 µM) and palmitoylcarnitine (50 µM). Values are from Banh et al (2016) or Wiens et al (2017) with the exception of mouse (strain C57BL/6N), Green frog (Lithobates pipiens) and Xenopus (X. laevis), which are all previously unpublished and were isolated and assayed according to the same methods described in Wiens et al (2017). Data are mean±SEM (n=3-6) with the exception of Xenopus which is mean ± range for n=2.…”