Abstract
Mitochondrial function can provide key insights into how fish will respond to climate change, due to its important role in heart performance, energy metabolism and oxidative stress. However, whether warm acclimation can maintain or improve the energetic status of the fish heart when exposed to short-term heat stress is not well understood. We acclimated Atlantic salmon, a highly aerobic eurythermal species, to 12 and 20 °C, then measured cardiac mitochondrial functionality and integrity at 20 °C and at 24, 26 and 28 °C (this species’ critical thermal maximum ± 2 °C). Acclimation to 20 °C vs. 12 °C enhanced many aspects of mitochondrial respiratory capacity and efficiency up to 24 °C, and preserved outer mitochondrial membrane integrity up to 26 °C. Further, reactive oxygen species (ROS) production was dramatically decreased at all temperatures. These data suggest that salmon acclimated to ‘normal’ maximum summer temperatures are capable of surviving all but the most extreme ocean heat waves, and that there is no ‘tradeoff’ in heart mitochondrial function when Atlantic salmon are acclimated to high temperatures (i.e., increased oxidative phosphorylation does not result in heightened ROS production). This study suggests that fish species may show quite different acclimatory responses when exposed to prolonged high temperatures, and thus, susceptibility to climate warming.
Highlights
Increases in average water temperatures and more frequent and extreme warming events are predicted to occur with climate change, and there is an urgent need to understand the effects of prolonged and short-term warming on the physiology of aquatic organisms, including fish[1,2,3,4,5]
The mitochondrial electron transport system (ETS) and oxidative phosphorylation are the primary processes involved in energy (ATP) production, but there are a number of temperature-related biochemical constraints that may set limits to animal performance that are associated with mitochondrial function
We examined the thermal sensitivity and acclimation potential of Atlantic salmon cardiac mitochondrial function to provide a more comprehensive picture of how acclimation to warm temperatures affects the metabolic capacity of this highly aerobic, moderately eurythermal, fish species at temperatures just below, at, and above their C TMax
Summary
Increases in average water temperatures and more frequent and extreme warming events (i.e., heat waves) are predicted to occur with climate change, and there is an urgent need to understand the effects of prolonged and short-term warming on the physiology of aquatic organisms, including fish[1,2,3,4,5]. Chung et al.[20] showed that northern and southern killifish (Fundulus heteroclitus) acclimated to 33 °C had decreased mitochondrial function at 38 °C compared to killifish acclimated to 15 °C Overall, these two studies support the ‘plastic floors and concrete ceilings’ p rinciples[28], and suggest that mitochondria from warm-acclimated fish could have limited or reduced scope to enhance their capacity upon acute exposure to higher temperatures (i.e., climate change related heat waves) because they have already reached their maximal acclimation potential. We measured several mitochondrial bioenergetic processes underlying mitochondrial thermal sensitivity and plasticity, including: (1) the contribution of NADH dehydrogenase (complex I; CI) to mitochondrial respiration (due to its known thermal sensitivity and plasticity32,33,35); (2) mitochondrial respiration through the principal complexes of the electron transport system (complexes I and II; I + II); (3) mitochondrial membrane potential; (4) reactive oxygen species (ROS) production (i.e., release rate); (5) outer and inner membrane integrity; and (6) the maximal capacity of the ETS (ETS-I + II) and CIV to identify limiting steps in the ETS
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