Improved mitochondrial function in salmon (Salmo salar) following high temperature acclimation suggests that there are cracks in the proverbial ‘ceiling’

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.

The transcriptomic responses of Atlantic salmon (Salmo salar) to high temperature stress alone, and in combination with moderate hypoxia

“…Under stressful conditions, reduced UCP mediated uncoupling (respiration uncoupling) may result in the attenuation of mitochondrial ROS production, and a lower expression of ucp2 could have been part of a feedback-induced decrease in ROS synthesis for cell protection [ 104 ]. Indeed, Gerber and co-workers reported that Atlantic salmon acclimated to 20 °C had reduced cardiac mitochondrial ROS production in comparison to fish acclimated to 12 °C [ 105 ]. Thus, alterations in mitochondrial function at high temperatures may be an important mechanism for thermal acclimation and thermal tolerance in this species.…”

Plasticity of Performance Curves in Ectotherms: Individual Variation Modulates Population Responses to Environmental Change

“…Reactive oxygen species (ROS) and heat shock proteins can be induced by acute heat or cold exposure ( Liu et al, 2018 ). Cold acclimation also increased ROS production in mosquitofish ( Loughland and Seebacher, 2020 ) and grass snakes ( Bury et al, 2018 ), and salmon acclimated to 20°C had greater rates of oxidative phosphorylation but reduced ROS production compared to 12°C acclimated fish ( Gerber et al, 2020 ). Mosquitofish with high acclimation capacity also have greater antioxidant capacities ( Loughland and Seebacher, 2020 ).…”

Temperature effects on the contractile performance and efficiency of oxidative muscle from a eurythermal versus a stenothermal salmonid

“…However, in the present study, net work was maximized in each preparation, and based on pressure–volume area and oxygen consumption relationships in working hearts, this should have maximized contractile efficiency ( Toorop et al, 1988 ; Westerhof, 2000 ). The lower efficiency in char might also reflect reduced mitochondrial coupling ( Iftikar and Hickey, 2013 ; Rodnick et al, 2014 ; Gerber et al, 2020 ). In support of the latter hypothesis, Penney et al (2014) showed that the State 2 and 4 respiration of cardiac mitochondria were consistently higher in 10°C-acclimated char than Atlantic salmon when measured at temperatures from 20 to 28°C, and that this resulted in 35% lower values for RCR between 20 and 24°C in char.…”

“…Rodnick et al (2004) report uncharacteristically high thermal tolerance in redband trout, a strain of rainbow trout that inhabits warm desert environments. Both Anttila et al (2014) and Gerber et al (2020) suggest that acclimating Atlantic salmon to 20°C [a temperature only 3°C below their maximum holding temperature (Hvas et al, 2017;Gamperl et al, 2020) and 6°C below their critical thermal maximum (CT max ) (Penney et al, 2014;Leeuwis et al, 2019)] improves this species' temperature of heart failure and cardiac mitochondrial function at elevated temperatures. Finally, although very warm temperatures impair the power output of red skeletal muscle in Pacific bonito (Sarda chiliensis), this effect is not seen in red muscle of the regionally endothermic yellowfin tuna (Thunnus albacares) (Altringham and Block, 1997).…”