High temperature impairs mitochondrial function in rainbow trout cardiac mitochondria

Abstract

Mitochondria provides cellular energy through oxidative phosphorylation, and thus temperature-induced constraints on mitochondrial function may be crucial to animal aerobic scope and thermal tolerance. Here, we report the effect of temperature in the range 5-30°C on respiration rates of isolated cardiac mitochondria from rainbow trout (Oncorhyncus mykiss) studied by high-resolution respirometry and spectrophotometric enzyme activity assays. Arrhenius breakpoint temperature analysis indicated that mitochondrial respiration rates under phosphorylating and fully uncoupled conditions increased exponentially up to 20°C, but stopped increasing at higher temperatures. In contrast, respiration rates measured under non-phosphorylating leak conditions continued to increase up to 30°C. The decrease in the ratio between phosphorylating and uncoupled respiration at high temperature indicated that phosphorylation was gradually impaired with increasing temperature, possibly because of the steadily increasing proton leak across the membrane. In addition, we found that complex I (NADH dehydrogenase) activity decreased above 20°C, similarly to mitochondrial respiration, and that complex I was unstable in the presence of detergents, suggesting that it may be particularly sensitive to changes in its interaction with membrane phospholipids. In contrast, complex II (succinate dehydrogenase) maintained activity at temperatures above 20°C, although succinate oxidation was insufficient to compensate for the loss of complex I activity in intact mitochondria. Together, these results indicate that the temperature-induced decrease in cardiac mitochondrial function coincides with the temperature at which trout aerobic scope peaks, and is largely due to impaired phosphorylation and complex I activity.

Swimming energetics of Atlantic salmon in relation to extended fasting at different temperatures

“…This discrepancy may be explained by the ṀO 2 only being an indirect measurement of aerobic metabolic rates ( Nelson, 2016 ), and that the relationship between oxygen uptake and energy production can vary between environmental conditions ( Salin et al, 2015 ). Specifically, mitochondrial functioning becomes less efficient at higher temperatures due to impaired phosphorylation caused by increased proton leakage and decreased activity of complex I ( Michaelsen et al, 2021 ; Roussel and Voituron, 2020 ). For instance, Atlantic salmon had a lower ATP produced to oxygen consumed ratio in cardiac mitochondria when acclimated to 20°C compared with 12°C acclimation ( Gerber et al, 2021 ).…”

A mitochondria-targeted molecular phototheranostics platform for NIR-II imaging-guided synergistic photothermal /photodynamic /immune therapy

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“…[16] Moreover, TPP targeting mitochondria for anticancer therapy is based on two points: (i) mitochondrial membrane is particularly sensitive to heat, and( ii) can be easily permeable by the damage of ROS. [17] A favorable mitochondria-targeting PS holds both PDT and PTT feathers upon NIR light will increase the therapeutic effect as well as reduce therapeutic dose for anticancer therapy. With the growing development of phototheranostics, photodiagnosis-guided phototherapy become more and more signi cant for cancer treatment.…”

Hypoxic and Thermal Stress: Many Ways Leading to the NOS/NO System in the Fish Heart

“…This is important for fish that, being ectotherms, need to optimize aerobic metabolism when temperature changes [ 132 , 133 ]. At temperatures acutely incremented to the thermal limit, fish cardiac mitochondrial function is altered in terms of proton leakage rates, oxidative phosphorylation, membranes integrity, protein complexes function, and oxidative imbalance due to increased ROS production [ 132 , 134 , 135 , 136 ]. However, as reported in the Atlantic salmon ( S. salar ), warming acclimation (20 °C, close to the upper thermal tolerance of the species) mitigates the impairment of cardiac mitochondrial function, suggesting a plasticity that can be beneficial for thermal tolerance.…”