The Effect of Temperature on Cardiac Energetics in the Rainbow Trout, Onchorhynchus mykiss

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Abstract

Acute changes in temperature have a significant impact on ectotherm metabolic function due to their inability to regulate internal temperatures. An alteration of metabolic rate will drive modulations in cardiac function in order to meet the changing oxygen demands of aerobically active tissues. The function of the fish heart therefore underpins an organism̢۪s ability to survive changing temperature. There have been multiple studies assessing the effects of temperature on the metabolism of fish tissue systems but relatively few on the heart. As such, the aims of this thesis were to study the effects of cooling and warming on cardiac metabolism of the rainbow trout. As mitochondria are responsible for producing the majority of ATP for cardiomyocytes and drive aerobic demand, the experiments in this thesis centred on the mitochondrial response to temperature change. In chapter 3, I provide the first thorough investigation into the effect of cold and warm acclimation on cardiac mitochondria morphology in fish. Cold acclimation induced mitochondrial proliferation and an upregulation of mitochondrial fusion, whilst warm acclimation did not increase mitochondrial content but is suggested to increase fission events. A lack of change in internal mitochondrial ultrastructure however doesn̢۪t suggest any change in energetic capacity. In chapter 4, I demonstrate that mitochondria are sensitive to acute temperature changes, although their response did not fit expectations. Cold acclimated mitochondria decreased respiratory rates when acutely warmed whilst acute cooling caused an increase in mitochondrial function in warm acclimated fish. This acute response demonstrated a narrowing of the thermal performance window in the cold acclimated fish with warm acclimation shifting the thermal optimum and lowering upper thermal limits. This repression of mitochondrial function may have a significant impact on rainbow trout fitness if exposed to changing temperatures. We found that ROS production was insensitive to temperature changes which may be a result of complex I and III remodelling or due to changes in antioxidant capacity. Metabolic enzymes from the TCA cycle, electron transport chain and fatty acid oxidation pathways demonstrated a limited capacity for remodelling following temperature changes. We show that cold acclimation sensitised metabolic enzymes to acute changes in temperature whilst warm acclimation induced a desensitisation. Cold acclimation did not induce a switch to fatty acid metabolism as might be expected and we demonstrated that citrate synthase is a poor biomarker for mitochondrial content in the rainbow trout heart. Overall, I have shown that the fish heart is sensitive to thermal changes which are reflected functionally and morphologically. Despite being sensitive to temperature changes rainbow trout mitochondria do not fi t traditional compensatory remodelling patterns and instead shift thermal optima. Cold acclimation leads a thermal sensitisation of metabolic enzymes which is not seen in the warm which displayed generally high metabolic activities. This metabolic remodelling may prove to be energetically costly and possibly detrimental to organismal fitness in the wild.

Keyword(s)

bioenergetics; cardiovascular; fish; mitochondria; thermal biology

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