Abstract
Temperature is a key factor that affects all levels of organization. Minute shifts away from thermal optima result in detrimental effects that impact growth, reproduction and survival. Metabolic rates of ectotherms are especially sensitive to temperature and for organisms exposed to high acute temperature changes, in particular intertidal species, energetic processes are often negatively impacted. Previous investigations exploring acute heat stress have implicated cardiac mitochondrial function in determining thermal tolerance. The brain, however, is by weight, one of the most metabolically active and arguably the most temperature sensitive organ. It is essentially aerobic and entirely reliant on oxidative phosphorylation to meet energetic demands, and as temperatures rise, mitochondria become less efficient at synthesising the amount of ATP required to meet the increasing demands. This leads to an energetic crisis. Here we used brain homogenate of three closely related triplefin fish species (Bellapiscis medius, Forsterygion lapillum, and Forsterygion varium) and measured respiration and ATP dynamics at three temperatures (15, 25 and 30 °C). We found that the intertidal B. medius and F. lapillum were able to maintain rates of ATP production above rates of ATP hydrolysis at high temperatures, compared to the subtidal F. varium, which showed no difference in rates at 30 °C. These results showed that brain mitochondria became less efficient at temperatures below their respective species thermal limits, and that energetic surplus of ATP synthesis over hydrolysis narrows. In subtidal species synthesis matches hydrolysis, leaving no scope to elevate ATP supply.
Highlights
Temperature exerts a profound effect on all levels of organization; with no single organism, capable of withstanding the full spectrum of temperatures across the b iosphere[1,2]
Differences were seen across all states at 25 °C (Fig. 3). Both F. lapillum and B. medius showed higher flux during CI-oxidative phosphorylation (OXPHOS) and CI&complex II (CII)-OXPOS compared with F. varium (Fig. 3a,b; B. medius: CI-OXPHOS, p = 0.007; CI&CII-OXPHOS, p = 0.025; F. lapillum: CI-OXPHOS, p = 0.001; CI&CII-OXPHOS, p < 0.0001)
electron transport system (ETS) rates differed between all three species, with F. lapillum having the highest rates compared with B. medius and F. varium (p < 0.0001)
Summary
Temperature exerts a profound effect on all levels of organization; with no single organism, capable of withstanding the full spectrum of temperatures across the b iosphere[1,2]. Temperature typically promotes a near exponential rise in metabolic rate until a critical threshold is reached, which is followed by a sharp decline[6] What mediates this metabolic collapse at high temperature remains controversial, and oxygen limitation has been proposed to underpin thermal tolerance in aquatic ectotherms[7,8]. While considerable focus has been placed on respiration and ATP production, few have considered how these relate to rates of ATP hydrolysis at high ambient temperatures This relatively simplistic concept of balance in cellular ATP-economics has yet to be followed in the contexts of temperature. Temperature have the ability to measure ATP production as well as a simplistic measure of ATP hydrolysis under variable thermal stresses This allowed us to generate a clearer picture with regard to energetic economy at high temperatures. Action potentials and consequent restoration of ion balance consumes up to 80% of total ATP in active neurons and these pathways, along with synaptic transmission, are thermally sensitive[28,29]
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