Do Mitochondria Limit Hot Fish Hearts? Understanding the Role of Mitochondrial Function with Heat Stress in Notolabrus celidotus
Open Access
- 28 May 2013
- journal article
- research article
- Published by Public Library of Science (PLoS) in PLOS ONE
- Vol. 8 (5), e64120
- https://doi.org/10.1371/journal.pone.0064120
Abstract
Hearts are the first organs to fail in animals exposed to heat stress. Predictions of climate change mediated increases in ocean temperatures suggest that the ectothermic heart may place tight constraints on the diversity and distribution of marine species with cardiovascular systems. For many such species, their upper temperature limits (Tmax) and respective heart failure (HF) temperature (THF) are only a few degrees from current environmental temperatures. While the ectothermic cardiovascular system acts as an “ecological thermometer,” the exact mechanism that mediates HF remains unresolved. We propose that heat-stressed cardiac mitochondria drive HF. Using a common New Zealand fish, Notolabrus celidotus, we determined the THF (27.5°C). Haemoglobin oxygen saturation appeared to be unaltered in the blood surrounding and within heat stressed hearts. Using high resolution respirometry coupled to fluorimeters, we explored temperature-mediated changes in respiration, ROS and ATP production, and overlaid these changes with THF. Even at saturating oxygen levels several mitochondrial components were compromised before THF. Importantly, the capacity to efficiently produce ATP in the heart is limited at 25°C, and this is prior to the acute THF for N. celidotus. Membrane leakiness increased significantly at 25°C, as did cytochrome c release and permeability to NADH. Maximal flux rates and the capacity for the electron transport system to uncouple were also altered at 25°C. These data indicate that mitochondrial membrane integrity is lost, depressing ATP synthesis capacity and promoting cytochrome c release, prior to THF. Mitochondria can mediate HF in heat stressed hearts in fish and play a significant role in thermal stress tolerance, and perhaps limit species distributions by contributing to HF.This publication has 99 references indexed in Scilit:
- Assessing mitochondrial dysfunction in cellsBiochemical Journal, 2011
- Thermal sensitivity of oxidative phosphorylation in rat heart mitochondria: Does pyruvate dehydrogenase dictate the response to temperature?Journal of Thermal Biology, 2010
- Fish cardiorespiratory physiology in an era of climate changeThe present review is one of a series of occasional review articles that have been invited by the Editors and will feature the broad range of disciplines and expertise represented in our Editorial Advisory Board.Canadian Journal of Zoology, 2009
- Impaired ATP turnover and ADP supply depress cardiac mitochondrial respiration and elevate superoxide in nonfailing spontaneously hypertensive rat heartsAmerican Journal of Physiology-Cell Physiology, 2009
- Hydrogen Sulfide Mediates Cardioprotection Through Nrf2 SignalingCirculation Research, 2009
- A Novel Kinetic Assay of Mitochondrial ATP-ADP Exchange Rate Mediated by the ANTBiophysical Journal, 2009
- How mitochondria produce reactive oxygen speciesBiochemical Journal, 2008
- Temperature‐ and exercise‐induced gene expression and metabolic enzyme changes in skeletal muscle of adult zebrafish (Danio rerio)Journal Of Physiology-London, 2006
- Thermal Physiology and Vertical Zonation of Intertidal Animals: Optima, Limits, and Costs of LivingIntegrative and Comparative Biology, 2002
- Ecological responses to recent climate changeNature, 2002