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      Do Mitochondria Limit Hot Fish Hearts? Understanding the Role of Mitochondrial Function with Heat Stress in Notolabrus celidotus

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      PLoS ONE

      Public Library of Science

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          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 (T max) and respective heart failure (HF) temperature (T HF) 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 T HF (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 T HF. Even at saturating oxygen levels several mitochondrial components were compromised before T HF. Importantly, the capacity to efficiently produce ATP in the heart is limited at 25°C, and this is prior to the acute T HF 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 T HF. 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.

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          Author and article information

          Contributors
          Role: Editor
          Journal
          PLoS One
          PLoS ONE
          plos
          plosone
          PLoS ONE
          Public Library of Science (San Francisco, USA )
          1932-6203
          2013
          28 May 2013
          : 8
          : 5
          Affiliations
          School of Biological Sciences, University of Auckland, Auckland, New Zealand
          Instituto Nacional de Cardiologia, Mexico
          Author notes

          Competing Interests: The authors have declared that no competing interests exist.

          Conceived and designed the experiments: FII AJRH. Performed the experiments: FII AJRH. Analyzed the data: FII AJRH. Contributed reagents/materials/analysis tools: AJRH. Wrote the paper: FII.

          Article
          PONE-D-12-40548
          10.1371/journal.pone.0064120
          3665896
          23724026

          This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

          Page count
          Pages: 15
          Funding
          This work was supported by a Royal Society of New Zealand Marsden grant (to AJRH). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
          Categories
          Research Article
          Biology
          Biochemistry
          Bioenergetics
          Energy-Producing Organelles
          Metabolism
          Metabolic Pathways
          Blood Chemistry
          Marine Biology
          Zoology
          Animal Physiology
          Ichthyology
          Medicine
          Cardiovascular
          Heart Failure

          Uncategorized

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