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The Role of Mitochondrial Uncoupling in Temperature

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The Role of Mitochondrial Uncoupling in Temperature THE ROLE OF MITOCHONDRIAL UNCOUPLING IN TEMPERATURE RESPONSES IN ATLANTIC KILLIFISH, FUNDULUS HETEROCLITUS by Heather Jean Bryant B.Sc., The University of British Columbia, 2015 A THESIS SUBMITTED IN PARTIAL FULFILLMENT OF THE REQUIREMENTS FOR THE DEGREE OF MASTER OF SCIENCE in THE FACULTY OF GRADUATE AND POSTDOCTORAL STUDIES (Zoology) THE UNIVERSITY OF BRITISH COLUMBIA (Vancouver) February 2018 © Heather Jean Bryant, 2018 Abstract Environmental temperature can greatly impact the functioning of ectothermic organisms through effects on mitochondria, which are crucial to aerobic metabolism. Changes in temperature have the potential to influence mitochondrial ATP production and production of reactive oxygen species (ROS), both of which are influenced by the activity of the mitochondrial electron transport system, which generates the proton gradient necessary for mitochondrial ATP production. Thus, I hypothesized that ectothermic organisms have a mechanism for modulating the proton gradient in the face of changes in environmental temperature to maintain ATP production, and that this mechanism may act through uncoupling proteins (UCPs) which can cause a decrease in the proton gradient independent of the production of ATP. Here, I investigate changes in UCPs and mitochondrial function following thermal acclimation in two populations of the eurythermal Atlantic killifish, Fundulus heteroclitus. I show that UCP mRNA expression is tissue-specific, changes with thermal acclimation, and differs between two populations of killifish. However, these changes vary depending on the isoform, tissue, and population (Chapter 2). I also demonstrate that changes in UCP function are not necessarily consistent with changes in mRNA expression in isolated liver and brain mitochondria, but that UCP function may differ in liver between the two populations (Chapter 3). Cold-acclimated northern killifish increase liver mitochondrial capacity and coupling as indicated by increases in state III, respiratory control and ADP/O ratios (Chapter 3). Interestingly, I also observed increases in proton conductance in isolated liver mitochondria from cold-acclimated northern killifish as indicated by increased O2 ii consumption rate at a common membrane potential (Chapter 3). Mitochondrial properties in southern killifish did not differ with thermal acclimation. Taken together, my data suggest that UCPs may play a role in thermal acclimation, although there is not a clear connection between UCP mRNA expression and function. Furthermore, my data indicate that northern killifish may have a greater capacity to respond to low temperature acclimation than southern killifish, suggesting a potential role for adaptive variation in mitochondrial responses to temperature. iii Lay Summary Changes in environmental temperature can have large impacts on the physiology of ectothermic organisms, whose body temperatures closely match environmental temperature. Many of the mechanisms involved in thermal responses occur at the level of the mitochondria, the organelle in the cell responsible for the production of the energy currency used to power biological processes. Uncoupling proteins (UCPs) are hypothesized to play a role in mitigating the negative side effects of thermal change in the mitochondria. I showed that UCPs may play a role in the response to thermal change in killifish. Furthermore, I demonstrated that populations of killifish that come from different local thermal conditions differ in their responses to temperature acclimation. Together, my data suggest that UCPs may be involved in responses to thermal change and that these responses may depend on geographic location, suggesting a putative role for mitochondria in thermal adaptation. iv Preface Chapter 2 is co-authored by Heather J. Bryant and Patricia M. Schulte. Experimental design was carried out by Heather J. Bryant and Patricia M. Schulte. Data collection, analysis, and write-up were performed by Heather J. Bryant. All work with animals was done in accordance with UBC ACC approved animal use protocol # A11-0732. Chapter 3 is co-authored by Heather J. Bryant and Patricia M. Schulte. Experimental design was conducted by Heather J. Bryant and Patricia M. Schulte. Data collection, analysis, and write-up were performed by Heather J. Bryant. All work with animals was done in accordance with UBC ACC approved animal use protocol # A16-0028. v Table of Contents Abstract .................................................................................................................................... ii Lay Summary ......................................................................................................................... iv Preface ...................................................................................................................................... v Table of Contents ................................................................................................................... vi List of Tables ........................................................................................................................... x List of Figures ......................................................................................................................... xi List of Abbreviations ............................................................................................................ xii Glossary ................................................................................................................................ xiv Acknowledgements ............................................................................................................... xv Chapter 1: Introduction ......................................................................................................... 1 1.1 Effects of changes in temperature in ectothermic organisms ................................... 1 1.1.1 Time-scales of temperature variation ................................................................ 1 1.1.2 Processes influenced by temperature ................................................................ 2 1.1.3 How does temperature constrain species ecology and distributions? ............... 3 1.1.4 Aerobic metabolism and the mitochondrion ..................................................... 4 1.2 Temperature and mitochondria in ectotherms .......................................................... 6 1.2.1 Effects of temperature on mitochondrial membranes ....................................... 6 1.2.2 Effects of thermal acclimation on mitochondrial respiratory capacity ............. 7 1.2.3 Effects of temperature on proton leak and mitochondrial coupling ................. 7 1.2.4 Effects of temperature on cellular oxidative damage ....................................... 9 1.3 Uncoupling proteins (UCPs) ..................................................................................... 9 vi 1.3.1 Uncoupling protein 1 (UCP1 a.k.a. thermogenin) .......................................... 10 1.3.2 Uncoupling proteins 2 and 3 (UCP2 and UCP3) ............................................ 11 1.3.3 Other UCPs (4, 5, and 3-like) ......................................................................... 12 1.3.4 Mechanism of UCP proton transport .............................................................. 13 1.3.5 Functional roles of UCPs ................................................................................ 13 1.4 Atlantic killifish as a model .................................................................................... 14 1.4.1 Atlantic killifish .............................................................................................. 14 1.4.2 Thermal acclimation effects on killifish physiology ...................................... 15 1.4.3 Thermal acclimation effects on killifish mitochondrial function ................... 16 1.5 Thesis objectives ..................................................................................................... 17 Chapter 2: Thermal acclimation effects on uncoupling protein mRNA expression in two populations of Atlantic killifish, Fundulus heteroclitus ..................................................... 18 2.1 Introduction ............................................................................................................. 18 2.2 Methods................................................................................................................... 20 2.2.1 Phylogenetic analysis ...................................................................................... 20 2.2.2 Animals and temperature acclimations ........................................................... 23 2.2.3 RNA isolations and cDNA synthesis .............................................................. 24 2.2.4 Quantitative real-time PCR (qRT-PCR) ......................................................... 24 2.2.5 Statistical analysis ........................................................................................... 25 2.3 Results ..................................................................................................................... 27 2.3.1 Phylogenetic analysis ...................................................................................... 27 2.3.2 Tissue-specific mRNA expression .................................................................. 27 vii 2.3.3 Thermal acclimation and population effects on Ucp isoform mRNA expression ......................................................................................................................
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