Cardiac responses to temperature in marine teleosts [electronic resource]

Through evolutionary and acclimatory processes, organisms, including marine teleosts, have modified a common set of biochemical structures and processes to compensate for challenges presented by changes in ambient temperature. Investigating these biological processes underlying thermal optima and thermal limits of ectothermic species is crucial to determining susceptibility of an organism to shifts in their environmental temperature. An insufficient supply of oxygen under thermal stress is thought to underlie thermal limits in aquatic animals including teleost fish. Therefore, to compensate for effects of temperature, organisms may induce an acclimatory response that enhances cardiac performance and oxygen delivery under a new temperature regime. These changes alter the critical threshold of a temperature stress for an organism and thereby maintain or increase its fitness in its environment. The dissertation research presented here investigates effects of temperature acclimation on whole organismal physiology and cellular and molecular processes in cardiac tissues in three physiologically and ecologically distinct perciforme teleosts -- Gillichthys mirabilis, Thunnus orientalis and Trematomus bernacchii. Chapter One focuses on effects of temperature acclimation on thermal limits, metabolic rate, heart rate, oxygen carrying capacity and plasma lactate levels in a highly eurythermal goby species, Gillichthys mirabilis, acclimated to 9oC, 19oC and 26oC for four weeks. Metabolic rate and heart rate measurements were made in fish at their acclimation temperature and when exposed an acute thermal stress. Metabolic rates and plasma lactate levels were also measured in fish recovering from an acute heat stress. Both resting metabolic rates and heart rates at their respective acclimation temperatures did not show a thermal compensatory response with acclimation and maintained elevated rates at warm temperatures. During recovery from an acute stress, only 26oC fish showed post-stress elevation in metabolic rate. Elevated routine and recovery metabolic rates at 26oC suggested an increased energetic cost associated with warm acclimation and when exposed to an acute heat stress; this increased energy demand is possibly to sustain an adequate cellular stress response at high temperatures. Fish acclimated at 19oC and 26oC were able to increase their upper thermal limit and onset of cardiac arrhythmia compared to 9oC-acclimated fish. These data illustrate the pronounced cardiac plasticity and associated phenotypic plasticity of this species. However, this capacity to induce an acclimatory response appears to decrease significantly at temperatures beyond 19oC in G. mirabilis. Chapter Two examined effects of acclimation on cardiac proteome in G. mirabilis acclimated to 9oC, 19oC and 26oC. Proteomic analysis revealed differential expression of proteins involved in cardiac energy metabolism, mitochondrial regulation, iron homeostasis, oxidative stress, cytoprotection against hypoxia, and cytoskeletal reorganization. Proteomic data coupled with in vitro enzyme assay data showed that cardiac energy metabolism, thus aerobic poise of cardiac tissues, is increased in 19oC-acclimated fish compared to 9oC and 26oC-acclimated fish. Overall findings from both Chapters One and Two illustrate that despite their capacity to tolerate a gradient of temperatures, Gillichthys mirabilis exhibit highest cardiac performance near ~19oC, a temperature close to their preferred temperature. Chapter Three investigates the effects of temperature acclimation on cardiorespiratory responses and cardiac and skeletal muscle energy metabolism in a highly stenothermal Antarctic notothenioid, Trematomus bernacchii. Acclimation had no effect on heart rates at resting conditions or the temperatures at which onset of cardiac arrhythmia occurred, suggesting lack of inducible thermal tolerance in cardiac performance in this fish. These data support the hypothesis that cardiac limitations may play a role in reduced thermal tolerance and thermal plasticity of T. bernacchii. Chapter Four examines the effects of acclimation on cardiac transcriptome of endothermic Pacific bluefin tuna Thunnus orientalis acclimated to 14oC, 20oC and 25oC. Overall data indicate that these fish have restored cellular homeostasis at 14oC, potentially optimizing bluefin tuna performance in colder oceans. In contrast, metabolic enzyme activity and gene expression data at 25oC suggest a decrease in total ATP production in cardiac cells, and reduced stress responses. Furthermore, at elevated temperatures cardiac tissues appear to be subjected to heightened oxidative stress and programmed cell death. Together, these data suggest a reduced cardiac performance at ecologically relevant warm temperatures for Pacific bluefin tuna.

Keywords: Biology.
Advisor: Somero George N. primary advisor. Thesis advisor
Gilly William advisor. Thesis advisor
Micheli Fiorenza advisor. Thesis advisor
Palumbi Stephen R. advisor. Thesis advisor