Cardiac Hypoxia Tolerance in Fish: From Functional Responses to Cell Signals

Abstract

Aquatic animals are increasingly challenged by O₂ fluctuations as a result of global warming, as well as eutrophication processes. Teleost fish show important species-specific adaptability to O₂ deprivation, moving from intolerance to a full tolerance of hypoxia and even anoxia. An example is provided by members of Cyprinidae which includes species that are amongst the most tolerant hypoxia/anoxia teleosts. Living at low water O₂ requires the mandatory preservation of the cardiac function to support the metabolic and hemodynamic requirements of organ and tissues which sustain whole organism performance. A number of orchestrated events, from metabolism to behavior, converge to shape the heart response to the restricted availability of the gas, also limiting the potential damages for cells and tissues. In cyprinids, the heart is extraordinarily able to activate peculiar strategies of functional preservation. Accordingly, by using these teleosts as models of tolerance to low O₂, we will synthesize and discuss literature data to describe the functional changes, and the major molecular events that allow the heart of these fish to sustain adaptability to O₂ deprivation. By crossing the boundaries of basic research and environmental physiology, this information may be of interest also in a translational perspective, and in the context of conservative physiology, in which the output of the research is applicable to environmental management and decision making.

Keywords: contractility; cyprinids; fish heart; metabolism; nitric oxide.

Figure 1

Model for alternative routes of pyruvate metabolism in the Carassius auratus heart. In the presence of O₂, pyruvate from glycolysis is converted to acetyl-CoA and addressed to mitochondria for the oxidative phosphorylation. Under hypoxia, a tight modulation of glycolysis enzymes may finely regulate anaerobic ATP production by modulating glycolytic vs. gluconeogenic flux. Pyruvate conversion to ethanol is reduced by a low cardiac expression of alternative PDHC sub-units (see the text for details). A hypoxia-dependent modulation of mitochondria dynamics in relation to the exposure time is proposed. HK: hexokinase; Aldo B: aldolase B; PDHC: pyruvate dehydrogenase complex.

Figure 2

Schematic overview of the NOS/NO-mediated intracellular pathways activated in goldfish cardiomyocytes under hypoxic stress. For details, see the text.