Mitochondrial physiology and reactive oxygen species production are altered by hypoxia acclimation in killifish (Fundulus heteroclitus)

Abstract

Many fish encounter hypoxia in their native environment, but the role of mitochondrial physiology in hypoxia acclimation and hypoxia tolerance is poorly understood. We investigated the effects of hypoxia acclimation on mitochondrial respiration, O 2 kinetics, emission of reactive oxygen species (ROS), and antioxidant capacity in the estuarine killifish (Fundulus heteroclitus). Killifish were acclimated to normoxia, constant hypoxia (5 kPa O 2 ) or intermittent diel cycles of nocturnal hypoxia (12 h:12 h normoxia: hypoxia) for 28-33 days and mitochondria were isolated from liver. Neither pattern of hypoxia acclimation affected the respiratory capacities for oxidative phosphorylation or electron transport, leak respiration, coupling control or phosphorylation efficiency. Hypoxia acclimation also had no effect on mitochondrial O 2 kinetics, but P 50 (the O 2 tension at which hypoxia inhibits respiration by 50%) was lower in the leak state than during maximal respiration, and killifish mitochondria endured anoxia-reoxygenation without any impact on mitochondrial respiration. However, both patterns of hypoxia acclimation reduced the rate of ROS emission from mitochondria when compared at a common O 2 tension. Hypoxia acclimation also increased the levels of protein carbonyls and the activities of superoxide dismutase and catalase in liver tissue (the latter only occurred in constant hypoxia). Our results suggest that hypoxia acclimation is associated with changes in mitochondrial physiology that decrease ROS production and may help improve hypoxia tolerance.

Turtles maintain mitochondrial integrity but reduce mitochondrial respiratory capacity in the heart after cold-acclimation and anoxia

“…This suggests that inhibition of mitochondrial respiration rate contributes to metabolic depression with cold acclimation, and that this may be a key part of anoxia tolerance. Our results are also consistent with studies on isolated mitochondria from anoxic turtles (Bundgaard et al, 2018;Galli et al, 2013;Pamenter et al, 2016) as well as others on anoxia-tolerant animals exposed to hypoxia, such as frogs (St-Pierre et al, 2000b), killifish (Fundulus heteroclitus) (Du et al, 2016;Duerr and Podrabsky, 2010), epaulette sharks (Hemiscyllum ocellatum) and shovel-nosed rays (Aptychotrema rostrata) (Hickey et al, 2012). Inhibition of mitochondrial respiration rate is also central to the response to hypoxia in mammalian cells (Kim et al, 2006;Papandreou et al, 2006;Semenza, 2007).…”

The metabolic consequences of repeated anoxic stress in the western painted turtle, Chrysemys picta bellii

“…Among other ectothermic and endothermic vertebrate species, there are numerous examples of enhanced anaerobic performance in response to prolonged or repeated reliance on anaerobic metabolism, such as chronic and intermittent hypoxia and repeated sprint exercise (Hoppeler and Vogt, 2001;Pinder and Burggren, 1983) (Clanton and Klawitter, 2001) (Barnett et al, 2004;Borowiec et al, 2015;Du et al, 2016). These studies have demonstrated that many species have plasticity that improves physiological performance, either during or following the insult.…”

Developmental plasticity of mitochondrial function in American alligators,Alligator mississippiensis

“…In particular, structural and functional remodeling of the mitochondria has emerged as a critical component of hypoxic survival (24, 53, 55). Mitochondrial volume density has been observed to decrease with chronic hypoxia in a range of adult vertebrates, and this is often associated with large-scale reductions in ETC Complex activities and aerobic capacity (15, 21, 24, 25, 33, 34, 42, 55, 56). Mitochondrial efficiency can be improved by CIV subunit switching which maximizes the yield of ATP per oxygen molecule consumed and minimizes the production of harmful ROS (23).…”