Distinct metabolic adjustments arise from acclimation to constant hypoxia and intermittent hypoxia in estuarine killifish (Fundulus heteroclitus)

Abstract

Many fish experience daily cycles of hypoxia in the wild, but the physiological strategies for coping with intermittent hypoxia are poorly understood. We examined how killifish adjust O 2 supply and demand during acute hypoxia, and how these responses are altered after prolonged acclimation to constant or intermittent patterns of hypoxia exposure. We acclimated killifish to normoxia (∼20 kPa O 2), constant hypoxia (2 kPa) or intermittent cycles of nocturnal hypoxia (12 h:12 h normoxia:hypoxia) for 28 days, and then compared whole-animal O 2 consumption rates (Ṁ O2) and tissue metabolites during exposure to 12 h of hypoxia followed by reoxygenation in normoxia. Normoxiaacclimated fish experienced a pronounced 27% drop in Ṁ O2 during acute hypoxia, and modestly increased Ṁ O2 upon reoxygenation. They strongly recruited anaerobic metabolism during acute hypoxia, indicated by lactate accumulation in plasma, muscle, liver, brain, heart and digestive tract, as well as a transient drop in intracellular pH, and they increased hypoxia inducible factor (HIF)-1α protein abundance in muscle. Glycogen, glucose and glucose-6-phosphate levels suggested that glycogen supported brain metabolism in hypoxia, while the muscle used circulating glucose. Acclimation to constant hypoxia caused a stable ∼50% decrease in Ṁ O2 that persisted after reoxygenation, with minimal recruitment of anaerobic metabolism, suggestive of metabolic depression. By contrast, fish acclimated to intermittent hypoxia maintained sufficient O 2 transport to support normoxic Ṁ O2 , modestly recruited lactate metabolism and increased Ṁ O2 dramatically upon reoxygenation. Both groups of hypoxia-acclimated fish had similar glycogen, ATP, intracellular pH and HIF-1α levels as normoxic controls. We conclude that different patterns of hypoxia exposure favour distinct strategies for matching O 2 supply and O 2 demand.

Loss of hypoxia-inducible factor 1α affects hypoxia tolerance in larval and adult zebrafish (Danio rerio)

“…The mechanisms contributing to the decrease in P crit in response to this particular hypoxia regimen does not appear to be linked to the Hif-1α pathway. The specific strategies fish employ to cope with hypoxia is dependent on the type of hypoxia stress [36,41]. In keeping with this paradigm, the impact of Hif-1α knockout on the aspects of the O 2 cascade that are altered to enhance O 2 uptake appears to differ in larval zebrafish depending on the duration and/or magnitude of hypoxic stress.…”

Interspecific variation in hypoxia tolerance and hypoxia acclimation responses in killifish from the family Fundulidae

“…Considerable variation in physiological tolerance of environmental stressors occurs across this family, and even closely related sister taxa can have very different tolerances (Griffith, 1974;Nordlie, 2006;Whitehead, 2010;Whitehead et al, 2013), making Fundulidae a particularly useful model for evolutionary physiology (Burnett et al, 2007). Fundulus heteroclitus exhibits significant plasticity to chronic hypoxia (Borowiec et al, 2015(Borowiec et al, , 2018Du et al, 2016;Martinez et al, 2006) as well as intraspecific variation in hypoxia tolerance (McBryan et al, 2016), but it is unclear how hypoxia tolerance and its plasticity vary across the family. Therefore, our first two objectives were to characterize (i) the interspecific variation in hypoxia tolerance across Fundulidae and (ii) whether there is interspecific variation in the plasticity of hypoxia tolerance in response to chronic hypoxia.…”

Warming waters beget smaller fish: evidence for reduced size and altered morphology in a desert fish following anthropogenic temperature change

“…Measurements of dissolved O 2 (DO) in Tecopa Bore between 2014 and 2016 indicate DO is considerably lower in Tecopa Bore (1.82-3.63 mg l −1 ; 25.8-40.8% saturation) than in the Amargosa River (6.32-11.85 mg l −1 ; 62.6-68.6%). While it is not known if DO conditions changed in Tecopa Bore between 2008 and 2013-2014, or if consistent exposure to low DO alone can induce the development of morphological traits mirroring those observed for pupfish in Tecopa Bore, it is well established that hypoxia can depress metabolic rate [38] and increase the expression of less-efficient metabolic pathways involving anaerobic enzymes such as lactate dehydrogenase (LDH) [39,40], with responses varying both with hypoxia duration and taxonomically [41,42]. Muscle LDH activity measured in pupfish collected from Tecopa Bore in 2014 was approximately 2× higher than in conspecifics from the Amargosa River, suggesting heightened anaerobic capacity [43].…”