Diel cycling hypoxia enhances hypoxia-tolerance in rainbow trout (<i>Oncorhynchus mykiss</i>): evidence of physiological and metabolic plasticity

Williams, Karen; Cassidy, Alicia A.; Verhille, Christine E.; Lamarre, Simon G.; MacCormack, Tyson J.

doi:10.1242/jeb.206045

Cited by 32 publications

(24 citation statements)

References 56 publications

(81 reference statements)

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“…Despite a cardiac output that was twice as high in the control relative to coronary-ligated trout immediately prior to P LOE , coronaryligated trout were only marginally less tolerant to acute hypoxia as their P LOE was only elevated by 0.6 kPa (∼3% air saturation). Moreover, the P crit for both treatment groups were within the range of previously reported values for rainbow trout (Williams et al, 2019;Wood, 2018), and while P crit was numerically slightly higher in the ligated fish (by 0.8 kPa), this was not statistically significant. Thus, it seems likely that the coronary-ligated fish initiated some response in hypoxia that compensated for the severely reduced capacity for circulatory O 2 delivery to the tissues, which in turn minimized the negative impacts of the coronary obstruction on overall hypoxia tolerance.…”

supporting

confidence: 82%

Coronary blood flow influences tolerance to environmental extremes in fish

Morgenroth

McArley

Gräns

et al. 2021

Journal of Experimental Biology

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Approximately half of all fishes have, in addition to the luminal venous O2 supply, a coronary circulation supplying the heart with fully oxygenated blood. Yet, it is not fully understood how coronary O2 delivery affects tolerance to environmental extremes such as warming and hypoxia. Hypoxia reduces arterial oxygenation, while warming increases overall tissue O2 demand. Thus, as both stressors are associated with reduced venous O2 supply to the heart, we hypothesised that coronary flow benefits hypoxia and warming tolerance. To test this hypothesis, we blocked coronary blood flow (via surgical coronary ligation) in rainbow trout (Oncorhynchus mykiss), and assessed how in vivo cardiorespiratory performance and whole-animal tolerance to acute hypoxia and warming was affected. While coronary ligation reduced routine stroke volume relative to trout with intact coronaries, cardiac output was maintained by increases in heart rate. However, in hypoxia, coronary ligated trout were unable to increase stroke volume to maintain cardiac output when bradycardia developed, which was associated with a slightly reduced hypoxia tolerance. Moreover, during acute warming coronary ligation caused cardiac function to collapse at lower temperatures, and reduced overall heat tolerance relative to trout with intact coronaries. We also found a positive relationship between individual hypoxia and heat tolerance across treatment groups, and tolerance to both environmental stressors was positively correlated with cardiac performance. Collectively, our findings show that coronary perfusion improves cardiac O2 supply, and therefore, cardiovascular function at environmental extremes, which benefits tolerance to natural and anthropogenically induced environmental perturbations.

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confidence: 82%

Coronary blood flow influences tolerance to environmental extremes in fish

Morgenroth

McArley

Gräns

et al. 2021

Journal of Experimental Biology

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“…There is limited information on the regulation of the mTOR pathway during hypoxia in fish. However, AMPK phosphorylation increased in goldfish and rainbow trout exposed to hypoxia, suggesting that the mTOR pathway should also be inhibited (Jibb and Richards, 2008;Williams et al, 2019). In mammals, there is also significant crosstalk between the three hypoxia-response pathways and each one (HIF, UPR or mTOR) can regulate the activity of one of the other pathways (Wouters and Koritzinsky, 2008).…”

Section: Introductionmentioning

confidence: 99%

Activation of oxygen-responsive pathways are associated with altered protein metabolism in Arctic char exposed to hypoxia

Cassidy

Lamarre

2019

Journal of Experimental Biology

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Fish exposed to fluctuating oxygen concentrations often alter their metabolism and/or behaviour to survive. Hypoxia tolerance is typically associated with the ability to reduce energy demand by supressing metabolic processes such as protein synthesis. Arctic char is amongst the most sensitive salmonid to hypoxia, and typically engage in avoidance behaviour when faced with lack of oxygen. We hypothesized that a sensitive species will still have the ability (albeit reduced) to regulate molecular mechanisms during hypoxia. We investigated the tissue-specific response of protein metabolism during hypoxia. Little is known about protein degradation pathways during hypoxia in fish and we predict that protein degradation pathways are differentially regulated and play a role in the hypoxia response. We also studied the regulation of oxygen-responsive cellular signalling pathways [hypoxia inducible factor (HIF), unfolded protein response (UPR) and mTOR pathways] since most of what we know comes from studies on cancerous mammalian cell lines. Arctic char were exposed to cumulative graded hypoxia trials for 3 h at four air saturation levels (100%, 50%, 30% and 15%). The rate of protein synthesis was measured using a flooding dose technique, whereas protein degradation and signalling pathways were assessed by measuring transcripts and phosphorylation of target proteins. Protein synthesis decreased in all tissues measured (liver, muscle, gill, digestive system) except for the heart. Salmonid hearts have preferential access to oxygen through a well-developed coronary artery, therefore the heart is likely to be the last tissue to become hypoxic. Autophagy markers were upregulated in the liver, whereas protein degradation markers were downregulated in the heart during hypoxia. Further work is needed to determine the effects of a decrease in protein degradation on a hypoxic salmonid heart. Our study showed that protein metabolism in Arctic char is altered in a tissue-specific fashion during graded hypoxia, which is in accordance with the responses of the three major hypoxia-sensitive pathways (HIF, UPR and mTOR). The activation pattern of these pathways and the cellular processes that are under their control varies greatly among tissues, sometimes even going in the opposite direction. This study provides new insights on the effects of hypoxia on protein metabolism. Adjustment of these cellular processes is likely to contribute to shifting the fish phenotype into a more hypoxia-tolerant one, if more than one hypoxia event were to occur. Our results warrant studying these adjustments in fish exposed to long-term and diel cycling hypoxia.

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“…The phosphorylation of this protein releases its inhibition on translation while its dephosphorylation deactivates protein synthesis. In a hypoxia sensitive species, the rainbow trout ( Oncorhynchus mykiss ), cardiac 4EBP1 phosphorylation is not affected by hypoxia (Williams et al, 2019). 4EBP1 therefore appears to be a key component in the downregulation of cardiac protein synthesis in the cichlid heart.…”

Section: Cichlid Heart Under Hypoxiamentioning

confidence: 99%

“…This situation presents great opportunity for conceptual advancement as it provides a natural and convenient experimental work platform in which to reveal “on‐off” switches and hypoxic recovery mechanisms. We have utilized this approach in the past (MacCormack et al, 2003a; MacCormack et al, 2006) with armoured catfish and have begun to examine the impact of diel O 2 cycling in hypoxia sensitive rainbow trout (Williams et al, 2019). The current paper suggests a number of experimental avenues that could provide step jumps in our understanding of the hypoxic response.…”

Section: Perspectives and Future Studiesmentioning

confidence: 99%

Contrasting strategies of hypoxic cardiac performance and metabolism in cichlids and armoured catfish

2021

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The heart of tropical fishes is a particularly useful model system in which to investigate mechanisms of hypoxic tolerance. Here we focus on insights gained from two groups of fishes, cichlids and armoured catfishes. Cichlids respond to hypoxia by entering a sustained hypometabolism with decreased heart performance to match whole animal circulatory needs. Heart rate is decreased along with protein turnover to reduce adenosine triphosphate demand. This occurs despite the inherent capacity for high levels of cardiac power development. Although highly hypoxic tolerant at the whole animal level, the heart of cichlids does not have high constitutive activities of glycolytic enzymes compared to other species. Information is conflicting with respect to changes in glycolytic gene expression and enzyme activity following hypoxic exposure with some studies showing increases and others decreases. In contrast to cichlids, species of armoured catfish, that are routinely exposed to water of low oxygen content, do not display hypoxic bradycardia. Under hypoxia there are early changes in glucose trafficking suggestive of activation of glycolysis before lactate accumulation. Thereafter, heart glycogen is mobilized and lactate accumulates in both heart and blood, in some species to very high levels. Heart performance under hypoxia is enhanced by defense of intracellular pH. A functional sarcoplasmic reticulum and binding of hexokinase to the outer mitochondrial membrane may also play a role in cardioprotection. Maintenance of heart performance under hypoxia may relate to a tradeoff between air breathing via a modified stomach and circulatory demands for digestion.

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Diel cycling hypoxia enhances hypoxia-tolerance in rainbow trout (Oncorhynchus mykiss): evidence of physiological and metabolic plasticity

Cited by 32 publications

References 56 publications

Coronary blood flow influences tolerance to environmental extremes in fish

Coronary blood flow influences tolerance to environmental extremes in fish

Activation of oxygen-responsive pathways are associated with altered protein metabolism in Arctic char exposed to hypoxia

Contrasting strategies of hypoxic cardiac performance and metabolism in cichlids and armoured catfish

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