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Data from: Calorespirometry reveals that goldfish prioritize aerobic metabolism over metabolic rate depression in all but near-anoxic environments
Regan, Matthew D.; Gill, Ivan; Richards, Jeffrey G. — 2016-11-22 Metabolic rate depression (MRD) has long been proposed as the key metabolic strategy of hypoxic survival, but surprisingly the effects of changes in hypoxic O2 tensions (PwO2) on MRD are largely unexplored. We simultaneously measured the O2 consumption rate (ṀO2) and metabolic heat of goldfish using calorespirometry to test the hypothesis that MRD is employed at hypoxic PwO2s and initiated just below Pcrit, the PwO2 below which ṀO2 is forced to progressively decline as the fish oxyconforms to decreasing PwO2. Specifically, we used closed-chamber and flow-through calorespirometry together with terminal sampling experiments to examine the effects of PwO2 and time on ṀO2, metabolic heat and anaerobic metabolism (lactate and ethanol production). The closed-chamber and flow-through experiments yielded slightly different results. Under closed-chamber conditions with a continually decreasing PwO2, goldfish showed a Pcrit of 3.0±0.3 kPa and metabolic heat production was only depressed at PwO2 between 0 and 0.67 kPa. Under flow-through conditions with PwO2 held at a variety of oxygen tensions for 1 and 4 h, goldfish also initiated MRD between 0 and 0.67 kPa but maintained ṀO2 to 0.67 kPa, indicating that Pcrit is at or below this PwO2. Anaerobic metabolism was strongly activated at PwO2 ≤1.3 kPa, but only used within the first hour at 1.3 and 0.67 kPa as anaerobic end-products did not accumulate between 1 and 4 h exposure. Taken together, it appears that goldfish reserve MRD for near-anoxia, supporting routine metabolic rate at sub-Pcrit PwO2s with the help of anaerobic glycolysis in the closed-chamber experiments, and aerobically after an initial (<1 h) activation of anaerobic metabolism in the flow-through experiments, even at 0.67 kPa PwO2. https://creativecommons.org/publicdomain/zero/1.0/
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Data from: Divergent transcriptional patterns are related to differences in hypoxia tolerance between the intertidal and the subtidal sculpins
Mandic, Milica; Ramon, Marina L.; Gracey, Andrew Y.; Richards, Jeffrey G. — 2014-11-19 Transcriptionally mediated phenotypic plasticity as a mechanism of modifying traits in response to an environmental challenge remains an important area of study. We compared the transcriptional responses to low-oxygen (hypoxia) of the hypoxia tolerant intertidal fish, the tidepool sculpin (Oligocottus maculosus) with the closely related hypoxia intolerant subtidal fish, the silverspotted sculpin (Blepsias cirrhosus) to determine if these species use different mechanisms to cope with hypoxia. Individuals from each species were exposed to environmental O2 tensions chosen to yield a similar level of tissue hypoxia and gene transcription was assessed in the liver over time. There was an effect of time in hypoxia, where the greatest transcriptional change in the silverspotted sculpin occurred between 3 to 24 hours in contrast to the tidepool sculpin where the largest transcriptional change occurred between 24 and 72 hours of hypoxia. A number of genes showed similar hypoxia-induced transcription patterns in both species (e.g. genes associated with glycolysis and apoptosis) suggesting they are involved in a conserved hypoxia response. A large set of genes showed divergent transcriptional patterns in the two species, including fatty acid oxidation and oxidative phosphorylation, suggesting that these biological processes may contribute to explaining variation in hypoxia tolerance in these species. When both species were exposed to a single environmental O2 tension, large transcriptional responses were seen in the hypoxia intolerant silverspotted sculpin while almost no response was observed in the hypoxia tolerant tidepool sculpin. Overall, divergent transcription patterns in response to both magnitude and duration of hypoxia provide insights into the processes that may determine an animal's capacity to tolerate frequent bouts of hypoxia in the wild.
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Data from: Rates of hypoxia induction alter mechanisms of O2 uptake and the critical O2 tension of goldfish
Regan, Matthew D.; Richards, Jeffrey G. — 2017-05-03 The rate of hypoxia induction (RHI) is an important but overlooked dimension of environmental hypoxia that may affect an organism’s survival. We hypothesized that, compared with rapid RHI, gradual RHI will afford an organism more time to alter plastic phenotypes associated with O2 uptake and subsequently reduce the critical O2 tension (Pcrit) of O2 uptake rate (ṀO2). We investigated this by determining Pcrit values for goldfish exposed to short (∼24 min), typical (∼84 min) and long (∼480 min) duration Pcrit trials to represent different RHIs. Consistent with our predictions, long duration Pcrit trials yielded significantly lower Pcrit values (1.0-1.4 kPa) than short and typical duration trials, which did not differ (2.6±0.3 and 2.5±0.2 kPa, respectively). Parallel experiments revealed these time-related shifts in Pcrit were associated with changes in aspects of the O2 transport cascade: gill surface areas and haemoglobin-O2 binding affinities were significantly higher in fish exposed to gradual RHIs over 480 min than fish exposed to rapid RHIs over 60 min. Our results also revealed that the choice of respirometric technique (i.e., closed versus intermittent) does not affect Pcrit or routine ṀO2, despite the significantly reduced water pH and elevated CO2 and ammonia levels measured following closed-circuit Pcrit trials of ∼90 min. Together, our results demonstrate that gradual RHIs result in alterations to physiological parameters that enhance O2 uptake in hypoxic environments. An organism’s innate Pcrit is therefore most accurately determined using rapid RHIs (<90 min) so as to avoid the confounding effects of hypoxic acclimation.
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Data from: Metabolic depression and the evolution of hypoxia tolerance in threespine stickleback, Gasterosteus aculeatus
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Regan, Matthew D.; Gill, Ivan S.; Richards, Jeffrey G. — 2017-10-12 Anthropogenic increases in global temperature and agricultural runoff are increasing the prevalence of aquatic hypoxia throughout the world. We investigated the potential for a relatively rapid evolution of hypoxia tolerance using two isolated (for less than 11 000 years) populations of threespine stickleback: one from a lake that experiences long-term hypoxia (Alta Lake, British Columbia) and one from a lake that does not (Trout Lake, British Columbia). Loss-of-equilibrium (LOE) experiments revealed that the Alta Lake stickleback were significantly more tolerant of hypoxia than the Trout Lake stickleback, and calorimetry experiments revealed that the enhanced tolerance of Alta Lake stickleback may be associated with their ability to depress metabolic rate (as indicated by metabolic heat production) by 33% in hypoxia. The two populations showed little variation in their capacities for O2 extraction and anaerobic metabolism. These results reveal that intraspecific variation in hypoxia tolerance can develop over relatively short geological timescales, as can metabolic rate depression, a complex biochemical response that may be favoured in long-term hypoxic environments.
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Data from: Migration, mitochondria, and the yellow-rumped warbler
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Toews, David P. L.; Mandic, Milica; Richards, Jeffrey G.; Irwin, Darren E. — 2013-08-19 Discordance between mitochondrial and nuclear DNA has been noted in many systems. Asymmetric introgression of mitochondria is a common cause of such discordances, although in most cases the drivers of introgression are unknown. In the yellow-rumped warbler, evidence suggests that mtDNA from the eastern, myrtle warbler, has introgressed across much of the range of the western form, the Audubon's warbler. Within the southwestern United States myrtle mtDNA comes into contact with another clade that occurs in the Mexican black-fronted warbler. Both northern forms exhibit seasonal migration, whereas black-fronted warblers are nonmigratory. We investigated the link between mitochondrial introgression, mitochondrial function, and migration using novel genetic, isotopic, biochemical, and phenotypic data obtained from populations in the transition zone. Isotopes suggest the zone is coincident with a shift in migration, with individuals in the south being resident and populations further north becoming increasingly more migratory. Mitochondrial respiration in flight muscles demonstrates that myrtle-type individuals have a significantly greater acceptor control ratio of mitochondria, suggesting it may be more metabolically efficient. To our knowledge this is the first time this type of intraspecific variation in mitochondrial respiration has been measured in wild birds and we discuss how such mitochondrial adaptations may have facilitated introgression.
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Data from: Mitochondrial responses to prolonged anoxia in brain of Red-eared slider turtles
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Pamenter, Matthew E.; Gomez, Crisostomo R.; Richards, Jeffrey G.; Milsom, William K. — 2015-12-17 Mitochondria are central to aerobic energy production and play a key role in neuronal signalling. During anoxia, however, the mitochondria of most vertebrates initiate deleterious cell death cascades. Nonetheless, a handful of vertebrate species, including some freshwater turtles, are remarkably tolerant of low oxygen environments and survive months of anoxia without apparent damage to brain tissue. This tolerance suggests that mitochondria in the brains of such species are adapted to withstand prolonged anoxia, but little is known about potential neuroprotective responses. In this study, we address such mechanisms by comparing mitochondrial function between brain tissues isolated from cold-acclimated red-eared slider turtles (Trachemys scripta elegans) exposed to two weeks of either normoxia or anoxia. We found that brain mitochondria from anoxia-acclimated turtles exhibited a unique phenotype of remodelling relative to normoxic controls, including: (i) decreased citrate synthase and F1FO-ATPase activity but maintained protein content, (ii) markedly reduced aerobic capacity, and (iii) mild uncoupling of the mitochondrial proton gradient. These data suggest that turtle brain mitochondria respond to low oxygen stress with a unique suite of changes tailored towards neuroprotection.

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(auteur : Richards, Jeffrey G.)

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