An official website of the United States government
ABSTRACT Respiratory plasticity is a beneficial response to chronic hypoxia in fish. Red drum, a teleost that commonly experiences hypoxia in the Gulf of Mexico, have shown respiratory plasticity following sublethal hypoxia exposure as juveniles, but implications of hypoxia exposure during development are unknown. We exposed red drum embryos to hypoxia (40% air saturation) or normoxia (100% air saturation) for 3 days post fertilization (dpf). This time frame encompasses hatch and exogenous feeding. At 3 dpf, there was no difference in survival or changes in size. After the 3-day hypoxia exposure, all larvae were moved and reared in common normoxic conditions. Fish were reared for ∼3 months and effects of the developmental hypoxia exposure on swim performance and whole-animal aerobic metabolism were measured. We used a cross design wherein fish from normoxia (N=24) were exercised in swim tunnels in both hypoxia (40%, n=12) and normoxia (100%, n=12) conditions, and likewise for hypoxia-exposed fish (n=10 in each group). Oxygen consumption, critical swim speed (Ucrit), critical oxygen threshold (Pcrit) and mitochondrial respiration were measured. Hypoxia-exposed fish had higher aerobic scope, maximum metabolic rate, and higher liver mitochondrial efficiency relative to control fish in normoxia. Interestingly, hypoxia-exposed fish showed increased hypoxia sensitivity (higher Pcrit) and recruited burst swimming at lower swim speeds relative to control fish. These data provide evidence that early hypoxia exposure leads to a complex response in later life.
more »
« less
The role of carbonic anhydrase-mediated tissue oxygen extraction in a marine teleost acclimated to hypoxia
With the growing prevalence of hypoxia (O2 levels ≤2 mg l−1) in aquatic and marine ecosystems, there is increasing interest in the adaptive mechanisms fish may employ to better their performance in stressful environments. Here, we investigated the contribution of a proposed strategy for enhancing tissue O2 extraction – plasma-accessible carbonic anhydrase (CA-IV) – under hypoxia in a species of estuarine fish (red drum, Sciaenops ocellatus) that thrives in fluctuating habitats. We predicted that hypoxia-acclimated fish would increase the prevalence of CA-IV in aerobically demanding tissues to confer more efficient tissue O2 extraction. Furthermore, we predicted the phenotypic changes to tissue O2 extraction that occur with hypoxia acclimation may improve respiratory and swim performance under 100% O2 conditions (i.e. normoxia) when compared with performance in fish that have not been acclimated to hypoxia. Interestingly, there were no significant differences in relative CA-IV mRNA expression, protein abundance or enzyme activity between the two treatments, suggesting CA-IV function is maintained under hypoxia. Likewise, respiratory performance of hypoxia-acclimated fish was similar to that of control fish when tested in normoxia. Critical swim speed (Ucrit) was significantly higher in hypoxia-acclimated fish but translated to marginal ecological benefits with an increase of ∼0.3 body lengths per second. Instead, hypoxia-acclimated fish may have relied more heavily on anaerobic metabolism during their swim trials, utilizing burst swimming 1.5 times longer than control fish. While the maintenance of CA-IV may still be an important contributor for hypoxia tolerance, our evidence suggests hypoxia-acclimated red drum are using other mechanisms to cope in an O2-depleted environment.
more »
« less
- PAR ID:
- 10499732
- Publisher / Repository:
- The Company of Biologists
- Date Published:
- Journal Name:
- Journal of Experimental Biology
- Volume:
- 225
- Issue:
- 21
- ISSN:
- 0022-0949
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
More Like this
-
-
null (Ed.)ABSTRACT Oxygen (O2) and carbon dioxide (CO2) transport are tightly coupled in many fishes as a result of the presence of Root effect hemoglobins (Hb), whereby reduced pH reduces O2 binding even at high O2 tensions. Red blood cell carbonic anhydrase (RBC CA) activity limits the rate of intracellular acidification, yet its role in O2 delivery has been downplayed. We developed an in vitro assay to manipulate RBC CA activity while measuring Hb-O2 offloading following a physiologically relevant CO2-induced acidification. RBC CA activity in red drum (Sciaenops ocellatus) was inhibited with ethoxzolamide by 53.7±0.5%, which prompted a significant reduction in O2 offloading rate by 54.3±5.4% (P=0.0206, two-tailed paired t-test; n=7). Conversely, a 2.03-fold increase in RBC CA activity prompted a 2.14-fold increase in O2 offloading rate (P<0.001, two-tailed paired t-test; n=8). This approximately 1:1 relationship between RBC CA activity and Hb-O2 offloading rate coincided with a similar allometric scaling exponent for RBC CA activity and maximum metabolic rate. Together, our data suggest that RBC CA is rate limiting for O2 delivery in red drum.more » « less
-
null (Ed.)Animals native to the hypoxic and cold environment at high altitude provide an excellent opportunity to elucidate the integrative mechanisms underlying the adaptive evolution and plasticity of complex traits. The capacity for aerobic thermogenesis can be a critical determinant of survival for small mammals at high altitude, but the physiological mechanisms underlying the evolution of this performance trait remain unresolved. We examined this issue by comparing high-altitude deer mice ( Peromyscus maniculatus ) with low-altitude deer mice and white-footed mice ( P. leucopus ). Mice were bred in captivity and adults were acclimated to each of four treatments: warm (25°C) normoxia, warm hypoxia (12 kPa O 2 ), cold (5°C) normoxia or cold hypoxia. Acclimation to hypoxia and/or cold increased thermogenic capacity in deer mice, but hypoxia acclimation led to much greater increases in thermogenic capacity in highlanders than in lowlanders. The high thermogenic capacity of highlanders was associated with increases in pulmonary O 2 extraction, arterial O 2 saturation, cardiac output and arterial–venous O 2 difference. Mechanisms underlying the evolution of enhanced thermogenic capacity in highlanders were partially distinct from those underlying the ancestral acclimation responses of lowlanders. Environmental adaptation has thus enhanced phenotypic plasticity and expanded the physiological toolkit for coping with the challenges at high altitude.more » « less
-
Abstract Hypoxia‐induced polymerization of sickle hemoglobin and the related ion diffusion across cell membrane can lead to changes in cell dielectric properties, which can potentially serve as label‐free, diagnostic biomarkers for sickle cell disease. This article presents a microfluidic‐based approach with on‐chip gas control for the impedance spectroscopy of suspended cells within the frequency range of 40 Hz to 110 MHz. A comprehensive bioimpedance of sickle cells under both normoxia and hypoxia is achieved rapidly (within ∼7 min) and is appropriated by small sample volumes (∼2.5 μL). Analysis of the sensing modeling is performed to obtain optimum conditions for dielectric spectroscopy of sickle cell suspensions and for extraction of single cell properties from the measured impedance spectra. The results of sickle cells show that upon hypoxia treatment, cell interior permittivity and conductivity increase, while cell membrane capacitance decreases. Moreover, the relative changes in cell dielectric parameters are found to be dependent on the sickle and fetal hemoglobin levels. In contrast, the changes in normal red blood cells between the hypoxia and normoxia states are unnoticeable. The results of sickle cells may serve as a reference to design dielectrophoresis‐based cell sorting and electrodeformation testing devices that require cell dielectric characteristics as input parameters. The demonstrated method for dielectric characterization of single cells from the impedance spectroscopy of cell suspensions can be potentially applied to other cell types and under varied gas conditions.more » « less
-
Neuroepithelial cells (NECs) within the fish gill contain the monoamine neurochemical serotonin (5-HT), sense changes in the partial pressure of oxygen (PO2) in the surrounding water and blood, and initiate the cardiovascular and ventilatory responses to hypoxia. The distribution of neuroepithelial cells (NECs) within the gill is known for some fish species but not for the Gulf toadfish, Opsanus beta, a fish that has always been considered hypoxia tolerant. Furthermore, whether NEC size, number, or distribution changes after chronic exposure to hypoxia, has never been tested. We hypothesize that toadfish NECs will respond to hypoxia with an increase in NEC size, number, and a change in distribution. Juvenile toadfish (N = 24) were exposed to either normoxia (21.4 ± 0.0 kPa), mild hypoxia (10.2 ± 0.3 kPa), or severe hypoxia (3.1 ± 0.2 kPa) for 7 days and NEC size, number, and distribution for each O2 regime were measured. Under normoxic conditions, juvenile toadfish have similar NEC size, number, and distribution as other fish species with NECs along their filaments but not throughout the lamellae. The distribution of NECs did not change with hypoxia exposure. Mild hypoxia exposure had no effect on NEC size or number, but fish exposed to severe hypoxia had a higher NEC density (# per mm filament) compared to mild hypoxia-exposed fish. Fish exposed to severe hypoxia also had longer gill filament lengths that could not be explained by body weight. These results point to signs of phenotypic plasticity in these juvenile, lab-bred fish with no previous exposure to hypoxia and a strategy to deal with hypoxia exposure that differs in toadfish compared to other fish.more » « less
- Free Publicly Accessible Full Text
-
Accepted Manuscript1.0
- Journal Article:
- https://doi.org/10.1242/jeb.244474
