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Haemoglobin (Hb)-O2 binding affinity typically decreases with increasing temperature, but several species of ectothermic and regionally endothermic fishes exhibit reduced Hb thermal sensitivity. Regionally endothermic sharks, including the common thresher shark (Alopias vulpinus) and lamnid sharks such as the shortfin mako shark (Isurus oxyrinchus), can maintain select tissues and organs warmer than ambient temperature by retaining metabolic heat with vascular heat exchangers. In the ectothermic bigeye thresher shark (Alopias superciliosus), diurnal movements above and below the thermocline subject the tissues, including the blood, to a wide range of operating temperatures. Therefore, blood-O2 transport must occur across internal temperature gradients in regionally endothermic species, and over the range of environmental temperatures encountered by the ectothermic bigeye thresher shark. While previous studies have shown temperature-independent Hb-O2 affinity in lamnid sharks, including shortfin mako, the Hb-O2 affinity of the common and bigeye thresher sharks is unknown. Therefore, we examined the effect of temperature on whole-blood Hb-O2 affinity in common thresher shark and bigeye thresher shark. For comparison, analyses were also conducted on the shortfin mako shark and two ectothermic species, blue shark (Prionace glauca) and spiny dogfish (Squalus acanthias). Blood-O2 binding affinity was temperature independent for common thresher shark and shortfin mako shark, which should prevent internal temperature gradients from negatively affecting blood-O2 transport. Blue shark and spiny dogfish blood-O2 affinity decreased with increasing temperature, as expected, but bigeye thresher shark blood exhibited both a reduced temperature dependence and a high Hb-O2 affinity, which likely prevents large changes in environment temperature and low environmental oxygen from affecting O2 uptake.
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Tiburones , Animales , Temperatura , Tiburones/metabolismo , Oxígeno/metabolismo , Regulación de la Temperatura Corporal , Transporte BiológicoRESUMEN
Smalleye Pacific opah and swordfish can conserve metabolic heat and maintain specific body regions warmer than ambient water temperature (i.e. regional heterothermy). Consequently, blood O2 uptake at the gills occurs at the environmental temperature at which the individual is found, but O2 offloading will occur at different temperatures in different tissues. While several regionally heterothermic fishes (e.g. billfishes, tunas and sharks) show a reduced temperature effect on haemoglobin (Hb)-O2 affinity, the temperature dependence of Hb-O2 affinity in opah and swordfish is unknown. We hypothesized that the Hb of opah and swordfish would also show a reduced temperature dependence. Opah whole-blood-O2 affinity exhibited a reverse temperature dependence above 50% Hb-O2 saturation (10-20°C, pH 7.2-8.0), while the temperature dependence of swordfish blood-O2 affinity (10-25°C) was saturation and pH dependent, becoming temperature independent below 50% Hb-O2 saturation and pH 7.4. Experiments on stripped haemolysates showed that adding ATP ([ATP]/[Hb]=30) decreased the temperature sensitivity of Hb-O2 affinity, changing the overall oxygenation enthalpy (ΔH') values of opah (10-20°C) and swordfish (10-25°C) Hbs at pH 7.4 from -15 and -42â kJâ mol-1 O2, respectively, to +84 and -9â kJâ mol-1 O2. Swordfish blood-O2 affinity was high compared with that of other large, pelagic, marine teleosts, which may be the result of unusually low ATP/Hb levels, but might also enable swordfish to forage in the potentially low-oxygenated water of the upper reaches of the oxygen minimum layer. The existence of Hbs with reduced temperature sensitivity in regionally heterothermic fishes may prevent marked changes in Hb-O2 affinity between the cold and warm tissues.
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Hemoglobinas , Perciformes , Adenosina Trifosfato , Animales , Peces/metabolismo , Hemoglobinas/metabolismo , Oxígeno/metabolismo , Perciformes/metabolismo , Temperatura , AguaRESUMEN
BACKGROUND: Viruses can impose energetic demands on organisms they infect, in part by hosts mounting resistance. Recognizing that oxygen uptake reliably indicates steady-state energy consumption in all vertebrates, we comprehensively evaluated oxygen uptake and select transcriptomic messaging in sockeye salmon challenged with either a virulent rhabdovirus (IHNV) or a low-virulent reovirus (PRV). We tested three hypotheses relating to the energetic costs of viral resistance and tolerance in this vertebrate system: (1) mounting resistance incurs a metabolic cost or limitation, (2) induction of the innate antiviral interferon system compromises homeostasis, and (3) antiviral defenses are weakened by acute stress. RESULTS: IHNV infections either produced mortality within 1-4 weeks or the survivors cleared infections within 1-9 weeks. Transcription of three interferon-stimulated genes (ISGs) was strongly correlated with IHNV load but not respiratory performance. Instead, early IHNV resistance was associated with a mean 19% (95% CI = 7-31%; p = 0.003) reduction in standard metabolic rate. The stress of exhaustive exercise did not increase IHNV transcript loads, but elevated host inflammatory transcriptional signaling up to sevenfold. For PRV, sockeye tolerated high-load systemic PRV blood infections. ISG transcription was transiently induced at peak PRV loads without associated morbidity, microscopic lesions, or major changes in aerobic or anaerobic respiratory performance, but some individuals with high-load blood infections experienced a transient, minor reduction in hemoglobin concentration and increased duration of excess post-exercise oxygen consumption. CONCLUSIONS: Contrary to our first hypothesis, effective resistance against life-threatening rhabdovirus infections or tolerance to high-load reovirus infections incurred minimal metabolic costs to salmon. Even robust systemic activation of the interferon system did not levy an allostatic load sufficient to compromise host homeostasis or respiratory performance, rejecting our second hypothesis that this ancient innate vertebrate antiviral defense is itself energetically expensive. Lastly, an acute stress experienced during testing did not weaken host antiviral defenses sufficiently to promote viral replication; however, a possibility for disease intensification contingent upon underlying inflammation was indicated. These data cumulatively demonstrate that fundamental innate vertebrate defense strategies against potentially life-threatening viral exposure impose limited putative costs on concurrent aerobic or energetic demands of the organism.
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Enfermedades de los Peces , Animales , Antivirales , Humanos , Virus de la Necrosis Hematopoyética Infecciosa , Interferones , Oxígeno , SalmónRESUMEN
Thermal dependence of growth and metabolism can influence thermal preference and tolerance in marine ectotherms, including threatened and data-deficient species. Here, we quantified the thermal dependence of physiological performance in neonates of a tropical shark species (blacktip reef shark, Carcharhinus melanopterus) from shallow, nearshore habitats. We measured minimum and maximum oxygen uptake rates (MO2 ), calculated aerobic scope, excess post-exercise oxygen consumption and recovery from exercise, and measured critical thermal maxima (CTmax), thermal safety margins, hypoxia tolerance, specific growth rates, body condition and food conversion efficiencies at two ecologically relevant acclimation temperatures (28 and 31°C). Owing to high post-exercise mortality, a third acclimation temperature (33°C) was not investigated further. Acclimation temperature did not affect MO2 or growth, but CTmax and hypoxia tolerance were greatest at 31°C and positively associated. We also quantified in vitro temperature (25, 30 and 35°C) and pH effects on haemoglobin-oxygen (Hb-O2) affinity of wild-caught, non-acclimated sharks. As expected, Hb-O2 affinity decreased with increasing temperatures, but pH effects observed at 30°C were absent at 25 and 35°C. Finally, we logged body temperatures of free-ranging sharks and determined that C. melanopterus neonates avoided 31°C in situ We conclude that C. melanopterus neonates demonstrate minimal thermal dependence of whole-organism physiological performance across a seasonal temperature range and may use behaviour to avoid unfavourable environmental temperatures. The association between thermal tolerance and hypoxia tolerance suggests a common mechanism warranting further investigation. Future research should explore the consequences of ocean warming, especially in nearshore, tropical species.
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Consumo de Oxígeno , Tiburones , Aclimatación , Animales , Hipoxia , Oxígeno , TemperaturaRESUMEN
Climate change-induced warming effects are already evident in river ecosystems, and projected increases in temperature will continue to amplify stress on fish communities. In addition, many rivers globally are impacted by dams, which have many negative effects on fishes by altering flow, blocking fish passage, and changing sediment composition. However, in some systems, dams present an opportunity to manage river temperature through regulated releases of cooler water. For example, there is a government mandate for Kenney dam operators in the Nechako river, British Columbia, Canada, to maintain river temperature <20°C in July and August to protect migrating sockeye salmon (Oncorhynchus nerka). However, there is another endangered fish species inhabiting the same river, Nechako white sturgeon (Acipenser transmontanus), and it is unclear if these current temperature regulations, or timing of the regulations, are suitable for spawning and developing sturgeon. In this study, we aimed to identify upper thermal thresholds in white sturgeon embryos and larvae to investigate if exposure to current river temperatures are playing a role in recruitment failure. We incubated embryos and yolk-sac larvae in three environmentally relevant temperatures (14, 18 and 21°C) throughout development to identify thermal thresholds across different levels of biological organization. Our results demonstrate upper thermal thresholds at 21°C across physiological measurements in embryo and yolk-sac larvae white sturgeon. Before hatch, both embryo survival and metabolic rate were reduced at 21°C. After hatch, sublethal consequences continued at 21°C because larval sturgeon had decreased thermal plasticity and a dampened transcriptional response during development. In recent years, the Nechako river has reached 21°C by the end of June, and at this temperature, a decrease in sturgeon performance is evident in most of the traits measured. As such, the thermal thresholds identified here suggest current temperature regulations may not be suitable for developing white sturgeon and future recruitment.
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The extinct Steller's sea cow (Hydrodamalis gigas; 1768) was a whale-sized marine mammal that manifested profound morphological specializations to exploit the harsh coastal climate of the North Pacific. Yet despite first-hand accounts of their biology, little is known regarding the physiological adjustments underlying their evolution to this environment. Here, the adult-expressed hemoglobin (Hb; α2ß/δ2) of this sirenian is shown to harbor a fixed amino acid replacement at an otherwise invariant position (ß/δ82LysâAsn) that alters multiple aspects of Hb function. First, our functional characterization of recombinant sirenian Hb proteins demonstrates that the Hb-O2 affinity of this sub-Arctic species was less affected by temperature than those of living (sub)tropical sea cows. This phenotype presumably safeguarded O2 delivery to cool peripheral tissues and largely arises from a reduced intrinsic temperature sensitivity of the H. gigas protein. Additional experiments on H. gigas ß/δ82AsnâLys mutant Hb further reveal this exchange renders Steller's sea cow Hb unresponsive to the potent intraerythrocytic allosteric effector 2,3-diphosphoglycerate, a radical modification that is the first documented example of this phenotype among mammals. Notably, ß/δ82LysâAsn moreover underlies the secondary evolution of a reduced blood-O2 affinity phenotype that would have promoted heightened tissue and maternal/fetal O2 delivery. This conclusion is bolstered by analyses of two Steller's sea cow prenatal Hb proteins (Hb Gower I; ζ2ε2 and HbF; α2γ2) that suggest an exclusive embryonic stage expression pattern, and reveal uncommon replacements in H. gigas HbF (γ38ThrâIle and γ101GluâAsp) that increased Hb-O2 affinity relative to dugong HbF. Finally, the ß/δ82LysâAsn replacement of the adult/fetal protein is shown to increase protein solubility, which may have elevated red blood cell Hb content within both the adult and fetal circulations and contributed to meeting the elevated metabolic (thermoregulatory) requirements and fetal growth rates associated with this species cold adaptation.
In 1741, shipwrecked naturalist Georg Wilhelm Steller made detailed observations of large marine mammals grazing on seaweed in the shallow waters surrounding a remote island in the North Pacific Ocean. Within thirty years, these 'Steller's sea cows' had been hunted to extinction. Unlike their remaining tropical relatives dugongs and manatees Steller's sea cows were specialized to cold, sub-Arctic environments. Measuring up to 10 meters long, they were much larger than other sea cow species. This, along with having very thick skin, helped them to reduce heat loss. Previous work showed that the hemoglobin protein which binds to and carries oxygen around mammalian bodies of Steller's sea cows had a decreased affinity for oxygen, resulting in greater delivery of oxygen to organs and tissues. It was thought that this could be an adaptation to fuel heightened metabolic heat production in cold conditions. Studies of ancient DNA also identified the substitution of a single building block in the Steller's sea cow hemoglobin protein that is not present in other mammals and was suspected to underlie this modification. To determine how this unique substitution affects Steller's sea cow hemoglobin function and whether it contributed to their ability to live in cold environments Signore et al. generated hemoglobin proteins of Steller's sea cows, dugongs and Florida manatees. Testing their biochemical properties showed that this single exchange profoundly alters multiple aspects of how the Steller's sea cow hemoglobin works. Alongside reducing hemoglobin's oxygen affinity, the Steller's sea cow substitution also makes the protein more soluble, potentially increasing the level of hemoglobin within red blood cells. Additionally, it eliminates hemoglobin sensitivity to a molecule involved in oxygen binding known as DPG saving energy by no longer requiring production of this molecule. Furthermore, the same substitution makes hemoglobin less sensitive to changes in temperature, which would have helped to safeguard the delivery of oxygen to cool limbs and other extremities, reducing costly heat loss. Together, these changes in hemoglobin would have helped the Steller's sea cow to more efficiently transport oxygen around the body. Importantly, generating and testing Steller's sea cow pre-natal hemoglobins suggested this substitution may have also helped to enhance the fetal growth rate of these immense marine mammals by improving gas exchange between the mother and fetus. Signore et al. have revealed how a mutated form of hemoglobin allowed an extinct mammal to adapt to an extreme environment. Similar methods could be used to understand the physiological attributes of other extinct animals. In the future, this increased understanding of hemoglobin mutations could aid the development of human hemoglobin substitutes for therapeutic uses.
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Dugong , Animales , Mamíferos , Hemoglobinas/genética , Clima , OxígenoRESUMEN
The prevalence and intensity of the trematode, Otodistomum hydrolagi, were determined for the first time in Spotted Ratfish, Hydrolagus colliei. Spotted Ratfish specimens were collected during bottom-trawl surveys in Queen Charlotte Sound (QCS, n = 31) and off the west coast of Vancouver Island (WCVI, n = 242). In all instances, the flukes were found within the abdominal cavity. Most flukes were mature (intrauterine eggs were present) and ranged in length from 9.1 to 61.5 mm, with a mean ± SD length of 28.5 ± 12.1 mm (n = 52). Fluke length was positively correlated with Spotted Ratfish precaudal length (PCL), and no Spotted Ratfish smaller than 247-mm PCL was infected by O. hydrolagi. The overall prevalence (95% confidence interval [CI]) and mean intensity (95% CI) of O. hydrolagi were 27.8% (22.6-33.6) and 1.24 (1.09-1.43), respectively. Neither prevalence nor mean intensity differed between host location or host sex. The majority (86%) of infected hosts harbored a single fluke (range 1-5), but 4 Spotted Ratfish were infected with 3 or more flukes, which accounted for 16% of all observed O. hydrolagi. The fluke population exhibited an aggregated distribution with 80% of individuals found in 21% of the hosts, but among infected hosts there was low variability in the intensity of infection. This is the first ecological study of O. hydrolagi from its Spotted Ratfish host, and the first record of this trematode in Canadian waters, which extends the range of O. hydrolagi to include Canadian coastal Pacific waters.
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Enfermedades de los Peces/epidemiología , Enfermedades de los Peces/parasitología , Trematodos/crecimiento & desarrollo , Infecciones por Trematodos/veterinaria , Cavidad Abdominal/parasitología , Animales , Colombia Británica/epidemiología , Femenino , Peces , Masculino , Océano Pacífico , Prevalencia , Infecciones por Trematodos/epidemiología , Infecciones por Trematodos/parasitologíaRESUMEN
The recent ubiquitous detection of PRV among salmonids has sparked international concern about the cardiorespiratory performance of infected wild and farmed salmon. Piscine orthoreovirus (PRV) has been shown to create substantial viremia in salmon by targeting erythrocytes for principle replication. In some instances, infections develop into heart and skeletal muscle inflammation (HSMI) or other pathological conditions affecting the respiratory system. Critical to assessing the seriousness of PRV infections are controlled infection studies that measure physiological impairment to critical life support systems. Respiratory performance is such a system and here multiple indices were measured to test the hypothesis that a low-virulence strain of PRV from Pacific Canada compromises the cardiorespiratory capabilities of Atlantic salmon. Contrary to this hypothesis, the oxygen affinity and carrying capacity of erythrocytes were unaffected by PRV despite the presence of severe viremia, minor heart pathology and transient cellular activation of antiviral response pathways. Similarly, PRV-infected fish had neither sustained nor appreciable differences in respiratory capabilities compared with control fish. The lack of functional harm to salmon infected with PRV in this instance highlights that, in an era of unprecedented virus discovery, detection of viral infection does not necessarily imply bodily harm and that viral load is not always a suitable predictor of disease within a host organism.
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[This corrects the article DOI: 10.3389/fphys.2019.00114.].
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Recent findings indicate that some teleost fishes may be able to greatly enhance hemoglobin-oxygen (Hb-O2) unloading at the tissues under conditions that result in catecholamine release. The putative mechanism relies on the high pH sensitivity of teleost hemoglobin (Hb), intracellular red blood cell (RBC) pH regulation via ß-adrenergic Na+/H+ exchanger (ß-NHE) activity, and plasma-accessible carbonic anhydrase at the tissues that short-circuits RBC pH regulation. Previous studies have shown that in rainbow trout, this system may double Hb-O2 unloading to red muscle compared to a situation without short-circuiting. The present study determined that: (1) in rainbow trout this system may be functional even at low concentrations of circulating catecholamines, as shown by conducting a dose-response analysis; (2) Atlantic and coho salmon also possess ß-NHE activity, as shown by changes in hematocrit in adrenergically stimulated cells; and (3) with ß-NHE short-circuiting, Atlantic and coho salmon may be able to increase Hb-O2 unloading by up to 74 and 159%, respectively, as determined by modeling based on O2 equilibrium curves. Together, these results indicate that a system to enhance Hb-O2 unloading may be common among salmonids and may be operational even under routine conditions. In view of the life histories of Atlantic and coho salmon, a system to enhance Hb-O2 unloading during exercise may help determine a successful spawning migration and thus reproductive success.
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Hemoglobinas/metabolismo , Oncorhynchus mykiss/metabolismo , Oxígeno/metabolismo , Salmón/metabolismo , Agonistas Adrenérgicos beta/farmacología , Migración Animal , Animales , Isoproterenol/farmacología , Intercambiadores de Sodio-Hidrógeno/metabolismoRESUMEN
Hemoglobin (Hb) multiplicity is common in fish, yet despite its ubiquitous nature, the functional significance is unclear. Here we explore the hypothesis that Hb multiplicity plays a role in hypoxia tolerance using the red drum (Sciaenops ocellatus). Red drum is an economically and ecologically important species native to coastal regions and estuaries of the Gulf of Mexico - habitats that routinely experience pronounced hypoxic events. Using a transcriptomic approach, we demonstrate that red drum red blood cells express 7 and 5 Hbα and Hbß isoforms, respectively. Phylogenetic analysis grouped these isoforms into distinct isoHb clades, and provided evidence of lineage specific expression of particular isoHbs. In normoxia, three isoHbs predominated (Hbα-3.1, -3.2, and Hbß-3.1). A three-week hypoxia acclimation (48 mmHg) resulted in significant up-regulation of Hbα-2, Hbα-3.2, and Hbß-3.1, effectively switching the predominantly expressed isoforms. Changes in subunit expression were correlated with a decrease in non-stripped hemolysate P50. Similarly, hypoxia acclimation resulted in a 20% reduction in whole animal critical oxygen threshold (Pcrit). Hypoxia acclimation was not associated with changes in gill morphology, hematocrit, or relative ventricular mass. Overall, these data provide support for the hypothesis that Hb isoform switching can provide a physiological benefit to counteract environmental stress in fishes.