RESUMEN
Warming in the region of the Western Antarctic Peninsula is occurring at an unprecedented rate, which may threaten the survival of Antarctic notothenioid fishes. Herein, we review studies characterizing thermal tolerance and cardiac performance in notothenioids - a group that includes both red-blooded species and the white-blooded, haemoglobinless icefishes - as well as the relevant biochemistry associated with cardiac failure during an acute temperature ramp. Because icefishes do not feed in captivity, making long-term acclimation studies unfeasible, we focus only on the responses of red-blooded notothenioids to warm acclimation. With acute warming, hearts of the white-blooded icefish Chaenocephalus aceratus display persistent arrhythmia at a lower temperature (8°C) compared with those of the red-blooded Notothenia coriiceps (14°C). When compared with the icefish, the enhanced cardiac performance of N. coriiceps during warming is associated with greater aerobic capacity, higher ATP levels, less oxidative damage and enhanced membrane integrity. Cardiac performance can be improved in N. coriiceps with warm acclimation to 5°C for 6-9â weeks, accompanied by an increase in the temperature at which cardiac failure occurs. Also, both cardiac mitochondrial and microsomal membranes are remodelled in response to warm acclimation in N. coriiceps, displaying homeoviscous adaptation. Overall, cardiac performance in N. coriiceps is malleable and resilient to warming, yet thermal tolerance and plasticity vary among different species of notothenioid fishes; disruptions to the Antarctic ecosystem driven by climate warming and other anthropogenic activities endanger the survival of notothenioids, warranting greater protection afforded by an expansion of marine protected areas.
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Ecosistema , Perciformes , Animales , Regiones Antárticas , Peces , CorazónRESUMEN
We tested the hypothesis that blackfin icefish (Chaenocephalus aceratus), one of the six species in the family Channichthyidae (the icefishes) that do not express haemoglobin and myoglobin, lack regulatory cardiovascular flexibility during acute warming and activity. The experimental protocols were designed to optimize the surgical protocol and minimize stress. First, minimally invasive heart rate (fH) measurements were made during a thermal ramp until cardiac failure in C. aceratus and compared with those from the closely related red-blooded black rockcod (Notothenia coriiceps). Then, integrative cardiovascular adjustments were more extensively studied using flow probes and intravascular catheters in C. aceratus during acute warming (from 0 to 8°C) at rest and after imposed activity. Chaenocephalus aceratus had a lower routine fH than N. coriiceps (9 beats min-1 versus 14 beats min-1) and a lower peak fH during acute warming (38 beats min-1 versus 55 beats min-1) with a similar cardiac breakpoint temperature (13 and 14°C, respectively). Routine cardiac output (QÌ) for C. aceratus at â¼0°C was much lower (26.6â mlâ min-1 kg-1) than previously reported, probably because fish in the present study had a low fH (12 beats min-1) indicative of a high routine vagal tone and low stress. Chaenocephalus aceratus increased oxygen consumption during acute warming and with activity. Correspondingly, QÌ increased considerably (maximally 86.3â mlâ min-1 kg-1), as did vascular conductance (5-fold). Thus, unlike earlier suggestions, these data provide convincing evidence that icefish can mount a well-developed cardiovascular regulation of heart rate, cardiac output and vascular conductance, and this regulatory capacity provides flexibility during acute warming.
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Fenómenos Fisiológicos Cardiovasculares , Calor/efectos adversos , Perciformes/fisiología , Animales , Regiones Antárticas , Gasto Cardíaco/fisiología , Sistema Cardiovascular/fisiopatología , Frecuencia Cardíaca/fisiología , Consumo de Oxígeno/fisiologíaRESUMEN
Studies in temperate fishes provide evidence that cardiac mitochondrial function and the capacity to fuel cardiac work contribute to thermal tolerance. Here, we tested the hypothesis that decreased cardiac aerobic metabolic capacity contributes to the lower thermal tolerance of the haemoglobinless Antarctic icefish, Chaenocephalus aceratus, compared with that of the red-blooded Antarctic species, Notothenia coriiceps. Maximal activities of citrate synthase (CS) and lactate dehydrogenase (LDH), respiration rates of isolated mitochondria, adenylate levels and changes in mitochondrial protein expression were quantified from hearts of animals held at ambient temperature or exposed to their critical thermal maximum (CTmax). Compared with C. aceratus, activity of CS, ATP concentration and energy charge were higher in hearts of N. coriiceps at ambient temperature and CTmax While state 3 mitochondrial respiration rates were not impaired by exposure to CTmax in either species, state 4 rates, indicative of proton leakage, increased following exposure to CTmax in C. aceratus but not N. coriiceps The interactive effect of temperature and species resulted in an increase in antioxidants and aerobic metabolic enzymes in N. coriiceps but not in C. aceratus Together, our results support the hypothesis that the lower aerobic metabolic capacity of C. aceratus hearts contributes to its low thermal tolerance.
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Calor , Mitocondrias Cardíacas/metabolismo , Perciformes/metabolismo , Adenosina Trifosfato/metabolismo , Animales , Regiones Antárticas , Citrato (si)-Sintasa/metabolismo , L-Lactato Deshidrogenasa/metabolismo , Miocardio/enzimología , Miocardio/metabolismoRESUMEN
The unusual pattern of expression of hemoglobin (Hb) and myoglobin (Mb) among Antarctic notothenioid fishes provides an exceptional model system for assessing the impact of these proteins on oxidative stress. We tested the hypothesis that the lack of oxygen-binding proteins may reduce oxidative stress. Levels and activity of pro-oxidants and small-molecule and enzymatic antioxidants, and levels of oxidized lipids and proteins in the liver, oxidative skeletal muscle and heart ventricle were quantified in five species of notothenioid fishes differing in the expression of Hb and Mb. Levels of ubiquitinated proteins and rates of protein degradation by the 20S proteasome were also quantified. Although levels of oxidized proteins and lipids, ubiquitinated proteins, and antioxidants were higher in red-blooded fishes than in Hb-less icefishes in some tissues, this pattern did not persist across all tissues. Expression of Mb was not associated with oxidative damage in the heart ventricle, whereas the activity of citrate synthase and the contents of heme were positively correlated with oxidative damage in most tissues. Despite some tissue differences in levels of protein carbonyls among species, rates of degradation by the 20S proteasome were not markedly different, suggesting either alternative pathways for eliminating oxidized proteins or that redox tone varies among species. Together, our data indicate that the loss of Hb and Mb does not correspond with a clear pattern of either reduced oxidative defense or oxidative damage.
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Hemoglobinas/metabolismo , Mioglobina/metabolismo , Estrés Oxidativo/fisiología , Perciformes/fisiología , Adaptación Fisiológica , Animales , Regiones Antárticas , Antioxidantes , Proteínas de Peces/metabolismo , Hemoglobinas/genética , Mioglobina/genética , Complejo de la Endopetidasa Proteasomal/metabolismo , Especies Reactivas de OxígenoRESUMEN
The family Channichthyidae or "icefishes" (suborder Notothenioidei) represents the only vertebrates lacking hemoglobin (Hb) as adults. Several icefish species also do not express cardiac myoglobin (Mb). We address how levels of proteins involved in iron (Fe) processing (transport, sequestration, and export) vary among white- and red-blooded notothenioids, and whether absence of Hb and/or Mb in channichthyids is accompanied by expansion of contents of Fe-binding proteins to protect against unchaperoned Fe. Levels of transferrin (Tf), ferritin (Ft), ceruloplasmin (Cp), and non-heme Fe were quantified in plasma, serum, and/or nonhematopoietic tissues (cardiac ventricle, skeletal muscle, and liver) from species of white-blooded (Chaenocephalus aceratus, Champsocephalus gunnari, Chionodraco rastrospinosus, Pseudochaenichthys georgianus) (the first two species not expressing Mb) and red-blooded (Notothenia coriiceps, Gobionotothen gibberifrons) notothenioids. We also measured levels of ascorbate (Asc), a mediator of Fe uptake. While plasma concentrations of Tf and tissue levels of Asc are similar among species, concentrations of plasma Asc are lower in white-blooded species. Concentrations of Ft and non-heme Fe and activities of Cp are also generally reduced in icefishes compared with red-blooded notothenioids. The presence of cardiac Mb in some icefish species does not appear to influence levels of proteins involved in Fe processing. To address further the question of Fe sequestration within a physiological context, we account for well-characterized differences in blood volume and heart mass among white- and red-blooded notothenioids. We report that total contents of plasma Tf are greater, while ventricle non-heme Fe is at least at parity in white- vs. red-blooded species.
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Ferritinas/metabolismo , Peces/anatomía & histología , Peces/metabolismo , Corazón/anatomía & histología , Hierro/metabolismo , Miocardio/metabolismo , Animales , Regiones Antárticas , Transporte Biológico Activo , Volumen de Eritrocitos , Peces/clasificación , Hemoglobinas/metabolismo , Mioglobina/metabolismo , Tamaño de los Órganos , Volumen Plasmático , Especificidad de la EspecieRESUMEN
Changes in oxidative capacities and phospholipid remodeling accompany temperature acclimation in ectothermic animals. Both responses may alter redox status and membrane susceptibility to lipid peroxidation (LPO). We tested the hypothesis that phospholipid remodeling is sufficient to offset temperature-driven rates of LPO and, thus, membrane susceptibility to LPO is conserved. We also predicted that the content of LPO products is maintained over a range of physiological temperatures. To assess LPO susceptibility, rates of LPO were quantified with the fluorescent probe C11-BODIPY in mitochondria and sarcoplasmic reticulum from oxidative and glycolytic muscle of striped bass (Morone saxatilis) acclimated to 7°C and 25°C. We also measured phospholipid compositions, contents of LPO products [i.e., individual classes of phospholipid hydroperoxides (PLOOH)], and two membrane antioxidants. Despite phospholipid headgroup and acyl chain remodeling, these alterations do not counter the effect of temperature on LPO rates (i.e., LPO rates are generally not different among acclimation groups when normalized to phospholipid content and compared at a common temperature). Although absolute levels of PLOOH are higher in muscles from cold- than warm-acclimated fish, this difference is lost when PLOOH levels are normalized to total phospholipid. Contents of vitamin E and two homologs of ubiquinone are more than four times higher in mitochondria prepared from oxidative muscle of warm- than cold-acclimated fish. Collectively, our data demonstrate that although phospholipid remodeling does not provide a means for offsetting thermal effects on rates of LPO, differences in phospholipid quantity ensure a constant proportion of LPO products with temperature variation.
Asunto(s)
Aclimatación , Lubina/metabolismo , Membrana Celular/metabolismo , Peroxidación de Lípido , Músculo Esquelético/metabolismo , Estrés Oxidativo , Temperatura , Animales , Membrana Celular/patología , Glucólisis , Cinética , Peróxidos Lipídicos/metabolismo , Mitocondrias Musculares/metabolismo , Músculo Esquelético/patología , Oxidación-Reducción , Fosfolípidos/metabolismo , Retículo Sarcoplasmático/metabolismo , Ubiquinona/análogos & derivados , Ubiquinona/metabolismo , Vitamina E/metabolismoRESUMEN
Cold temperature generally induces an enhancement of oxidative capacities, a greater content of intracellular lipids, and a remodeling of lipids in biological membranes. These physiological responses may pose a heightened risk of lipid peroxidation (LPO), while warm temperature could result in greater risk of LPO since rates involving reactive oxygen species and LPO will be elevated. The current study examines responses of the glutathione system of antioxidant defense after temperature acclimation. We measured total glutathione (tGSH), and protein levels of GPx1, GPx4, and GST (cardiac and skeletal muscles), and enzymatic activity (skeletal muscle) of glutathione-dependent antioxidants (GPx, GPx4, and GST) in tissues from striped bass (Morone saxatilis) acclimated for six weeks to 7 °C or 25 °C. tGSH of cardiac muscle from cold-acclimated animals was 1.2-times higher than in warm-bodied counterparts, but unchanged with temperature acclimation in skeletal muscle. A second low molecular weight antioxidant, ascorbate was 1.4- and 1.5-times higher in cardiac and skeletal muscle, respectively in warm- than cold-acclimated animals. Despite 1.2-times higher oxidative capacities (as indicated by citrate synthase activity), in skeletal muscle from cold- versus warm-acclimated fish, levels and activities of antioxidant enzymes were similar between acclimation groups. Lipid peroxidation products (as indicated by TBARS), normalized to tissue wet weight, were more than 2-times higher in skeletal muscle from cold- than warm-acclimated animals, however, when normalized to phospholipid content there was no statistical difference between acclimation groups. Our results demonstrate that the physiological changes, associated with acclimation to low temperature in the eurythermal striped bass, are not accompanied by an enhanced antioxidant defense in the glutathione-dependent system.
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Lubina , Glutatión/metabolismo , Músculo Esquelético , Miocardio/metabolismo , Aclimatación/fisiología , Animales , Antioxidantes/metabolismo , Antioxidantes/fisiología , Lubina/metabolismo , Lubina/fisiología , Frío , Glutatión/fisiología , Peroxidación de Lípido/fisiología , Redes y Vías Metabólicas/fisiología , Músculo Esquelético/metabolismo , Músculo Esquelético/fisiología , Oxidación-Reducción , Especies Reactivas de Oxígeno/metabolismoRESUMEN
Antarctic icefishes have a significantly lower critical thermal maximum (CT(max)) compared with most red-blooded notothenioid fishes. We hypothesized that the lower thermal tolerance of icefishes compared with red-blooded notothenioids may stem from a greater vulnerability to oxidative stress as temperature increases. Oxidative muscles of icefishes have high volume densities of mitochondria, rich in polyunsaturated fatty acids, which can promote the production of reactive oxygen species (ROS). Moreover, icefishes have lower levels of antioxidants compared with red-blooded species. To test our hypothesis, we measured levels of oxidized proteins and lipids, and transcript levels and maximal activities of antioxidants in heart ventricle and oxidative pectoral adductor muscle of icefishes and red-blooded notothenioids held at 0°C and exposed to their CT(max). Levels of oxidized proteins and lipids increased in heart ventricle of some icefishes but not in red-blooded species in response to warming, and not in pectoral adductor muscle of any species. Thus, increases in oxidative damage in heart ventricles may contribute to the reduced thermal tolerance of icefishes. Despite an increase in oxidative damage in hearts of icefishes, neither transcript levels nor activities of antioxidants increased, nor did they increase in any tissue of any species in response to exposure to CT(max). Rather, transcript levels of the enzyme superoxide dismutase (SOD) decreased in hearts of icefishes and the activity of SOD decreased in hearts of the red-blooded species Gobionotothen gibberifrons. These data suggest that notothenioids may have lost the ability to elevate levels of antioxidants in response to heat stress.
Asunto(s)
Antioxidantes/metabolismo , Ventrículos Cardíacos/metabolismo , Estrés Oxidativo , Perciformes/fisiología , Especies Reactivas de Oxígeno/metabolismo , Animales , Regiones Antárticas , Catalasa/genética , Catalasa/metabolismo , Proteínas de Peces/genética , Proteínas de Peces/metabolismo , Calor , Mitocondrias Cardíacas/enzimología , Mitocondrias Cardíacas/metabolismo , Oxidación-Reducción , Músculos Pectorales/metabolismo , Factor 1 de Elongación Peptídica/genética , Factor 1 de Elongación Peptídica/metabolismo , Superóxido Dismutasa/genética , Superóxido Dismutasa/metabolismoRESUMEN
The Southern Ocean surrounding the Western Antarctic Peninsula region is rapidly warming. Survival of members of the dominant suborder of Antarctic fishes, the Notothenioidei, will likely require thermal plasticity and adaptive capacity in key traits delimiting thermal tolerance. Herein, we have assessed the thermal plasticity of several cellular and biochemical pathways, many of which are known to be associated with thermal tolerance in notothenioids, including mitochondrial function, activities of aerobic and anaerobic enzymes, antioxidant defences, protein ubiquitination and degradation in cardiac, oxidative skeletal muscles and gill of Notothenia coriiceps warm acclimated to 4°C for 22 days or 5°C for 42 days. Levels of triacylglycerol (TAG) were measured in liver and oxidative and glycolytic skeletal muscles, and glycogen in liver and glycolytic muscle to assess changes in energy stores. Metabolic pathways displayed minimal thermal plasticity, yet antioxidant defences were lower in heart and oxidative skeletal muscles of warm-acclimated animals compared with animals held at ambient temperature. Despite higher metabolic rates at elevated temperature, energy storage depots of TAG and glycogen increase in liver and remain unchanged in muscle with warm acclimation. Overall, our studies reveal that N. coriiceps displays thermal plasticity in some key traits that may contribute to their survival as the Southern Ocean continues to warm.
RESUMEN
Biological membranes can be protected from lipid peroxidation by antioxidant enzymes including catalase (CAT) and selenium-dependent glutathione peroxidases 1 and 4 (GPx1 and GPx4). Unlike GPx1, GPx4 can directly detoxify lipid hydroperoxides in membranes without prior action of phospholipase A(2). We hypothesized that (1) GPx4 is enhanced in species that contain elevated levels of highly oxidizable polyunsaturated fatty acids (PUFA) and (2) activities of antioxidant enzymes are prioritized to meet species-specific oxidative stresses. In this study we examined (i) activities of the oxidative enzyme citrate synthase (CS) and antioxidant (CAT, GPx1 and GPx4) enzymes, (ii) GPx4 protein expression, and (iii) phospholipid composition in livers of five species of marine fish (Myxine glutinosa, Petromyzon marinus, Squalus acanthias, Fundulus heteroclitus and Myoxocephalus octodecemspinosus) that contain a range of PUFA. GPx4 activity was, on average, 5.8 times higher in F. heteroclitus and S. acanthias than in the other three marine fish species sampled. Similarly, activities of CAT and GPx1 were highest in S. acanthias and F. heteroclitus, respectively. GPx4 activity for all species correlates with membrane unsaturation, as well as oxidative activity as indicated by CS. These data support our hypothesis that GPx4 level in marine fish is a function, at least in part, of high PUFA content in these animals. GPx1 activity was also correlated with membrane unsaturation, indicating that marine species partition resources among glutathione-dependent defenses for protection from the initial oxidative insult (e.g. H(2)O(2)) and to repair damaged lipids within biological membranes.
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Antioxidantes/metabolismo , Ácidos Grasos/metabolismo , Proteínas de Peces/metabolismo , Peces/metabolismo , Glutatión Peroxidasa/metabolismo , Animales , Catalasa/metabolismo , Membrana Celular/metabolismo , Citrato (si)-Sintasa/metabolismo , Ácidos Grasos Insaturados/metabolismo , Oxidación-ReducciónRESUMEN
It is unknown whether Antarctic fishes can defend themselves against oxidative stress induced by elevations in temperature. We hypothesized that Antarctic icefishes, lacking the oxygen-binding protein hemoglobin, might be more vulnerable to temperature-induced oxidative stress compared with red-blooded notothenioids because of differences in their mitochondrial properties. Mitochondria from icefishes have higher densities of phospholipids per mg of mitochondrial protein compared with red-blooded species, and these phospholipids are rich in polyunsaturated fatty acids (PUFA), which can promote the formation of reactive oxygen species (ROS). Additionally, previous studies have shown that multiple tissues in icefishes have lower levels of antioxidants compared with red-blooded species. We quantified several properties of mitochondria, including proton leak, rates of ROS production, membrane composition and susceptibility to lipid peroxidation (LPO), the activity of superoxide dismutase (SOD) and total antioxidant power (TAOP) in mitochondria isolated from hearts of icefishes and red-blooded notothenioids. Mitochondria from icefishes were more tightly coupled than those of red-blooded fishes at both 2°C and 10°C, which increased the production of ROS when the electron transport chain was disrupted. The activity of SOD and TAOP per mg of mitochondrial protein was equivalent between icefishes and red-blooded species, but TAOP normalized to mitochondrial phospholipid content was significantly lower in icefishes compared with red-blooded fishes. Additionally, membrane susceptibility to peroxidation was only detectable in icefishes at 1°C and not in red-blooded species. Together, our results suggest that the high density of mitochondrial phospholipids in hearts of icefishes may make them particularly vulnerable to oxidative stress as temperatures rise.
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Peces/metabolismo , Mitocondrias/metabolismo , Estrés Oxidativo , Animales , Regiones Antárticas , Proteínas de Peces/metabolismo , Peroxidación de Lípido , Especies Reactivas de Oxígeno/metabolismo , Superóxido Dismutasa/metabolismoRESUMEN
As temperatures continue to rise, adjustments to biological membranes will be key for maintenance of function. It is largely unknown to what extent Antarctic notothenioids possess the capacity to remodel their biological membranes in response to thermal change. In this study, physical and biochemical properties were examined in membranes prepared from gill epithelia (plasma membranes), cardiac ventricles (microsomes, mitochondria), and brains (synaptic membranes, myelin, mitochondria) from Notothenia coriiceps following acclimation to 5 °C (or held at ambient temperature, 0 °C) for a minimum of 6 weeks. Fluidity was measured between 0 and 30 °C in all membranes, and polar lipid compositions and cholesterol contents were analyzed in a subset of biological membranes from all tissues. Osmotic permeability was measured in gills at 0 and 4 °C. Gill plasma membranes, cardiac mitochondria, and cardiac microsomes displayed reduced fluidity following acclimation to 5 °C, indicating compensation for elevated temperature. In contrast, no fluidity changes with acclimation were observed in any of the membranes prepared from brain. In all membranes, adjustments to the relative abundances of major phospholipid classes, and to the extent of fatty acid unsaturation, were undetectable following thermal acclimation. However, alterations in cholesterol contents and acyl chain length, consistent with the changes in fluidity, were observed in membranes from gill and cardiac tissue. Water permeability was reduced with 5 °C acclimation in gills, indicating near-perfect homeostatic efficacy. Taken together, these results demonstrate a homeoviscous response in gill and cardiac membranes, and limited plasticity in membranes from the nervous system, in an Antarctic notothenioid.
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Branquias , Perciformes , Aclimatación , Animales , Regiones Antárticas , Encéfalo , Membrana Celular , TemperaturaRESUMEN
Antarctic notothenioids are noted for extreme stenothermy, yet underpinnings of their thermal limits are not fully understood. We hypothesized that properties of ventricular membranes could explain previously observed differences among notothenioids in temperature onset of cardiac arrhythmias and persistent asystole. Microsomes were prepared using ventricles from six species of notothenioids, including four species from the hemoglobin-less (Hb-) family Channichthyidae (icefishes), which also differentially express cardiac myoglobin (Mb), and two species from the (Hb+) Nototheniidae. We determined membrane fluidity and structural integrity by quantifying fluorescence depolarization of 1,6-diphenyl-1,3,5-hexatriene (DPH) and leakage of 5(6)-carboxyfluorescein, respectively, over a temperature range from ambient (0 °C) to 20 °C. Compositions of membrane phospholipids and cholesterol contents were also quantified. Membranes from all four species of icefishes exhibited greater fluidity than membranes from the red-blooded species N. coriiceps. Thermal sensitivity of fluidity did not vary among species. The greatest thermal sensitivity to leakage occurred between 0 and 5 °C for all species, while membranes from the icefish, Chaenocephalus aceratus (Hb-/Mb-) displayed leakage that was nearly 1.5-fold greater than leakage in N. coriiceps (Hb+/Mb+). Contents of phosphatidylethanolamine (PE) were approximately 1.5-fold greater in icefishes than in red-blooded fishes, and phospholipids had a higher degree of unsaturation in icefishes than in Hb + notothenioids. Cholesterol contents were lowest in Champsocephalus gunnari (Hb-/Mb-) and highest in the two Hb+/Mb + species, G. gibberifrons and N. coriiceps. Our results reveal marked differences in membrane properties and indicate a breach in membrane fluidity and structural integrity at a lower temperature in icefishes than in red-blooded notothenioids.
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Membrana Celular/metabolismo , Proteínas de Peces/metabolismo , Corazón/fisiología , Hemoglobinas/metabolismo , Mioglobina/metabolismo , Perciformes/metabolismo , Adaptación Fisiológica , Animales , Regiones Antárticas , Fluidez de la Membrana , TemperaturaAsunto(s)
Adaptación Fisiológica , Conservación de los Recursos Naturales , Explotaciones Pesqueras/ética , Peces/fisiología , Hemoglobinas/deficiencia , Animales , Regiones Antárticas , Evolución Biológica , Cambio Climático , Frío , Explotaciones Pesqueras/legislación & jurisprudencia , Industria de Alimentos/legislación & jurisprudencia , Humanos , Océanos y MaresRESUMEN
Disruption of neuronal function is likely to influence limits to thermal tolerance. We hypothesized that with acute warming the structure and function of neuronal membranes in the Antarctic notothenioid fish Chaenocephalus aceratus are more vulnerable to perturbation than membranes in the more thermotolerant notothenioid Notothenia coriiceps. Fluidity was quantified in synaptic membranes, mitochondrial membranes, and myelin from brains of both species of Antarctic fishes. Polar lipid compositions and cholesterol contents were analyzed in myelin; cholesterol was measured in synaptic membranes. Thermal profiles were determined for activities of two membrane-associated proteins, acetylcholinesterase (AChE) and Na+/K+-ATPase (NKA), from brains of animals maintained at ambient temperature or exposed to their critical thermal maxima (CTMAX). Synaptic membranes of C. aceratus were consistently more fluid than those of N. coriiceps (P < 0.0001). Although the fluidities of both myelin and mitochondrial membranes were similar among species, sensitivity of myelin fluidity to in vitro warming was greater in N. coriiceps than in C. aceratus (P < 0.001), which can be explained by lower cholesterol contents in myelin of N. coriiceps (P < 0.05). Activities of both enzymes, AChE and NKA, declined upon CTMAX exposure in C. aceratus, but not in N. coriiceps. We suggest that hyper-fluidization of synaptic membranes with warming in C. aceratus may explain the greater stenothermy in this species, and that thermal limits in notothenioids are more likely to be influenced by perturbations in synaptic membranes than in other membranes of the nervous system.
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Membranas Mitocondriales/fisiología , Vaina de Mielina/fisiología , Neuronas/fisiología , Perciformes/fisiología , Membranas Sinápticas/fisiología , Termotolerancia/fisiología , Animales , Regiones Antárticas , Fluidez de la Membrana , Especificidad de la Especie , TemperaturaRESUMEN
Antarctic notothenioid fishes are highly stenothermal, yet their tolerance for warming is species-dependent. Because a body of literature points to the loss of cardiac function as underlying thermal limits in ectothermic animals, we investigated potential relationships among properties of ventricular mitochondrial membranes in notothenioids with known differences in both cardiac mitochondrial metabolism and organismal thermal tolerance. Fluidity of mitochondrial membranes was quantified by fluorescence depolarization for the white-blooded Chaenocephalus aceratus and the red-blooded Notothenia coriiceps. In these same membranes, lipid compositions and products of lipid peroxidation, the latter of which can disrupt membrane order, were analyzed in both species and in a second icefish, Pseudochaenichthys georgianus. Mitochondrial membranes from C. aceratus were significantly more fluid than those of the more thermotolerant species N. coriiceps (Pâ¯<â¯.0001). Consistent with this, ratios of total phosphatidylethanolamine (PE) to total phosphatidylcholine (PC) were lower in membranes from both species of icefishes, compared to those of N. coriiceps (Pâ¯<â¯.05). However, membranes of N. coriiceps displayed a greater unsaturation index (Pâ¯<â¯.0001). No differences among species were found in membrane products of lipid peroxidation. With rising temperatures, greater contents of PC in mitochondrial membranes from ventricles of icefishes are likely to promote membrane hyperfluidization at a lower temperature than for cardiac mitochondrial membranes from the red-blooded notothenioid. We propose that physical and chemical properties of the mitochondrial membranes may contribute to some of the observed differences in thermal sensitivity of physiological function among these species.
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Lípidos de la Membrana/metabolismo , Miocardio/metabolismo , Perciformes/metabolismo , Fosfolípidos/metabolismo , Animales , Regiones Antárticas , Calentamiento Global , Peroxidación de Lípido , Fluidez de la Membrana , Lípidos de la Membrana/química , Membranas Mitocondriales/metabolismo , Fosfolípidos/química , Especificidad de la Especie , TermotoleranciaRESUMEN
Antarctic notothenioids, some of which lack myoglobin (Mb) and/or haemoglobin (Hb), are considered extremely stenothermal, which raises conservation concerns since Polar regions are warming at unprecedented rates. Without reliable estimates of maximum cardiac output ([Formula: see text]), it is impossible to assess their physiological scope in response to warming seas. Therefore, we compared cardiac performance of two icefish species, Chionodraco rastrospinosus (Hb-Mb+) and Chaenocephalus aceratus (Hb-Mb-), with a related notothenioid, Notothenia coriiceps (Hb+Mb+) using an in situ perfused heart preparation. The maximum [Formula: see text], heart rate (f H), maximum cardiac work (W C) and relative ventricular mass of N. coriiceps at 1°C were comparable to temperate-water teleosts, and acute warming to 4°C increased f H and W C, as expected. In contrast, icefish hearts accommodated a higher maximum stroke volume (V S) and maximum [Formula: see text] at 1°C, but their unusually large hearts had a lower f H and maximum afterload tolerance than N. coriiceps at 1°C. Furthermore, maximum V S, maximum [Formula: see text] and f H were all significantly higher for the Hb-Mb+ condition compared with the Hb-Mb- condition, a potential selective advantage when coping with environmental warming. Like N. coriiceps, both icefish species increased f H at 4°C. Acutely warming C. aceratus increased maximum [Formula: see text], while C. rastrospinosus (like N. coriiceps) held at 4°C for 1 week maintained maximum [Formula: see text] when tested at 4°C. These experiments involving short-term warming should be followed up with long-term acclimation studies, since the maximum cardiac performance of these three Antarctic species studied seem to be tolerant of temperatures in excess of predictions associated with global warming.
RESUMEN
The Southern Ocean has experienced stable, cold temperatures for over 10 million years, yet particular regions are currently undergoing rapid warming. To investigate the impacts of warming on cardiovascular oxygen transport, we compared the cardio-respiratory performance in an Antarctic notothenioid (Notothenia coriiceps) that was maintained at 0 or 5°C for 6.0-9.5 weeks. When compared at the fish's respective acclimation temperature, the oxygen consumption rate and cardiac output were significantly higher in 5°C-acclimated than 0°C-acclimated fish. The 2.7-fold elevation in cardiac output in 5°C-acclimated fish (17.4 vs. 6.5 ml min-1 kg-1) was predominantly due to a doubling of stroke volume, likely in response to increased cardiac preload, as measured by higher central venous pressure (0.15 vs. 0.08 kPa); tachycardia was minor (29.5 vs. 25.2 beats min-1). When fish were acutely warmed, oxygen consumption rate increased by similar amounts in 0°C- and 5°C-acclimated fish at equivalent test temperatures. In both acclimation groups, the increases in oxygen consumption rate during acute heating were supported by increased cardiac output achieved by elevating heart rate, while stroke volume changed relatively little. Cardiac output was similar between both acclimation groups until 12°C when cardiac output became significantly higher in 5°C-acclimated fish, driven largely by their higher stroke volume. Although cardiac arrhythmias developed at a similar temperature (~14.5°C) in both acclimation groups, the hearts of 5°C-acclimated fish continued to pump until significantly higher temperatures (CTmax for cardiac function 17.7 vs. 15.0°C for 0°C-acclimated fish). These results demonstrate that N. coriiceps is capable of increasing routine cardiac output during both acute and chronic warming, although the mechanisms are different (heart rate-dependent versus primarily stroke volume-dependent regulation, respectively). Cardiac performance was enhanced at higher temperatures following 5°C acclimation, suggesting cardiovascular function may not constrain the capacity of N. coriiceps to withstand a warming climate.
RESUMEN
Elasmobranch fishes are an ancient group of vertebrates that have unusual lipid metabolism whereby storage lipids are mobilized from the liver for peripheral oxidation largely as ketone bodies rather than as nonesterified fatty acids under normal conditions. This reliance on ketones, even when feeding, implies that elasmobranchs are chronically ketogenic. Compared to specimens sampled within 2 d of capture (recently captured), spiny dogfish Squalus acanthias that were held for 16-33 d without apparent feeding displayed a 4.5-fold increase in plasma concentration of d- beta -hydroxybutyrate (from 0.71 to 3.2 mM) and were considered ketotic. Overt activity of carnitine palmitoyltransferase-1 in liver mitochondria from ketotic dogfish was characterized by an increased apparent maximal activity, a trend of increasing affinity (reduced apparent K(m); P=0.09) for l-carnitine, and desensitization to the inhibitor malonyl-CoA relative to recently captured animals. Acetoacetyl-CoA thiolase (ACoAT) activity in isolated liver mitochondria was also markedly increased in the ketotic dogfish compared to recently captured fish, whereas no difference in 3-hydroxy-3-methylglutaryl-CoA synthase activity was found between these groups, suggesting that ACoAT plays a more important role in the activation of ketogenesis in spiny dogfish than in mammals and birds.