The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. I. Intraspecific responses to seasonal differences in temperature

Mauro, N. A.; Mangum, Charlotte P.

doi:10.1002/jez.1402190207

Cited by 55 publications

(17 citation statements)

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“…However, it is critical to note that the method used (22,24) Not only is nutritional history an important consideration in elucidating genetic modulation of pentose-shunt metabolism in M. senile, it also plays a pivotal role in determining the pattern of metabolic reorganizations that accompany thermal adaptation in this species. The present results conditionally confirm the increased relative importance of pentose-shunt metabolism in poikilotherms at colder temperatures that has been described in other studies in which glucose utilization was not measured (34,35). However, increased fractional contribution of the pentose shunt between 15°C and 5°C was observed in fed anemones only, not in fasted ones.…”

Section: Resultssupporting

confidence: 92%

Allozymes of glucose-6-phosphate isomerase differentially modulate pentose-shunt metabolism in the sea anemone Metridium senile.

Zamer

Hoffmann

1989

Proc. Natl. Acad. Sci. U.S.A.

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We tested the hypothesis that kinetic differences among allelic variants of glucose--phosphate isomerase (GPI; D-glucose-6-phosphate ketol-isomerase, EC 5.3.1.9) from the sea anemone Metridium senile differentially modulate glucose metabolism at the glycolysis,-pentose-shunt branch point. Fractional contribution of pentose shunt and absolute flux of glucose in glycolysis were measured in fasted or fed anemones acclimated to 50C or 15°C. When fed, anemones of genotype Gpiss routed a greater fraction of glucose through the shunt than did Gpifanemones; the effect was more pronounced at 5°C than at 15TC. This confirms predictions from kinetic and population data and is consistent with thermal selection maintaining the variation. Relative levels of shunt metabolism increased at 5°C, compared with 15°C, in fed anemones regardless of genotype, but the proportion of glucose metabolized by the pentose shunt was unchanged by temperature in fasted anemones. Glucose flux through the shunt was constant at approximately 5 pmol mg-4ihr'1 in fed anemones at 50C and 15°C and in fasted anemones at 15°C, indicating apparently near-perfect thermal acclimation of the absolute flux of glucose through the shunt in fed, but not in fasted, anemones. Rates of glucose oxidation and flux through the shunt in freshly collected anemones were similar to those ofanemones fed and acclimated at 150C in the laboratory. If these differences affect organismallevel processes, Gpi variation could contribute to Darwinian fitness in thermally varying environments.A central issue in evolutionary biology is the elucidation of mechanisms by which genetic variation might lead to differences in fitness among individuals in a population. Many studies have shown on the basis of in vitro kinetics that functional differences may exist among allelic enzyme variants (allozymes) (1)(2)(3)(4)(5)(6)(7)(8). In several important cases, this biochemical approach has been extended to include organismal-level correlates of genetic variation. Physiological and behavioral differences among individuals have been accurately predicted from kinetic differences among enzyme variants, and persuasive arguments have been made that natural selection acts ultimately upon organismal-level differences deriving from kinetic differences among allozymes (9-15).Recent theoretical considerations suggest that variation in properties of any single enzyme in a pathway may have little effect on pathway flux (16, 17), a view supported by work with alcohol dehydrogenase mutants in Drosophila melanogaster (18). Nonetheless, a few studies show that allozyme variation may influence metabolism. For example, variants of glucose-6-phosphate dehydrogenase and 6-phosphogluconate dehydrogenase alter pentose-shunt metabolism in Drosophila (19), and rates of alanine accumulation during osmotic stress are influenced by activity variants ofglutamicpyruvic transaminase (alanine aminotransferase) in a copepod, Tigriopus californicus (20). Preliminary data suggest that allozymes of glucose-6-phosphate i...

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Section: Resultssupporting

confidence: 92%

Allozymes of glucose-6-phosphate isomerase differentially modulate pentose-shunt metabolism in the sea anemone Metridium senile.

Zamer

Hoffmann

1989

Proc. Natl. Acad. Sci. U.S.A.

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“…7, 8, 27-29). Hemocyanin characteristics suggest that O 2 binding at the gills may become insufficient at high temperature and O 2 unloading in the tissues may be incomplete at low temperature (29). In our study, release of O 2 from hemocyanin is likely to explain the tailing in the PO 2 decrease between 23 and 32°C visible at a hemolymph PO 2 of 24.5 Ϯ 6.5 mmHg (Fig.…”

Section: Discussionmentioning

confidence: 50%

Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab,Maja squinado

Frederich

Pörtner

2000

American Journal of Physiology-Regulatory, Integrative and Comp

318

273

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Frederich, Markus, and Hans O. Pö rtner. Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab, Maja squinado. Am J Physiol Regulatory Integrative Comp Physiol 279: R1531-R1538, 2000.-Geographic distribution limits of ectothermal animals appear to be correlated with thermal tolerance thresholds previously identified from the onset of anaerobic metabolism. Transition to these critical temperatures was investigated in the spider crab (Maja squinado) with the goal of identifying the physiological processes limiting thermal tolerance. Heart and ventilation rates as well as PO 2 in the hemolymph were recorded on-line during progressive temperature change between 12 and 0°C (1°C/h) and between 12 and 40°C (2°C/h). Lactate and succinate were measured in tissues and hemolymph after intermediate or final temperatures were reached. High levels of hemolymph oxygenation suggest that an optimum range of aerobic performance exists between 8 and 17°C. Thermal limitation may already set in at the transition from optimum to pejus (pejus ϭ turning worse, progressively deleterious) range, characterized by the onset of a decrease in arterial PO 2 due to reduced ventilatory and cardiac performance. Hemolymph PO 2 values fell progressively toward both low and high temperature extremes until critical temperatures were reached at ϳ1 and 30°C, as indicated by low PO 2 and the onset of anaerobic energy production by mitochondria. In conclusion, the limited capacity of ventilation and circulation at extreme temperatures causes insufficient O 2 supply, thereby limiting aerobic scope and, finally, thermal tolerance. aerobic capacity; anaerobic metabolism; optodes; partial pressure of oxygen CRITICAL TEMPERATURES (T c ) have been defined for different marine invertebrate and fish species as being characterized by the onset of anaerobic metabolism, which is caused by a mismatch of O 2 demand and O 2 supply (for review, see Refs. 35 and 36). Extended exposure to temperatures above high T c or below low T c finally leads to death of the animal unless thermal acclimation, i.e., a shift of T c values, occurs (40, 51). One hypothesis is that the adjustment of mitochondrial density and capacity is involved in setting thermal tolerance limits and is therefore related to geographic distribution (35, 36). As a consequence, the relationship between O 2 availability to tissues and O 2 demand appears to be crucial for survival of exposure to temperature extremes. Study of the processes of O 2 uptake by ventilation and O 2 distribution by circulation therefore appear important to further our understanding of the O 2 limitation of thermal tolerance. Therefore, we chose to study these systemic aspects of thermal tolerance, selecting a crustacean, Maja squinado (Herbst), as a model organism. As yet, physiological studies of crustaceans have addressed temperature effects on O 2 consumption, heart and ventilatory performance, or growth (12-14, 16, 23, 34, 44). In most of these studies, temperatures were chosen wit...

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“…A final point of interest in the present results is the absence in C. borealis and M. mercenaria of two adaptations found in C. sapidus (Mauro and Mangum, 1982). There is no indication in either species examined here of different thermal sensitivities of metabolism in different tissues which could be due to a reorganization of intermediary metabolism in only one.…”

mentioning

confidence: 70%

“…The consequences of shifting from the transport of 0, by a carrier-mediated process to transport entirely in the free form are not as great in C. borealis as in Callinectes sapidus (Mauro and Mangum, 1982), either metabolically or behaviorally. But the potential of a temperature insensitive metabolic rate in motor muscle is not exploited in the animal, which does become noticeably less active.…”

mentioning

confidence: 96%

The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. II. Interspecific adaptations to latitudinal changes

Mauro

Mangum

1982

J. Exp. Zool.

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The effects of acclimation temperature on hemocyanin-oxygen (HcO,) transport were examined in two species of decapod crustaceans representing different geographic and thermal ranges. In the coldwater species Cancer borealis and the warmwater species Menippe mercenan'a, the performance of the HcO, transport system is maximized at 15 "C, a summer temperature in the northern habitat and a winter temperature in the southern habitat. In C. borealis little unloading at the tissues occurs at 5 "C, and in M. mercenan'a oxygenation at the gill is incomplete at 25 "C. The temperature coefficients describing rates of ventilation, heartbeat, and total oxidative metabolism fall within a narrow range (Q,, =1.9-3.6), providing no indication of ventilatory or cardiovascular adjustments that would allow the HcO, transport system to function at the maximum level at different temperatures. Comparison of the Hc02 equilibrium properties suggests that HcO, affinity has been selected for a particular thermal range, but not cooperativity or pH dependence. The thermal limits of the 0, transport system are set by both the direct effect of temperature on HcO, equilibrium and the indirect effect via the Bohr shift that accompanies the change in blood pH with temperature.Redmonds ('55, '68) investigation of the oxygen equilibrium properties of the blood of panulirid lobsters suggested that the crustacean hemocyanins have been selected for functioning under different thermal regimes. The hemocyanin-oxygen (HcO,) affinities in the temperate zone species Palinurus interruptus and the subtropical species P. argus are approximately the same when measured at a common pH but a t different temperatures representing a mean annual value for the habitat, viz. 15°C for P. interruptus and 25°C for P. argus. When measured at the same temperature (25"c, pH 7.5), the numerical values (P5,,) differ by a factor of two. The generalization of higher HcO, affinities in species found in warmer waters and lower Hc0, affinities in crustaceans found in colder waters is supported by data for more than 35 species representing tropical, temperate zone, and boreal habitats, although exceptions implicate the influence of other factors as well (Mangum, 198 1 a,b).The degree to which the differences in P,, permit the HcO, transport system to work effectively under the thermal regimes prevailing at different latitudes is not known. The functioning of the system depends on other 0, equilibrium variables, such as cooperativity, that determine oxygenation states of often greater physiological relevance. The functioning of the system also depends on physiological variables such as blood pH and PO,. The geographic trends in these variables, and of the fluid convection mechanisms that influence the in vivo determinants, are not known. In many cold-blooded animals, higher rates of respiratory and metabolic variables at a given temperature are observed in species found in colder habitats than in warmer habitats, which is interpreted as a compensatory adaptation for latit...

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The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. I. Intraspecific responses to seasonal differences in temperature

Cited by 55 publications

References 19 publications

Allozymes of glucose-6-phosphate isomerase differentially modulate pentose-shunt metabolism in the sea anemone Metridium senile.

Allozymes of glucose-6-phosphate isomerase differentially modulate pentose-shunt metabolism in the sea anemone Metridium senile.

Oxygen limitation of thermal tolerance defined by cardiac and ventilatory performance in spider crab,Maja squinado

The role of the blood in the temperature dependence of oxidative metabolism in decapod crustaceans. II. Interspecific adaptations to latitudinal changes

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