Krogh’s diffusion coefficient for oxygen in isolated<i>Xenopus</i>skeletal muscle fibers and rat myocardial trabeculae at maximum rates of oxygen consumption

Laarse, Willem J. van der; Tombe, Ariane L. des; Beek-Harmsen, Brechje J. van; Groot, M.B.E. Lee-de; Jaspers, Richard T.

doi:10.1152/japplphysiol.00470.2005

Cited by 44 publications

(44 citation statements)

References 43 publications

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“…The value used here was based on in vivo measures of oxygen diffusion using phosphorescence quenching microscopy (32). Although this estimate is considerably lower than Krogh's original estimate (33), it is within two-to threefold of many current estimates from various tissues-particularly those using in vivo methods (34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44)(45)(46). The diffusion constant was adjusted for temperature to 38°C in our analysis of endotherms and to 25°C for ectotherms, based on a reported Q10 of 1.1 (47).…”

Section: Methodsmentioning

confidence: 95%

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Gillooly

Gómez

Mavrodiev

et al. 2016

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

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The area and thickness of respiratory surfaces, and the constraints they impose on passive oxygen diffusion, have been linked to differences in oxygen consumption rates and/or aerobic activity levels in vertebrates. However, it remains unclear how respiratory surfaces and associated diffusion rates vary with body mass across vertebrates, particularly in relation to the body mass scaling of oxygen consumption rates. Here we address these issues by first quantifying the body mass dependence of respiratory surface area and respiratory barrier thickness for a diversity of endotherms (birds and mammals) and ectotherms (fishes, amphibians, and reptiles). Based on these findings, we then use Fick's law to predict the body mass scaling of oxygen diffusion for each group. Finally, we compare the predicted body mass dependence of oxygen diffusion to that of oxygen consumption in endotherms and ectotherms. We find that the slopes and intercepts of the relationships describing the body mass dependence of passive oxygen diffusion in these two groups are statistically indistinguishable from those describing the body mass dependence of oxygen consumption. Thus, the area and thickness of respiratory surfaces combine to match oxygen diffusion capacity to oxygen consumption rates in both air-and water-breathing vertebrates. In particular, the substantially lower oxygen consumption rates of ectotherms of a given body mass relative to those of endotherms correspond to differences in oxygen diffusion capacity. These results provide insights into the long-standing effort to understand the structural attributes of organisms that underlie the body mass scaling of oxygen consumption.allometry | metabolic theory | respiration rate | metabolism | oxygen consumption S ince the classic debates of Krogh and Bohr (1), the relationship of passive oxygen diffusion to oxygen consumption has remained the focus of considerable research (2). Still, we have much to learn about how oxygen diffusion across respiratory surfaces relates to whole-organism oxygen consumption (3). In particular, we have much to learn about how the structural constraints on oxygen diffusion capacity, namely the thickness and area of respiratory surfaces, relate to the body mass scaling of oxygen consumption in vertebrates-a pattern that reflects the scaling of species' energy use (3).Studies on the body mass dependence of oxygen diffusion have been undertaken over the last century in all major classes of vertebrates, typically using respiratory surface area as a metric of diffusion capacity (2, 3). Less commonly, studies have also considered potentially relevant changes in respiratory barrier thickness with mass (4). In many cases, these studies have concluded that the body mass scaling of oxygen diffusion relative to that of oxygen consumption differs between endotherms and ectotherms (3,5,6). This has led to very different conclusions regarding the structure and function of respiratory systems among classes of vertebrates, as explained below.Among endotherms, particularly...

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Section: Methodsmentioning

confidence: 95%

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Gillooly

Gómez

Mavrodiev

et al. 2016

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

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“…mass of the preparation was 0.13±0.0068 g and the length was 14.06±0.0068 mm. We used methods described elsewhere (van der Laarse et al, 2005) to ascertain that limits to oxygen diffusion did not constrain oxygen consumption of muscle preparations.…”

Section: Isolated Muscle Mechanicsmentioning

confidence: 99%

The cost of muscle power production: muscle oxygen consumption per unit work increases at low temperatures inXenopus laevisDaudin

Seebacher

Tallis

James

2014

Journal of Experimental Biology

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Metabolic energy (ATP) supply to muscle is essential to support activity and behaviour. It is expected, therefore, that there is strong selection to maximise muscle power output for a given rate of ATP use. However, the viscosity and stiffness of muscle increases with a decrease in temperature, which means that more ATP may be required to achieve a given work output. Here, we tested the hypothesis that ATP use increases at lower temperatures for a given power output in Xenopus laevis. To account for temperature variation at different time scales, we considered the interaction between acclimation for 4 weeks (to 15 or 25°C) and acute exposure to these temperatures. Cold-acclimated frogs had greater sprint speed at 15°C than warm-acclimated animals. However, acclimation temperature did not affect isolated gastrocnemius muscle biomechanics. Isolated muscle produced greater tetanus force, and faster isometric force generation and relaxation, and generated more work loop power at 25°C than at 15°C acute test temperature. Oxygen consumption of isolated muscle at rest did not change with test temperature, but oxygen consumption while muscle was performing work was significantly higher at 15°C than at 25°C, regardless of acclimation conditions. Muscle therefore consumed significantly more oxygen at 15°C for a given work output than at 25°C, and plastic responses did not modify this thermodynamic effect. The metabolic cost of muscle performance and activity therefore increased with a decrease in temperature. To maintain activity across a range of temperature, animals must increase ATP production or face an allocation trade-off at lower temperatures. Our data demonstrate the potential energetic benefits of warming up muscle before activity, which is seen in diverse groups of animals such as bees, which warm flight muscle before take-off, and humans performing warm ups before exercise.

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“…However, spatial gradients in the redox state of isolated frog skeletal muscle fibers suggest that O 2 gradients may influence rates of oxidative phosphorylation even under conditions of high extracellular P O2 (Hogan et al, 2005). Further, measurements of O 2 consumption rates and force production in isolated frog skeletal muscle fibers and rat myocardial trabeculae suggest that maximal respiration rates cannot be attained in vivo because O 2 diffusive flux is insufficient to prevent anoxia in the fiber core (van der Laarse et al, 2005).…”

Section: Evaluating Diffusion-dependent Processes In Musclementioning

confidence: 99%

Molecules in motion: influences of diffusion on metabolic structure and function in skeletal muscle

Kinsey

Locke

Dillaman

2011

Journal of Experimental Biology

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When examining a single tissue type, D is comparatively invariant over physiological time scales, so the extent to which diffusion influences cell structure and function is largely governed by the interaction between diffusion distance and reaction flux rate. In skeletal muscle fibers rates of reaction fluxes and diffusion distances can vary over several orders of magnitude. For instance, aerobic metabolic rate in white muscle from fishes and crustaceans Accepted 25 August 2010 Summary Metabolic processes are often represented as a group of metabolites that interact through enzymatic reactions, thus forming a network of linked biochemical pathways. Implicit in this view is that diffusion of metabolites to and from enzymes is very fast compared with reaction rates, and metabolic fluxes are therefore almost exclusively dictated by catalytic properties. However, diffusion may exert greater control over the rates of reactions through: (1) an increase in reaction rates; (2) an increase in diffusion distances; or (3) a decrease in the relevant diffusion coefficients. It is therefore not surprising that skeletal muscle fibers have long been the focus of reaction-diffusion analyses because they have high and variable rates of ATP turnover, long diffusion distances, and hindered metabolite diffusion due to an abundance of intracellular barriers. Examination of the diversity of skeletal muscle fiber designs found in animals provides insights into the role that diffusion plays in governing both rates of metabolic fluxes and cellular organization. Experimental measurements of metabolic fluxes, diffusion distances and diffusion coefficients, coupled with reaction-diffusion mathematical models in a range of muscle types has started to reveal some general principles guiding muscle structure and metabolic function. Foremost among these is that metabolic processes in muscles do, in fact, appear to be largely reaction controlled and are not greatly limited by diffusion. However, the influence of diffusion is apparent in patterns of fiber growth and metabolic organization that appear to result from selective pressure to maintain reaction control of metabolism in muscle.

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Krogh’s diffusion coefficient for oxygen in isolatedXenopusskeletal muscle fibers and rat myocardial trabeculae at maximum rates of oxygen consumption

Cited by 44 publications

References 43 publications

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

Body mass scaling of passive oxygen diffusion in endotherms and ectotherms

The cost of muscle power production: muscle oxygen consumption per unit work increases at low temperatures inXenopus laevisDaudin

Molecules in motion: influences of diffusion on metabolic structure and function in skeletal muscle

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