Does intracellular metabolite diffusion limit post-contractile recovery in burst locomotor muscle?

Kinsey, Stephen T.; Pathi, Pragyansri; Hardy, Kristin M.; Jordan, Amanda; Locke, Bruce R.

doi:10.1242/jeb.01686

Cited by 22 publications

(63 citation statements)

References 54 publications

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“…However, total mitochondrial volume density was 0.0074±0.0001 for juvenile lobsters and 0.0067±0.0001 for adult lobsters. These volume densities are similar to those in white muscle from other crustaceans for which we have measured rates of aerobic ATP production (Kinsey et al, 2005;Jimenez et al, 2008). Based on this prior work, we believe that a maximal aerobic rate of cellular ATPases (V max ) of 1.2mmoll -1 ATPmin -1 is the most reasonable rate for lobster abdominal fibers.…”

Section: Balancing Maintenance Costs and Diffusion Constraintssupporting

confidence: 73%

“…based on mitochondrial volume density and previous work (Kinsey et al, 2005;Jimenez et al, 2008), fibers could grow to considerably larger sizes and not reach diffusion limitation. This finding would seem to be at odds with the optimal fiber size hypothesis.…”

Section: Discussionmentioning

confidence: 86%

“…These anaerobic pathways rely on endogenous fuels, and the abundance of phosphagen kinases and glycolytic enzymes that are present throughout the sarcoplasm make diffusion distances very short. However, diffusion limitation of aerobic metabolism, which depends on the movement of oxygen from the blood to the mitochondria, could affect the rate of post-contractile recovery and therefore limit an animal's ability to undergo multiple high-force escape responses during predator-prey interactions (Kinsey et al, 2005;Nyack et al, 2007;Jimenez et al, 2008). Nevertheless, large increases in diffusion distances in muscle due to hypertrophic growth are prevalent among many animals including mammals, although the most extreme cases are found in anaerobic muscle fibers of crustaceans and fish species (Boyle et al, 2003;Johnson et al, 2004;Nyack et al, 2007;Jimenez et al, 2008).…”

Section: Discussionmentioning

confidence: 99%

“…Spectra were collected every 3min using a 90deg excitation pulse and a relaxation delay of 12s, which ensured that the phosphorus nuclei were fully relaxed and peak integrals for the metabolites were proportional to their relative concentrations. The area under each peak was integrated using TopSpin-NMR software (Bruker) to yield relative concentrations of each metabolite, and these values were converted to concentration by assuming a total high-energy phosphate (HEP) concentration of 50mmoll -1 , which is characteristic of crustacean white muscle (Kinsey et al, 2005).…”

Section: Cost Of Metabolic Processesmentioning

confidence: 99%

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An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain?

Jiménez

Dasika

Locke

et al. 2011

Journal of Experimental Biology

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SUMMARYLarge muscle fiber size imposes constraints on muscle function while imparting no obvious advantages, making it difficult to explain why muscle fibers are among the largest cell type. Johnston and colleagues proposed the 'optimal fiber size' hypothesis, which states that some fish have large fibers that balance the need for short diffusion distances against metabolic cost savings associated with large fibers. We tested this hypothesis in hypertrophically growing fibers in the lobster Homarus americanus. Mean fiber diameter was 316±11m in juveniles and 670±26m in adults, leading to a surface area to volume ratio (SA:V) that was 2-fold higher in juveniles. Na -ATPase over a broad fiber size range showed that if fibers were much smaller than those observed, maintenance of the membrane potential would constitute a large fraction of whole-animal metabolic rate, suggesting that the fibers grow large to reduce maintenance costs. However, a reaction-diffusion model of aerobic metabolism indicated that fibers in adults could attain still larger sizes without diffusion limitation, although further growth would have a negligible effect on cost. Therefore, it appears that decreased fiber SA:V makes larger fibers in H. americanus less expensive to maintain, which is consistent with the optimal fiber size hypothesis.

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Section: Balancing Maintenance Costs and Diffusion Constraintssupporting

confidence: 73%

Section: Discussionmentioning

confidence: 86%

Section: Discussionmentioning

confidence: 99%

Section: Cost Of Metabolic Processesmentioning

confidence: 99%

See 2 more Smart Citations

An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain?

Jiménez

Dasika

Locke

et al. 2011

Journal of Experimental Biology

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“…Large muscle fibers could have been favored in the evolution of notothenioids, since the decrease in the fiber surface to volume ratio will decrease the cost of maintaining ion homeostasis in these fibers. This idea, called the 'optimal fiber size hypothesis', was proposed by Johnston et al (2003Johnston et al ( , 2004 for notothenioids and Arctic char evolution and by Kinsey et al (2005) for blue crabs.…”

Section: Physiological Adaptation To Extreme Conditionsmentioning

confidence: 99%

Fishes of southern South America: a story driven by temperature

Cussac

Fernández

Gómez

et al. 2008

Fish Physiol Biochem

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The latitudinal extension of southern South America imposes a thermal gradient that affects the structure of marine and freshwater fish assemblages and the biology of the species through direct exposure to the temperature gradients or by means of a web of historical and ecological relationships. We have reviewed biological and ecological data of marine and freshwater fishes from the southern Neotropics, including Patagonia, and report several examples of dependence on temperature, from glacial times to today's climate change. We were able to identify historic and present effects on the diversity of fish assemblages, isolation, southern limits for the distribution of species, and morphological variation among populations. There is a wide range of characteristics that exemplify an adaptation to low temperatures, including biochemical peculiarities, physiological adjustments, and alternative life history patterns, and these appear in both freshwater and marine, and native and exotic fishes. The consequences of stable temperature regimes in both the ocean and thermal streams deserve special mention as these shape specialists under conditions of low selective pressure. At present, habitat use and interactions among species are being subject to changes as consequences of water temperature, and some of these are already evident in the northern and southern hemispheres.

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Reaction–diffusion constraints in living tissue: Effectiveness factors in skeletal muscle design

Dasika

Kinsey

Locke

2010

Biotech & Bioengineering

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A mathematical model was developed to analyze the effects of intracellular diffusion of O(2) and high-energy phosphate metabolites on aerobic energy metabolism in skeletal muscle. We tested the hypotheses that in a range of muscle fibers from different species (1) aerobic metabolism was not diffusion limited and (2) that fibers had a combination of rate and fiber size that placed them at the brink of substantial diffusion limitation. A simplified chemical reaction rate law for mitochondrial oxidative phosphorylation was developed utilizing a published detailed model of isolated mitochondrial function. This rate law was then used as a boundary condition in a reaction-diffusion model that was further simplified using the volume averaging method and solved to determine the rates of oxidative phosphorylation as functions of the volume fraction of mitochondria, the size of the muscle cell, and the amount of oxygen delivered by the capillaries. The effectiveness factor, which is the ratio of reaction rate in the system with finite rates of diffusion to those in the absence of any diffusion limitations, defined the regions where intracellular diffusion of metabolites and O(2) may limit aerobic metabolism in both very small, highly oxidative fibers as well as in larger fibers with lower aerobic capacity. Comparison of model analysis with experimental data revealed that none of the fibers was strongly limited by diffusion, as expected. However, while some fibers were near substantial diffusion limitation, most were well within the domain of reaction control of aerobic metabolic rate. This may constitute a safety factor in muscle that provides a level of protection from diffusion constraints under conditions such as hypoxia.

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Does intracellular metabolite diffusion limit post-contractile recovery in burst locomotor muscle?

Cited by 22 publications

References 54 publications

An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain?

An evaluation of muscle maintenance costs during fiber hypertrophy in the lobster Homarus americanus: are larger muscle fibers cheaper to maintain?

Fishes of southern South America: a story driven by temperature

Reaction–diffusion constraints in living tissue: Effectiveness factors in skeletal muscle design

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