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COMPARATIVE AND EVOLUTIONARY PHYSIOLOGY

Scaling of postcontractile phosphocreatine recovery in fish white muscle: effect of intracellular diffusion

¹Department of Biology and Marine Biology, University of North Carolina Wilmington, Wilmington, North Carolina; and ²Department of Chemical and Biomedical Engineering, Florida A&M University-Florida State University College of Engineering, Tallahassee, Florida

Submitted 5 July 2006 ; accepted in final form 18 January 2007

In some fish, hypertrophic growth of white muscle leads to very large fibers. The associated low-fiber surface area-to-volume ratio (SA/V) and potentially long intracellular diffusion distances may influence the rate of aerobic processes. We examined the effect of intracellular metabolite diffusion on mass-specific scaling of aerobic capacity and an aerobic process, phosphocreatine (PCr) recovery, in isolated white muscle from black sea bass (Centropristis striata). Muscle fiber diameter increased during growth and was >250 µm in adult fish. Mitochondrial volume density and cytochrome-c oxidase activity had similar small scaling exponents with increasing body mass (–0.06 and –0.10, respectively). However, the mitochondria were more clustered at the sarcolemmal membrane in large fibers, which may offset the low SA/V, but leads to greater intracellular diffusion distances between mitochondrial clusters and ATPases. Despite large differences in intracellular diffusion distances, the postcontractile rate of PCr recovery was largely size independent, with a small scaling exponent for the maximal rate (–0.07) similar to that found for the indicators of aerobic capacity. Consistent with this finding, a mathematical reaction-diffusion analysis indicated that the resynthesis of PCr (and other metabolites) was too slow to be substantially limited by diffusion. These results suggest that the recovery rate in these fibers is primarily limited by low mitochondrial density. Additionally, the change in mitochondrial distribution with increasing fiber size suggests that low SA/V and limited O₂ flux are more influential design constraints in fish white muscle, and perhaps other fast-twitch vertebrate muscles, than is intracellular metabolite diffusive flux.

hypertrophy; creatine kinase; mitochondria