Reaction-diffusion analysis of the effects of temperature on high-energy phosphate dynamics in goldfish skeletal muscle.

Abstract

Thermal acclimation results in dramatic changes in the fractional volume of mitochondria within skeletal muscle of teleost fish. We investigated the hypothesis that changes in mitochondrial volume represent a compensatory response to temperature-induced changes in intracellular diffusion coefficients (D) of the high-energy phosphate compounds ATP and creatine phosphate (PCr). Using 31P nuclear magnetic resonance spectroscopy, we determined DPCr and DATP in goldfish (Carassius auratus) skeletal muscle at 25 degrees C and 5 degrees C: DPCr was 3.28 +/- 0.18 x 10(-6) cm2s-1 at 25 degrees C and 2.00 +/- 0.90 x 10(-6) cm2s-1 at 5 degrees C: DATP was 2.13 +/- 0.16 x 10(-6) cm2s-1 at 25 degrees C and was estimated to be 1.30 x 10(-6) cm2s-1 at 5 degrees C. There was no evidence for an effect of acclimation temperature or fiber type on DATP or DPCr. A mathematical reaction-diffusion model was used to calculate profiles of [ATP], [PCr] and the free energy of ATP hydrolysis (delta GATP) in activated goldfish muscle fibers at 5 degrees C and 25 degrees C. The results showed spatial and temporal constancy of [ATP], [PCr] and delta GATP in red fibers at both temperatures, regardless of changes in acclimation temperature or mitochondrial density. The model also showed spatial and temporal constancy of [ATP] in white fibers at 5 degrees C and 25 degrees C, but gradients in [PCr] and delta GATP developed in white fibers under all conditions of temperature and acclimation temperature. These gradients were attenuated in cold-acclimated animals by cold-induced increases in mitochondrial density. However, the model shows that the proximal stimulus for temperature-induced changes in mitochondrial volume density in muscle is not a disruption in intracellular diffusion of high-energy phosphates.