The influence of oxygen and high-energy phosphate diffusion on metabolic scaling in three species of tail-flipping crustaceans

Abstract

SUMMARYWe examined the influence of intracellular diffusion of O 2 and high-energy phosphate (HEP) molecules on the scaling with body mass of the post-exercise whole-animal rate of O 2 consumption (V O 2) and muscle arginine phosphate (AP) resynthesis rate, as well as muscle citrate synthase (CS) activity, in three groups of tail-flipping crustaceans. Two size classes in each of three taxa (Palaemonetes pugio, Penaeus spp. and Panulirus argus) were examined that together encompassed a 27,000-fold range in mean body mass. In all species, muscle fiber size increased with body mass and ranged in diameter from 70±1.5 to 210±8.8 μm. Thus, intracellular diffusive path lengths for O 2 and HEP molecules were greater in larger animals. The body mass scaling exponent, b, for post-tail flipping V O 2 (b=-0.21) was not similar to that for the initial rate of AP resynthesis (b=-0.12), which in turn was different from that of CS activity (b=0.09). We developed a mathematical reaction-diffusion model that allowed an examination of the influence of O 2 and HEP diffusion on the observed rate of aerobic flux in muscle. These analyses revealed that diffusion limitation was minimal under most conditions, suggesting that diffusion might act on the evolution of fiber design but usually does not directly limit aerobic flux. However, both within and between species, fibers were more diffusion limited as they grew larger, particularly when hemolymph P O 2 was low, which might explain some of the divergence in the scaling exponents of muscle aerobic capacity and muscle aerobic flux.

The formation and functional consequences of heterogeneous mitochondrial distributions in skeletal muscle

“…The mitochondrial death rules were consistent with previous studies concerning the selective (targeted) death of mitochondria based on ROS production levels (He and Klionsky, 2009;Kim et al, 2007;Yen and Klionsky, 2008;Zhang et al, 2008) and hypoxia (Band et al, 2009). Also, in contrast to low spatial variation in ADP, substantial spatial variation is observed in the oxygen concentration (Fig.1C), as seen previously (Jimenez et al, 2008;Kinsey et al, 2011). Thus, significant spatial variation in oxygen concentration is consistent with the view that there is a nonuniform signal for mitochondrial death (i.e.…”

“…AMP was not explicitly evaluated in the model, but it is in equilibrium with ADP, which was evaluated, through the adenylate kinase reaction. ADP, and hence AMP, concentration was uniform across all of the fibers (Fig.1G,H), as seen previously (Jimenez et al, 2008;Locke and Kinsey, 2008;Kinsey et al, 2011), and so the model results are consistent with the idea that spatial variation in biogenesis signals will have little effect on the mitochondrial distribution.…”

“…In support of this view, shifts in mitochondrial distribution toward the fiber periphery during hypertrophic fiber growth in a variety of comparative models appear to be independent of opposing shifts in nuclear distribution toward the fiber center (Nyack et al, 2007;Hardy et al, 2009;Hardy et al, 2010;Priester et al, 2011), and experiments with isolated cells indicate that mitochondrial DNA replication is independent of proximity to nuclei (Magnusson et al, 2003). Moreover, reactiondiffusion models indicate that spatial gradients in high-energy phosphate molecules like AMP are very slight in muscle (Jimenez et al, 2008;Dasika et al, 2011;Pathi et al, 2011), and we know of no biogenesis signals that vary spatially across the radius of the fiber. In contrast, as mentioned above, mitochondrial degradation is a regionally variable, selective process, whereby damaged mitochondria are specifically targeted and removed.…”

“…The intracellular partial pressure of O 2 (P O2 ) in the model was set as a fixed parameter as in our previous studies (Jimenez et al, 2008;Dasika et al, 2011;Pathi et al, 2011) based on literature indicating that this is a reasonable estimation of the concentration of oxygen available at the capillaries (2666.45Pa, i.e. 35.1mmoll -1 ) in fishes (Egginton et al, 2002) and mammals (Groebe, 1995).…”

“…In contrast, as mentioned above, mitochondrial degradation is a regionally variable, selective process, whereby damaged mitochondria are specifically targeted and removed. For instance, a mitochondrion present at the muscle fiber core that is frequently exposed to hypoxic conditions may suffer increased damage by ROS and be targeted for removal as a cytoprotective response and, unlike biogenesis signals such as AMP, there may be steep oxygen gradients across the radius of fibers from mammals (Groebe et al, 2010;Schroeder et al, 2010;Pathi et al, 2011), fishes (Egginton et al, 2002) and crustaceans (Jimenez et al, 2008). Thus, although it is easy to envision how the balance between mitochondrial biogenesis and degradation governs mitochondrial volume density, it appears that only pathways of mitochondrial death, coupled with spatial gradients in key molecules such as oxygen, provide a means of generating a heterogeneous mitochondrial distribution.…”