In cells, oxygen, small metabolites and macromolecules move around by molecular diffusion. Small cells have shorter diffusion distances than large cells, so the molecules are able to reach their destination more quickly. It is especially important that these various molecules reach their targets rapidly in metabolically active tissues.

Aerobic (dark) muscle fibres are metabolically active tissues that power sustained locomotion. Oxygen must diffuse from the blood through muscle cells to the energy producing mitochondria so that ATP (the energy currency of the cell) can be produced to power contraction. In contrast, anaerobic (light)muscle fibres only require oxygen to recover from short bursts of activity,which are not considered to be as energetically costly. As light muscle fibres are less dependent on oxygen than dark muscle fibres, researchers hypothesize that light muscle fibres may be able to endure larger diffusion distances compared with dark muscle fibres.

Kristin Hardy from the University of North Carolina Wilmington and colleagues from Florida State University sought to determine how diffusion influences muscle cell structure in the blue crab Callinectes sapidus. Incredibly, adult blue crab muscle fibres are 7 times larger than the juveniles' muscle fibres, making them an excellent model to examine these questions. Using various microscopy techniques, the authors examined light and dark muscle fibres from juvenile and adult blue crabs. They determined the location of mitochondria and nuclei in the individual fibres and quantified the network of haemolymph vessels (analogous to blood vessels)supplying the light and dark fibres.

The team found that the distribution of mitochondria and nuclei in light muscle fibres changed radically during growth. Juvenile light muscle fibres contained evenly distributed mitochondria, while the mitochondria in adult light muscle fibres were limited to the edge of the fibre, in close proximity to the haemolymph. The distribution of nuclei yielded exactly the opposite pattern: in juveniles, nuclei from the periphery moved to become distributed throughout the adults' light muscle fibres. The authors suggest that as light muscle fibres grow, mitochondria migrate to the periphery of the fibre to be close to the oxygen-rich haemolymph in order to minimize diffusion distances for oxygen. Nuclei relocate throughout the cell since they require the diffusion of large, slow, macromolecules found in the cystol.

Interestingly, the team found no change in the location of mitochondria and nuclei during growth in dark muscle fibres. However, the authors found an intricate network of subdivisions within the dark fibres, allowing haemolymph to circulate freely. Dark muscle fibres primarily limited their mitochondria and nuclei to the edge of the subdivisions, thereby minimizing diffusion distances from the haemolymph.

Next, the researchers used mathematical models to compare how metabolic reaction rates will change depending on whether the mitochondria are located at the edges or throughout a muscle fibre. Clustering mitochondria around the periphery of large light muscle fibres allowed a much higher rate of ATP turnover compared with a simple uniform distribution throughout the cell. Furthermore, they established that dark muscle fibres could not come close to sustaining even a moderate rate of ATP turnover without the network of subdivisions.

This study demonstrates that light and dark muscle fibres in blue crab have completely different strategies to cope with diffusion limitations during extreme fibre growth. Furthermore, the findings suggest that diffusion limitations result in changes to cellular structure during growth. The next step will be to establish whether these patterns hold true in less extraordinary species and cells.

Hardy, K. M., Dillaman, R. M., Locke, B. R. and Kinsey, S. T. (
). A skeletal muscle model of extreme hypertrophic growth reveals the influence of diffusion on cellular design.
Am. J. Physiol. Regul. Integr. Comp. Physiol.