Ultrastructural Analysis Reveals Mitochondrial Placement Independent of Synapse Placement in Fine Caliber C. elegans Neurons

Abstract

Neurons rely on mitochondria for an efficient supply of ATP and other metabolites. However, while neurons are highly elongated, mitochondria are discrete and limited in number. Due to the slow rates of metabolite diffusion over long distances, it follows that neurons would benefit from an ability to control the distribution of mitochondria to sites of high metabolic activity such as synapses. Ultrastructural data over substantial portions of a neuron's extent that would allow for tests of such hypotheses are scarce. Here, we mined the Caenorhabditis elegans’ electron micrographs of John White and Sydney Brenner and found systematic differences in average mitochondrial length (ranging from 1.3 to 2.4 µm), diameter (0.18–0.24 µm) and volume density (3.7%–6.5%) between neurons of different function and neurotransmitter type, but found limited differences in mitochondrial length, diameter, and density between axons and dendrites of the same neurons. In analyses of mitochondrial distribution, mitochondria were found to be distributed randomly with respect to presynaptic sites. Presynaptic sites were primarily localized to varicosities, but mitochondria were no more likely to be found in synaptic varicosities than non-synaptic varicosities. Consistently, mitochondrial volume density was no greater in synaptic varicosities than non-synaptic varicosities. Therefore, beyond the capacity to disperse mitochondria throughout their length, at least in C. elegans, fine caliber neurons manifest limited subcellular control of mitochondrial size and distribution.