Ultrastructural analysis reveals mitochondrial placement independent of synapse placement in fine caliber C. elegans neurons

• Published in: bioRxiv
• Main Authors: Riboul, Danielle V, Crill, Sarah, Oliva, Carlos D, Restifo, Maria G, Joseph, Reggie, Joseph, Kerdes, Nguyen, Ken Cq, Hall, David H, Fily, Yaouen, Macleod, Gregory T
• Format: Journal Article
• Language: English
• Published: United States 02.03.2024
• ISSN: 2692-8205; 2692-8205
• DOI: 10.1101/2023.05.30.542959

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 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. It is assumed that neurons' possess this capacity, but 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), volume density (3.7% to 6.5%) and diameter (0.18 to 0.24 μm) between neurons of different neurotransmitter type and function, but found limited differences in mitochondrial morphometrics between axons and dendrites of the same neurons. Analyses of distance intervals found mitochondria to be distributed randomly with respect to presynaptic specializations, and an indication that mitochondria were displaced from postsynaptic specializations. Presynaptic specializations 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 varicosities with synapses. Therefore, beyond the capacity to disperse mitochondria throughout their length, at least in C. elegans, fine caliber neurons manifest limited sub-cellular control of mitochondrial size and distribution.