Evolutionary origin of synapses and neurons - Bridging the gap.

Pawel Burkhardt,Simon G. Sprecher

doi:10.1002/bies.201700024

Pawel Burkhardt, Simon G. Sprecher

Open Access

https://doi.org/10.1002/bies.201700024

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Abstract

The evolutionary origin of synapses and neurons is an enigmatic subject that inspires much debate. Non-bilaterian metazoans, both with and without neurons and their closest relatives already contain many components of the molecular toolkits for synapse functions. The origin of these components and their assembly into ancient synaptic signaling machineries are particularly important in light of recent findings on the phylogeny of non-bilaterian metazoans. The evolution of synapses and neurons are often discussed only from a metazoan perspective leaving a considerable gap in our understanding. By taking an integrative approach we highlight the need to consider different, but extremely relevant phyla and to include the closest unicellular relatives of metazoans, the ichthyosporeans, filastereans and choanoflagellates, to fully understand the evolutionary origin of synapses and neurons. This approach allows for a detailed understanding of when and how the first pre- and postsynaptic signaling machineries evolved.

Highlights

Recent sequencing of genomes from non-bilaterian metazoans and their closest relatives has greatly enhanced our understanding on the origin of synapses, a central characteristic of neurons
That even in close relatives of metazoans some proto-synaptic genes seem to be co-regulated at the transcriptional level and suggests that parts of the synaptic signaling machinery might have been co-opted from ancestral roles that may still be observable today in their close relatives
The specific upregulation of voltage gated Na–channels and secretory soluble N-ethylmaleimide-sensitive-factor attachment receptors (SNAREs) in S. rosetta colonies makes it tempting to speculate that choanoflagellate cells can communicate with each other by electrical and/or chemical signaling using proto-synaptic proteins, a hypothesis that can be tested in the future with cell labeling, electrophysiological experiments, calcium imaging, and even proteomic interaction studies

Summary

Review essays

The evolutionary origin of synapses and neurons is an enigmatic subject that inspires much debate. In the metazoan nervous system, the interplay between specialized presynaptic and postsynaptic molecular machineries allows the translation of electrical membrane currents into chemical signals in the presynaptic cell, which in turn elicit electrical currents (or intracellular signaling pathways) in the postsynaptic cell It is worth mentioning, that even in metazoans with synapses and neurons synaptic proteins are functionally diverse and fulfil different roles in other cell types (Fig. 2) [52]. Biochemical and structural studies on choanoflagellate CaMKII provided direct evidence into how subunits of CaMKII can interchange and spread information [67] (Fig. 3C box) and is another exciting example for how close relatives of metazoans can reveal important, previously unknown insights into the molecular mechanism of metazoan synaptic protein function. Sponge globular cells, placozoan gland cells, and neurons in all other metazoans have evolved from a primordial secretory or sensory cell [74, 75]

When looking at the first appearance of

Concluding remarks