Choanoflagellates and the ancestry of neurosecretory vesicles

Golhde, R; Naumann, B; Laundon, D; Imig, C; McDonald, K; Cooper, BH; Varoqueaux, F; Fasshauer, D; Burkhardt, P. 2021 Choanoflagellates and the ancestry of neurosecretory vesicles. Philosophical Transactions of the Royal Society of London Series B-Biological Sciences, 376 (1821). https://doi.org/10.1098/rstb.2019.0759

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Abstract/Summary

Neurosecretory vesicles are highly specialized trafficking organelles that store neurotransmitters that are released at presynaptic nerve endings and are, therefore, important for animal cell–cell signalling. Despite considerable anatomical and functional diversity of neurons in animals, the protein composition of neurosecretory vesicles in bilaterians appears to be similar. This similarity points towards a common evolutionary origin. Moreover, many putative homologues of key neurosecretory vesicle proteins predate the origin of the first neurons, and some even the origin of the first animals. However, little is known about the molecular toolkit of these vesicles in non-bilaterian animals and their closest unicellular relatives, making inferences about the evolutionary origin of neurosecretory vesicles extremely difficult. By comparing 28 proteins of the core neurosecretory vesicle proteome in 13 different species, we demonstrate that most of the proteins are present in unicellular organisms. Surprisingly, we find that the vesicular membrane-associated soluble N-ethylmaleimide-sensitive factor attachment protein receptor protein synaptobrevin is localized to the vesicle-rich apical and basal pole in the choanoflagellate Salpingoeca rosetta. Our 3D vesicle reconstructions reveal that the choanoflagellates S. rosetta and Monosiga brevicollis exhibit a polarized and diverse vesicular landscape reminiscent of the polarized organization of chemical synapses that secrete the content of neurosecretory vesicles into the synaptic cleft. This study sheds light on the ancestral molecular machinery of neurosecretory vesicles and provides a framework to understand the origin and evolution of secretory cells, synapses and neurons.

Item Type: Publication - Article
Subjects: Biology
Marine Sciences
Divisions: Marine Biological Association of the UK > Knowledge Exchange
Depositing User: Tamar Atkinson
Date made live: 09 Feb 2022 14:31
Last Modified: 09 Feb 2022 14:31
URI: http://plymsea.ac.uk/id/eprint/9546

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