Layden, M. J. | Search bioRxiv

bioRxiv2018

The origin and evolution of acetylcholine signaling through AchRs in metazoans

BackgroundAcetylcholine is a cell signaling molecule that has been identified in plants, bacteria, and metazoans to play multiple roles in cells and as a neurotransmitter capable of exciting both neurons and muscle. While cell-cell communication activity has been reported in all phyla that have been investigated, its role as a neurotransmitter is less clear. Work within cnidarians implies that neurotransmitter activity emerged within or prior to the emergence of the cnidarian-bilaterian ancestor, but whether or not it is able to excite both muscles and neurons has not been addressed.\n\nResultsTo investigate the evolution of acetylcholine signaling we characterized the expression pattern of acetylcholine receptors (AchRs) and the neurotransmitter activity of acetylcholine in Nematostella vectensis. Expression patterns for 13 of the 21 known NvAchRs are consistent with acetylcholine acting as a cell signaling molecule and a neurotransmitter in neurons, muscles, or both. To dissect neurotransmitter activity we investigated the mechanism by which acetylcholine activates tentacular contractions in Nematostella. Tentacular contractions induced by application of acetylcholine are suppressed by inactivating voltage gated sodium channels with lidocaine indicating that acetylcholine specifically activates neurons in the tentacular contractile circuit.\n\nConclusionOur results verify that acetylcholines neurotransmitter activity emerged prior to cnidarian-bilaterian divergence and that non-neuronal roles were likely retained in Nematostella. Additionally, we found no evidence to support a muscle activating role for acetylcholine indicating that its role in muscle excitability evolved during bilaterian evolution.

developmental biology↗

bioRxiv2017

Characterization Of NvLWamide-Like Neurons Reveals Stereotypy In Nematostella Nerve Net Development

Cnidarian nervous systems are traditionally described as diffuse nerve nets lacking true organization. However, there are examples of stereotypical structure in the nerve nets of multiple cnidarian species that suggest nerve nets are organized. We previously demonstrated that the NvashA target gene NvLWamide-like is expressed in a small subset of the Nematostella nerve net and speculated that observing a few neurons within the developing nerve net would provide a better indication of potential stereotypy. Here we document NvLWamide-like expression more systematically. NvLWamide-like is initially expressed in the typical neurogenic salt and pepper pattern within the ectoderm at the gastrula stage, and expression expands to include endodermal salt and pepper expression at the planula larval stage. Expression persists in both ectoderm and endoderm in adults. We generated an NvLWamide-like::mCherry transgenic reporter line to visualize the neural architecture. NvLWamide-like is expressed in six neural subtypes identifiable by neural morphology and location. Upon completing development the numbers of neurons in each neural subtype are minimally variable between animals and the projection patterns of each subtype are consistent. Between the juvenile polyp and adult stages the number of neurons for each subtype increases. We conclude that cnidarian nerve nets are organized, develop in a stereotyped fashion, and that one aspect of generating the adult nervous system is to modify the juvenile nervous system by increasing neural number proportionally with size.

developmental biology↗