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bioRxiv · 10.1101/2024.10.04.616757

Cholinergic regulation of sleep in the upside-down jellyfish Cassiopea

Abrams, M. J.·Ohdera, A. H.·Francis, D. A.·Donayre, O.·Chen, H.·Lu, K. Y.·Harland, R. M.
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Abstract

Perhaps nothing is stronger evidence of the importance of sleep than its conservation across animals [1], but the extent of its regulatory conservation is unknown. The upside-down jelly-fish Cassiopea xamachana sleeps [2], and this behavior is controlled by radially-spaced marginal ganglia. After defining a sleep-wake threshold, we compared gene expression profiles of ganglia from animals sleep-deprived for two nights and found differential expression in many sleep-related genes including GABAergic, melatonergic, and cholinergic receptors. We focused on a nicotinic acetylcholine receptor alpha subunit-like (Chrnal-E), based on its differential expression, and selected animals for a second round of RNAseq that included both light-based and mechanically-based sleep-deprivation. Combining datasets revealed a short list of differentially expressed genes, of which chrnal-E is the most recognizable and well-supported, so we investigated its potential role in sleep regulation. First, we found that chemical cholinergic neuromodulators positively regulate pacemaker activity. Then, we showed by in situ hybridization that chrnal-E is expressed primarily within the ganglia, and that the area of expression expands after sleep deprivation. Next, we developed RNAi for use in Cassiopea and determined that Chrnal-E promotes wakefulness. Finally, we sampled circadian timepoints in the field and found in control conditions, chrnal-E has lowest expression late at night, but in sleep deprived animals, chrnal-E peaks at this time, supporting a link to wakefulness. Our finding that Cassiopea sleep is regulated by the cholinergic system underscores that mechanisms of sleep conservation are deeply conserved in animal evolution.

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Abrams, M. J., Ohdera, A. H., Francis, D. A., Donayre, O., Chen, H., Lu, K. Y., Harland, R. M.. 2024-10-05. Cholinergic regulation of sleep in the upside-down jellyfish Cassiopea. https://doi.org/10.1101/2024.10.04.616757

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