A sleep-like state in <i>Hydra</i> unravels conserved sleep mechanisms during the evolutionary development of the central nervous system

Abstract

Sleep behaviors are observed even in nematodes and arthropods, yet little is known about how sleep-regulatory mechanisms have emerged during evolution. Here, we report a sleep-like state in the cnidarian <i>Hydra vulgaris</i> with a primitive nervous organization. <i>Hydra</i> sleep was shaped by homeostasis and necessary for cell proliferation, but it lacked free-running circadian rhythms. Instead, we detected 4-hour rhythms that might be generated by ultradian oscillators underlying <i>Hydra</i> sleep. Microarray analysis in sleep-deprived <i>Hydra</i> revealed sleep-dependent expression of 212 genes, including cGMP-dependent protein kinase 1 (PRKG1) and ornithine aminotransferase. Sleep-promoting effects of melatonin, GABA, and PRKG1 were conserved in <i>Hydra</i> However, arousing dopamine unexpectedly induced <i>Hydra</i> sleep. Opposing effects of ornithine metabolism on sleep were also evident between <i>Hydra</i> and <i>Drosophila</i>, suggesting the evolutionary switch of their sleep-regulatory functions. Thus, sleep-relevant physiology and sleep-regulatory components may have already been acquired at molecular levels in a brain-less metazoan phylum and reprogrammed accordingly.