DNA damage modulates sleep drive in basal cnidarians with divergent chronotypes
Raphaël Aguillon, Amir Harduf, Dana Sagi, Noa Simon‐Blecher, Oren Levy, Lior Appelbaum
Abstract
Sleep is a conserved behavior across all animals with a nervous system, ranging from cnidarians to humans. Considering the survival risks, why sleep evolved in basal lineages and what essential benefits it provides to the simple nerve net of nocturnal and diurnal invertebrates remain elusive. We used behavioral criteria to empirically define sleep in the upside-down jellyfish Cassiopea andromeda and the starlet sea anemone Nematostella vectensis. Light and homeostasis were the primary drivers of sleep in C. andromeda, which slept at night and napped at midday in both the laboratory and the natural habitat. In contrast, both the circadian clock and homeostatic processes regulated sleep in N. vectensis, which increased sleep at dawn. Similar to humans, C. andromeda, wild-type (WT) and Clock mutant (NvClkΔ/Δ) N. vectensis slept about one-third of the day, irrespective of the daily timing and architecture of sleep, and melatonin promoted sleep in accordance with the species-specific chronotype. Notably, sleep deprivation, ultraviolet radiation, and mutagens increased neuronal DNA damage and sleep pressure, while spontaneous and induced sleep facilitated genome stability in both the diurnal and crepuscular cnidarians. These results suggest that DNA damage and cellular stress in simple nerve nets may have driven the evolution of sleep. Here, the authors use the diurnal upside-down jellyfish and the crepuscular starlet sea anemone as simple nerve net models to examine the potential evolutionary origins of sleep. They describe and define sleep patterns in these species, finding that sleep deprivation increases neuronal DNA damage and that sleep facilitates genome stability.