A Cryptochrome adopts distinct moon- and sunlight states and functions as sun- versus moonlight interpreter in monthly oscillator entrainment

Abstract The moon’s monthly cycle synchronizes reproduction in countless marine organisms. The mass-spawning bristle worm Platynereis dumerilii uses an endogenous monthly oscillator to phase reproduction to specific days. Classical work showed that this oscillator is set by full moon. But how do organisms recognize such a specific moon phase? We uncover that the light receptor L-Cryptochrome (L-Cry) is able to discriminate between different moonlight durations, as well as between sun- and moonlight. Consistent with L-Cry’s function as light valence interpreter, its genetic loss leads to a faster re-entrainment under artificially strong nocturnal light. This suggests that L-Cry blocks “wrong” light from impacting on the monthly oscillator. A biochemical characterization of purified L-Cry protein, exposed to naturalistic sun- or moonlight, reveals the formation of distinct sun- and moonlight states characterized by different photoreduction- and recovery kinetics of L-Cry’s co-factor Flavin Adenine Dinucleotide. In vivo, L-Cry’s sun-versus moonlight states correlate with distinct sub-cellular localizations, indicating different signalling. In contrast, r-Opsin1, the most abundant ocular opsin, is not required for monthly oscillator entrainment. Our work reveals a new concept for correct moonlight interpretation involving a “valence interpreter” that provides entraining photoreceptor(s) with light source and moon phase information. These findings advance our mechanistic understanding of a fundamental biological phenomenon: moon-controlled monthly timing. Such level of understanding is also an essential prerequisite to tackle anthropogenic threats on marine ecology.