Two light sensors decode moonlight versus sunlight to adjust a plastic circadian/circalunidian clock to moon phase

Abstract

Significance The moon provides highly reliable time information to organisms. Whereas sunlight is known to set daily animal timing systems, mechanistic insight into the impact of moonlight on such systems remains scarce. We establish that the marine bristleworm Platynereis dumerilii times the precise hours of mass spawning by integrating lunar light information into a plastic daily timing system able to run with circadian (∼24 h) or circalunidian (∼24.8 h) periodicity. The correct interpretation of moonlight is mediated by the interplay of two light sensors: a cryptochrome and a melanopsin ortholog provide information on light valence and moonrise time, respectively. Besides its ecological relevance, our work provides a plausible explanation for long-standing observations of light intensity–dependent differences in circadian clock periods.

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

“…In an independent study that focused on the impact of moonlight on daily timing, we identified r-Opsin1 as a lunar light receptor that mediates moonlight effects on the worms’ ~24 h clock 36 . We tested if r-opsin1 is similarly important for mediating the moonlight effects on the monthly oscillator of the worm, analyzed here.…”

“…Additionally, the L-Cry dimer enables the formation of a third distinct partially photoreduced moonlight state in addition to the dark- and sunlight states. All these molecular properties of L-Cry are required to define the full moon phase as the moon phase with the highest moonlight intensity and longest duration on the night sky: The low light sensing L-Cry monomer detects moonlight (this study) and measures its intensity via the dose-dependent FAD photoreduction rate 36 . In turn, the moonlight duration is measured by the interconversion between the three L-Cry states.…”

A fast and versatile method for simultaneous HCR, immunohistochemistry and EdU labeling (SHInE)

“…One of the interesting aspects about Platynereis dumerilii is its use as a functional molecular model system for chronobiological analyses (Özpolat et al, 2021b; Raible and Tessmar-Raible, 2014). At least two endogenous timing systems – a ~24hr (plastic circadian-circalunidian) and a monthly (circalunar) one – co-exist in Platynereis and are influenced by ambient light conditions (Zantke et al, 2013) (Poehn et al, 2022; Zurl et al, 2022). Period is a key gene of the circadian clock (Glossop and Hardin, 2002).…”

“…To test the compatibility of SHInE with IHC, immunostainings were performed on the same samples using antibodies raised against Platynereis L-Cryptochrome (L-Cry). L-Cry is a photoreceptor that shares regions of expression with period and is well described also on the sub-cellular level for P.dumerilii (Poehn et al, 2022; Zurl et al, 2022). In line with the published expression patterns, the acquisition of SHInE-processed heads revealed expression of L-Cry in the medial brain nuclei and in the eyes (Figure 2C,D), in the same region as period RNA (Figure 2A,D).…”

Common Ground between Biological Rhythms and Forensics

“…Additionally, biological rhythms are not necessarily separately acting mechanisms, but their ways of interactions and influences on each other have to be clarified further. Recently, a study revealed that moon light also impacts the timing of daily behavior in addition to its known impact on the timing of monthly behavior in P. dumerilii [ 136 ]. Thus, future studies need to determine the presence and role of circannual and circalunar rhythms in humans in order to evaluate potential relevance to the PMI or age determination in later studies, together with the already existing knowledge of individual chronotypes and circadian rhythms.…”