How animals use their circalunar clock to control sexual maturation and reproduction

International research team deciphers molecular mechanism that allows bristle worms to discriminate between sun- and moonlight

13 September 2022

How animals are able to interpret natural light sources to adjust their physiology and behavior is poorly understood. The labs of biologists Professor Eva Wolf of Johannes Gutenberg University Mainz (JGU) and the Institute of Molecular Biology in Mainz and Professor Kristin Tessmar-Raible of the Max Perutz Labs in Vienna, the Alfred Wegener Institute in Bremerhaven, und Carl von Ossietzky University of Oldenburg have now revealed that a molecule called L-cryptochrome (L-Cry) has the biochemical properties to discriminate between sun- and moonlight and even between different moon phases. Their findings, published in Nature Communications, show that L-Cry can interpret moonlight to entrain the monthly circalunar clock of a marine worm to control and optimize sexual maturation and reproduction.

Many marine organisms, including brown algae, fish, corals, turtles and bristle worms, synchronize their behavior and reproduction with the lunar cycle. For some species, such as the bristle worm Platynereis dumerilii, lab experiments have shown that moonlight exerts its timing function by entraining an inner monthly calendar, also called circalunar clock. Under lab conditions, mimicking the duration of the full moon is sufficient to entrain these circalunar clocks. However, in natural habitats light conditions can vary considerably. Even the regular interplay of sun- and moon creates highly complex patterns. Organisms using the lunar light for their timing thus need to discriminate between specific moon phases and between sun and moonlight. This ability is not well understood. "We have now revealed that a light receptive molecule, called L-Cry, is able to discriminate between different light valences," said Professor Kristin Tessmar-Raible. L-Cry serves as a light sensor that is able to measure light intensity and duration, thus helping the animals to choose the right light to adequately adjust their monthly timing system.

The research team characterized L-Cry from its biochemistry to functional genetics. "We found that the ability of L-Cry to interpret light correlates with distinct molecular states of L-Cry," explained Professor Eva Wolf. Particularly, the cryptochrome contains cofactors, i.e., non-protein components, essential for its function. These co-factors, called flavin adenine dinucleotides (FAD), undergo biochemical changes under the influence of light, where dark-adapted oxidized FAD transitions to a photoreduced FAD state. The Mainz-based researchers worked out that L-Cry proteins exposed to naturalistic moonlight accumulate the low photon numbers of the moonlight over hours, but at most only half of the FADs get photoreduced. In contrast, the more than 10,000-fold higher photon number of the naturalistic sunlight used in the experiments causes a rapid photoreduction of all FAD molecules within minutes. The authors suggest that consequently, L-Cry acquires distinct structural and biochemical properties depending on the combinatorial status of the FADs in its dimer. Thereby it serves not only as an efficient, but also discriminatory light sensor over an extremely wide-range of natural light intensities. The research team headed by Professor Kristin Tessmar-Raible was also able to show that L-Cry undergoes changes in its subcellular localization, depending on its exposure to sunlight or moonlight. How this differential localization translates into different signaling pathways that control behavior and physiology, and how the light-induced transport of L-Cry between nucleus and cytoplasm is achieved, are key questions that will be the subjects of further studies. 

Threat of artificial light sources at night

This molecular mechanism is also relevant for other biological clocks and light-controlled processes: "We think that what we have uncovered goes beyond the monthly timing system. It could be a more general process that helps organisms to recognize light sources," said Professor Eva Wolf. And Professor Kristin Tessmar-Raible added: "This is of key ecological importance for any organism that adjusts its physiology and behavior by light. Moonlight is not just a dim version of sunlight, it has very different temporal-ecological implications for organisms." Consequently, perturbations through nocturnal light pollution pose serious threats to natural ecosystems and also human health. A better understanding of how moon light is sensed and processed may also help assess and mitigate the negative impacts of artificial light.