The endogenous calendar of marine animals

The bristle worm, Platynereis dumerilii, possess a monthly (circalunar) clock that runs independently of the oscillations of its daily (circadian) clock. However, both clocks jointly regulate the level of specific transcripts, as well as locomotor behavior.

HFSP Young Investigator Grant holders Kristin Tessmar-Raible and Tomoko Ishikawa and colleagues
authored on Fri, 13 December 2013

Obviously, animals neither possess watches nor calendars. However, they do exhibit physiological or behavioral rhythms on very different time scales. If such rhythms continue even in the absence of external stimuli, it means that endogenous oscillators, so-called molecular clocks, control them.

In addition to the daily cycles provided by the sun, many marine animals – ranging from corals to vertebrates – utilize the steady cycle of the moon to synchronize reproductive behaviour and sexual maturation on a monthly schedule. It has been shown that several of these species indeed possess an endogenous monthly oscillator (called a circalunar clock) in addition to their circadian clocks. The molecular mechanisms of such non-circadian clocks, however, have remained obscure. Even the seemingly simple question if the circalunar clock requires the circadian clock for its function had remained open. Young Investigator Grant holders, Kristin Tessmar-Raible (Max F. Perutz Lab., University of Vienna) and Tomoko Ishikawa (Osaka University), in collaboration with Andrew Straw from the Institute for Molecular Pathology (IMP), laid the first molecular groundwork to understand the circalunar clock of the bristle worm Platynereis dumerilii. Most interestingly, by blocking the function of casein kinase1∂/ε, a key regulator of animal circadian clocks, it was found that the circalunar clock is independent of the oscillations of the worm’s circadian clock. This strongly suggests that circadian and circalunar clocks are molecularly distinct. In turn, however, it was also found that the circalunar clock impacts on the worm’s circadian locomotor behavior: whereas during “new moon” days, worms were mostly active during the night, they showed much shorter activity cycles and more activity during the day when analyzed two weeks later when they expected to be in a “full moon” period. Notably, the worms exhibited this behavioral change, even if the dim nocturnal light stimulus that signals ‘full moon’ to them was omitted in these experiments, providing strong evidence that the change is indeed controlled by their internal circalunar oscillator, and not simply a response to nocturnal light.

A key prerequisite for the study was that the molecular basis for the circadian clock in the worm had to be established. Similar to data from Steven Reppert’s group for the monarch butterfly, it was found that Platynereis possesses both a fruit fly-like and a vertebrate-type cryptochrome and thereby represents a more ancestral circadian clock repertoire. This is where the collaborations within the HFSP team have been especially important and in part are already documented in the recently published manuscript. Tomoko Ishikawa’s and Takeshi Todo’s teams have started to biochemically characterize the worm’s cryptochrome and photolyase-type molecules.

This work presents an entry point into understanding how different clocks interact within an organism that likely never left the marine habitat in which animal life is thought to have evolved. Inevitably, it also raises the question to which extent such non-circadian clocks may still “tick” in creatures whose ancestors left the sea a long time ago. The answer to this is open, but it might be interesting to consider how meaningful the different rhythmic changes of nature might have been to our ancestors at times when humans were not surrounded by plenty of artificial light, clocks and calendars.

Reference

Circadian and circalunar clock interactions in a marine annelid. Zantke J, Ishikawa-Fujiwara T, Arboleda E, Lohs C, Schipany K, Hallay N, Straw AD, Todo T, Tessmar-Raible K.Cell Rep.2013 Oct 17;5(1):99-113. doi: 10.1016/j.celrep.2013.08.031. Epub 2013 Sep 26.

Pubmed link

Link to Cell Reports article