Circadian and Circalunar Clock Interactions in a Marine Annelid

Juliane Zantke,Tomoko Ishikawa-Fujiwara,Enrique Arboleda,Claudia Lohs,Katharina Schipany,Natalia Hallay,Andrew D Straw,Takeshi Todo,Kristin Tessmar-Raible

doi:10.1016/j.celrep.2013.08.031

Juliane Zantke, Tomoko Ishikawa-Fujiwara + Show 7 more

Open Access

https://doi.org/10.1016/j.celrep.2013.08.031

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Abstract

SummaryLife is controlled by multiple rhythms. Although the interaction of the daily (circadian) clock with environmental stimuli, such as light, is well documented, its relationship to endogenous clocks with other periods is little understood. We establish that the marine worm Platynereis dumerilii possesses endogenous circadian and circalunar (monthly) clocks and characterize their interactions. The RNAs of likely core circadian oscillator genes localize to a distinct nucleus of the worm’s forebrain. The worm’s forebrain also harbors a circalunar clock entrained by nocturnal light. This monthly clock regulates maturation and persists even when circadian clock oscillations are disrupted by the inhibition of casein kinase 1δ/ε. Both circadian and circalunar clocks converge on the regulation of transcript levels. Furthermore, the circalunar clock changes the period and power of circadian behavior, although the period length of the daily transcriptional oscillations remains unaltered. We conclude that a second endogenous noncircadian clock can influence circadian clock function.

Highlights

Most, if not all, organisms feed periodic changes in light conditions into molecular clockworks that allow them to anticipate rhythmic changes in their environment and to synchronize their behavior and physiology (Cold Spring Harbor Symposia on Quantitative Biology, 2007; Roenneberg and Merrow, 2005)
We establish that the marine worm Platynereis dumerilii possesses endogenous circadian and circalunar clocks and characterize their interactions
The worm’s forebrain harbors a circalunar clock entrained by nocturnal light. This monthly clock regulates maturation and persists even when circadian clock oscillations are disrupted by the inhibition of casein kinase 1d/ε

Summary

Introduction

If not all, organisms feed periodic changes in light conditions into molecular clockworks that allow them to anticipate rhythmic changes in their environment and to synchronize their behavior and physiology (Cold Spring Harbor Symposia on Quantitative Biology, 2007; Roenneberg and Merrow, 2005). One of the critical mechanisms driving animal circadian clocks are transcriptional/translational feedback loops formed by a set of regulatory genes. These genes are partially shared between insect and mammalian models, arguing for a common origin of animal circadian clocks. The feedback loops continue to run under constant conditions and are coordinated with the animal’s environment by entrainment (Cold Spring Harbor Symposia on Quantitative Biology, 2007; Roenneberg and Merrow, 2005). As with circadian rhythms, such noncircadian (e.g., annual and monthly) rhythms are often driven by internal oscillators (circannual and circalunar clocks, respectively), which use light cues (photoperiod and moonlight, respectively) for the adjustment with the outer environmental conditions (Dupreand Loudon, 2007; Franke, 1985; Lincoln et al, 2006; Naylor, 2010; Hazlerigg and Lincoln, 2011; Kaiser et al, 2011)

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