Differential Impacts of the Head on Platynereis dumerilii Peripheral Circadian Rhythms.

Enrique Arboleda,Monika Waldherr,Kristin Tessmar-Raible,Martin Zurl

doi:10.3389/fphys.2019.00900

Enrique Arboleda, Monika Waldherr + Show 2 more

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https://doi.org/10.3389/fphys.2019.00900

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Abstract

The marine bristle worm Platynereis dumerilii is a useful functional model system for the study of the circadian clock and its interplay with others, e.g., circalunar clocks. The focus has so far been on the worm’s head. However, behavioral and physiological cycles in other animals typically arise from the coordination of circadian clocks located in the brain and in peripheral tissues. Here, we focus on peripheral circadian rhythms and clocks, revisit and expand classical circadian work on the worm’s chromatophores, investigate locomotion as read-out and include molecular analyses. We establish that different pieces of the trunk exhibit synchronized, robust oscillations of core circadian clock genes. These circadian core clock transcripts are under strong control of the light-dark cycle, quickly losing synchronized oscillation under constant darkness, irrespective of the absence or presence of heads. Different wavelengths are differently effective in controlling the peripheral molecular synchronization. We have previously shown that locomotor activity is under circadian clock control. Here, we show that upon decapitation worms exhibit strongly reduced activity levels. While still following the light-dark cycle, locomotor rhythmicity under constant darkness is less clear. We also observe the rhythmicity of pigments in the worm’s individual chromatophores, confirming their circadian pattern. These size changes continue under constant darkness, but cannot be re-entrained by light upon decapitation. Our works thus provides the first basic characterization of the peripheral circadian clock of P. dumerilii. In the absence of the head, light is essential as a major synchronization cue for peripheral molecular and locomotor circadian rhythms, while circadian changes in chromatophore size can continue for several days in the absence of light/dark changes and the head. Thus, in Platynereis the dependence on the head depends on the type of peripheral rhythm studied. These data show that peripheral circadian rhythms and clocks should also be considered in “non-conventional” molecular model systems, i.e., outside Drosophila melanogaster, Danio rerio, and Mus musculus, and build a basic foundation for future investigations of interactions of clocks with different period lengths in marine organisms.

Highlights

Extensive research focusing on drosophilids and mice showed that the daily behavioral, physiological and metabolic cycles in animals arise from coordination of central circadian clocks located in the brain and peripheral clocks present in multiple tissues (Richards and Gumz, 2012; Mure et al, 2018; Pilorz et al, 2018)
A post hoc pairwise Tukey analysis for the interaction shows that the low relative mRNA levels at ZT5 on trunks under LD conditions is the main difference between these two conditions
We find that the overall circadian clock transcript oscillations of the trunk are under strong control of the LD cycle and do not show synchronized oscillation under constant darkness, irrespective of the absence or presence of heads

Summary

Introduction

Extensive research focusing on drosophilids and mice showed that the daily behavioral, physiological and metabolic cycles in animals arise from coordination of central circadian clocks located in the brain and peripheral clocks present in multiple tissues (Richards and Gumz, 2012; Mure et al, 2018; Pilorz et al, 2018). The master central clock in the suprachiasmatic nucleus (SCN) of the brain (often referred to as a “conductor”) synchronizes internal clock timing to the environmental solar day by passing the information to the peripheral clocks via endocrine and systemic cues (Mohawk et al, 2012; Partch et al, 2014). These peripheral clocks have self-sustained circadian oscillators, with the master clock coordinating their phase to prevent desynchronization among peripheral tissues, rather than acting as a pacemaker responsible for the periodicity of the cycling itself (Yoo et al, 2004). Besides being phase-controlled by the “SCN conductor,” several mammalian peripheral clocks (e.g., in liver and kidney) have been shown to directly respond to non-photic entrainment cues, like food or exercise (Tahara and Shibata, 2018)

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