Behavioral circatidal rhythms require Bmal1 in Parhyale hawaiensis

Kwiatkowski, Erica; Schnytzer, Yisrael; Rosenthal, Joshua J. C.; Emery, Patrick

doi:10.1016/j.cub.2023.03.015

Cited by 13 publications

(9 citation statements)

References 67 publications

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“…A possible model for the circatidal clock is shown in the righthand panel. BMAL1 (also see ref [ 36 ] and CK1ε (and perhaps CLK) are common to both mechanisms but the circatidal negative regulators are unknown at this time.…”

Section: Discussionmentioning

confidence: 99%

The circadian clock gene bmal1 is necessary for co-ordinated circatidal rhythms in the marine isopod Eurydice pulchra (Leach)

Lin,

Green,

Webster

et al. 2023

PLoS Genet

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Circadian clocks in terrestrial animals are encoded by molecular feedback loops involving the negative regulators PERIOD, TIMELESS or CRYPTOCHROME2 and positive transcription factors CLOCK and BMAL1/CYCLE. The molecular basis of circatidal (~12.4 hour) or other lunar-mediated cycles (~15 day, ~29 day), widely expressed in coastal organisms, is unknown. Disrupting circadian clockworks does not appear to affect lunar-based rhythms in several organisms that inhabit the shoreline suggesting a molecular independence of the two cycles. Nevertheless, pharmacological inhibition of casein kinase 1 (CK1) that targets PERIOD stability in mammals and flies, affects both circadian and circatidal phenotypes in Eurydice pulchra (Ep), the speckled sea-louse. Here we show that these drug inhibitors of CK1 also affect the phosphorylation of EpCLK and EpBMAL1 and disrupt EpCLK-BMAL1-mediated transcription in Drosophila S2 cells, revealing a potential link between these two positive circadian regulators and circatidal behaviour. We therefore performed dsRNAi knockdown of Epbmal1 as well as the major negative regulator in Eurydice, Epcry2 in animals taken from the wild. Epcry2 and Epbmal1 knockdown disrupted Eurydice’s circadian phenotypes of chromatophore dispersion, tim mRNA cycling and the circadian modulation of circatidal swimming, as expected. However, circatidal behaviour was particularly sensitive to Epbmal1 knockdown with consistent effects on the power, amplitude and rhythmicity of the circatidal swimming cycle. Thus, three Eurydice negative circadian regulators, EpCRY2, in addition to EpPER and EpTIM (from a previous study), do not appear to be required for the expression of robust circatidal behaviour, in contrast to the positive regulator EpBMAL1. We suggest a neurogenetic model whereby the positive circadian regulators EpBMAL1-CLK are shared between circadian and circatidal mechanisms in Eurydice but circatidal rhythms require a novel, as yet unknown negative regulator.

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Section: Discussionmentioning

confidence: 99%

The circadian clock gene bmal1 is necessary for co-ordinated circatidal rhythms in the marine isopod Eurydice pulchra (Leach)

Lin,

Green,

Webster

et al. 2023

PLoS Genet

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“…Separate circadian and circatidal clocks were also reported in the intertidal isopod Eurydice pulchra [64] and mangrove cricket Apteronemobius asahinai [65]. Nevertheless, the core clock genes still encode functional proteins with conserved domains (S6E Fig), and we cannot exclude the possibility that some core circadian clock genes are necessary for tidal rhythms [66, 67], even though they lose free-running transcription rhythmicity. These circadian clock genes may also be useful during the larval dispersal stage of the shrimp, which may take place in the photic zone [68].…”

Section: Resultsmentioning

confidence: 84%

Circatidal control of gene expression in the deep-sea hot vent shrimpRimicaris leurokolos

Zhang,

Yahagi,

Miyamoto

et al. 2024

Preprint

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Biological clocks are a ubiquitous feature of all life, enabling the use of natural environmental cycles to track time. Although studies on circadian rhythms have contributed greatly to the knowledge of chronobiology, biological rhythms in dark biospheres such as the deep sea remain poorly understood. Despite a lack of day-night cycles, the deep sea is still affected by the tide, and some recent evidences suggest that the tidal cycle likely has non-negligible temporal effects on deep-sea organisms. Here, based on a free-running experiment, we reveal potentially endogenous biological rhythms in the gene expression of the deep-sea hydrothermal vent shrimp Shinkaicaris leurokolos. Oscillations with ~12-hour periods, likely reflecting tidal influence, greatly prevail over others in the temporal transcriptome. The tidal oscillated rhythms exhibit an antiphased expression pattern divided into two internally synchronized clusters, correlated with wide-ranging biological processes in the nucleus and cytoplasm, respectively. In some cases, circadian clock genes are necessary for circatidal rhythms and can be adjusted to tidal frequency. However, almost none of the identified S. leurokolos circadian clock genes show obvious rhythmicity, likely indicating an independent circatidal clock. These findings provide new insights into the temporal adaptations in deep-sea organisms and suggest that deep-sea hydrothermal vent organisms may be intriguing models for chronobiological studies.

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“…Although we found hundreds of genes oscillating in a circadian and circatidal period, it remains unclear whether snails possess independent circatidal clocks alongside circadian clocks or a shared timekeeping system between circadian and circatidal rhythms. The latter hypothesis is gaining support, particularly in studies on biological clocks in marine species (Schnytzer et al 2018 ; Tran et al 2020 ; Mat et al 2020 ; Kwiatkowski et al 2023 ). Further investigations are needed to elucidate the genetic mechanisms underlying circatidal clocks in freshwater snails.…”

Section: Discussionmentioning

confidence: 98%

“…Notably, certain circadian clock genes in the Pacific oyster Crassostrea gigas exhibit oscillation at tidal frequencies under tidal conditions (Mat et al 2016 ; Tran et al 2020 ). In the amphipod crustacean Parhyale hawaiensis , the core circadian clock gene Bmal1 is suggested to be essential for circatidal rhythms (Kwiatkowski et al 2023 ). These studies give rise to the hypothesis that the circadian and circatidal rhythms may be generated by a single biological timekeeping system, with circatidal clocks sharing some molecular components with circadian clocks.…”

Section: Introductionmentioning

confidence: 99%

Plasticity of circadian and circatidal rhythms in activity and transcriptomic dynamics in a freshwater snail

Yokomizo,

Takahashi

2024

Heredity

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Organisms have diverse biological clocks synchronised with environmental cycles depending on their habitats. Anticipation of tidal changes has driven the evolution of circatidal rhythms in some marine species. In the freshwater snail, Semisulcospira reiniana, individuals in nontidal areas exhibit circadian rhythms, whereas those in tidal areas exhibit both circadian and circatidal rhythms. We investigated whether the circatidal rhythms are genetically determined or induced by environmental cycles. The exposure to a simulated tidal cycle did not change the intensity of circatidal rhythm in individuals in the nontidal population. However, snails in the tidal population showed different activity rhythms depending on the presence or absence of the exposure. Transcriptome analysis revealed that genes with circatidal oscillation increased due to entrainment to the tidal cycle in both populations and dominant rhythmicity was consistent with the environmental cycle. These results suggest plasticity in the endogenous rhythm in the gene expression in both populations. Note that circatidal oscillating genes were more abundant in the tidal population than in the nontidal population, suggesting that a greater number of genes are associated with circatidal clocks in the tidal population compared to the nontidal population. This increase of circatidal clock–controlled genes in the tidal population could be caused by genetic changes in the biological clock or the experience of tidal cycle in the early life stage. Our findings suggest that the plasticity of biological rhythms may have contributed to the adaptation to the tidal environment in S. reiniana.

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Behavioral circatidal rhythms require Bmal1 in Parhyale hawaiensis

Cited by 13 publications

References 67 publications

The circadian clock gene bmal1 is necessary for co-ordinated circatidal rhythms in the marine isopod Eurydice pulchra (Leach)

The circadian clock gene bmal1 is necessary for co-ordinated circatidal rhythms in the marine isopod Eurydice pulchra (Leach)

Circatidal control of gene expression in the deep-sea hot vent shrimpRimicaris leurokolos

Plasticity of circadian and circatidal rhythms in activity and transcriptomic dynamics in a freshwater snail

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