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

Abstract

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.

The rhythmic transcriptional landscape inCaenorhabditis elegans: daily, circadian and novel 16-hour cycling gene expression revealed by RNA-sequencing

“…Ultradian (< 24-hour) rhythms have been widely reported in nature, including 12-hour harmonics of the circadian rhythm in mouse and human transcriptomic data [92,104] and also in C. elegans (again from the 2010 dataset) [93]. Circatidal rhythms, rhythms of a similar periodicity synchronised by tides, can also be seen in marine organisms across phyla, in some cases being contingent on expression of TTFL-essential genes and proteins [114][115][116][117][118][119]. However, the 16-hour co-expression we observe is distinct in period from these harmonics along with other shorter periodic events in C. elegans including defecation [120,121], egg laying [122] and pulsatile developmental gene expression [123].…”

Editorial: Rising stars in chronobiology 2022

“…Chronobiology is the study of biological rhythms. The majority of studies in chronobiology to date have largely focused on circadian or 24-h rhythms, but there have been increasing interests in non-circadian biological rhythms, including seasonal rhythms ( Wood and Loudon, 2014 ; Liams et al, 2019 ; Rohr et al, 2019 ; Abrieux et al, 2020 ) and circatidal rhythms ( Kwiatkowski et al, 2023 ; Lin et al, 2023 ). The understanding of circadian rhythm has come a long way since Jean-Jacques d’Ortous de Mairan’s 1729 observations that the daily rhythm of leaf movement in Mimosa pudica plants persisted even when plants were placed in the dark ( de Mairan 1729 ).…”