CLOCK evolved in cnidaria to synchronize internal rhythms with diel environmental cues

• Published in: eLife 2024-05, Vol.12
• Main Authors: Aguillon, Raphael, Rinsky, Mieka, Simon-Blecher, Noa, Doniger, Tirza, Appelbaum, Lior, Levy, Oren
• Format: Article
• Language: English
• Subjects: Animals; Behavior; Biosphere; Cell differentiation; Cell division; Circadian Clocks - genetics; Circadian rhythm; Circadian Rhythm - genetics; Circadian rhythms; Clock gene; CLOCK Proteins - genetics; CLOCK Proteins - metabolism; Cnidaria - genetics; Cnidaria - physiology; CRISPR; Evolutionary Biology; Gene expression; Genetic engineering; genetic mutant; Genomes; Genotype & phenotype; Hybridization; Light; light-pathway; Nematostella vectensis; Organisms; Pacemakers; Photoperiod; Phylogenetics; Polyps; Polyps (organisms); Proteins; Sea Anemones - genetics; Sea Anemones - physiology; transcriptome; Transcriptomics
• ISSN: 2050-084X; 2050-084X
• DOI: 10.7554/eLife.89499

The circadian clock enables anticipation of the day/night cycle in animals ranging from cnidarians to mammals. Circadian rhythms are generated through a transcription-translation feedback loop (TTFL or pacemaker) with CLOCK as a conserved positive factor in animals. However, CLOCK's functional evolutionary origin and mechanism of action in basal animals are unknown. In the cnidarian , pacemaker gene transcript levels, including (the ortholog), appear arrhythmic under constant darkness, questioning the role of NvCLK. Utilizing CRISPR/Cas9, we generated a allele mutant ( ), revealing circadian behavior loss under constant dark (DD) or light (LL), while maintaining a 24 hr rhythm under light-dark condition (LD). Transcriptomics analysis revealed distinct rhythmic genes in wild-type (WT) polypsunder LD compared to DD conditions. In LD, polyps exhibited comparable numbers of rhythmic genes, but were reduced in DD. Furthermore, under LD, the polyps showed alterations in temporal pacemaker gene expression, impacting their potential interactions. Additionally, differential expression of non-rhythmic genes associated with cell division and neuronal differentiation was observed. These findings revealed that a light-responsive pathway can partially compensate for circadian clock disruption, and that the gene has evolved in cnidarians to synchronize rhythmic physiology and behavior with the diel rhythm of the earth's biosphere.