In cnidarians, long-term ecological success relies on sexual reproduction. The sea anemone Nematostella vectensis, which has emerged as an important model organism for developmental studies, can be induced for spawning by temperature elevation and light exposure. To uncover molecular mechanisms and pathways underlying spawning, we characterized the transcriptome of Nematostella females before and during spawning induction. We identified an array of processes involving numerous receptors, circadian clock components, cytoskeleton, and extracellular transcripts that are upregulated upon spawning induction. Concurrently, processes related to the cell cycle, fatty acid metabolism, and other housekeeping functions are downregulated. Real-time qPCR revealed that light exposure has a minor effect on expression levels of most examined transcripts, implying that temperature change is a stronger inducer for spawning in Nematostella. Our findings reveal the potential mechanisms that may enable the mesenteries to serve as a gonad-like tissue for the developing oocytes and expand our understanding of sexual reproduction in cnidarians.

Studying chronobiology in reef-building corals is challenging due to the tightly coupled symbiosis with their photosynthetic algae, Symbiodiniaceae. Although symbiosis requires metabolic synchronization and coordination of cellular processes in the holobiont, the cross-talk between the host and symbiont’s clocks is still puzzling. Here, we use the mesophotic coral Euphyllia paradivisa to examine temporal gene expression patterns in symbiotic and aposymbiotic morphs exposed to natural light/dark cycles and constant darkness. Our comparative transcriptomic analyses revealed circadian and circatidal cycles of gene expression with a predominant diel pattern in both coral morphs. We found a substantial number of transcripts consistently rhythmic under both light conditions, including genes likely involved in the cnidarians’ circadian clock, thus indicating that an endogenous clock, which can oscillate independently from the Symbiodiniaceae clock, exists in E. paradivisa. The analysis further manifests the remarkable impacts of symbiosis on transcriptional rhythms and implies that the algae’s presence influences the host’s biorhythm.

Organisms’ survival is associated with the ability to respond to natural or anthropogenic environmental stressors. Frequently, these responses involve changes in gene regulation and expression, consequently altering physiology, development, or behavior. Here, we present modifications in response to heat exposure that mimics extreme summertime field conditions of lab-cultured and field-conditioned Nematostella vectensis. Using ATAC-seq and RNA-seq data, we found that field-conditioned animals had a more concentrated reaction to short-term thermal stress, expressed as enrichment of the DNA repair mechanism pathway. By contrast, lab animals had a more diffuse reaction that involved a larger number of differentially expressed genes and enriched pathways, including amino acid metabolism. Our results demonstrate that pre-conditioning affects the ability to respond efficiently to heat exposure in terms of both chromatin accessibility and gene expression and reinforces the importance of experimentally addressing ecological questions in the field.

The circadian clock is a crucial biological mechanism that enables organisms to anticipate the daily light/dark cycle. While the circadian clock factors underlying the molecular mechanism were characterized in a few model organisms, the evolutionary functional origin of the core clock proteins is unclear. In cnidarians, the expression of the putative core clock genes is rhythmic under light/dark cycles but is arrhythmic under constant light conditions. Thus, it is unclear how the core circadian genes regulate rhythmic behavior. Here, we studied the function of the evolutionarily conserved bHLH transcription factorClockin the sea anemoneNematostella vectensis. The CRISPR/Cas9 system was employed to generate aClockmutant (Clock-/-)N. vectensis. InClock-/-N. vectensis, rhythmic locomotor activity was observed under light/dark cycles, but the rhythmicity was abolished under constant dark or light conditions. Likewise, transcriptome profiling inClock-/-N. vectensisrevealed an array of clock-controlled genes (CCG). Additionally, we observed a co-operation betweenClockand light to shape core clock genes transcription rhythmicity. Notably, loss of CLOCK resulted in hundreds of differential expressed genes, which mainly regulate the cell cycle and the development of the nervous system. Overall, our results suggest that the CLOCK protein evolved to modulates the ancient hierarchy between light- and circadian clock-regulated physiology and behavior.

In cnidarians, long-term ecological success relies on sexual reproduction. The sea anemone Nematostella vectensis, which has emerged as an important model organism for developmental studies, can be induced for spawning by temperature elevation and light exposure. To uncover molecular mechanisms and pathways underlying spawning, we characterized the transcriptome of Nematostella females before and during spawning induction. We identified an array of processes involving numerous receptors, circadian clock components, cytoskeleton, and extracellular transcripts that are upregulated upon spawning induction. Concurrently, processes related to the cell cycle, fatty acid metabolism, and other housekeeping functions are downregulated. Real-time qPCR revealed that light exposure has a minor effect on expression levels of most examined transcripts, implying that temperature change is a stronger inducer for spawning in Nematostella. Our findings reveal the mechanisms that may enable the mesenteries to serve as a gonad-like tissue for the developing oocytes and expand our understanding of sexual reproduction in cnidarians.