Transcriptional remodelling upon light removal in a model cnidarian: Losses and gains in gene expression

Jul 3, 2019Molecular ecology

Changes in gene activity after light is removed in a simple sea animal

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Abstract

Direct light exposure resulted in significant expression changes for hundreds of genes in the sea anemone Nematostella vectensis.

More than 200 genes exhibited rhythmic expression with a 24-hour cycle under light:dark conditions.
80% of genes with rhythmic expression lost significance within 1 day after light cue removal.
Most hypothesized cnidarian circadian genes were among those that lost rhythmic expression following light removal.
70% of candidate circadian genes experienced phase shifts after the removal of light exposure.
Thousands of genes related to oxidative stress, DNA damage response, and chromatin modification showed significant expression changes within 24 hours after light removal.
Findings indicate that gene expression changes in anemones under diel lighting are primarily driven by direct light response rather than a circadian clock.

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Organismal responses to light:dark cycles can result from two general processes: (a) direct response to light or (b) a free-running rhythm (i.e., a circadian clock). Previous research in cnidarians has shown that candidate circadian clock genes have rhythmic expression in the presence of diel lighting, but these oscillations appear to be lost quickly after removal of the light cue. Here, we measure whole-organism gene expression changes in 136 transcriptomes of the sea anemone Nematostella vectensis, entrained to a light:dark environment and immediately following light cue removal to distinguish two broadly defined responses in cnidarians: light entrainment and circadian regulation. Direct light exposure resulted in significant differences in expression for hundreds of genes, including more than 200 genes with rhythmic, 24-hr periodicity. Removal of the lighting cue resulted in the loss of significant expression for 80% of these genes after 1 day, including most of the hypothesized cnidarian circadian genes. Further, 70% of these candidate genes were phase-shifted. Most surprisingly, thousands of genes, some of which are involved in oxidative stress, DNA damage response and chromatin modification, had significant differences in expression in the 24 hr following light removal, suggesting that loss of the entraining cue may induce a cellular stress response. Together, our findings suggest that a majority of genes with significant differences in expression for anemones cultured under diel lighting are largely driven by the primary photoresponse rather than a circadian clock when measured at the whole animal level. These results provide context for the evolution of cnidarian circadian biology and help to disassociate two commonly confounded factors driving oscillating phenotypes.

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Transcriptional remodelling upon light removal in a model cnidarian: Losses and gains in gene expression

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