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Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis
Circadian clocks infer time of day by integrating information from cyclic environmental factors called zeitgebers, including light and temperature. Single zeitgebers entrain circadian rhythms, but few studies have addressed how multiple, simultaneous zeitgeber cycles interact to affect clock behavio...
Autores principales: | , |
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Formato: | Online Artículo Texto |
Lenguaje: | English |
Publicado: |
eLife Sciences Publications, Ltd
2023
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Materias: | |
Acceso en línea: | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10188108/ https://www.ncbi.nlm.nih.gov/pubmed/37022138 http://dx.doi.org/10.7554/eLife.81084 |
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author | Berger, Cory A Tarrant, Ann M |
author_facet | Berger, Cory A Tarrant, Ann M |
author_sort | Berger, Cory A |
collection | PubMed |
description | Circadian clocks infer time of day by integrating information from cyclic environmental factors called zeitgebers, including light and temperature. Single zeitgebers entrain circadian rhythms, but few studies have addressed how multiple, simultaneous zeitgeber cycles interact to affect clock behavior. Misalignment between zeitgebers (‘sensory conflict’) can disrupt circadian rhythms, or alternatively clocks may privilege information from one zeitgeber over another. Here, we show that temperature cycles modulate circadian locomotor rhythms in Nematostella vectensis, a model system for cnidarian circadian biology. We conduct behavioral experiments across a comprehensive range of light and temperature cycles and find that Nematostella’s circadian behavior is disrupted by chronic misalignment between light and temperature, which involves disruption of the endogenous clock itself rather than a simple masking effect. Sensory conflict also disrupts the rhythmic transcriptome, with numerous genes losing rhythmic expression. However, many metabolic genes remained rhythmic and in-phase with temperature, and other genes even gained rhythmicity, implying that some rhythmic metabolic processes persist even when behavior is disrupted. Our results show that a cnidarian clock relies on information from light and temperature, rather than prioritizing one signal over the other. Although we identify limits to the clock’s ability to integrate conflicting sensory information, there is also a surprising robustness of behavioral and transcriptional rhythmicity. |
format | Online Article Text |
id | pubmed-10188108 |
institution | National Center for Biotechnology Information |
language | English |
publishDate | 2023 |
publisher | eLife Sciences Publications, Ltd |
record_format | MEDLINE/PubMed |
spelling | pubmed-101881082023-05-17 Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis Berger, Cory A Tarrant, Ann M eLife Ecology Circadian clocks infer time of day by integrating information from cyclic environmental factors called zeitgebers, including light and temperature. Single zeitgebers entrain circadian rhythms, but few studies have addressed how multiple, simultaneous zeitgeber cycles interact to affect clock behavior. Misalignment between zeitgebers (‘sensory conflict’) can disrupt circadian rhythms, or alternatively clocks may privilege information from one zeitgeber over another. Here, we show that temperature cycles modulate circadian locomotor rhythms in Nematostella vectensis, a model system for cnidarian circadian biology. We conduct behavioral experiments across a comprehensive range of light and temperature cycles and find that Nematostella’s circadian behavior is disrupted by chronic misalignment between light and temperature, which involves disruption of the endogenous clock itself rather than a simple masking effect. Sensory conflict also disrupts the rhythmic transcriptome, with numerous genes losing rhythmic expression. However, many metabolic genes remained rhythmic and in-phase with temperature, and other genes even gained rhythmicity, implying that some rhythmic metabolic processes persist even when behavior is disrupted. Our results show that a cnidarian clock relies on information from light and temperature, rather than prioritizing one signal over the other. Although we identify limits to the clock’s ability to integrate conflicting sensory information, there is also a surprising robustness of behavioral and transcriptional rhythmicity. eLife Sciences Publications, Ltd 2023-04-06 /pmc/articles/PMC10188108/ /pubmed/37022138 http://dx.doi.org/10.7554/eLife.81084 Text en © 2023, Berger and Tarrant https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited. |
spellingShingle | Ecology Berger, Cory A Tarrant, Ann M Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis |
title | Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis |
title_full | Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis |
title_fullStr | Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis |
title_full_unstemmed | Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis |
title_short | Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis |
title_sort | sensory conflict disrupts circadian rhythms in the sea anemone nematostella vectensis |
topic | Ecology |
url | https://www.ncbi.nlm.nih.gov/pmc/articles/PMC10188108/ https://www.ncbi.nlm.nih.gov/pubmed/37022138 http://dx.doi.org/10.7554/eLife.81084 |
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