Cargando…

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...

Descripción completa

Detalles Bibliográficos
Autores principales: Berger, Cory A, Tarrant, Ann M
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2023
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
_version_ 1785042844680978432
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
work_keys_str_mv AT bergercorya sensoryconflictdisruptscircadianrhythmsintheseaanemonenematostellavectensis
AT tarrantannm sensoryconflictdisruptscircadianrhythmsintheseaanemonenematostellavectensis