Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis

  1. Cory A Berger  Is a corresponding author
  2. Ann M Tarrant  Is a corresponding author
  1. Woods Hole Oceanographic Institution, United States

Abstract

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.

Data availability

Raw RNA-seq data have been uploaded to the NCBI Sequence Read Archive (SRA), Bioproject PRJNA826898.R code used for analysis is available athttps://github.com/caberger1/Sensory-Conflict-in-Nematostella-vectensis.

The following data sets were generated
The following previously published data sets were used

Article and author information

Author details

  1. Cory A Berger

    Biology Department, Woods Hole Oceanographic Institution, Woods Hole, United States
    For correspondence
    cberger@whoi.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-6003-1955
  2. Ann M Tarrant

    Biology Department, Woods Hole Oceanographic Institution, Woods Hole, United States
    For correspondence
    atarrant@whoi.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-1909-7899

Funding

Woods Hole Oceanographic Institution (Ocean Ventures Fund)

  • Cory A Berger

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Kristin Tessmar-Raible, University of Vienna, Austria

Version history

  1. Preprint posted: April 12, 2022 (view preprint)
  2. Received: June 15, 2022
  3. Accepted: April 5, 2023
  4. Accepted Manuscript published: April 6, 2023 (version 1)
  5. Version of Record published: May 16, 2023 (version 2)

Copyright

© 2023, Berger & Tarrant

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Cory A Berger
  2. Ann M Tarrant
(2023)
Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis
eLife 12:e81084.
https://doi.org/10.7554/eLife.81084

Share this article

https://doi.org/10.7554/eLife.81084

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