Sensory conflict disrupts circadian rhythms in the sea anemone Nematostella vectensis.
Elife
; 122023 04 06.
Article
em En
| MEDLINE
| ID: mdl-37022138
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.
Almost all living things exhibit circadian rhythms internally driven biological processes which regulate important bodily functions, including sleep and wake cycles, over a roughly 24-hour period. Circadian clocks govern these rhythms by receiving information from the environment that allows them to tell what time of day it is. Two of the most important environmental signals, known as 'zeitgebers' meaning 'time giver' are light and temperature. In nature, circadian clocks must integrate information from multiple zeitgebers simultaneously. Typically, over a 24-hour period, temperature increases and decreases with the light cycle, getting warmer during the day and colder at night. However, artificial light pollution and circadian disruption such as shift work can impact the natural relationship between light and temperature. This 'sensory conflict', where two zeitgebers provide conflicting information about the time of day, can impact ecosystems such as coral reefs; and is also linked to poor health in humans. How circadian clocks behave in complex multi-zeitgeber environments and specifically, whether they prioritize one zeitgeber over another is not fully understood. To investigate how cnidarians a group of marine animals including corals and jellyfish respond to sensory conflict, Berger and Tarrant varied the relationship between light and temperature cycles using the sea anemone Nematostella vectensis as a model system. Nematostella is a nocturnal cnidarian, meaning it moves most at night. First, Berger and Tarrant kept Nematostella in dark conditions with 24-hour temperature cycles starting cold, increasing to a peak in the middle of the day before decreasing towards the end of the day. Monitoring Nematostella movement revealed that they moved most during the cold phase, showing that temperature cycles alone can maintain rhythmic behavior. Similarly, when temperature and light cycles were aligned such that both rose and fell together, nocturnal behavior was preserved. However, when large misalignments between light and temperature cycles were introduced such that temperature decreased during light periods and increased in the dark nocturnal behavior was almost completely lost. This suggests that both light and temperature interact to produce complex patterns of circadian behavior, with neither signal being prioritized over the other. Additionally, Berger and Tarrant investigated how sensory conflict impacts the activity of Nematostella genes. While many genes remained rhythmic, suggesting some gene expression persists when behavior is disturbed, others that were rhythmic became arrhythmic. In contrast, a selection of genes that do not normally display rhythmic behavior gained rhythmic expression. Genes related to protein metabolism and other energy-intensive processes were particularly disrupted. In an increasingly 24/7 society, it is important to understand how complex multi-sensory environments impact circadian rhythms and as a result, health and fitness. The findings show that certain light and temperature regimes severely disrupt Nematostella behavior and could be useful in predicting how other organisms might respond to disruptions such as light pollution. In the future, such information could be used to design optimal light regimes for ecosystems in which the relationship between light cycles and other environmental signals is disrupted by human behavior.
Palavras-chave
Texto completo:
1
Coleções:
01-internacional
Base de dados:
MEDLINE
Assunto principal:
Anêmonas-do-Mar
/
Relógios Circadianos
Tipo de estudo:
Prognostic_studies
Limite:
Animals
Idioma:
En
Revista:
Elife
Ano de publicação:
2023
Tipo de documento:
Article