Carolina M Peralta, Eric Feunteun, Julien Guillaudeau, Dušica Briševac, Tobias S Kaiser
{"title":"How Light at Night Sets the Circalunar Clock in the Marine Midge <i>Clunio marinus</i>.","authors":"Carolina M Peralta, Eric Feunteun, Julien Guillaudeau, Dušica Briševac, Tobias S Kaiser","doi":"10.1177/07487304241286936","DOIUrl":"10.1177/07487304241286936","url":null,"abstract":"<p><p>Many organisms inhabiting the interface between land and sea have evolved biological clocks corresponding to the period of the semilunar (14.77 days) or the lunar (29.53 days) cycle. Since tidal amplitude is modulated across the lunar cycle, these circasemilunar or circalunar clocks not only allow organisms to adapt to the lunar cycle, but also to specific tidal situations. Biological clocks are synchronized to external cycles via environmental cues called <i>zeitgebers</i>. Here, we explore how light at night sets the circalunar and circasemilunar clocks of <i>Clunio marinus</i>, a marine insect that relies on these clocks to control timing of emergence. We first characterized how moonlight intensity is modulated by the tides by measuring light intensity in the natural habitat of <i>C. marinus</i>. In laboratory experiments, we then explored how different moonlight treatments set the phase of the clocks of two <i>C. marinus</i> strains, one with a lunar rhythm and one with a semilunar rhythm. Light intensity alone does not affect the phase of the lunar rhythm. Presenting moonlight during different 2-h or 4-h windows during the night shows that (1) the required duration of moonlight is strain-specific, (2) there are strain-specific moonlight sensitivity windows and (3) timing of moonlight can shift the phase of the lunar rhythm to stay synchronized with the lowest low tides. Experiments simulating natural moonlight patterns confirm that the phase is set by the timing of moonlight. Simulating natural moonlight at field-observed intensities leads to the best synchronization. Taken together, we show that there is a complex and strain-specific integration of intensity, duration and timing of light at night to precisely entrain the lunar and semilunar rhythms. The observed fine-tuning of the rhythms under natural moonlight regimes lays the foundation for a better chronobiological and genetic dissection of the circa(semi)lunar clock in <i>C. marinus</i>.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-11-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142590687","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Hierarchy or Heterarchy of Mammalian Circadian Timekeepers?","authors":"William Bechtel","doi":"10.1177/07487304241286573","DOIUrl":"https://doi.org/10.1177/07487304241286573","url":null,"abstract":"<p><p>Mammalian circadian biologists commonly characterize the relation between circadian clocks as hierarchical, with the clock in the suprachiasmatic nucleus at the top of the hierarchy. The lineage of research since the suprachiasmatic nucleus (SCN) was first identified as <i>the clock</i> in mammals has challenged this perspective, revealing clocks in peripheral tissues, showing that they respond to their own zeitgebers, coordinate oscillations among themselves, and in some cases modify the behavior of the SCN. Increasingly circadian timekeepers appear to constitute a heterarchical network, with control distributed and operating along multiple pathways. One reason for the continued invocation of hierarchy in mammalian circadian biology is that it is difficult to understand how a heterarchical system could operate effectively so as to maintain the organism. Evolved mechanisms, however, need not respect hierarchy and those that have survived have demonstrated the ability of heterarchical organizaton to maintain organisms.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-24","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142500939","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Corrigendum to \"Transcriptomic plasticity of the circadian clock in response to photoperiod: A study in male melatonin-competent mice\".","authors":"","doi":"10.1177/07487304241289753","DOIUrl":"10.1177/07487304241289753","url":null,"abstract":"","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-22","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142466150","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Detecting Rhythmic Gene Expression in Single-cell Transcriptomics.","authors":"Bingxian Xu, Dingbang Ma, Katharine Abruzzi, Rosemary Braun","doi":"10.1177/07487304241273182","DOIUrl":"10.1177/07487304241273182","url":null,"abstract":"<p><p>An autonomous, environmentally synchronizable circadian rhythm is a ubiquitous feature of life on Earth. In multicellular organisms, this rhythm is generated by a transcription-translation feedback loop present in nearly every cell that drives daily expression of thousands of genes in a tissue-dependent manner. Identifying the genes that are under circadian control can elucidate the mechanisms by which physiological processes are coordinated in multicellular organisms. Today, transcriptomic profiling at the single-cell level provides an unprecedented opportunity to understand the function of cell-level clocks. However, while many cycling detection algorithms have been developed to identify genes under circadian control in bulk transcriptomic data, it is not known how best to adapt these algorithms to single-cell RNA seq data. Here, we benchmark commonly used circadian detection methods on their reliability and efficiency when applied to single-cell RNA seq data. Our results provide guidance on adapting existing cycling detection methods to the single-cell domain and elucidate opportunities for more robust and efficient rhythm detection in single-cell data. We also propose a subsampling procedure combined with harmonic regression as an efficient strategy to detect circadian genes in the single-cell setting.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-08","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142390787","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Daniel Appenroth, Chandra S Ravuri, Sara K Torppa, Shona H Wood, David G Hazlerigg, Alexander C West
{"title":"The Reindeer Circadian Clock Is Rhythmic and Temperature-compensated But Shows Evidence of Weak Coupling Between the Secondary and Core Molecular Clock Loops.","authors":"Daniel Appenroth, Chandra S Ravuri, Sara K Torppa, Shona H Wood, David G Hazlerigg, Alexander C West","doi":"10.1177/07487304241283066","DOIUrl":"https://doi.org/10.1177/07487304241283066","url":null,"abstract":"<p><p>Circadian rhythms synchronize the internal physiology of animals allowing them to anticipate daily changes in their environment. Arctic habitats may diminish the selective advantages of circadian rhythmicity by relaxing daily rhythmic environmental constraints, presenting a valuable opportunity to study the evolution of circadian rhythms. In reindeer, circadian control of locomotor activity and melatonin release is weak or absent, and the molecular clockwork is reportedly non-functional. Here we present new evidence that the circadian clock in cultured reindeer fibroblasts is rhythmic and temperature-compensated. Compared with mouse fibroblasts, however, reindeer fibroblasts have a short free-running period, and temperature cycles have an atypical impact on clock gene regulation. In reindeer cells, <i>Per2</i> and <i>Bmal1</i> reporters show rapid responses to temperature cycles, with a disintegration of their normal antiphasic relationship. The antiphasic <i>Per2-Bmal1</i> relationship re-emerges immediately after release from temperature cycles, but without complete temperature entrainment and with a marked decline in circadian amplitude. Experiments using <i>Bmal1</i> promoter reporters with mutated RORE sites showed that a reindeer-like response to temperature cycles can be mimicked in mouse or human cell lines by decoupling <i>Bmal1</i> reporter activity from ROR/REV-ERB-dependent transcriptional regulation. We suggest that weak coupling between core and secondary circadian feedback loops accounts for the observed behavior of reindeer fibroblasts in vitro. Our findings highlight diversity in how the thermal environment affects the temporal organization of mammals living under different thermoenergetic constraints.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142380915","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"Sex-Related Variation in Circadian Rhythms in the Bumble Bee <i>Bombus terrestris</i>.","authors":"Ozlem Gonulkirmaz-Cancalar, Guy Bloch","doi":"10.1177/07487304241283863","DOIUrl":"10.1177/07487304241283863","url":null,"abstract":"<p><p>Mating success depends on many factors, but first of all, a male and a female need to meet at the same place and time. The circadian clock is an endogenous system regulating activity and sex-related behaviors in animals. We studied bumble bees (<i>Bombus terrestris</i>) in which the influence of circadian rhythms on sexual behavior has been little explored. We characterized circadian rhythms in adult emergence and locomotor activity under different illumination regimes for males and gynes (unmated queens). We developed a method to monitor adult emergence from the pupal cocoon and found no circadian rhythms in this behavior for either males or gynes. These results are not consistent with the hypothesis that the circadian clock regulates emergence from the pupa in this species. Consistent with this premise, we found that both gynes and males do not show circadian rhythms in locomotor activity during the first 3 days after pupal emergence, but shortly after developed robust circadian rhythms that are readily shifted by a phase delay in illumination regime. We conclude that the bumble bees do not need strong rhythms in adult emergence and during early adult life in their protected and regulated nest environment, but do need strong activity rhythms for timing flights and mating-related behaviors. Next, we tested the hypothesis that the locomotor activity of males and gynes have a similar phase, which may improve mating success. We found that both males and gynes have strong endogenous circadian rhythms that are entrained by the illumination regime, but males show rhythms at an earlier age, their rhythms are stronger, and their phase is slightly advanced relative to that of gynes. An earlier phase may be advantageous to males competing to mate a receptive gyne. Our results are consistent with the hypothesis that sex-related variations in circadian rhythms is shaped by sexual selection.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-06","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"142380914","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Manabu Sekiguchi, Nils Reinhard, Ayumi Fukuda, Shun Katoh, Dirk Rieger, Charlotte Helfrich-Förster, Taishi Yoshii
{"title":"A Detailed Re-Examination of the <i>Period</i> Gene Rescue Experiments Shows That Four to Six Cryptochrome-Positive Posterior Dorsal Clock Neurons (DN<sub>1p</sub>) of <i>Drosophila melanogaster</i> Can Control Morning and Evening Activity.","authors":"Manabu Sekiguchi, Nils Reinhard, Ayumi Fukuda, Shun Katoh, Dirk Rieger, Charlotte Helfrich-Förster, Taishi Yoshii","doi":"10.1177/07487304241263130","DOIUrl":"10.1177/07487304241263130","url":null,"abstract":"<p><p>Animal circadian clocks play a crucial role in regulating behavioral adaptations to daily environmental changes. The fruit fly <i>Drosophila melanogaster</i> exhibits 2 prominent peaks of activity in the morning and evening, known as morning (M) and evening (E) peaks. These peaks are controlled by 2 distinct circadian oscillators located in separate groups of clock neurons in the brain. To investigate the clock neurons responsible for the M and E peaks, a cell-specific gene expression system, the GAL4-UAS system, has been commonly employed. In this study, we re-examined the two-oscillator model for the M and E peaks of <i>Drosophila</i> by utilizing more than 50 Gal4 lines in conjunction with the <i>UAS-period<sup>16</sup></i> line, which enables the restoration of the clock function in specific cells in the <i>period</i> (<i>per</i>) null mutant background. Previous studies have indicated that the group of small ventrolateral neurons (s-LN<sub>v</sub>) is responsible for controlling the M peak, while the other group, consisting of the 5<sup>th</sup> ventrolateral neuron (5<sup>th</sup> LN<sub>v</sub>) and the three cryptochrome (CRY)-positive dorsolateral neurons (LN<sub>d</sub>), is responsible for the E peak. Furthermore, the group of posterior dorsal neurons 1 (DN<sub>1p</sub>) is thought to also contain M and E oscillators. In this study, we found that Gal4 lines directed at the same clock neuron groups can lead to different results, underscoring the fact that activity patterns are influenced by many factors. Nevertheless, we were able to confirm previous findings that the entire network of circadian clock neurons controls M and E peaks, with the lateral neurons playing a dominant role. In addition, we demonstrate that 4 to 6 CRY-positive DN<sub>1p</sub> cells are sufficient to generate M and E peaks in light-dark cycles and complex free-running rhythms in constant darkness. Ultimately, our detailed screening could serve as a catalog to choose the best Gal4 lines that can be used to rescue <i>per</i> in specific clock neurons.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141855610","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
{"title":"The Estrous Cycle Coordinates the Circadian Rhythm of Eating Behavior in Mice.","authors":"Victoria M Alvord, Julie S Pendergast","doi":"10.1177/07487304241262356","DOIUrl":"10.1177/07487304241262356","url":null,"abstract":"<p><p>The estrous cycle regulates rhythms of locomotor activity, body temperature, and circadian gene expression. In female mice, activity increases on the night of proestrus, when elevated estrogens cause ovulation. Exogenous estradiol regulates eating behavior rhythms in female mice fed a high-fat diet, but it is unknown whether endogenous estrogens regulate eating rhythms. In this study, we investigated whether diurnal and circadian eating behavior rhythms change systematically across the estrous cycle. We first studied diurnal eating behavior rhythms in female C57BL/6J mice in 12L:12D. Estrous cycle stages were determined by vaginal cytology while eating behavior and wheel revolutions were continuously measured. The mice had regular 4- to 5-day estrous cycles. Consistent with prior studies, the greatest number of wheel revolutions occurred on the night of proestrus into estrus when systemic levels of estrogens peak. The amplitude, or robustness, of the eating behavior rhythm also fluctuated with 4- to 5-day cycles and peaked primarily during proestrus or estrus. The phases of eating behavior rhythms fluctuated, but not at 4- or 5-day intervals, and phases did not correlate with estrous cycle stages. After ovariectomy, the eating behavior rhythm amplitude fluctuated at irregular intervals. In constant darkness, the amplitude of the circadian eating behavior rhythm peaked every 4 or 5 days and coincided with the circadian day that had the greatest number of wheel revolutions, a marker of proestrus. These data suggest that fluctuations of ovarian hormones across the estrous cycle temporally organize the robustness of circadian eating behavior rhythms so that it peaks during ovulation and sexual receptivity.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11416336/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141855625","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Sumit Saurabh, Ruth J Meier, Liliya M Pireva, Rabab A Mirza, Daniel J Cavanaugh
{"title":"Overlapping Central Clock Network Circuitry Regulates Circadian Feeding and Activity Rhythms in Drosophila.","authors":"Sumit Saurabh, Ruth J Meier, Liliya M Pireva, Rabab A Mirza, Daniel J Cavanaugh","doi":"10.1177/07487304241263734","DOIUrl":"10.1177/07487304241263734","url":null,"abstract":"<p><p>The circadian system coordinates multiple behavioral outputs to ensure proper temporal organization. Timing information underlying circadian regulation of behavior depends on a molecular circadian clock that operates within clock neurons in the brain. In <i>Drosophila</i> and other organisms, clock neurons can be divided into several molecularly and functionally discrete subpopulations that form an interconnected central clock network. It is unknown how circadian signals are coherently generated by the clock network and transmitted across output circuits that connect clock cells to downstream neurons that regulate behavior. Here, we have exhaustively investigated the contribution of clock neuron subsets to the control of two prominent behavioral outputs in <i>Drosophila</i>: locomotor activity and feeding. We have used cell-specific manipulations to eliminate molecular clock function or induce electrical silencing either broadly throughout the clock network or in specific subpopulations. We find that clock cell manipulations produce similar changes in locomotor activity and feeding, suggesting that overlapping central clock circuitry regulates these distinct behavioral outputs. Interestingly, the magnitude and nature of the effects depend on the clock subset targeted. Lateral clock neuron manipulations profoundly degrade the rhythmicity of feeding and activity. In contrast, dorsal clock neuron manipulations only subtly affect rhythmicity but produce pronounced changes in the distribution of activity and feeding across the day. These experiments expand our knowledge of clock regulation of activity rhythms and offer the first extensive characterization of central clock control of feeding rhythms. Despite similar effects of central clock cell disruptions on activity and feeding, we find that manipulations that prevent functional signaling in an identified output circuit preferentially degrade locomotor activity rhythms, leaving feeding rhythms relatively intact. This demonstrates that activity and feeding are indeed dissociable behaviors, and furthermore suggests that differential circadian control of these behaviors diverges in output circuits downstream of the clock network.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141766117","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}
Reshma R, Tobias Prüser, Nora K E Schulz, Paula M F Mayer, Maite Ogueta, Ralf Stanewsky, Joachim Kurtz
{"title":"Deciphering a Beetle Clock: Individual and Sex-Dependent Variation in Daily Activity Patterns.","authors":"Reshma R, Tobias Prüser, Nora K E Schulz, Paula M F Mayer, Maite Ogueta, Ralf Stanewsky, Joachim Kurtz","doi":"10.1177/07487304241263619","DOIUrl":"10.1177/07487304241263619","url":null,"abstract":"<p><p>Circadian clocks are inherent to most organisms, including cryptozoic animals that seldom encounter direct light, and regulate their daily activity cycles. A conserved suite of clock genes underpins these rhythms. In this study, we explore the circadian behaviors of the red flour beetle <i>Tribolium castaneum</i>, a significant pest impacting stored grain globally. We report on how daily light and temperature cues synchronize distinct activity patterns in these beetles, characterized by reduced morning activity and increased evening activity, anticipating the respective environmental transitions. Although less robust, rhythmicity in locomotor activity is maintained in constant dark and constant light conditions. Notably, we observed more robust rhythmic behaviors in males than females with individual variation exceeding those previously reported for other insect species. RNA interference targeting the <i>Clock</i> gene weakened locomotor activity rhythms. Our findings demonstrate the existence of a circadian clock and of clock-controlled behaviors in <i>T. castaneum</i>. Furthermore, they highlight substantial individual differences in circadian activity, laying the groundwork for future research on the relevance of individual variation in circadian rhythms in an ecological and evolutionary context.</p>","PeriodicalId":15056,"journal":{"name":"Journal of Biological Rhythms","volume":null,"pages":null},"PeriodicalIF":2.9,"publicationDate":"2024-10-01","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"https://www.ncbi.nlm.nih.gov/pmc/articles/PMC11416735/pdf/","citationCount":null,"resultStr":null,"platform":"Semanticscholar","paperid":"141855624","PeriodicalName":null,"FirstCategoryId":null,"ListUrlMain":null,"RegionNum":3,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":"OA","EPubDate":null,"PubModel":null,"JCR":null,"JCRName":null,"Score":null,"Total":0}