Cited by 111Circadian rhythm and melatoninPhysiological and biochemical adaptationsLight effects on plants

The DOI matches its Crossref record; 142 of the 148 references it cites were found in a registry or an index; none of the 83 sources its claims cite is checked for support yet.

The Still Dark Side of the Moon: Molecular Mechanisms of Lunar-Controlled Rhythms and Clocks

Open access
Andreatta, Gabriele, Tessmar-Raible, Kristin·2020·Journal of Molecular Biology

Abstract

Starting with the beginning of the last century, a multitude of scientific studies has documented that the lunar cycle times behaviors and physiology in many organisms. It is plausible that even the first life forms adapted to the different rhythms controlled by the moon. Consistently, many marine species exhibit lunar rhythms, and also the number of documented "lunar-rhythmic" terrestrial species is increasing. Organisms follow diverse lunar geophysical/astronomical rhythms, which differ significantly in terms of period length: from hours (circalunidian and circatidal rhythms) to days (circasemilunar and circalunar cycles). Evidence for internal circatital and circalunar oscillators exists for a range of species based on past behavioral studies, but those species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies. Thus, the underlying molecular mechanisms are largely obscure: the dark side of the moon. Here we review findings that start to connect molecular pathways with moon-controlled physiology and behaviors. The present data indicate connections between metabolic/endocrine pathways and moon-controlled rhythms, as well as interactions between circadian and circatidal/circalunar rhythms. Moreover, recent high-throughput analyses provide useful leads toward pathways, as well as molecular markers. However, for each interpretation, it is important to carefully consider the, partly substantially differing, conditions used in each experimental paradigm. In the future, it will be important to use lab experiments to delineate the specific mechanisms of the different solar- and lunar-controlled rhythms, but to also start integrating them together, as life has evolved equally long under rhythms of both sun and moon.

Overview

AI snapshot

Written from the paper’s full text.

TL;DR

This review synthesizes evidence that lunar-controlled rhythms, from circatidal to circalunar periods, are widespread and that molecular links are emerging with circadian clock genes, metabolic/endocrine pathways, and high-throughput markers. It argues that mechanisms remain largely obscure because species with well-documented behavioral free-running lunar rhythms are rarely used for molecular work and experimental conditions vary widely.

Key findings

  • Lunar geophysical cycles span hours to days: lunidian ~24.8 h, semilunar ~14.8 days, synodic ~29.5 days; other lunar months include sidereal 27.32166 days, anomalistic 27.55 days, draconic 27.212220 days, and tropical 27.321582 days.
  • Circadian clock genes interact with lunar rhythms but not uniformly: in *Platynereis dumerilii*, free-running FM showed significantly higher mRNA for *pdp1*, *period*, *clock*, and *tim*; the CK1δ/ε inhibitor PF-670462 rendered clock gene transcription and locomotor activity arrhythmic but left monthly spawning unaffected. In *Eurydice pulchra*, circatidal timekeeping was independent of PER and TIM cycles, no circatidal oscillations were found in core clock genes, only *tim* showed a clear circadian profile, and peroxiredoxin plus 10 of 11 detected mitochondrial genes followed circatidal patterns.
  • Endocrine and metabolic pathways are implicated: melatonin levels were reduced around FM in several fish, melatonin receptors and *aanat* showed lunar-phase-dependent expression, and *Platynereis* GnRH-like/corazonin1 was differentially expressed across the circalunar cycle.
  • High-throughput studies provide candidate markers: coral spawning transcriptomes showed downregulation of clock genes and upregulation of GPCR, calcium signaling, and respiratory genes; in *Platynereis* heads, about 25% of the analyzed proteome was differentially regulated between NM and free-running FM, a much higher circalunar regulation than at the transcript level.

Methods

  • Narrative review, not a primary experimental study; it synthesizes behavioral, molecular, pharmacological, genetic linkage, transcriptomic, and proteomic findings across marine and terrestrial organisms.
  • Data/sample: published literature on corals, *Platynereis dumerilii*, *Eurydice pulchra*, *Clunio marinus*, fish, mollusks, *Drosophila*, rodents, and humans, among others.
  • Main analysis: compares experimental paradigms—natural versus artificial moonlight, free-running versus entrainment, field versus laboratory conditions—and highlights candidate pathways and molecular markers.

Limitations

  • Stated: the underlying molecular mechanisms are largely obscure; species with well-documented behaviorally free-running lunar rhythms are not typically used for molecular studies; data variability likely arises from differing experimental regimes; current resolution may be insufficient to distinguish among different lunar cycles; laboratory versus field discrepancies exist; functional studies, knockouts, and transgenic models are needed.
  • Stated: many interpretations require careful consideration of partly substantially differing experimental conditions, and some analyses, such as those on the HPG axis and lunar rhythmicity, are inconclusive.
  • Evident: as a review, it reports no new primary data; cited studies show conflicting results, and many candidate mechanisms remain functionally untested.

Model-written summary. Check it against the paper before relying on it.

Integrity signals

Registry

Crossref · 10.1016/j.jmb.2020.03.009

Cites

142 of 142 references verified0 citation errors · 0 not checkable

Statistics

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Figures

Graphical abstract
Graphical abstract CC BY-NC-ND · PubMed Central
Figure 1 Schematized representations of the known astronomical and geophysical rhythms dictated by the moon. (A) Lunidian rhythm, the period between two consecutive maximal heights of the moon in the sky (meridian transits). (B) Tidal rhythm: water levels increase twice every day in two opposite sites on earth, with one being the closest to our satellite. (C) Semilunar rhythm: the alignment of moon, earth and sun potentiate tidal variations, creating spring (during FM and NM) and neap (during FQM and LQM) tides cycles. (D) Synodic and sidereal months. The first gives rise to the known lunar phases: NM, FQM, FM, and LQM or third quarter moon. (E) Anomalistic month. (F) Draconic month. The plane described by moon's orbit is inclined (5.14°) compared to the plane on which the sun and the earth lay, and the two planes cross in two points called nodes (purple circles). (G) Tropical month: the clockwise rotation of earth's axis affects moon's relative trajectory in the sky (declination). Thus, periodically, the moon faces a more northern or southern portion of earth relative to the Equator, and this affects both moonlight intensity and tides. Moonlight depicted in the figure is a reflection of sunlight. The sun was purposely left away from the scheme for the sake of clarity. For further details, see text. Sources: [5,6]; https://en.wikipedia.org/wiki/Lunar_month;https://www.youtube.com/watch?v=jWCBhVfeAQU;https://www.youtube.com/watch?v=Z6DpPQ8QdLg;https://www.youtube.com/watch?v=adzx547ptck;http://www.antikythera-mechanism.gr/faq/astronomical-questions/what-are-the-different-months;https://moonblink.info/Eclipse/why/months;https://www.slideshare.net/RAFIULALAM006/month-57977849).
Figure 1 Schematized representations of the known astronomical and geophysical rhythms dictated by the moon. (A) Lunidian rhythm, the period between two consecutive maximal heights of the moon in the sky (meridian transits). (B) Tidal rhythm: water levels increase twice every day in two opposite sites on earth, with one being the closest to our satellite. (C) Semilunar rhythm: the alignment of moon, earth and sun potentiate tidal variations, creating spring (during FM and NM) and neap (during FQM and LQM) tides cycles. (D) Synodic and sidereal months. The first gives rise to the known lunar phases: NM, FQM, FM, and LQM or third quarter moon. (E) Anomalistic month. (F) Draconic month. The plane described by moon's orbit is inclined (5.14°) compared to the plane on which the sun and the earth lay, and the two planes cross in two points called nodes (purple circles). (G) Tropical month: the clockwise rotation of earth's axis affects moon's relative trajectory in the sky (declination). Thus, periodically, the moon faces a more northern or southern portion of earth relative to the Equator, and this affects both moonlight intensity and tides. Moonlight depicted in the figure is a reflection of sunlight. The sun was purposely left away from the scheme for the sake of clarity. For further details, see text. Sources: [5,6]; https://en.wikipedia.org/wiki/Lunar_month;https://www.youtube.com/watch?v=jWCBhVfeAQU;https://www.youtube.com/watch?v=Z6DpPQ8QdLg;https://www.youtube.com/watch?v=adzx547ptck;http://www.antikythera-mechanism.gr/faq/astronomical-questions/what-are-the-different-months;https://moonblink.info/Eclipse/why/months;https://www.slideshare.net/RAFIULALAM006/month-57977849).CC BY-NC-ND · PubMed Central
Figure 2 Circadian clock genes expression is affected by the lunar cycle or laboratory conditions mimicking moonlight cues. Gray areas on the left of each panel describe the environmental conditions or laboratory experimental settings employed. Green circles indicate experiments conducted under natural conditions, whereas orange circles refer to artificial (lab) experimental conditions. (A) The expression of A. millepora cry1, cry2, clk, and cyc is influenced by the lunar cycle. (B) Expression of a set of clock genes in P. dumerilii is regulated by an endogenous circalunar clock, as shown by experiments under lunar free-running conditions (absence of artificial moonlight cue at night). (C) Altered night illumination affect the expression of clock genes in a lunar phase-dependent manner in S. guttatus. For references, see [[26], [27], [28], [29]].
Figure 2 Circadian clock genes expression is affected by the lunar cycle or laboratory conditions mimicking moonlight cues. Gray areas on the left of each panel describe the environmental conditions or laboratory experimental settings employed. Green circles indicate experiments conducted under natural conditions, whereas orange circles refer to artificial (lab) experimental conditions. (A) The expression of A. millepora cry1, cry2, clk, and cyc is influenced by the lunar cycle. (B) Expression of a set of clock genes in P. dumerilii is regulated by an endogenous circalunar clock, as shown by experiments under lunar free-running conditions (absence of artificial moonlight cue at night). (C) Altered night illumination affect the expression of clock genes in a lunar phase-dependent manner in S. guttatus. For references, see [[26], [27], [28], [29]].CC BY-NC-ND · PubMed Central
Figure 3 Tidal activity rhythm in E. pulchra generates antisense tidal cycles of metabolism but is independent from classical clock genes oscillation. (A) Swimming activity pattern of Eurydice specimens shows a period of 12.5 h in free-running conditions, with maxima during predicted high water (HW). (B) Representative western blot of overoxidized peroxiredoxin. (C) Relative intensity of overoxidized head peroxiredoxin. (D and E) Relative expression of mitochondrially-encoded genes (ND = NADH dehydrogenase subunits, COX = cytochrome oxidase subunits; CYTB = cytochrome B) under free-running laboratory conditions. (F) None of Eurydice circadian clock genes exhibit a tidal rhythm at the transcript level, and curiously, only tim shows a clear circadian profile (red arrows show the time of expected high water). For references, see [10,54]. Orange circles: artificial (lab) conditions.
Figure 3 Tidal activity rhythm in E. pulchra generates antisense tidal cycles of metabolism but is independent from classical clock genes oscillation. (A) Swimming activity pattern of Eurydice specimens shows a period of 12.5 h in free-running conditions, with maxima during predicted high water (HW). (B) Representative western blot of overoxidized peroxiredoxin. (C) Relative intensity of overoxidized head peroxiredoxin. (D and E) Relative expression of mitochondrially-encoded genes (ND = NADH dehydrogenase subunits, COX = cytochrome oxidase subunits; CYTB = cytochrome B) under free-running laboratory conditions. (F) None of Eurydice circadian clock genes exhibit a tidal rhythm at the transcript level, and curiously, only tim shows a clear circadian profile (red arrows show the time of expected high water). For references, see [10,54]. Orange circles: artificial (lab) conditions.CC BY-NC-ND · PubMed Central
Figure 4 Summary table showing the experimental conditions, the main findings, and patterns of a sample of the high-throughput analysis reviewed. NM = new moon; FQM = first quarter moon; FM = full moon; LQM = last quarter moon; SP = spawning; NS = not spawning; T/L = regulated by the interaction between temperature and lunar cycle; D/L = regulated by the interaction between daily and lunar cycles; D/L/T = regulated by the interaction among daily, lunar, and temperature cues; TR = tidally regulated; T = transcript; P = protein. For references, see [57,79,86,89,91].
Figure 4 Summary table showing the experimental conditions, the main findings, and patterns of a sample of the high-throughput analysis reviewed. NM = new moon; FQM = first quarter moon; FM = full moon; LQM = last quarter moon; SP = spawning; NS = not spawning; T/L = regulated by the interaction between temperature and lunar cycle; D/L = regulated by the interaction between daily and lunar cycles; D/L/T = regulated by the interaction among daily, lunar, and temperature cues; TR = tidally regulated; T = transcript; P = protein. For references, see [57,79,86,89,91].CC BY-NC-ND · PubMed Central

Verification

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  • The paper relies on this without support.

    Life has evolved equally long under both lunar and solar influences.

    “As the moon formed about 4.51 billion years ago, life evolved equally long under both lunar and solar influences”
  • The paper relies on this without support.

    The lunar cycle is a reliable and steady environmental cue.

    “Animals exploit reliable and steady environmental cues to synchronize crucial events of their life”
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Citations

Cites

Research works printed but not linked: 3

  1. Szmant-Froelich, 1985, Sexual reproduction of Favia fragum (ESPER): lunar patterns of gametogenesis, embryogenesis and planulation in Puerto Rico, Bull. Mar. Sci., 37, 880
  2. Ranzi, 1931, Ricerche sulla biologia sessuale degli Anellidi, Pubbl. Del Stn. Zool. Napoli., 11, 271
  3. Decoursey, 1990, Circadian photoentrainment in nocturnal mammals—ecological overtones, Biol. Behav., 15, 213

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Metadata

Authors
Andreatta, G., & Tessmar-Raible, K.
Affiliations
University of Vienna (AT)
Venue
Journal of Molecular Biology
Publisher
Elsevier BV
Published
2020-05
Volume
432
Issue
12
Pages
3525-3546
ISSN
0022-2836 (ISSN-L)
OpenAlex
W3012359533
Cited by
111
References
148
Citations by year
2026: 16 · 2025: 22 · 2024: 20 · 2023: 17 · 2022: 20 · 2021: 12 · 2020: 4
FWCI
1.79
Type
journal article
Language
en
Open access
Locations
  • Journal of Molecular Biology (publishedVersion, cc-by-nc-nd)
  • PubMed Central (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Padua Research Archive (University of Padova) (submittedVersion, cc-by-nc-nd)
Funders
  • Seventh Framework Programme
  • Horizon 2020 Framework Programme (819952)
  • European Research Council (337011)
  • Austrian Science Fund (P28970, SFB F78)
  • Universität Wien
Topics
  • Life Sciences › Neuroscience › Endocrine and Autonomic Systems › Circadian rhythm and melatonin
  • Physical Sciences › Environmental Science › Ecology › Physiological and biochemical adaptations
  • Life Sciences › Agricultural and Biological Sciences › Plant Science › Light effects on plants
Keywords
lunar rhythms, circatidal rhythm, circalunar rhythm, circadian rhythm, molecular clock mechanisms, metabolic pathways, endocrine pathways, molecular markers, free-running rhythm, marine organisms, terrestrial organisms
MeSH terms
Adaptation, Physiological, Animals, Circadian Rhythm, Light, Moon, Metabolic Networks and Pathways, Circadian Clocks

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