Molecular circadian rhythms are robust in marine annelids lacking rhythmic behavior

PLoS Biol. 2024 Apr 11;22(4):e3002572. doi: 10.1371/journal.pbio.3002572. eCollection 2024 Apr.

Abstract

The circadian clock controls behavior and metabolism in various organisms. However, the exact timing and strength of rhythmic phenotypes can vary significantly between individuals of the same species. This is highly relevant for rhythmically complex marine environments where organismal rhythmic diversity likely permits the occupation of different microenvironments. When investigating circadian locomotor behavior of Platynereis dumerilii, a model system for marine molecular chronobiology, we found strain-specific, high variability between individual worms. The individual patterns were maintained for several weeks. A diel head transcriptome comparison of behaviorally rhythmic versus arrhythmic wild-type worms showed that 24-h cycling of core circadian clock transcripts is identical between both behavioral phenotypes. While behaviorally arrhythmic worms showed a similar total number of cycling transcripts compared to their behaviorally rhythmic counterparts, the annotation categories of their transcripts, however, differed substantially. Consistent with their locomotor phenotype, behaviorally rhythmic worms exhibit an enrichment of cycling transcripts related to neuronal/behavioral processes. In contrast, behaviorally arrhythmic worms showed significantly increased diel cycling for metabolism- and physiology-related transcripts. The prominent role of the neuropeptide pigment-dispersing factor (PDF) in Drosophila circadian behavior prompted us to test for a possible functional involvement of Platynereis pdf. Differing from its role in Drosophila, loss of pdf impacts overall activity levels but shows only indirect effects on rhythmicity. Our results show that individuals arrhythmic in a given process can show increased rhythmicity in others. Across the Platynereis population, rhythmic phenotypes exist as a continuum, with no distinct "boundaries" between rhythmicity and arrhythmicity. We suggest that such diel rhythm breadth is an important biodiversity resource enabling the species to quickly adapt to heterogeneous or changing marine environments. In times of massive sequencing, our work also emphasizes the importance of time series and functional tests.

MeSH terms

  • Animals
  • Circadian Clocks* / genetics
  • Circadian Rhythm / genetics
  • Drosophila / metabolism
  • Drosophila Proteins* / metabolism
  • Drosophila melanogaster / metabolism
  • Humans
  • Motor Activity

Substances

  • Drosophila Proteins

Grants and funding

This work was supported with a Helmholtz distinguished professorship by the Alfred Wegener Institute Helmholtz Centre for Polar and Marine Research;the FP7 Ideas: European Research Council, ERC Grant Agreement 792 #337011, Wissenschaftsfond FWF, SFB F78 and H2020 European Research Council, ERC Grant Agreement #819952 to KT-R; by the Wissenschaftsfonds FWF, Lise-Meitner fellowship M2820 to NSH; by the KU Leuven Research Council, C16/19/003 to IB and LS; the Research Foundation Flanders, FWO G0B5322N to IB; the Wissenschaftfond FWF, #I2972 and SFB F78, FP7 Ideas: European Research Council, #260564 to FR; and the H2020 European Research Council, Marie 796 Skłodowska-Curie Grant Agreement #847548 to AMM. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.