Robust, coherent and synchronized circadian clock-controlled oscillations along Anabaena filaments
- Weizmann Institute of Science, Israel
- Universita di Firenze, Italy
- Consiglio Nazionale delle Ricerche, Italy
- CSIC and Universidad de Sevilla, Spain
- Universita di Firenze, INFN and CSDC, Italy
Abstract
Circadian clocks display remarkable reliability despite significant stochasticity in biomolecular reactions. We study the dynamics of a circadian clock-controlled gene at the individual cell level in Anabaena sp. PCC 7120, a multicellular filamentous cyanobacterium. We found significant synchronization and spatial coherence along filaments, clock coupling due to cell-cell communication, and gating of the cell cycle. Furthermore, we observed low-amplitude circadian oscillatory transcription of kai genes comprising the post-transcriptional core oscillatory circuit, and high-amplitude oscillations of rpaA coding for the master regulator transducing the core clock output. Transcriptional oscillations of rpaA suggest an additional level of regulation. A stochastic, one-dimensional toy model of coupled clock cores and their phosphorylation states shows that demographic noise can seed stochastic oscillations outside the region where deterministic limit cycles with circadian periods occur. The model reproduces the observed spatio-temporal coherence along filaments, and provides a robust description of coupled circadian clocks in a multicellular organism.
Data availability
Source data files, Movie 1 and Table of key resources have been deposited in Dryad (doi:10.5061/dryad.sxksn031n).
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Demographic noise seeds robust synchronized oscillations in the circadian clock of AnabaenaDryad Digital Repository, doi:10.5061/dryad.sxksn031n.
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Complete Genomic Sequence of the Filamentous Nitrogen-fixing Cyanobacterium Anabaena sp. Strain PCC 7120Accession numbers, AP003581 (nucleotide positions 1-348,050), AP003582 (348,001- 690,650), AP003583 (690,601-1,030,250), AP003584 (1,030,251-1,378,550), AP003585 (1,378,501-1,720,550), AP003586 (1,720,501-2,069,550), AP003587 (2,069,501- 2,413,050), AP003588 (2,413,001-2,747,520), AP003589 (2,747,471-3,089,350), AP003590 (3,089,301-3,422,800), AP003591 (3,422,751-3,770,150), AP003592 (3,770,101- 4,118,350), AP003593 (4,118,301-4,451,850), AP003594 (4,451,801-4,795,050), AP003595 (4,795,001-5,142,550), AP003596 (5,142,501-5,491,050), AP003597 (5,491,001- 5,833,850), AP003598 (5,833,801-6,176,600), and AP003599 (6,176,551-6,413,771).
Article and author information
Author details
Funding
Minerva Foundation
- Joel Stavans
Fondazione Ente Cassa di Risparmio di Firenze
- Duccio Fanelli
European Regional Development Fund Plan Nacional de Investigacion Spain (BUF2016-77097-P)
- Antonia Herrero
European Regional Development Fund, Plan Nacional de Investigacion, Spain (BFU2017-88202-P)
- Enrique Flores
Italian Ministry of Foreign Affairs and Iternational Cooperation (EXPLICS)
- Francesca Di Patti
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Copyright
© 2021, Arbel-Goren et al.
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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Robust, coherent and synchronized circadian clock-controlled oscillations along Anabaena filaments
eLife 10:e64348.
https://doi.org/10.7554/eLife.64348
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