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Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments

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 synchronizat...

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Autores principales: Arbel-Goren, Rinat, Buonfiglio, Valentina, Di Patti, Francesca, Camargo, Sergio, Zhitnitsky, Anna, Valladares, Ana, Flores, Enrique, Herrero, Antonia, Fanelli, Duccio, Stavans, Joel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: eLife Sciences Publications, Ltd 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8064755/
https://www.ncbi.nlm.nih.gov/pubmed/33749592
http://dx.doi.org/10.7554/eLife.64348
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author Arbel-Goren, Rinat
Buonfiglio, Valentina
Di Patti, Francesca
Camargo, Sergio
Zhitnitsky, Anna
Valladares, Ana
Flores, Enrique
Herrero, Antonia
Fanelli, Duccio
Stavans, Joel
author_facet Arbel-Goren, Rinat
Buonfiglio, Valentina
Di Patti, Francesca
Camargo, Sergio
Zhitnitsky, Anna
Valladares, Ana
Flores, Enrique
Herrero, Antonia
Fanelli, Duccio
Stavans, Joel
author_sort Arbel-Goren, Rinat
collection PubMed
description 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 encoding 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.
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spelling pubmed-80647552021-04-29 Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments Arbel-Goren, Rinat Buonfiglio, Valentina Di Patti, Francesca Camargo, Sergio Zhitnitsky, Anna Valladares, Ana Flores, Enrique Herrero, Antonia Fanelli, Duccio Stavans, Joel eLife Physics of Living Systems 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 encoding 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. eLife Sciences Publications, Ltd 2021-03-22 /pmc/articles/PMC8064755/ /pubmed/33749592 http://dx.doi.org/10.7554/eLife.64348 Text en © 2021, Arbel-Goren et al https://creativecommons.org/licenses/by/4.0/This article is distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use and redistribution provided that the original author and source are credited.
spellingShingle Physics of Living Systems
Arbel-Goren, Rinat
Buonfiglio, Valentina
Di Patti, Francesca
Camargo, Sergio
Zhitnitsky, Anna
Valladares, Ana
Flores, Enrique
Herrero, Antonia
Fanelli, Duccio
Stavans, Joel
Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments
title Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments
title_full Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments
title_fullStr Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments
title_full_unstemmed Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments
title_short Robust, coherent, and synchronized circadian clock-controlled oscillations along Anabaena filaments
title_sort robust, coherent, and synchronized circadian clock-controlled oscillations along anabaena filaments
topic Physics of Living Systems
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8064755/
https://www.ncbi.nlm.nih.gov/pubmed/33749592
http://dx.doi.org/10.7554/eLife.64348
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