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

  1. Rinat Arbel-Goren
  2. Valentina Buonfiglio
  3. Francesca Di Patti
  4. Sergio Camargo
  5. Ana Valladares
  6. Enrique Flores
  7. Antonia Herrero
  8. Duccio Fanelli
  9. Joel Stavans  Is a corresponding author
  1. Weizmann Institute of Science, Israel
  2. Universita di Firenze, Italy
  3. Consiglio Nazionale delle Ricerche, Italy
  4. CSIC and Universidad de Sevilla, Spain
  5. 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).

The following data sets were generated
The following previously published data sets were used
    1. Takakazu Kaneko
    2. Yasukazu Nakamura
    3. C. Peter Wolk
    4. Tanya Kuritz
    5. Shigemi Sasamoto
    6. Akiko Watanabe
    7. Mayumi Iriguchi
    8. Atsuko Ishikawa
    9. Kumiko Kawashima
    10. Takaharu Kimura
    11. Yoshie Kishida
    12. Mitsuyo Kohara
    13. Midori Matsumoto
    14. Ai Matsuno
    15. Akiko Muraki
    16. Naomi Nakazaki
    17. Sayaka Shimpo
    18. Masako Sugimoto
    19. Masaki Takazawa
    20. Manabu Yamada
    21. Miho Yasuda
    22. Satoshi Tabata
    (2001) Complete Genomic Sequence of the Filamentous Nitrogen-fixing Cyanobacterium Anabaena sp. Strain PCC 7120
    Accession 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

  1. Rinat Arbel-Goren

    Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7253-2036
  2. Valentina Buonfiglio

    Dipartimento di Fisica e Astronomia, Universita di Firenze, Sesto Fiorentino, Italy
    Competing interests
    The authors declare that no competing interests exist.
  3. Francesca Di Patti

    Istituto dei Sistemi Complessi, Consiglio Nazionale delle Ricerche, Sesto Fiorentino, Italy
    Competing interests
    The authors declare that no competing interests exist.
  4. Sergio Camargo

    Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Ana Valladares

    Instituto de Bioquimica Vegetal y Fotosintesis, CSIC and Universidad de Sevilla, Sevilla, Spain
    Competing interests
    The authors declare that no competing interests exist.
  6. Enrique Flores

    Instituto de Bioquimica Vegetal y Fotosintesis, CSIC and Universidad de Sevilla, Sevilla, Spain
    Competing interests
    The authors declare that no competing interests exist.
  7. Antonia Herrero

    Instituto de Bioquimica Vegetal y Fotosintesis, CSIC and Universidad de Sevilla, Sevilla, Spain
    Competing interests
    The authors declare that no competing interests exist.
  8. Duccio Fanelli

    Dipartimento di Fisica e Astronomia, Universita di Firenze, INFN and CSDC, Sesto Fiorentino, Italy
    Competing interests
    The authors declare that no competing interests exist.
  9. Joel Stavans

    Physics of Complex Systems, Weizmann Institute of Science, Rehovot, Israel
    For correspondence
    joel.stavans@weizmann.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-0396-7797

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.

Reviewing Editor

  1. Sandeep Krishna, National Centre for Biological Sciences­‐Tata Institute of Fundamental Research, India

Version history

  1. Received: October 26, 2020
  2. Accepted: March 20, 2021
  3. Accepted Manuscript published: March 22, 2021 (version 1)
  4. Version of Record published: April 23, 2021 (version 2)

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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  1. Rinat Arbel-Goren
  2. Valentina Buonfiglio
  3. Francesca Di Patti
  4. Sergio Camargo
  5. Ana Valladares
  6. Enrique Flores
  7. Antonia Herrero
  8. Duccio Fanelli
  9. Joel Stavans
(2021)
Robust, coherent and synchronized circadian clock-controlled oscillations along Anabaena filaments
eLife 10:e64348.
https://doi.org/10.7554/eLife.64348

Share this article

https://doi.org/10.7554/eLife.64348

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