Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation

Yoriko Murayama, Hiroshi Kori, Chiaki Oshima, Takao Kondo, Hideo Iwasaki, Hiroshi Ito

    Research output: Contribution to journalArticle

    6 Citations (Scopus)

    Abstract

    Cold temperatures lead to nullification of circadian rhythms in many organisms. Two typical scenarios explain the disappearance of rhythmicity: The first is oscillation death, which is the transition from self-sustained oscillation to damped oscillation that occurs at a critical temperature. The second scenario is oscillation arrest, in which oscillation terminates at a certain phase. In the field of nonlinear dynamics, these mechanisms are called the Hopf bifurcation and the saddle-node on an invariant circle bifurcation, respectively. Although these mechanisms lead to distinct dynamical properties near the critical temperature, it is unclear to which scenario the circadian clock belongs. Here we reduced the temperature to dampen the reconstituted circadian rhythm of phosphorylation of the recombinant cyanobacterial clock protein KaiC. The data led us to conclude that Hopf bifurcation occurred at ∼ 19 °C. Below this critical temperature, the self-sustained rhythms of KaiC phosphorylation transformed to damped oscillations, which are predicted by the Hopf bifurcation theory. Moreover, we detected resonant oscillations below the critical temperature when temperature was periodically varied, which was reproduced by numerical simulations. Our findings suggest that the transition to a damped oscillation through Hopf bifurcation contributes to maintaining the circadian rhythm of cyanobacteria through resonance at cold temperatures.

    Original languageEnglish
    Pages (from-to)5641-5646
    Number of pages6
    JournalProceedings of the National Academy of Sciences of the United States of America
    Volume114
    Issue number22
    DOIs
    Publication statusPublished - 2017 May 30

    Fingerprint

    Circadian Clocks
    Cyanobacteria
    Temperature
    Circadian Rhythm
    Phosphorylation
    Nonlinear Dynamics
    Periodicity
    Proteins

    Keywords

    • Circadian rhythms
    • Cyanobacteria
    • Hopf bifurcation
    • In vitro
    • Low temperature

    ASJC Scopus subject areas

    • General

    Cite this

    Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation. / Murayama, Yoriko; Kori, Hiroshi; Oshima, Chiaki; Kondo, Takao; Iwasaki, Hideo; Ito, Hiroshi.

    In: Proceedings of the National Academy of Sciences of the United States of America, Vol. 114, No. 22, 30.05.2017, p. 5641-5646.

    Research output: Contribution to journalArticle

    Murayama, Yoriko ; Kori, Hiroshi ; Oshima, Chiaki ; Kondo, Takao ; Iwasaki, Hideo ; Ito, Hiroshi. / Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation. In: Proceedings of the National Academy of Sciences of the United States of America. 2017 ; Vol. 114, No. 22. pp. 5641-5646.
    @article{54e5ff698d7a40c6936a44501d217e13,
    title = "Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation",
    abstract = "Cold temperatures lead to nullification of circadian rhythms in many organisms. Two typical scenarios explain the disappearance of rhythmicity: The first is oscillation death, which is the transition from self-sustained oscillation to damped oscillation that occurs at a critical temperature. The second scenario is oscillation arrest, in which oscillation terminates at a certain phase. In the field of nonlinear dynamics, these mechanisms are called the Hopf bifurcation and the saddle-node on an invariant circle bifurcation, respectively. Although these mechanisms lead to distinct dynamical properties near the critical temperature, it is unclear to which scenario the circadian clock belongs. Here we reduced the temperature to dampen the reconstituted circadian rhythm of phosphorylation of the recombinant cyanobacterial clock protein KaiC. The data led us to conclude that Hopf bifurcation occurred at ∼ 19 °C. Below this critical temperature, the self-sustained rhythms of KaiC phosphorylation transformed to damped oscillations, which are predicted by the Hopf bifurcation theory. Moreover, we detected resonant oscillations below the critical temperature when temperature was periodically varied, which was reproduced by numerical simulations. Our findings suggest that the transition to a damped oscillation through Hopf bifurcation contributes to maintaining the circadian rhythm of cyanobacteria through resonance at cold temperatures.",
    keywords = "Circadian rhythms, Cyanobacteria, Hopf bifurcation, In vitro, Low temperature",
    author = "Yoriko Murayama and Hiroshi Kori and Chiaki Oshima and Takao Kondo and Hideo Iwasaki and Hiroshi Ito",
    year = "2017",
    month = "5",
    day = "30",
    doi = "10.1073/pnas.1620378114",
    language = "English",
    volume = "114",
    pages = "5641--5646",
    journal = "Proceedings of the National Academy of Sciences of the United States of America",
    issn = "0027-8424",
    number = "22",

    }

    TY - JOUR

    T1 - Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation

    AU - Murayama, Yoriko

    AU - Kori, Hiroshi

    AU - Oshima, Chiaki

    AU - Kondo, Takao

    AU - Iwasaki, Hideo

    AU - Ito, Hiroshi

    PY - 2017/5/30

    Y1 - 2017/5/30

    N2 - Cold temperatures lead to nullification of circadian rhythms in many organisms. Two typical scenarios explain the disappearance of rhythmicity: The first is oscillation death, which is the transition from self-sustained oscillation to damped oscillation that occurs at a critical temperature. The second scenario is oscillation arrest, in which oscillation terminates at a certain phase. In the field of nonlinear dynamics, these mechanisms are called the Hopf bifurcation and the saddle-node on an invariant circle bifurcation, respectively. Although these mechanisms lead to distinct dynamical properties near the critical temperature, it is unclear to which scenario the circadian clock belongs. Here we reduced the temperature to dampen the reconstituted circadian rhythm of phosphorylation of the recombinant cyanobacterial clock protein KaiC. The data led us to conclude that Hopf bifurcation occurred at ∼ 19 °C. Below this critical temperature, the self-sustained rhythms of KaiC phosphorylation transformed to damped oscillations, which are predicted by the Hopf bifurcation theory. Moreover, we detected resonant oscillations below the critical temperature when temperature was periodically varied, which was reproduced by numerical simulations. Our findings suggest that the transition to a damped oscillation through Hopf bifurcation contributes to maintaining the circadian rhythm of cyanobacteria through resonance at cold temperatures.

    AB - Cold temperatures lead to nullification of circadian rhythms in many organisms. Two typical scenarios explain the disappearance of rhythmicity: The first is oscillation death, which is the transition from self-sustained oscillation to damped oscillation that occurs at a critical temperature. The second scenario is oscillation arrest, in which oscillation terminates at a certain phase. In the field of nonlinear dynamics, these mechanisms are called the Hopf bifurcation and the saddle-node on an invariant circle bifurcation, respectively. Although these mechanisms lead to distinct dynamical properties near the critical temperature, it is unclear to which scenario the circadian clock belongs. Here we reduced the temperature to dampen the reconstituted circadian rhythm of phosphorylation of the recombinant cyanobacterial clock protein KaiC. The data led us to conclude that Hopf bifurcation occurred at ∼ 19 °C. Below this critical temperature, the self-sustained rhythms of KaiC phosphorylation transformed to damped oscillations, which are predicted by the Hopf bifurcation theory. Moreover, we detected resonant oscillations below the critical temperature when temperature was periodically varied, which was reproduced by numerical simulations. Our findings suggest that the transition to a damped oscillation through Hopf bifurcation contributes to maintaining the circadian rhythm of cyanobacteria through resonance at cold temperatures.

    KW - Circadian rhythms

    KW - Cyanobacteria

    KW - Hopf bifurcation

    KW - In vitro

    KW - Low temperature

    UR - http://www.scopus.com/inward/record.url?scp=85020014234&partnerID=8YFLogxK

    UR - http://www.scopus.com/inward/citedby.url?scp=85020014234&partnerID=8YFLogxK

    U2 - 10.1073/pnas.1620378114

    DO - 10.1073/pnas.1620378114

    M3 - Article

    VL - 114

    SP - 5641

    EP - 5646

    JO - Proceedings of the National Academy of Sciences of the United States of America

    JF - Proceedings of the National Academy of Sciences of the United States of America

    SN - 0027-8424

    IS - 22

    ER -