Abstract
Although chronobiologists have postulated self-sustainability in circadian clocks, we report here two examples of damped oscillation in the cyanobacterial circadian system. First, low temperature transformed the self-sustained KaiC phosphorylation rhythm into damped oscillations. Second, deletion of the kaiA gene showed damped oscillation in the bioluminescent rhythm. These damped rhythms resonated with periodical environmental changes and then recovered their oscillation amplitudes. Numerical experiments confirmed that biochemical networks with the characteristic of self-sustained oscillation are rare. Evolutionary searches revealed that photoperiodism might contribute to evolving the self-sustainability of circadian rhythms. Although damped oscillators have not received substantial chronobiological analyses, our findings suggest that the circadian clock can easily transform into a damped oscillator by environmental or genetic perturbation and might function as a semi-clock system.
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Notes
- 1.
Using the terms of bifurcation theory, conversion of a 5-node, non-self-sustained (or self-sustained) oscillator into a 6-node, self-sustained (or non-self-sustained) oscillator can be described as follows: We have a 6-node system and two control parameters that represent intensity of regulations from node 5 to 6 and from 6 to 4. Some type of bifurcation occurs as the parameter values are increased from 0 (no regulation) toward large values.
Abbreviations
- DD:
-
constant darkness
- LD:
-
light dark cycle
- LL:
-
constant light
- PTO:
-
post-transcriptional oscillator
- SNIC:
-
saddle-node bifurcation on an invariant circle
- TTFL:
-
transcriptional-translational feedback loop
References
Bieniawska Z, Espinoza C, Schlereth A et al (2008) Disruption of the Arabidopsis circadian clock is responsible for extensive variation in the cold-responsive transcriptome. Plant Physiol 147:263–279
Bünning E (1931) Untersuchungen über die autonomen tagesperiodischen Bewungen der Primärblätter von Phaseolus multiflorus. Jahrb Wiss Bot 75:439–480
Bünning E (1960) Opening address: biological clocks. Cold Spring Harb Symp Quant Biol 25:1–9
Bünning E (1964) The physiological clock: endogenous diurnal rhythms and biological chronometry. Springer-Verlag, Berlin
Bünning E (1975) Wilhelm Pfeffer: Apotheker, chemiker, botaniker, physiologe 1845–1920. English edition: Bünning E (1989). Ahead of his time: Wilhelm Pfeffer, early advances in plant biology (trans: Pfeffer HW), Carleton University Press, Ottawa
Bünning E (1977) Fifty years of research in the wake of Wilhelm Pfeffer. Annu Rev Plant Physiol 28:1–23
Bünning E, Stern K (1929) Über die tagesperiodischen Bewegungen der Primärblätter von Phaseolus multiflorus I. Der Einfluss der Temperatur auf die Bewegungen. Ber d bot Ges 47:565–584
Darwin C, Darwin F (1880) The power of movement in plants. John Murray, London
Dodd AN, Salathia N, Hall A et al (2005) Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630–633
Dvornyk V, Vinogradova O, Nevo E (2003) Origin and evolution of circadian clock genes in prokaryotes. Proc Natl Acad Sci U S A 100:2495–2500
Francis CD, Sargent ML (1979) Effects of temperature perturbations on circadian conidiation in Neurospora. Plant Physiol 64:1000–1004
Gould PD, Domijan M, Greenwood M et al (2018) Coordination of robust single cell rhythms in the Arabidopsis circadian clock via spatial waves of gene expression. elife 7:e31700
Grobbelaar N, Huang T, Lin H et al (1986) Dinitrogen-fixing endogenous rhythm in Synechococcus RF-1. FEMS Microbiol Lett 37:173–177
Guckenheimer J, Holmes PJ (1983) Nonlinear oscillations, dynamical systems, and bifurcations of vector fields, applied mathematical sciences, vol 42. Springer-Verlag, New York
Hastings JW, Sweeney BM (1957) On the mechanism of temperature independence in a biological clock. Proc Natl Acad Sci U S A 43:804–811
Hatakeyama TS, Kaneko K (2012) Generic temperature compensation of biological clocks by autonomous regulation of catalyst concentration. Proc Natl Acad Sci U S A 109:8109–8114
Holtzendorff J, Partensky F, Mella D et al (2008) Genome streamlining results in loss of robustness of the circadian clock in the marine cyanobacterium Prochlorococcus marinus PCC 9511. J Biol Rhythm 23:187–199
Ishiura M, Kutsuna S, Aoki S et al (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281:1519–1523
Ito H, Kageyama H, Mutsuda M et al (2007) Autonomous synchronization of the circadian KaiC phosphorylation rhythm. Nat Struct Mol Biol 14:1084–1088
Izhikevich EM (2007) Dynamical systems in neuroscience: the geometry of excitability and bursting. MIT Press, Cambridge
Johnson CH, Zhao C, Xu Y et al (2017) Timing the day: what makes bacterial clocks tick? Nat Rev Microbiol 15:232–242
Kawamoto N, Ito H, Tokuda IT et al (2020) Damped circadian oscillation in the absence of KaiA in Synechococcus. Nat Commun 11:2242
Kitayama Y, Nishiwaki T, Terauchi K et al (2008) Dual KaiC-based oscillations constitute the circadian system of cyanobacteria. Genes Dev 22:1513–1521
Kobayashi Y, Shibata T, Kuramoto Y et al (2010) Evolutionary design of oscillatory genetic networks. Eur Phys J B 76:167–178
Kondo T, Tsudzuki T (1980) Phase progress under low temperature treatment of the potassium uptake rhythm in a duckweed, Lemna gibba G3. Plant Cell Physiol 21:95–103
Kondo T, Strayer CA, Kulkarni RD et al (1993) Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A 90:5672–5676
Lambert G, Chew J, Rust MJ (2016) Costs of clock-environment misalignment in individual cyanobacterial cells. Biophys J 111:883–891
Ma P, Mori T, Zhao C et al (2016) Evolution of KaiC-dependent timekeepers: a proto-circadian timing mechanism confers adaptive fitness in the purple bacterium Rhodopseudomonas palustris. PLoS Genet 12:e1005922
Martino-Catt S, Ort DR (1992) Low temperature interrupts circadian regulation of transcriptional activity in chilling-sensitive plants. Proc Natl Acad Sci U S A 89:3731–3735
Mihalcescu I, Hsing W, Leibler S (2004) Resilient circadian oscillator revealed in individual cyanobacteria. Nature 430:81–85
Moye M, Diekman C (2018) Data assimilation methods for neuronal state and parameter estimation. J Math Neurosci 8:11
Murayama Y, Kori H, Oshima C et al (2017) Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation. Proc Natl Acad Sci U S A 114:5641–5646
Nagoshi E, Saini C, Bauer C et al (2004) Circadian gene expression in individual fibroblasts cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 119:693–705
Nakajima M, Imai K, Ito H et al (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414–415
Njus D, McMurry L, Hastings JW (1977) Conditionality of circadian rhythmicity: synergistic action of light and temperature. J Comp Physiol 117:335–344
Ouyang Y, Andersson CR, Kondo T et al (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A 95:8660–8664
Pfeffer W (1915) Beiträge zur Kenntnis der Entstehung der Schlafbewegungen. Ber. d. math.-phys. KI. d. Koenigl. Sächs. Gesellsch. d. Wissensch 34 (I–VI):1–154
Pittayakanchit W, Lu Z, Chew J et al (2018) Biophysical clocks face a trade-off between internal and external noise resistance. elife 7:e37624
Pittendrigh CS (1976) Circadian clocks: what are they? In: Hastings JW, Schweiger HG (eds) The molecular basis of circadian rhythms. Abakon Verlagsgesellschaft, Berlin, pp 11–48
Ramos A, Pérez-SolÃs E, Ibáñez C et al (2005) Winter disruption of the circadian clock in chestnut. Proc Natl Acad Sci U S A 102:7037–7042
Roberts SKDF (1962) Circadian activity rhythms in cockroaches. II Entrainment and phase shifting. J Cell Comp Physiol 59:175–186
Roy S, Letourneau L, Morse D (2014) Cold-induced cysts of the photosynthetic dinoflagellate Lingulodinium polyedrum have an arrested circadian bioluminescence rhythm and lower levels of protein phosphorylation. Plant Physiol 164:966–977
Strogatz SH (1994) Nonlinear dynamics and chaos: with applications to physics, biology, chemistry, and engineering. Addison-Wesley, Reading, MA
Sweeney B (1987) Rhythmic phenomena in plants. Academic Press, San Diego, CA
Tazawa H (2009) Biological clock coming out from beans: the story of Erwin Bünning. (in Japanese) Gakkai Shuppan, Tokyo
Ukai H, Kobayashi TJ, Nagano M et al (2007) Melanopsin-dependent photo-perturbation reveals desynchronization underlying the singularity of mammalian circadian clocks. Nat Cell Biol 9:1327–1334
Welsh DK, Yoo SH, Liu AC et al (2004) Bioluminescence imaging of individual fibroblasts reveals persistent, independently phased circadian rhythms of clock gene expression. Curr Biol 14:2289–2295
Wever R (1965) Pendulum versus relaxation oscillation. In: Aschoff J (ed) Circadian clocks. North-Holland Publication, Amsterdam, pp 74–83
Yeang HY (2013) Solar rhythm in the regulation of photoperiodic flowering of long-day and short-day plants. J Exp Bot 64:2643–2652
Yoshida T, Murayama Y, Ito H et al (2009) Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle. Proc Natl Acad Sci U S A 106:1648–1653
Zimmerman WF (1969) On the absence of circadian rhythmicity in Drosophila pseudoobscura pupae. Biol Bull 136:494–500
Acknowledgments
We thank Takao Kondo, Kumiko Miwa, Isao Tokuda, Hiroshi Kori, and Chiaki Oshima for fruitful discussion and collaboration during the course of our studies. This study was supported in part by a Grant-in-Aid for Scientific Research (KAKENHI) from JSPS (Grant nos. 18K19349 and 23657138 to H. Iwasaki, 18H05474 to H. Ito, 16J40136 to Y.M.) and by the Education and Research Center for Mathematical and Data Science (Kyushu University to H. Ito).
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Ito, H., Murayama, Y., Kawamoto, N., Seki, M., Iwasaki, H. (2021). Damped Oscillation in the Cyanobacterial Clock System. In: Johnson, C.H., Rust, M.J. (eds) Circadian Rhythms in Bacteria and Microbiomes. Springer, Cham. https://doi.org/10.1007/978-3-030-72158-9_12
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