Functioning and Robustness of a Bacterial Circadian Clock

Overview

Journal Mol Syst Biol

Specialty Molecular Biology

Date 2007 Mar 14

PMID 17353932

Citations 49

Authors

Sebastien Clodong

Ulf Duhring

Luiza Kronk

Annegret Wilde

Ilka Axmann

Hanspeter Herzel

Markus Kollmann

Affiliations

Soon will be listed here.

Abstract

Cyanobacteria are the simplest known cellular systems that regulate their biological activities in daily cycles. For the cyanobacterium Synechococcus elongatus, it has been shown by in vitro and in vivo experiments that the basic circadian timing process is based on rhythmic phosphorylation of KaiC hexamers. Despite the excellent experimental work, a full systems level understanding of the in vitro clock is still lacking. In this work, we provide a mathematical approach to scan different hypothetical mechanisms for the primary circadian oscillator, starting from experimentally established molecular properties of the clock proteins. Although optimised for highest performance, only one of the in silico-generated reaction networks was able to reproduce the experimentally found high amplitude and robustness against perturbations. In this reaction network, a negative feedback synchronises the phosphorylation level of the individual hexamers and has indeed been realised in S. elongatus by KaiA sequestration as confirmed by experiments.

Citing Articles

Two KaiABC systems control circadian oscillations in one cyanobacterium.

Kobler C, Schmelling N, Wiegard A, Pawlowski A, Pattanayak G, Spat P Nat Commun. 2024; 15(1):7674.

PMID: 39227593 PMC: 11372060. DOI: 10.1038/s41467-024-51914-5.

Data-driven modelling captures dynamics of the circadian clock of Neurospora crassa.

Singh A, Li C, Diernfellner A, Hofer T, Brunner M PLoS Comput Biol. 2022; 18(8):e1010331.

PMID: 35951637 PMC: 9397904. DOI: 10.1371/journal.pcbi.1010331.

Mathematical Modeling in Circadian Rhythmicity.

Del Olmo M, Grabe S, Herzel H Methods Mol Biol. 2022; 2482:55-80.

PMID: 35610419 DOI: 10.1007/978-1-0716-2249-0_4.

Evolution of the repression mechanisms in circadian clocks.

Tyler J, Lu Y, Dunlap J, Forger D Genome Biol. 2022; 23(1):17.

PMID: 35012616 PMC: 8751359. DOI: 10.1186/s13059-021-02571-0.

Mechanism for the Generation of Robust Circadian Oscillations through Ultransensitivity and Differential Binding Affinity.

Behera A, Del Junco C, Vaikuntanathan S J Phys Chem B. 2021; 125(40):11179-11187.

PMID: 34609867 PMC: 8515790. DOI: 10.1021/acs.jpcb.1c05915.

References

Emberly E, Wingreen N . Hourglass model for a protein-based circadian oscillator. Phys Rev Lett. 2006; 96(3):038303. PMC: 1995810. DOI: 10.1103/PhysRevLett.96.038303. View

LOWRY O, ROSEBROUGH N, FARR A, RANDALL R . Protein measurement with the Folin phenol reagent. J Biol Chem. 1951; 193(1):265-75. View

Kageyama H, Nishiwaki T, Nakajima M, Iwasaki H, Oyama T, Kondo T . Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the KaiC phosphorylation cycle in vitro. Mol Cell. 2006; 23(2):161-71. DOI: 10.1016/j.molcel.2006.05.039. View

Takai N, Nakajima M, Oyama T, Kito R, Sugita C, Sugita M . A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc Natl Acad Sci U S A. 2006; 103(32):12109-14. PMC: 1832256. DOI: 10.1073/pnas.0602955103. View

Hayashi F, Iwase R, Uzumaki T, Ishiura M . Hexamerization by the N-terminal domain and intersubunit phosphorylation by the C-terminal domain of cyanobacterial circadian clock protein KaiC. Biochem Biophys Res Commun. 2006; 348(3):864-72. DOI: 10.1016/j.bbrc.2006.07.143. View

Kurosawa G, Aihara K, Iwasa Y . A model for the circadian rhythm of cyanobacteria that maintains oscillation without gene expression. Biophys J. 2006; 91(6):2015-23. PMC: 1557573. DOI: 10.1529/biophysj.105.076554. View

Wijnen H, Young M . Interplay of circadian clocks and metabolic rhythms. Annu Rev Genet. 2006; 40:409-48. DOI: 10.1146/annurev.genet.40.110405.090603. View

Woelfle M, Johnson C . No promoter left behind: global circadian gene expression in cyanobacteria. J Biol Rhythms. 2006; 21(6):419-31. PMC: 3431602. DOI: 10.1177/0748730406294418. View

Mehra A, Hong C, Shi M, Loros J, Dunlap J, Ruoff P . Circadian rhythmicity by autocatalysis. PLoS Comput Biol. 2006; 2(7):e96. PMC: 1523307. DOI: 10.1371/journal.pcbi.0020096. View

10.

Johnson C, Golden S . Circadian programs in cyanobacteria: adaptiveness and mechanism. Annu Rev Microbiol. 1999; 53:389-409. DOI: 10.1146/annurev.micro.53.1.389. View

11.

Nishiwaki T, Iwasaki H, Ishiura M, Kondo T . Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc Natl Acad Sci U S A. 2000; 97(1):495-9. PMC: 26691. DOI: 10.1073/pnas.97.1.495. View

12.

von Dassow G, Meir E, Munro E, Odell G . The segment polarity network is a robust developmental module. Nature. 2000; 406(6792):188-92. DOI: 10.1038/35018085. View

13.

Nair U, Ditty J, Min H, Golden S . Roles for sigma factors in global circadian regulation of the cyanobacterial genome. J Bacteriol. 2002; 184(13):3530-8. PMC: 135120. DOI: 10.1128/JB.184.13.3530-3538.2002. View

14.

Iwasaki H, Kondo T . Circadian timing mechanism in the prokaryotic clock system of cyanobacteria. J Biol Rhythms. 2004; 19(5):436-44. DOI: 10.1177/0748730404269060. View

15.

Tomita J, Nakajima M, Kondo T, Iwasaki H . No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science. 2004; 307(5707):251-4. DOI: 10.1126/science.1102540. View

16.

Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y, Iwasaki H . Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science. 2005; 308(5720):414-5. DOI: 10.1126/science.1108451. View

17.

Hitomi K, Oyama T, Han S, Arvai A, Getzoff E . Tetrameric architecture of the circadian clock protein KaiB. A novel interface for intermolecular interactions and its impact on the circadian rhythm. J Biol Chem. 2005; 280(19):19127-35. DOI: 10.1074/jbc.M411284200. View

18.

Kutsuna S, Nakahira Y, Katayama M, Ishiura M, Kondo T . Transcriptional regulation of the circadian clock operon kaiBC by upstream regions in cyanobacteria. Mol Microbiol. 2005; 57(5):1474-84. DOI: 10.1111/j.1365-2958.2005.04781.x. View

19.

Kollmann M, Lovdok L, Bartholome K, Timmer J, Sourjik V . Design principles of a bacterial signalling network. Nature. 2005; 438(7067):504-7. DOI: 10.1038/nature04228. View

20.

Iwase R, Imada K, Hayashi F, Uzumaki T, Morishita M, Onai K . Functionally important substructures of circadian clock protein KaiB in a unique tetramer complex. J Biol Chem. 2005; 280(52):43141-9. DOI: 10.1074/jbc.M503360200. View