Resilient circadian oscillator revealed in individual cyanobacteria

Circadian oscillators, which provide internal daily periodicity, are found in a variety of living organisms, including mammals, insects, plants, fungi and cyanobacteria. Remarkably, these biochemical oscillators are resilient to external and internal modifications, such as temperature and cell division cycles. They have to be ‘fluctuation (noise) resistant’ because relative fluctuations in the number of messenger RNA and protein molecules forming the intracellular oscillators are likely to be large. In multicellular organisms, the strong temporal stability of circadian clocks, despite molecular fluctuations, can easily be explained by intercellular interactions. Here we study circadian rhythms and their stability in unicellular cyanobacteria Synechoccocus elongatus. Low-light-level microscopy has allowed us to measure gene expression under circadian control in single bacteria, showing that the circadian clock is indeed a property of individual cells. Our measurements show that the oscillators have a strong temporal stability with a correlation time of several months. In contrast to many circadian clocks in multicellular organisms, this stability seems to be ensured by the intracellular biochemical network, because the interactions between oscillators seem to be negligible.

[1]  Tetsuya Mori,et al.  Independence of Circadian Timing from Cell Division in Cyanobacteria , 2001, Journal of Bacteriology.

[2]  S. Golden,et al.  Circadian Rhythms in Rapidly Dividing Cyanobacteria , 1997, Science.

[3]  S. Golden,et al.  cpmA, a Gene Involved in an Output Pathway of the Cyanobacterial Circadian System , 1999, Journal of bacteriology.

[4]  S. Yamaguchi,et al.  Synchronization of Cellular Clocks in the Suprachiasmatic Nucleus , 2003, Science.

[5]  S. Golden,et al.  Blue and red light reversibly control psbA expression in the cyanobacterium Synechococcus sp. strain PCC 7942. , 1994, The Journal of biological chemistry.

[6]  Jeffrey C. Hall,et al.  Resetting the Circadian Clock by Social Experience in Drosophila melanogaster , 2002, Science.

[7]  C. Strayer,et al.  Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[8]  S. Kay,et al.  Time zones: a comparative genetics of circadian clocks , 2001, Nature Reviews Genetics.

[9]  Steven H. Strogatz,et al.  Cellular Construction of a Circadian Clock: Period Determination in the Suprachiasmatic Nuclei , 1997, Cell.

[10]  S. Golden,et al.  Circadian orchestration of gene expression in cyanobacteria. , 1995, Genes & development.

[11]  P. Swain,et al.  Stochastic Gene Expression in a Single Cell , 2002, Science.

[12]  B. Binder,et al.  Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[13]  A. Winfree The geometry of biological time , 1991 .

[14]  Jürgen Kurths,et al.  Synchronization: Phase locking and frequency entrainment , 2001 .

[15]  Pierre Gaspard,et al.  The correlation time of mesoscopic chemical clocks , 2002 .

[16]  John L Hudson,et al.  Emerging Coherence in a Population of Chemical Oscillators , 2002, Science.

[17]  S. Leibler,et al.  Biological rhythms: Circadian clocks limited by noise , 2000, Nature.

[18]  Jürgen Kurths,et al.  Synchronization - A Universal Concept in Nonlinear Sciences , 2001, Cambridge Nonlinear Science Series.

[19]  A. Goldbeter,et al.  Robustness of circadian rhythms with respect to molecular noise , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[20]  A. Goldbeter Computational approaches to cellular rhythms , 2002, Nature.