Circadian rhythms in gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus.

In the cyanobacterium Synechococcus elongatus (PCC 7942) the kai genes A, B, and C and the sasA gene encode the functional protein core of the timing mechanism essential for circadian clock regulation of global gene expression. The Kai proteins comprise the central timing mechanism, and the sensor kinase SasA is a primary transducer of temporal information. We demonstrate that the circadian clock also regulates a chromosome compaction rhythm. This chromosome compaction rhythm is both circadian clock-controlled and kai-dependent. Although sasA is required for global gene expression rhythmicity, it is not required for these chromosome compaction rhythms. We also demonstrate direct control by the Kai proteins on the rate at which the SasA protein autophosphorylates. Thus, to generate and maintain circadian rhythms in gene expression, the Kai proteins keep relative time, communicate temporal information to SasA, and may control access to promoter elements by imparting rhythmic chromosome compaction.

[1]  V. Stewart,et al.  Discrimination between structurally related ligands nitrate and nitrite controls autokinase activity of the NarX transmembrane signal transducer of Escherichia coli K‐12 , 1997, Molecular microbiology.

[2]  S. Golden,et al.  A cyanobacterial circadian timing mechanism. , 2003, Annual review of genetics.

[3]  R. D. Rudic,et al.  Histone Acetyltransferase-dependent Chromatin Remodeling and the Vascular Clock* , 2004, Journal of Biological Chemistry.

[4]  S. Golden,et al.  A New Circadian Class 2 Gene, opcA, Whose Product Is Important for Reductant Production at Night in Synechococcus elongatus PCC 7942 , 2000, Journal of bacteriology.

[5]  L. Shapiro,et al.  The choreographed dynamics of bacterial chromosomes. , 2005, Trends in microbiology.

[6]  T. Cavalier-smith,et al.  Chloroplast Evolution: Secondary Symbiogenesis and Multiple Losses , 2002, Current Biology.

[7]  S. Golden,et al.  Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: A potential clock input mechanism , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[8]  Takao Kondo,et al.  Global gene repression by KaiC as a master process of prokaryotic circadian system. , 2004, Proceedings of the National Academy of Sciences of the United States of America.

[9]  Jay C Dunlap,et al.  The Neurospora Circadian System , 2004, Journal of biological rhythms.

[10]  T. Kondo,et al.  Circadian Rhythms in the Synthesis and Degradation of a Master Clock Protein KaiC in Cyanobacteria* , 2004, Journal of Biological Chemistry.

[11]  Steven A. Brown,et al.  PERIOD1-Associated Proteins Modulate the Negative Limb of the Mammalian Circadian Oscillator , 2005, Science.

[12]  M. Merrow,et al.  Life before the Clock: Modeling Circadian Evolution , 2002, Journal of biological rhythms.

[13]  C. Johnson,et al.  Phase Determination of Circadian Gene Expression in Synechococcus Elongatus PCC 7942 , 2004, Journal of biological rhythms.

[14]  S. Golden,et al.  Biochemical Properties of CikA, an Unusual Phytochrome-like Histidine Protein Kinase That Resets the Circadian Clock in Synechococcus elongatus PCC 7942* , 2003, Journal of Biological Chemistry.

[15]  S. Golden,et al.  A KaiC-Interacting Sensory Histidine Kinase, SasA, Necessary to Sustain Robust Circadian Oscillation in Cyanobacteria , 2000, Cell.

[16]  S. Bonotto,et al.  [Circadian rhythm in the inulin content of "Acetabularia mediterranea" chloroplasts]. , 1968, Archives internationales de physiologie et de biochimie.

[17]  J. Shelton,et al.  Application of bioluminescence to the study of circadian rhythms in cyanobacteria. , 2000, Methods in enzymology.

[18]  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.

[19]  Ueli Schibler,et al.  Rhythmic CLOCK-BMAL1 binding to multiple E-box motifs drives circadian Dbp transcription and chromatin transitions , 2006, Nature Genetics.

[20]  U. Klein,et al.  Endogenous Fluctuations of DNA Topology in the Chloroplast of Chlamydomonas reinhardtii , 1998, Molecular and Cellular Biology.

[21]  S. Golden,et al.  Circadian clock mutants of cyanobacteria. , 1994, Science.

[22]  Paul Smolen,et al.  Simulation of Drosophila circadian oscillations, mutations, and light responses by a model with VRI, PDP-1, and CLK. , 2004, Biophysical journal.

[23]  Takao Kondo,et al.  Circadian Formation of Clock Protein Complexes by KaiA, KaiB, KaiC, and SasA in Cyanobacteria* , 2003, The Journal of Biological Chemistry.

[24]  Takao Kondo,et al.  Circadian expression of genes involved in the purine biosynthetic pathway of the cyanobacterium Synechococcus sp. strain PCC 7942 , 1996, Molecular microbiology.

[25]  C. Johnson,et al.  Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. , 1998, Science.

[26]  S. Golden,et al.  Structure of the N-terminal domain of the circadian clock-associated histidine kinase SasA. , 2004, Journal of molecular biology.

[27]  Andrew J. Roger,et al.  A Cyanobacterial Gene in Nonphotosynthetic Protists—An Early Chloroplast Acquisition in Eukaryotes? , 2002, Current Biology.

[28]  T. Kondo,et al.  Circadian rhythms of cyanobacteria: monitoring the biological clocks of individual colonies by bioluminescence , 1994, Journal of bacteriology.

[29]  J. Stock,et al.  Histidine protein kinases: key signal transducers outside the animal kingdom , 2002, Genome Biology.

[30]  Sabine Cornelsen,et al.  Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[31]  Tetsuya Mori,et al.  Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[32]  G. W. Hatfield,et al.  DNA topology-mediated control of global gene expression in Escherichia coli. , 2002, Annual review of genetics.

[33]  Norio Iijima,et al.  Circadian and Light-Induced Transcription of Clock Gene Per1 Depends on Histone Acetylation and Deacetylation , 2004, Molecular and Cellular Biology.

[34]  S. Golden,et al.  Expression of the psbDII gene in Synechococcus sp. strain PCC 7942 requires sequences downstream of the transcription start site , 1991, Journal of bacteriology.

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

[36]  A. J. Bendich,et al.  Changes in the structure of DNA molecules and the amount of DNA per plastid during chloroplast development in maize. , 2004, Journal of molecular biology.

[37]  V. Stewart,et al.  Genetic Analysis of Pathogenic Bacteria: A Laboratory Manual , 1995 .

[38]  T. Kondo,et al.  Reconstitution of Circadian Oscillation of Cyanobacterial KaiC Phosphorylation in Vitro , 2005, Science.

[39]  G. McFadden,et al.  A Phylogenetic Assessment of the Eukaryotic Light-Harvesting Antenna Proteins, with Implications for Plastid Evolution , 1999, Journal of Molecular Evolution.

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

[41]  Takao Kondo,et al.  No Transcription-Translation Feedback in Circadian Rhythm of KaiC Phosphorylation , 2005, Science.

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