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Volume 155, Issue 2

Stability and lability of circadian period of gene expression in the cyanobacterium Free

Abstract

Molecular aspects of the circadian clock in the cyanobacterium have been described in great detail. Three-dimensional structures have been determined for the three proteins, KaiA, KaiB and KaiC, that constitute a central oscillator of the clock. Moreover, a temperature-compensated circadian rhythm of KaiC phosphorylation can be reconstituted with the addition of KaiA, KaiB and ATP. These data suggest a relatively simple circadian system in which a single oscillator provides temporal information for all downstream processes. However, the situation is more complex, and additional components contribute to the maintenance of a normal period, the resetting of relative phases of circadian oscillations, and the control of rhythms of gene expression. We show here that two well-studied promoters in the genome report different circadian periods of expression under a given set of conditions in wild-type as well as mutant genetic backgrounds. Moreover, the period differs between these promoters with respect to modulation by light intensity, growth phase, and the presence or absence of a promoter-recognition subunit of RNA polymerase. These data contrast sharply with the current clock model in which a single Kai-based oscillator governs circadian period. Overall, these findings suggest that complex interactions among the circadian oscillator, perhaps other oscillators, and other cellular machinery result in a clock that is plastic and sensitive to the environment and to the physiological state of the cell.

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Keyword(s): CT, circadian time , LL, constant light and WT, wild-type
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2009-02-01
2024-04-20
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References

  1. Andersson C. R., Tsinoremas N. F., Shelton J., Lebedeva N. V., Yarrow J., Min H., Golden S. S. 2000; Application of bioluminescence to the study of circadian rhythms in cyanobacteria. Methods Enzymol 305:527–542
     [Google Scholar]
  2. Asayama M., Imamura S., Yoshihara S., Miyazaki A., Yoshida N., Sazuka T., Kaneko T., Ohara O., Tabata S. other authors 2004; SigC, the group 2 sigma factor of RNA polymerase, contributes to the late-stage gene expression and nitrogen promoter recognition in the cyanobacterium Synechocystis sp. strain PCC 6803. Biosci Biotechnol Biochem 68:477–487
     [Google Scholar]
  3. Aschoff J. 1981; Freerunning and entrained circadian rhythms. In Handbook of Behavioral Neurobiology: Biological Rhythms pp 81–93 Edited by Aschoff J. New York: Plenum Press;
     [Google Scholar]
  4. Bell-Pedersen D., Cassone V. M., Earnest D. J., Golden S. S., Hardin P. E., Thomas T. L., Zoran M. J. 2005; Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat Rev Genet 6:544–556
     [Google Scholar]
  5. Bustos S. A., Golden S. S. 1991; Expression of the psbDII gene in Synechococcus sp. strain PCC 7942 requires sequences downstream of the transcription start site. J Bacteriol 173:7525–7533
     [Google Scholar]
  6. Clerico E. M., Ditty J. L., Golden S. S. 2007; Specialized techniques for site-directed mutagenesis in cyanobacteria. Methods Mol Biol 362:155–171
     [Google Scholar]
  7. Ditty J. L., Williams S. B., Golden S. S. 2003; A cyanobacterial circadian timing mechanism. Annu Rev Genet 37:513–543
     [Google Scholar]
  8. Ishiura M., Kutsuna S., Aoki S., Iwasaki H., Andersson C. R., Tanabe A., Golden S. S., Johnson C. H., Kondo T. 1998; Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281:1519–1523
     [Google Scholar]
  9. Ivleva N. B., Bramlett M. R., Lindahl P. A., Golden S. S. 2005; LdpA: a component of the circadian clock senses redox state of the cell. EMBO J 24:1202–1210
     [Google Scholar]
  10. Ivleva N. B., Gao T., LiWang A. C., Golden S. S. 2006; Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock. Proc Natl Acad Sci U S A 103:17468–17473
     [Google Scholar]
  11. Iwasaki H., Williams S. B., Kitayama Y., Ishiura M., Golden S. S., Kondo T. 2000; A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223–233
     [Google Scholar]
  12. Katayama M., Tsinoremas N. F., Kondo T., Golden S. S. 1999; cpmA , a gene involved in an output pathway of the cyanobacterial circadian system. J Bacteriol 181:3516–3524
     [Google Scholar]
  13. Katayama M., Kondo T., Xiong J., Golden S. S. 2003; ldpA encodes an iron-sulfur protein involved in light-dependent modulation of the circadian period in the cyanobacterium Synechococcus elongatus PCC 7942. J Bacteriol 185:1415–1422
     [Google Scholar]
  14. Kitayama Y., Nishiwaki T., Terauchi K., Kondo T. 2008; Dual KaiC-based oscillations constitute the circadian system of cyanobacteria. Genes Dev 22:1513–1521
     [Google Scholar]
  15. Kondo T., Strayer C. A., Kulkarni R. D., Taylor W., Ishiura M., Golden S. S., Johnson C. H. 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
     [Google Scholar]
  16. Kondo T., Mori T., Lebedeva N. V., Aoki S., Ishiura M., Golden S. S. 1997; Circadian rhythms in rapidly dividing cyanobacteria. Science 275:224–227
     [Google Scholar]
  17. Liu Y., Tsinoremas N. F., Johnson C. H., Lebedeva N. V., Golden S. S., Ishiura M., Kondo T. 1995; Circadian orchestration of gene expression in cyanobacteria. Genes Dev 9:1469–1478
     [Google Scholar]
  18. Mackey S. R., Ditty J. L., Clerico E. M., Golden S. S. 2007; Detection of rhythmic bioluminescence from luciferase reporters in cyanobacteria. Methods Mol Biol 362:115–129
     [Google Scholar]
  19. Mihalcescu I., Hsing W., Leibler S. 2004; Resilient circadian oscillator revealed in individual cyanobacteria. Nature 430:81–85
     [Google Scholar]
  20. Mori T., Williams D. R., Byrne M. O., Qin X., Egli M., McHaourab H. S., Stewart P. L., Johnson C. H. 2007; Elucidating the ticking of an in vitro circadian clockwork. PLoS Biol 5:e93
     [Google Scholar]
  21. Mulvey M. R., Loewen P. C. 1989; Nucleotide sequence of katF of Escherichia coli suggests KatF protein is a novel sigma transcription factor. Nucleic Acids Res 17:9979–9991
     [Google Scholar]
  22. Nair U., Ditty J. L., Min H., Golden S. S. 2002; Roles for sigma factors in global circadian regulation of the cyanobacterial genome. J Bacteriol 184:3530–3538
     [Google Scholar]
  23. Nakajima M., Imai K., Ito H., Nishiwaki T., Murayama Y., Iwasaki H., Oyama T., Kondo T. 2005; Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro . Science 308:414–415
     [Google Scholar]
  24. Plautz J. D., Kaneko M., Hall J. C., Kay S. A. 1997; Independent photoreceptive circadian clocks throughout Drosophila. Science 278:1632–1635
     [Google Scholar]
  25. Roenneberg T., Morse D. 1993; Two circadian oscillators in one cell. Nature 362:362–364
     [Google Scholar]
  26. Sambrook J., Fritsch E. F., Maniatis T. 1989 Molecular Cloning: a Laboratory Manual , 2nd edn. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory;
  27. Smith R. M., Williams S. B. 2006; Circadian rhythms in gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus . Proc Natl Acad Sci U S A 103:8564–8569
     [Google Scholar]
  28. Takai N., Nakajima M., Oyama T., Kito R., Sugita C., Sugita M., Kondo T., Iwasaki H. 2006; A KaiC-associating SasA-RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc Natl Acad Sci U S A 103:12109–12114
     [Google Scholar]
  29. Tsinoremas N. F., Ishiura M., Kondo T., Andersson C. R., Tanaka K., Takahashi H., Johnson C. H., Golden S. S. 1996; A sigma factor that modifies the circadian expression of a subset of genes in cyanobacteria. EMBO J 15:2488–2495
     [Google Scholar]
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Stability and lability of circadian period of gene expression in the cyanobacterium Synechococcus elongatus
Microbiology 155, 635 (2009); https://doi.org/10.1099/mic.0.022343-0
/content/journal/micro/10.1099/mic.0.022343-0
/content/journal/micro/10.1099/mic.0.022343-0
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