Cyanobacteria are the simplest organisms known to exhibit circadian rhythms and have provided experimental model systems for the dissection of basic properties of circadian organization at the molecular, physiological, and ecological levels. This review focuses on the molecular and genetic mechanisms of circadian rhythm generation in cyanobacteria. Recent analyses have revealed the existence of multiple feedback processes in the prokaryotic circadian system and have led to a novel molecular oscillator model. Here, the authors summarize current understanding of, and open questions about, the cyanobacterial oscillator.
Aronson BD, Johnson KA, Loros JJ, and Dunlap JC (1994) Negative feedback defining a circadian clock: Autoregulation of the clock gene frequency. Science263:1578-1584.
2.
Ditty JL, Williams SB, and Golden SS (2003) A cyanobacterial circadian timing mechanism. Annu Rev Genet37:513-543.
3.
Dunlap JC (1999) Molecular bases for circadian clocks. Cell96:271-290.
4.
Etchegaray JP, Lee C, Wade PA, and Reppert SM (2003) Rhythmic histone acetylation underlies transcription in the mammalian circadian clock. Nature421:177-182.
5.
Garces RG, Wu N, Gillon W, and Pai EF (2004) Anabaena circadian clock proteins KaiA and KaiB reveal a potential common binding site to their partner KaiC. EMBO J23:1688-1698.
6.
Goldbeter A (1996) Biochemical Oscillations and Cellular Rhythms. Cambridge, UK: Cambridge University Press.
7.
Golden SS and Canales SR (2003) Cyanobacterial circadian clocks: Timing is everything. Nat Rev Microbiol1:191-199.
8.
Golden SS, Ishiura M, Johnson CH, and Kondo T (1997) Cyanobacterial circadian rhythms. Annu Rev Plant Physiol Plant Mol Biol48:327-354.
9.
Grobbelaar N, Huang TC, Lin HY, and Chow TJ (1986) Dinitrogen-fixing endogenous rhythm in Synechococcus RF-1. FEMS Microbiol Lett37:173-177.
10.
Hayashi F, Suzuki H, Iwase R, Uzumaki T, Miyake A, Shen JR, Imada K, Furukawa Y, Yonekura K, Namba K, et al. (2003) ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells8:287-296.
11.
Ishiura M, Kutsuna K, Aoki S, Iwasaki H, Andersson CR, Tanabe A, Golden SS, Johnson CH, and Kondo T (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science281:1519-1523.
12.
Iwasaki H and Dunlap JC (2000) Microbial circadian oscillatory systems in Neurospora and Synechococcus: Models for cellular clocks. Curr Opin Microbiol3:189-196.
13.
Iwasaki H and Kondo T (2000) The current state and problems of circadian clock studies in cyanobacteria. Plant Cell Physiol41:1013-1020.
14.
Iwasaki H, Nishiwaki T, Kitayama Y, Nakajima M, and Kondo T (2002) KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci U S A99:15788-15793.
15.
Iwasaki H, Taniguchi Y, Ishiura M, and Kondo T (1999) Physical interactions among circadian clock proteins, KaiA, KaiB and KaiC, in cyanobacteria. EMBO J18:1137-1145.
16.
Iwasaki H, Williams SB, Kitayama Y, Ishiura M, Golden SS, and Kondo T (2000) AKaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell101:223-233.
17.
Johnson CH (2004) Global orchestration of gene expression by the biological clock of cyanobacteria. Genome Biol5:217.1-217.4.
18.
Kageyama H, Kondo T, and Iwasaki H (2003) Circadian formation of clock protein complexes by KaiA, KaiB, KaiC, and SasA in cyanobacteria. J Biol Chem278:2388-2395.
19.
Katayama M, Tsinoremas NF, Kondo T, and Golden SS (1999) cpmA, a gene involved in an output pathway of the cyanobacterial circadian system. J Bacteriol181:3516-3524.
20.
Kitayama Y, Iwasaki H, Nishiwaki T, and Kondo T (2003) KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial clock system. EMBO J22:2127-2134.
21.
Kondo T, Mori T, Lebedeva NV, Aoki S, Ishiura M, and Golden SS (1997) Circadian rhythms in rapidly dividing cyanobacteria. Science275:224-227.
22.
Kondo T, Strayer CA, Kulkarni RD, Taylor W, Ishiura M, Golden SS, and Johnson CH (1993) Circadian rhythms in prokaryotes: Luciferase as a reporter of circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A90:5672-5676.
23.
Kondo T, Tsinoremas NF, Golden SS, Johnson CH, Kutsuna S, and Ishiura M (1994) Circadian clock mutants of cyanobacteria. Science266:1233-1236.
24.
Lakin-Thomas P (2000) Circadian rhythms: New functions for old clock genes. Trends Genet16:135-142.
25.
Leipe DD, Aravind L, Grishin NV, and Koonin EV (2000) The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res10:5-16.
26.
Lin RF, Chou HM, and Huang TC (1999) Priority of light/dark entrainment over temperature in setting the circadian rhythms of the prokaryote Synechococcus RF-1. Planta209:202-206.
27.
Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV, Golden SS, Ishiura M, and Kondo T (1995) Circadian orchestration of gene expression in cyanobacteria. Genes Dev9:1469-1478.
28.
Merrow M, Brunner M, and Roenneberg T (1999) Assignment of circadian function for the Neurospora clock gene frequency. Nature399:584-586.
29.
Mihalcescu I, Hsing W, and Leibler S (2004) Resilient circadian oscillator revealed in individual cyanobacteria. Nature430:81-85.
30.
Min H, Liu Y, Johnson CH, and Golden SS (2004) Phase determination of circadian gene expression in Synechococcus elongatus PCC 7942. J Biol Rhythms19:103-112.
31.
Mori T, Binder B, and Johnson CH (1996) Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. Proc Natl Acad Sci U S A93:10183-10188.
32.
Mori T and Johnson CH (2001) Circadian programming in cyanobacteria. Semin Cell Dev Biol12:271-278.
33.
Mori T, Saveliev SV, Xu Y, Stafford WF, Cox MM, Inman RB, and Johnson CH (2002) Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci U S A99:17203-17208.
34.
Morse D, Hastings JW, and Roenneberg T (1994) Different phase responses of the two circadian oscillators in Gonyaulax. J Biol Rhythms9:263-274.
35.
Nair U, Ditty JL, Min H, and Golden SS (2002) Roles for sigma factors in global circadian regulation of the cyanobacterial genome. J Bacteriol184:3530-3538.
36.
Nakahira Y, Katayama M, Miyashita H, Kutsuna S, Iwasaki H, Oyama T, and Kondo T (2004) Global gene repression by KaiC as a master process of prokaryotic circadian system. Proc Natl Acad Sci U S A101:881-885.
37.
Nishiwaki T, Iwasaki H, Ishiura M, and Kondo T (2000) Nucleotide binding and autophosphorylation of clock protein KaiC as a circadian timing process of cyanobacteria. Proc Natl Acad Sci U S A97:495-499.
38.
Ouyang Y, Andersson CR, Kondo T, Golden SS, and Johnson CH (1998) Resonating circadian clocks enhance fitness in cyanobacteria. Proc Natl Acad Sci U S A95:8660-8664.
39.
Pruss GJ and Drilica K (1989) DNA supercoiling and prokaryotic transcription. Cell56:521-523.
40.
Roenneberg T and Merrow M (1999) Circadian systems and metabolism. J Biol Rhythms14:449-459.
41.
Roenneberg T and Merrow M (2003) Circadian light input: Omnes viae Romam ducunt. Curr Biol10:R742-R745.
42.
Salvador ML, Klein U, and Bogorad L (1998) Endogenous fluctuations of DNA topology in the chloroplast of Chlamydomonas reinhardtii. Mol Cell Biol18:7235-7242.
43.
Schmitz O, Williams SB, Katayama M, Kondo T, and Golden SS (2000) CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science289:765-768.
44.
Ueda HR, Matsumoto A, Kawamura M, Iino M, Tanimura T, and Hashimoto S (2002) Genome-wide transcriptional orchestration of circadian rhythms in Drosophila. J Biol Chem277:14048-14052.
45.
Uzumaki T, Fujita M, Nakatsu T, Hayashi F, Shibata H, Itoh N, Kato H, and Ishiura M (2004) Crystal structure of the C-terminal clock-oscillator domain of the cyanobacterial KaiA protein. Nat Struct Mol Biol11:623-631.
46.
Vakonakis I and LiWang AC (2004) Structure of the C-terminal domain of the clock protein KaiA in complex with a KaiC-derived peptide: Implications for KaiC regulation. Proc Natl Acad Sci U S A101:10925-10930.
47.
Vakonakis I, Sun J, Wu T, Holzenburg A, Golden SS, and LiWang AC (2004) NMR structure of the KaiC-interacting C-terminal domain of KaiA, a circadian clock protein: Implications for KaiA-KaiC interaction. Proc Natl Acad Sci U S A101:1479-1484.
48.
Williams SB, Vakonakis I, Golden SS, and LiWang AC (2002) Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: A potential clock input mechanism. Proc Natl Acad Sci U S A99:15357-15362.
49.
Xu Y, Mori T, and Johnson CH (2000) Circadian clock-protein expression in cyanobacteria: Rhythms and phase setting. EMBO J19:3349-3357.
50.
Xu Y, Mori T, and Johnson CH (2003) Cyanobacterial circadian clockwork: Roles of KaiA, KaiB, and the kaiBC promoter in regulating KaiC. EMBO J22:2117-2126.
51.
Ye S, Vakonakis I, Ioerger TR, LiWang AC, and Sacchetini JC (2004) Crystal structure of circadian clock protein KaiA from Synechococcus elongatus. J Biol Chem279:20511-20518.
52.
Young MW and Kay SA (2001) Time zones: A comparative genetics of circadian clocks. Nat Rev Genet2:702-715.