Abstract
By only mixing the cyanobacterial (Synechococcus elongatus PCC 7942) circadian clock proteins KaiC, KaiA, and KaiB with ATP in a test tube, the phosphorylation status of KaiC shows a circadian rhythm. The major component KaiC is a typical adenosine triphosphatase (ATPase). Although ATPase activity of KaiC is extremely low, the ATPase activity of KaiC by itself shows temperature compensation and correlates with the rate of circadian rhythm (oscillation frequency), indicating that it defines the temperature compensation and period of the circadian rhythm as a pacemaker. The Kai clock system based on this activity shows the existence of a completely novel circadian clock mechanism that does not require transcription/translation or molecular interactions, etc., which has been assumed so far for prokaryotic and eukaryotic organisms. In this chapter, we describe a model for the cyanobacterial circadian clock system that we have derived from our analyses of KaiC ATPase activity.
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References
Abe J, Hiyama TB, Mukaiyama A et al (2015) Atomic-scale origins of slowness in the cyanobacterial circadian clock. Science 349:312–316
Bünning E (1967) The physiological clock. SpringerVerlag, Berlin
Dong G, Yang Q, Wang Q et al (2010) Elevated ATPase activity of KaiC applies a circadian checkpoint on cell division in Synechococcus elongatus. Cell 140(4):529–539
Dunlap JC, Loros JJ, DeCoursey PJ (eds) (2004) Chronobiology: biological timekeeping. Sinauer Associates Inc, Sunderland, MA
Edgar RS, Green EW, Zhao Y et al (2012) Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–464
Ishiura M, Kutsuna S, Aoki S et al (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281:1519–1523
Ito-Miwa K, Furuike Y, Akiyama S et al (2020) Tuning the circadian period of cyanobacteria up to 6.6 days by the single amino acid substitutions in KaiC. Proc Natl Acad Sci U S A 117(34):20926–20931
Iwasaki H, Taniguchi Y, Ishiura M, Kondo T (1999) Physical interactions among circadian clock proteins KaiA, KaiB and KaiC in cyanobacteria. EMBO J 18(5):1137–1145
Iwasaki H, Nishiwaki T, Kitayama Y et al (2002) KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci U S A 99(24):15788–15793
Kim YI, Dong G, Carruthers CW et al (2008) The day/night switch in KaiC, a central oscillator component of the circadian clock of cyanobacteria. Proc Natl Acad Sci U S A 105(35):12825–12830
Kitahara R, Oyama K, Kawamura T et al (2019) Pressure accelerates the circadian clock of cyanobacteria. Sci Rep 9:12395
Kitayama Y, Iwasaki H, Nishiwaki T et al (2003) KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J 22(9):2127–2134
Leipe DD, Aravind L, Grishin NV et al (2000) The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res 10:5–16
Ma P, Mori T, Zhao C et al (2016) Evolution of KaiC-dependent timekeepers: A proto-circadian timing mechanism confers adaptive fitness in the purple bacterium Rhodopseudomonas palustris. PLoS Genet 12(3):e1005922
Mukaiyama A, Furuike Y, Abe J et al (2018) Conformational rearrangements of the C1 ring in KaiC measure the timing of assembly with KaiB. Sci Rep 8:8803
Murayama Y, Mukaiyama A, Imai K et al (2011) Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J 30(1):68–78
Murayama Y, Kori H, Oshima C et al (2017) Low temperature nullifies the circadian clock in cyanobacteria through Hopf bifurcation. Proc Natl Acad Sci U S A 114(22):5641–5646
Mutoh R, Nishimura A, Yasui S et al (2013) The ATP-mediated regulation of KaiB-KaiC interaction in the cyanobacterial circadian clock. PLoS One 8(11):e80200
Nakajima M, Imai K, Ito H et al (2005) Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414–415
Nishiwaki T, Iwasaki H, Ishiura M et al (2000) Nucleotide binding and auto- phosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc Natl Acad Sci U S A 97(1):495–499
Nishiwaki T, Satomi Y, Nakajima M et al (2004) Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc Natl Acad Sci U S A 101(38):13927–13932
Nishiwaki T, Satomi Y, Kitayama Y et al (2007) A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J 26(17):4029–4037
Nishiwaki-Ohkawa T, Kitayama Y, Ochiai E et al (2014) Exchange of ADP with ATP in the CII ATPase domain promotes autophosphorylation of cyanobacterial clock protein KaiC. Proc Natl Acad Sci U S A 111(12):4455–4460
Njus D, Gooch VD, Hasting JW (1981) Precision of the Gonyaulax circadian clock. Cell Biophys 3(3):223–231
Nobel PS (1991) Characteristics of crossing membranes. In: Nobel PS (ed) Physicochemical and environmental plant physiology. Academic, Cambridge, pp 139–156
Oyama K, Azai C, Nakamura K et al (2016) Conversion between two conformational states of KaiC is induced by ATP hydrolysis as a trigger for cyanobacterial circadian oscillation. Sci Rep 6:32443
Oyama K, Azai C, Matsuyama J et al (2018) Phosphorylation at Thr432 induces structural destabilization of the CII ring in the circadian oscillator KaiC. FEBS Lett 592(1):36–45
Phong C, Markson JS, Wilhoite CM et al (2013) Robust and tunable circadian rhythms from differentially sensitive catalytic domains. Proc Natl Acad Sci U S A 110(3):1124–1129
Pittendrigh CS (1960) Circadian rhythms and the circadian organization of living systems. Cold Spring Harb Symp 125:159–184
Terauchi K, Kitayama Y, Nishiwaki T et al (2007) ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria. Proc Natl Acad Sci U S A 104(41):16377–16381
Tseng R, Goularte NF, Chavan A et al (2017) Structural basis of the day-night transition in a bacterial circadian clock. Science 355:1174–1180
Wiegard A, Köbler C, Oyama K et al (2020) Synechocystis KaiC3 displays temperature- and KaiB-dependent ATPase activity and is important for growth in darkness. J Bacteriol 202(4):e00478–e00419
Xu Y, Mori T, Johnson CH (2003) Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J 22(9):2117–2126
Yoshida T, Murayama Y, Ito H et al (2009) Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle. Proc Natl Acad Sci U S A 106(5):1648–1653
Acknowledgment
This review summarizes our studies on the mechanisms of circadian rhythm generation based on the functions of KaiC ATPase that we have performed since around 2010 at Nagoya University. The results summarizing this study are now in preparation for submission as a paper, together with the results of a number of experiments supporting a coupling model of CI and CII. We thank Dr. Keiko Okano-Imai (Kansai Medical University), Dr. Yoriko Murayama (Waseda University), Dr. Naoki Takai (Tokyo Metropolitan Institute of Medical Science), and Dr. Tomoaki Muranaka (Kagoshima University), who contributed greatly to our analyses. This study was supported by JST CREST Grant number JPMJCR07O2 to T.K. and Grants-in-Aid for Scientific Research (24000016 and 17H01427 to T.K).
Editor’s Note: For a complementary view on this chapter, please also see Takao Kondo’s chapter, “Around the Circadian Clock: Review 1 and Preview”.
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Ito-Miwa, K., Terauchi, K., Kondo, T. (2021). Mechanism of the Cyanobacterial Circadian Clock Protein KaiC to Measure 24 Hours. In: Johnson, C.H., Rust, M.J. (eds) Circadian Rhythms in Bacteria and Microbiomes. Springer, Cham. https://doi.org/10.1007/978-3-030-72158-9_5
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