Skip to main content

Structural Aspects of the Cyanobacterial KaiABC Circadian Clock

  • Chapter
Bacterial Circadian Programs

Abstract

The KaiABC circadian clock in the cyanobacterium Synechococcus elongatus can be reconstituted in vitro from three proteins in the presence of ATP. This oscillator displays the pertinent features of circadian rhythms including a self-sustained 24-h period and temperature compensation. At every phase of the cycle there is a mixture of types of Kai complexes and the proportions of the various types are oscillating. The KaiC protein is an auto-kinase and auto-phosphatase whose phosphorylation levels oscillate over the daily period whereby KaiA and KaiB interact with KaiC to increase and decrease its phosphorylation, respectively. This chapter provides an overview of the three-dimensional (3D) structural characterization of Kai proteins and the understanding of the KaiA–KaiC interaction gained by NMR and 3D electron microscopy (EM). Despite impressive advances in the structural realm, many open questions remain regarding the control of KaiC phosphorylation by KaiA and KaiB and conformational changes accompanying the transition between the hypo- and hyper-phosphorylated states of KaiC.

This is a preview of subscription content, log in via an institution to check access.

Access this chapter

Chapter
USD 29.95
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
eBook
USD 129.00
Price excludes VAT (USA)
  • Available as PDF
  • Read on any device
  • Instant download
  • Own it forever
Softcover Book
USD 169.99
Price excludes VAT (USA)
  • Compact, lightweight edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info
Hardcover Book
USD 169.99
Price excludes VAT (USA)
  • Durable hardcover edition
  • Dispatched in 3 to 5 business days
  • Free shipping worldwide - see info

Tax calculation will be finalised at checkout

Purchases are for personal use only

Institutional subscriptions

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  • Abrahams JP, Leslie AGW, Lutter R, Walker JE (1994) Structure at 2.8 Ă… resolution of F1 ATPase from bovine heart mitochondria. Nature 370:621–628

    Article  PubMed  CAS  Google Scholar 

  • Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The protein data bank. Nucleic Acids Res 28:235–242

    Article  PubMed  CAS  Google Scholar 

  • Egli M, Pattanayek R, Pattanayek S (2007) Protein–protein interactions in the cyanobacterial KaiABC circadian clock. In: Boeyens JCA, Ogilvie JF (eds) Models, mysteries, and magic of molecules; proceedings of the INDABA-5 conference, Kruger National Park, South Africa, August 20–25, 2006. Springer, Dordrecht, pp 287–303

    Google Scholar 

  • Garces RG, Wu N, Gillon W, Pai EF (2004) Anabaena circadian clock proteins KaiA and KaiB reveal potential common binding site to their partner KaiC. EMBO J 23:1688–1698

    Article  PubMed  CAS  Google Scholar 

  • Golden SS (2004) Meshing the gears of the cyanobacterial circadian clock. Proc Natl Acad Sci USA 101:13697–13698

    Article  PubMed  CAS  Google Scholar 

  • Golden SS, Cassone VM, LiWang A (2007) Shifting nanoscopic clock gears. Nat Struct Mol Biol 14:362–363

    Article  PubMed  CAS  Google Scholar 

  • Hayashi F, Suzuki H, Iwase R, Uzumaki T, Miyake A, Shen J-R, Imada K, Furukawa Y, Yonekura K, Namba K, Ishiura M (2003) ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 8:287–296

    Article  PubMed  CAS  Google Scholar 

  • Hayashi F, Itoh N, Uzumaki T, Iwase R, Tsuchiya Y, Yamakawa H, Morishita M, Onai K, Itoh S, Ishiura M (2004a) Roles of two ATPase-motif-containing domains in cyanobacterial circadian clock protein KaiC. J Biol Chem 50:52331–52337

    Article  Google Scholar 

  • Hayashi F, Ito H, Fujita M, Iwase R, Uzumaki T, Ishiura M (2004b) Stoichiometric interactions between cyanobacterial clock proteins KaiA and KaiC. Biochem Biophys Res Comm 316:195–202

    Article  CAS  Google Scholar 

  • Hayashi F, Iwase R, Uzumaki T, Ishiura M (2006) Hexamerization by the N-terminal domain and intersubunit phosphorylation by the C-terminal domain of cyanobacterial circadian clock protein KaiC. Biochem Biophys Res Comm 318:864–872

    Article  Google Scholar 

  • Hitomi K, Oyama T, Han S, Arvai AS, Getzoff ED (2005) Tetrameric architecture of the circadian clock protein KaiB: a novel interface for intermolecular interactions and its impact on the cir-cadian rhythm. J Biol Chem 280:18643–18650

    Article  Google Scholar 

  • Ishiura M, Kutsuna S, Aoki S, Iwasaki H, Andersson CR, Tanabe A, Golden SS, Johnson CH, Kondo T (1998) Expression of a gene cluster kaiABC as a circadian feedback process in cyano-bacteria. Science 281:1519–1523

    Article  PubMed  CAS  Google Scholar 

  • Ito H, Kageyama H, Mutsuda M, Nakajima M, Oyama T, Kondo T (2007) Autonomous synchronization of the circadian KaiC phosphorylation rhythm. Nat Struct Mol Biol 14:1084–1088

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki H, Williams SB, Kitayama, Y, Ishiura M, Golden SS, Kondo T (2000) A KaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobac-teria. Cell 101:223–233

    Article  PubMed  CAS  Google Scholar 

  • Iwasaki H, Nishiwaki T, Kitayama Y, Nakajima M, Kondo T (2002) KaiA-stimulated KaiC phospho-rylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci USA 99:15788–15793

    Article  PubMed  CAS  Google Scholar 

  • Iwase R, Imada K, Hayashi F, Uzumaki T, Morishita M, Onai K, Furukawa Y, Namba K, Ishiura M (2005) Functionally important substructures of circadian clock protein KaiB in a unique tetramer complex. J Biol Chem 280:43141–43149

    Article  PubMed  CAS  Google Scholar 

  • Johnson CH, Egli M (2004) Visualizing a biological clockwork's cogs. Nat Struct Mol Biol 11:584–585

    Article  PubMed  CAS  Google Scholar 

  • Kageyama H, Nishiwaki T, Nakajima M, Iwasaki H, Oyama T, Kondo T (2006) Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the KaiC phosphorylation cycle in vitro. Mol Cell 23:161–171

    Article  PubMed  CAS  Google Scholar 

  • Kitayama Y, Iwasaki H, Nishiwaki T, Kondo T (2003) KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J 22:1–8

    Article  Google Scholar 

  • Leipe DD, Aravind L, Grishin N V, Koonin EV (2000) The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res 10:5–16

    PubMed  CAS  Google Scholar 

  • Mori T, Johnson CH (2001) Circadian programming in cyanobacteria. Semin Cell Dev Biol 12:271–278

    Article  PubMed  CAS  Google Scholar 

  • Mori T, Saveliev SV, Xu Y, Stafford WF, Cox MM, Inman RB, Johnson CH (2002) Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci USA 99:17203–17208

    Article  PubMed  CAS  Google Scholar 

  • Mori T, Williams DR, Byrne M, Qin X, Egli M, Mchaourab H, Stewart PL, Johnson CH (2007) Elucidating the ticking of an in vitro circadian clockwork. PLoS Biol 5:841–853

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Nishiwaki T, Iwasaki H, Ishiura M, Kondo T (2000) Nucleotide binding and autophosphorylation of the clock protein KaiC as a circadian timing process of cyanobacteria. Proc Natl Acad Sci USA 97:495–499

    Article  PubMed  CAS  Google Scholar 

  • Nishiwaki T, Satomi Y, Nakajima M, Lee C, Kiyohara R, Kageyama H, Kitayama Y, Temamoto M, Yamaguchi A, Hijikata A, Go M, Iwasaki H, Takao T, Kondo T (2004) Role of KaiC phos-phorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc Natl Acad Sci USA 101:13927–13932

    Article  PubMed  CAS  Google Scholar 

  • Nishiwaki T, Satomi Y, Kitayama Y, Terauchi K, Kiyohara R, Takao T, Kondo T (2007) A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J 26:4029–4037

    Article  PubMed  CAS  Google Scholar 

  • Pattanayek R, Wang J, Mori T, Xu Y, Johnson CH, Egli M (2004) Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol Cell 15:375–388

    Article  PubMed  CAS  Google Scholar 

  • Pattanayek R, Williams DR, Pattanayek S, Xu Y, Mori T, Johnson CH, Stewart PL, Egli M (2006) Analysis of KaiA–KaiC protein interactions in the cyanobacterial circadian clock using hybrid structural methods. EMBO J 25:2017–2038

    Article  PubMed  CAS  Google Scholar 

  • Pattanayek R, Williams DR, Pattanayek S, Mori T, Johnson CH, Stewart PL, Egli M (2008) Structural model of the circadian clock KaiB-KaiC complex and mechanism for modulation of KaiC phosphorylation. EMBO J 27:1767–1778

    Article  PubMed  CAS  Google Scholar 

  • Pettersen EF (2004) UCSF chimera – a visualization system for exploratory research and analysis. J Comput Chem 25:1605–1612

    Article  PubMed  CAS  Google Scholar 

  • Rust MJ, Markson JS, Lane WS, Fisher DS, O'Shea EK (2007) Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318:809–812

    Article  PubMed  CAS  Google Scholar 

  • Schmitz O, Katayama M, Williams SB, Kondo T, and Golden SS (2000) CikA, a bacteriophyto-chrome that resets the cyanobacterial circadian clock. Science 289:765–768

    Article  PubMed  CAS  Google Scholar 

  • Taniguchi Y, Yamaguchi A, Hijikata A, Iwasaki H, Kamagata K, Ishiura M, Go M, Kondo T (2001) Two KaiA-binding domains of cyanobacterial circadian clock protein KaiC. FEBS Lett 496:86–90

    Article  PubMed  CAS  Google Scholar 

  • Terauchi K, Kitayama Y, Nishiwaki T, Miwa K, Murayama Y, Oyama T, Kondo T (2007) The ATPase activity of KaiC determines the basic timing for circadian clock in cyanobacteria. Proc Natl Acad Sci USA 104:16377–16381

    Article  PubMed  CAS  Google Scholar 

  • Tomita J, Nakajima M, Kondo T, Iwasaki H (2005) Circadian rhythm of KaiC phosphorylation without transcription-translation feedback. Science 307:251–254

    Article  PubMed  CAS  Google Scholar 

  • Uzumaki T, Fujita M, Nakatsu T, Hayashi F, Shibata H, Itoh N, Kato H, Ishiura M (2004) Crystal structure of the C-terminal clock-oscillator domain of the cyanobacterial KaiA protein. Nat Struct Mol Biol 11:623–631

    Article  PubMed  CAS  Google Scholar 

  • Vakonakis I, 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 USA 101:10925–10930

    Article  PubMed  CAS  Google Scholar 

  • Vakonakis I, Sun J, Wu T, Holzenburg A, Golden SS, LiWang AC (2004a) NMR structure of the KaiC-interacting C-terminal domain of KaiA, a circadian clock protein: Implications for the KaiA–KaiC Interaction. Proc Natl Acad Sci USA 101:1479–1484

    Article  CAS  Google Scholar 

  • Vakonakis I, Klewer DA, Williams SB, Golden SS, LiWang AC (2004b) Structure of the N-termi-nal domain of the circadian clock-associated histidine kinase SasA. J Mol Biol 342:9–17

    Article  CAS  Google Scholar 

  • Wang J (2005) Recent cyanobacterial Kai protein structures suggest a rotary clock. Structure 13:735–741

    Article  PubMed  CAS  Google Scholar 

  • Williams SB, Vakonakis I, Golden SS, LiWang AC (2002) Structure and function from the circa-dian clock protein KaiA of Synechococcus elongatus: a potential clock input mechanism. Proc Natl Acad Sci USA 99:15357–15362

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Mori T, Johnson CH (2003) Cyanobacterial circadian clockwork: roles of KaiA, KaiB, and the kaiBC promoter in regulating KaiC. EMBO J 22:2117–2126

    Article  PubMed  CAS  Google Scholar 

  • Xu Y, Mori T, Pattanayek R, Pattanayek S, Egli M, Johnson CH (2004) Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc Natl Acad Sci USA 101:13933–13938

    Article  PubMed  CAS  Google Scholar 

  • Ye S, Vakonakis I, Ioerger TR, LiWang AC, Sacchettini JC (2004) Crystal structure of circadian clock protein KaiA from Synechococcus elongatus. J Biol Chem 279:20511–20518

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Editor information

Editors and Affiliations

Rights and permissions

Reprints and permissions

Copyright information

© 2009 Springer-Verlag Berlin Heidelberg

About this chapter

Cite this chapter

Egli, M., Stewart, P.L. (2009). Structural Aspects of the Cyanobacterial KaiABC Circadian Clock. In: Ditty, J.L., Mackey, S.R., Johnson, C.H. (eds) Bacterial Circadian Programs. Springer, Berlin, Heidelberg. https://doi.org/10.1007/978-3-540-88431-6_7

Download citation

Publish with us

Policies and ethics