1887

Abstract

Cyanobacteria have been shown to have a circadian clock system that consists mainly of three protein components: KaiA, KaiB and KaiC. This system is well understood in the cyanobacterium PCC 7942, for which robust circadian oscillations have been shown. Like many other cyanobacteria, the chromosome of the model cyanobacterium sp. PCC 6803 contains additional and gene copies besides the standard gene cluster. The respective gene products differ significantly in their amino acid sequences, especially in their C-terminal regions, suggesting different functional characteristics. Here, phosphorylation assays of the three sp. PCC 6803 KaiC proteins revealed that KaiC1 phosphorylation depends on KaiA, as is well documented for the PCC 7942 KaiC protein, whereas KaiC2 and KaiC3 autophosphorylate independently of KaiA. This was confirmed by protein–protein interaction studies, which demonstrate that only KaiC1 interacts with KaiA. Furthermore, we demonstrate that the three different Kai proteins form only homomeric complexes . As only KaiC1 phosphorylation depends on KaiA, a prerequisite for robust oscillations, we suggest that the gene cluster in sp. PCC 6803 controls circadian timing in a manner similar to the clock described in PCC 7942.

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2013-05-01
2024-03-29
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References

  1. Akiyama S., Nohara A., Ito K., Maéda Y. ( 2008). Assembly and disassembly dynamics of the cyanobacterial periodosome. Mol Cell 29:703–716 [View Article][PubMed]
    [Google Scholar]
  2. Aoki S., Onai K. ( 2009). Circadian clocks of Synechocystis sp. strain PCC 6803, Thermosynechococcus elongatus, Prochlorococcus spp., Trichodesmium spp. and other species. Bacterial circadian programs259–282 Ditty J. L., Mackey S. R., Johnson C. H. Berlin: Springer; [View Article]
    [Google Scholar]
  3. Axmann I. M., Dühring U., Seeliger L., Arnold A., Vanselow J. T., Kramer A., Wilde A. ( 2009). Biochemical evidence for a timing mechanism in Prochlorococcus. . J Bacteriol 191:5342–5347 [View Article][PubMed]
    [Google Scholar]
  4. Bensadoun A., Weinstein D. ( 1976). Assay of proteins in the presence of interfering materials. Anal Biochem 70:241–250 [View Article][PubMed]
    [Google Scholar]
  5. Bradford M. M. ( 1976). A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein–dye binding. Anal Biochem 72:248–254 [View Article][PubMed]
    [Google Scholar]
  6. Brettschneider C., Rose R. J., Hertel S., Axmann I. M., Heck A. J. R., Kollmann M. ( 2010). A sequestration feedback determines dynamics and temperature entrainment of the KaiABC circadian clock. Mol Syst Biol 6:389 [View Article][PubMed]
    [Google Scholar]
  7. Clodong S., Dühring U., Kronk L., Wilde A., Axmann I., Herzel H., Kollmann M. ( 2007). Functioning and robustness of a bacterial circadian clock. Mol Syst Biol 3:90 [View Article][PubMed]
    [Google Scholar]
  8. Dvornyk V., Knudsen B. ( 2005). Functional divergence of the circadian clock proteins in prokaryotes. Genetica 124:247–255 [View Article][PubMed]
    [Google Scholar]
  9. Dvornyk V., Vinogradova O., Nevo E. ( 2003). Origin and evolution of circadian clock genes in prokaryotes. Proc Natl Acad Sci U S A 100:2495–2500 [View Article][PubMed]
    [Google Scholar]
  10. Edgar R. S., Green E. W., Zhao Y., van Ooijen G., Olmedo M., Qin X., Xu Y., Pan M., Valekunja U. K. et al. ( 2012). Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–464[PubMed]
    [Google Scholar]
  11. Egli M., Mori T., Pattanayek R., Xu Y., Qin X., Johnson C. H. ( 2012). Dephosphorylation of the core clock protein KaiC in the cyanobacterial KaiABC circadian oscillator proceeds via an ATP synthase mechanism. Biochemistry 51:1547–1558 [View Article][PubMed]
    [Google Scholar]
  12. Goujon M., McWilliam H., Li W., Valentin F., Squizzato S., Paern J., Lopez R. ( 2010). A new bioinformatics analysis tools framework at EMBL–EBI. Nucleic Acids Res 38:Web Server issueW695–W699 [View Article][PubMed]
    [Google Scholar]
  13. Hayashi F., Suzuki H., Iwase R., Uzumaki T., Miyake A., Shen J. R., Imada K., Furukawa Y., Yonekura K. et al. ( 2003). ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 8:287–296 [View Article][PubMed]
    [Google Scholar]
  14. Hertel S., Brettschneider C., Axmann I. M. ( 2013). Revealing a two-loop transcriptional feedback mechanism in the cyanobacterial circadian clock. PLOS Comput Biol in press
    [Google Scholar]
  15. Holtzendorff J., Partensky F., Mella D., Lennon J. F., Hess W. R., Garczarek L. ( 2008). Genome streamlining results in loss of robustness of the circadian clock in the marine cyanobacterium Prochlorococcus marinus PCC 9511. J Biol Rhythms 23:187–199 [View Article][PubMed]
    [Google Scholar]
  16. Imai K., Nishiwaki T., Kondo T., Iwasaki H. ( 2004). Circadian rhythms in the synthesis and degradation of a master clock protein KaiC in cyanobacteria. J Biol Chem 279:36534–36539 [View Article][PubMed]
    [Google Scholar]
  17. 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 [View Article][PubMed]
    [Google Scholar]
  18. Ito H., Mutsuda M., Murayama Y., Tomita J., Hosokawa N., Terauchi K., Sugita C., Sugita M., Kondo T., Iwasaki H. ( 2009). Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. . Proc Natl Acad Sci U S A 106:14168–14173 [View Article][PubMed]
    [Google Scholar]
  19. Iwasaki H., Kondo T. ( 2004). Circadian timing mechanism in the prokaryotic clock system of cyanobacteria. J Biol Rhythms 19:436–444 [View Article][PubMed]
    [Google Scholar]
  20. Iwasaki H., Taniguchi Y., Ishiura M., Kondo T. ( 1999). Physical interactions among circadian clock proteins KaiA, KaiB and KaiC in cyanobacteria. EMBO J 18:1137–1145 [View Article][PubMed]
    [Google Scholar]
  21. Iwasaki H., Nishiwaki T., Kitayama Y., Nakajima M., Kondo T. ( 2002). KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc Natl Acad Sci U S A 99:15788–15793 [View Article][PubMed]
    [Google Scholar]
  22. 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 [View Article][PubMed]
    [Google Scholar]
  23. Jukes T. H., Cantor C. R. ( 1969). Evolution of protein molecules. Mammalian Protein Metabolism vol. 321–132 Munro H. N. New York: Academic Press;
    [Google Scholar]
  24. Kim Y.-I., Dong G., Carruthers C. W. Jr, Golden S. S., LiWang A. ( 2008). The day/night switch in KaiC, a central oscillator component of the circadian clock of cyanobacteria. Proc Natl Acad Sci U S A 105:12825–12830 [View Article][PubMed]
    [Google Scholar]
  25. 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 22:2127–2134 [View Article][PubMed]
    [Google Scholar]
  26. Kuchmina E., Wallner T., Kryazhov S., Zinchenko V. V., Wilde A. ( 2012). An expression system for regulated protein production in Synechocystis sp. PCC 6803 and its application for construction of a conditional knockout of the ferrochelatase enzyme. J Biotechnol 162:75–80 [View Article][PubMed]
    [Google Scholar]
  27. Kucho K.-i., Okamoto K., Tsuchiya Y., Nomura S., Nango M., Kanehisa M., Ishiura M. ( 2005). Global analysis of circadian expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J Bacteriol 187:2190–2199 [View Article][PubMed]
    [Google Scholar]
  28. Laemmli U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685 [View Article][PubMed]
    [Google Scholar]
  29. Lowry O. H., Rosebrough N. J., Farr A. L., Randall R. J. ( 1951). Protein measurement with the Folin phenol reagent. J Biol Chem 193:265–275[PubMed]
    [Google Scholar]
  30. Mackinney G. ( 1941). Absorption of light by chlorophyll solutions. J Biol Chem 140:315–322
    [Google Scholar]
  31. Mori T., Saveliev S. V., Xu Y., Stafford W. F., Cox M. M., Inman R. B., Johnson C. H. ( 2002). Circadian clock protein KaiC forms ATP-dependent hexameric rings and binds DNA. Proc Natl Acad Sci U S A 99:17203–17208 [View Article][PubMed]
    [Google Scholar]
  32. Mullineaux C. W., Stanewsky R. ( 2009). The rolex and the hourglass: a simplified circadian clock in prochlorococcus?. J Bacteriol 191:5333–5335 [View Article][PubMed]
    [Google Scholar]
  33. Murayama Y., Mukaiyama A., Imai K., Onoue Y., Tsunoda A., Nohara A., Ishida T., Maéda Y., Terauchi K. et al. ( 2011). Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J 30:68–78 [View Article][PubMed]
    [Google Scholar]
  34. 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 [View Article][PubMed]
    [Google Scholar]
  35. Nakajima M., Ito H., Kondo T. ( 2010). In vitro regulation of circadian phosphorylation rhythm of cyanobacterial clock protein KaiC by KaiA and KaiB. FEBS Lett 584:898–902 [View Article][PubMed]
    [Google Scholar]
  36. Nicholas K. B., Nicholas H. B. Jr, Deerfield D. W. I. ( 1997). GeneDoc: Analysis and Visualization of Genetic Variation. EMBNEW NEWS 4:14
    [Google Scholar]
  37. Nishiwaki T., Kondo T. ( 2012). Circadian autodephosphorylation of cyanobacterial clock protein KaiC occurs via formation of ATP as intermediate. J Biol Chem 287:18030–18035 [View Article][PubMed]
    [Google Scholar]
  38. Nishiwaki T., Satomi Y., Nakajima M., Lee C., Kiyohara R., Kageyama H., Kitayama Y., Temamoto M., Yamaguchi A. et al. ( 2004). Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc Natl Acad Sci U S A 101:13927–13932 [View Article][PubMed]
    [Google Scholar]
  39. 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 [View Article][PubMed]
    [Google Scholar]
  40. O’Neill J. S., Reddy A. B. ( 2011). Circadian clocks in human red blood cells. Nature 469:498–503 [View Article][PubMed]
    [Google Scholar]
  41. O’Neill J. S., van Ooijen G., Dixon L. E., Troein C., Corellou F., Bouget F.-Y., Reddy A. B., Millar A. J. ( 2011). Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–558 [View Article][PubMed]
    [Google Scholar]
  42. Pattanayek R., Wang J., Mori T., Xu Y., Johnson C. H., Egli M. ( 2004). Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol Cell 15:375–388 [View Article][PubMed]
    [Google Scholar]
  43. Pattanayek R., Williams D. R., Pattanayek S., Xu Y., Mori T., Johnson C. H., Stewart P. L., Egli M. ( 2006). Analysis of KaiA–KaiC protein interactions in the cyano-bacterial circadian clock using hybrid structural methods. EMBO J 25:2017–2028 [View Article][PubMed]
    [Google Scholar]
  44. Peter E., Salinas A., Wallner T., Jeske D., Dienst D., Wilde A., Grimm B. ( 2009). Differential requirement of two homologous proteins encoded by sll1214 and sll1874 for the reaction of Mg protoporphyrin monomethylester oxidative cyclase under aerobic and micro-oxic growth conditions. Biochim Biophys Acta 1787:1458–1467 [View Article][PubMed]
    [Google Scholar]
  45. Qin X., Byrne M., Mori T., Zou P., Williams D. R., McHaourab H., Johnson C. H. ( 2010). Intermolecular associations determine the dynamics of the circadian KaiABC oscillator. Proc Natl Acad Sci U S A 107:14805–14810 [View Article][PubMed]
    [Google Scholar]
  46. Rippka R., Deruelles J., Waterbury J. B., Herdman M., Stanier R. Y. ( 1979). Generic assignments, strain histories and properties of pure cultures of cyanobacteria. J Gen Microbiol 111:1–61 [CrossRef]
    [Google Scholar]
  47. Rust M. J., Markson J. S., Lane W. S., Fisher D. S., O’Shea E. K. ( 2007). Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318:809–812 [View Article][PubMed]
    [Google Scholar]
  48. Schägger H., von Jagow G. ( 1987). Tricine-sodium dodecyl sulfate-polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal Biochem 166:368–379 [View Article][PubMed]
    [Google Scholar]
  49. Sievers F., Wilm A., Dineen D., Gibson T. J., Karplus K., Li W., Lopez R., McWilliam H., Remmert M. et al. ( 2011). Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7:539 [View Article][PubMed]
    [Google Scholar]
  50. Tartof K. D., Hobbs C. A. ( 1987). Improved media for growing plasmid and cosmid clones. . Focus 9:12
    [Google Scholar]
  51. Terauchi K., Kitayama Y., Nishiwaki T., Miwa K., Murayama Y., Oyama T., Kondo T. ( 2007). ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria. Proc Natl Acad Sci U S A 104:16377–16381 [View Article][PubMed]
    [Google Scholar]
  52. Tomita J., Nakajima M., Kondo T., Iwasaki H. ( 2005). No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307:251–254 [View Article][PubMed]
    [Google Scholar]
  53. 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 [View Article][PubMed]
    [Google Scholar]
  54. Vakonakis I., LiWang A. C. ( 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 A 101:10925–10930 [View Article][PubMed]
    [Google Scholar]
  55. Vakonakis I., Sun J., Wu T., Holzenburg A., Golden S. S., LiWang A. C. ( 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 A 101:1479–1484 [View Article][PubMed]
    [Google Scholar]
  56. Vijayan V., Zuzow R., O’Shea E. K. ( 2009). Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc Natl Acad Sci U S A 106:22564–22568 [View Article][PubMed]
    [Google Scholar]
  57. Williams S. B., Vakonakis I., Golden S. S., LiWang A. C. ( 2002). Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: a potential clock input mechanism. Proc Natl Acad Sci U S A 99:15357–15362 [View Article][PubMed]
    [Google Scholar]
  58. Xu Y., Mori T., Johnson C. H. ( 2000). Circadian clock-protein expression in cyanobacteria: rhythms and phase setting. EMBO J 19:3349–3357 [View Article][PubMed]
    [Google Scholar]
  59. Xu Y., Mori T., Johnson C. H. ( 2003). Cyanobacterial circadian clockwork: roles of KaiA, KaiB and the kaiBC promoter in regulating KaiC. EMBO J 22:2117–2126 [View Article][PubMed]
    [Google Scholar]
  60. Xu Y., Mori T., Pattanayek R., Pattanayek S., Egli M., Johnson C. H. ( 2004). Identification of key phosphorylation sites in the circadian clock protein KaiC by crystallographic and mutagenetic analyses. Proc Natl Acad Sci U S A 101:13933–13938 [View Article][PubMed]
    [Google Scholar]
  61. Xu Y., Mori T., Qin X., Yan H., Egli M., Johnson C. H. ( 2009). Intramolecular regulation of phosphorylation status of the circadian clock protein KaiC. PLoS ONE 4:e7509 [View Article][PubMed]
    [Google Scholar]
  62. Zinchenko V. V., Piven I. V., Melnik V. A., Shestakov S. V. ( 1999). Vectors for the complementation analysis of cyanobacterial mutants. Russ J Genet 35:228–232
    [Google Scholar]
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