Biochemical analysis of three putative KaiC clock proteins from Synechocystis sp. PCC 6803 suggests their functional divergence

Microbiology (United Kingdom)

Volumn 159, Issue PART 5, 2013, Pages 948-958

  Wiegard, Anika ^a   Dörrich, Anja K ^b   Deinzer, Hans Tobias ^b   Beck, Christian ^a   Wilde, Annegret ^b   Holtzendorff, Julia ^b   Axmann, Ilka M ^a  

^a CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^b JUSTUS LIEBIG UNIVERSITY   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

BACTERIAL PROTEIN; KAIC PROTEIN; UNCLASSIFIED DRUG;

ARTICLE; BACTERIAL STRAIN; CIRCADIAN RHYTHM; CONTROLLED STUDY; GENE CLUSTER; GENE FUNCTION; GENETIC VARIABILITY; IN VIVO STUDY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SYNECHOCOCCUS ELONGATUS; SYNECHOCYSTIS; THERMOSYNECHOCOCCUS;

CYANOBACTERIA; KAIA; SYNECHOCOCCUS ELONGATUS PCC 6301; SYNECHOCOCCUS ELONGATUS PCC 7942; SYNECHOCYSTIS SP.; SYNECHOCYSTIS SP. PCC 6803;

EID: 84876931666     PISSN: 13500872     EISSN: 14652080     Source Type: Journal    
DOI: 10.1099/mic.0.065425-0     Document Type: Article

References (62)

1. Akiyama, S., Nohara, A., Ito, K. & Mae ́ da, Y. (2008). Assembly and disassembly dynamics of the cyanobacterial periodosome. Mol Cell 29, 703-716.
2. Aoki, S. & Onai, K. (2009). Circadian clocks of Synechocystis sp. Strain PCC 6803, Thermosynechococcus elongatus, Prochlorococcus spp., Trichodesmium spp. and other species. In Bacterial circadian programs pp. 259-282. Edited by J. L. Ditty, S. R. Mackey & C. H. Johnson. Berlin: Springer.
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.
4. Bensadoun, A. & Weinstein, D. (1976). Assay of proteins in the presence of interfering materials. Anal Biochem 70, 241-250.
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.
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.
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.
8. Dvornyk, V. & Knudsen, B. (2005). Functional divergence of the circadian clock proteins in prokaryotes. Genetica 124, 247-255.
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.
10. Edgar, R. S., Green, E. W., Zhao, Y., van Ooijen, G., Olmedo, M., Qin, X., Xu, Y., Pan, M., Valekunja, U. K. & other authors (2012). Peroxiredoxins are conserved markers of circadian rhythms. Nature 485, 459-464.
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.
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 issue), W695-W699.
13. Hayashi, F., Suzuki, H., Iwase, R., Uzumaki, T., Miyake, A., Shen, J. R., Imada, K., Furukawa, Y., Yonekura, K. & other authors (2003). ATP-induced hexameric ring structure of the cyanobacterial circadian clock protein KaiC. Genes Cells 8, 287-296.
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)
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.
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.
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.
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.
19. Iwasaki, H. & Kondo, T. (2004). Circadian timing mechanism in the prokaryotic clock system of cyanobacteria. J Biol Rhythms 19, 436-444.
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.
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.
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.
23. Jukes, T. H. & Cantor, C. R. (1969). Evolution of protein molecules. In Mammalian Protein Metabolism, vol. 3, pp. 21-132. Edited by H. N. Munro. New York: Academic Press.
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.
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.
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.
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.
28. Laemmli, U. K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
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.
30. Mackinney, G. (1941). Absorption of light by chlorophyll solutions. J Biol Chem 140, 315-322.
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.
32. Mullineaux, C. W. & Stanewsky, R. (2009). The rolex and the hourglass: a simplified circadian clock in prochlorococcus? J Bacteriol 191, 5333-5335.
33. Murayama, Y., Mukaiyama, A., Imai, K., Onoue, Y., Tsunoda, A., Nohara, A., Ishida, T., Maéda, Y., Terauchi, K. & other authors (2011). Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J 30, 68-78.
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.
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.
36. Nicholas, K. B., Nicholas, H. B., Jr & Deerfield, D. W. I. (1997). GeneDoc: Analysis and Visualization of Genetic Variation. EMBNEW NEWS 4, 14.
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.
38. Nishiwaki, T., Satomi, Y., Nakajima, M., Lee, C., Kiyohara, R., Kageyama, H., Kitayama, Y., Temamoto, M., Yamaguchi, A. & other authors (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.
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.
40. O'Neill, J. S. & Reddy, A. B. (2011). Circadian clocks in human red blood cells. Nature 469, 498-503.
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.
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.
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.
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.
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.
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.
47. Rust, M. J., Markson, J. S., Lane, W. S., Fisher, D. S. & O'Shea, E. K. (2007). Ordered phosphorylation governs oscillation of a threeprotein circadian clock. Science 318, 809-812.
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.
49. Sievers, F., Wilm, A., Dineen, D., Gibson, T. J., Karplus, K., Li, W., Lopez, R., McWilliam, H., Remmert, M. & other authors (2011). Fast, scalable generation of high-quality protein multiple sequence alignments using CLUSTAL Omega. Mol Syst Biol 7, 539.
50. Tartof, K. D. & Hobbs, C. A. (1987). Improved media for growing plasmid and cosmid clones. Focus 9, 12.
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.
52. Tomita, J., Nakajima, M., Kondo, T. & Iwasaki, H. (2005). No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307, 251-254.
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.
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.
55. Vakonakis, I., Sun, J., Wu, T., Holzenburg, A., Golden, S. S. & Li Wang, 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.
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.
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.
58. Xu, Y., Mori, T. & Johnson, C. H. (2000). Circadian clock-protein expression in cyanobacteria: rhythms and phase setting. EMBO J 19, 3349-3357.
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.
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.
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.
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.