Giving Time Purpose: The Synechococcus elongatus Clock in a Broader Network Context

Annual Review of Genetics

Volumn 49, Issue , 2015, Pages 485-505

  Shultzaberger, Ryan K ^a,b   Boyd, Joseph S ^a,c   Diamond, Spencer ^a,c   Greenspan, Ralph J ^a,b   Golden, Susan S ^a,c  

^a San Diego   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Circadian rhythms; Global regulation; kai oscillator; RpaA

Indexed keywords

ALGAL PROTEIN; ALGAL RNA; CIKA PROTEIN; KAIB PROTEIN; KAIC PROTEIN; RPAA PROTEIN; SASA PROTEIN; TRANSCRIPTION FACTOR CLOCK; UNCLASSIFIED DRUG;

ARTICLE; CELL METABOLISM; CHROMATIN IMMUNOPRECIPITATION; CIRCADIAN RHYTHM; GENE EXPRESSION; GENETIC VARIABILITY; HIGH THROUGHPUT SCREENING; METABOLIC REGULATION; METABOLOMICS; MOLECULAR GENETICS; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; RNA SEQUENCE; SYNECHOCOCCUS ELONGATUS; TRANSCRIPTION REGULATION; ADAPTATION; CYTOLOGY; EVOLUTION; GENE EXPRESSION REGULATION; PHYSIOLOGY; SIGNAL TRANSDUCTION; SYNECHOCOCCUS;

ADAPTATION, BIOLOGICAL; BIOLOGICAL EVOLUTION; CIRCADIAN RHYTHM; GENE EXPRESSION REGULATION, BACTERIAL; SIGNAL TRANSDUCTION; SYNECHOCOCCUS;

EID: 84948773277     PISSN: 00664197     EISSN: 15452948     Source Type: Book Series    
DOI: 10.1146/annurev-genet-111212-133227     Document Type: Article

References (98)

1. Arita K, Hashimoto H, Igari K, Akaboshi M, Kutsuna S, et al. 2007. Structural and biochemical characterization of a cyanobacterium circadian clock-modifier protein. J. Biol. Chem. 282:1128-35
2. Ashby MK, Mullineaux CW. 1999. Cyanobacterial ycf27 gene products regulate energy transfer from phycobilisomes to photosystems I and II. FEMS Microbiol. Lett. 181:253-60
3. Axmann IM, Duhring U, Seeliger L, Arnold A, Vanselow JT, et al. 2009. Biochemical evidence for a timing mechanism in Prochlorococcus. J. Bacteriol. 191:5342-47
4. Baca I, Sprockett D, Dvornyk V. 2010. Circadian input kinases and their homologs in cyanobacteria: evolutionary constraints versus architectural diversification. J. Mol. Evol. 70:453-65
5. Bell-Pedersen D, Cassone VM, Earnest DJ, Golden SS, Hardin PE, et al. 2005. Circadian rhythms from multiple oscillators: lessons from diverse organisms. Nat. Rev. Genet. 6:544-56
6. Boyd JS, Bordowitz JR, Bree AC, Golden SS. 2013. An allele of the crm gene blocks cyanobacterial circadian rhythms. PNAS 110:13950-55
7. Chang YG, Cohen SE, PhongC,MyersWK,Kim YI, et al. 2015. A protein fold switch joins the circadian oscillator to clock output in cyanobacteria. Science 349:324-28
8. Chang YG, Tseng R, Kuo NW, LiWang A. 2012. Rhythmic ring-ring stacking drives the circadian oscillator clockwise. PNAS 109:16847-51
9. Diamond S, Jun D, RubinBE, Golden SS. 2015. The circadian oscillator in Synechococcus elongatus controls metabolite partitioning during diurnal growth. PNAS 112:E1916-25
10. Dodd AN, SalathiaN,Hall A,Kevei E,T othR, et al. 2005. Plant circadian clocks increase photosynthesis, growth, survival, and competitive advantage. Science 309:630-33
11. Doi R, Oishi K, Ishida N. 2010. CLOCK regulates circadian rhythms of hepatic glycogen synthesis through transcriptional activation of Gys2. J. Biol. Chem. 285:22114-21
12. DoolittleWF, Singer RA. 1974. Mutational analysis of dark endogenous metabolism in the blue-green bacterium Anacystis nidulans. J. Bacteriol. 119:677-83
13. Dunlap JC, Loros JJ, DeCoursey PJ. 2004. Chronobiology: Biological Timekeeping. Sunderland, MA: Sinauer Assoc
14. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M, et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459-64
15. Egli M. 2014. Intricate protein-protein interactions in the cyanobacterial circadian clock. J. Biol. Chem. 289:21267-75
16. Espinosa J, Boyd JS, Cantos R, Salinas P, Golden SS, Contreras A. 2015. Cross-talk and regulatory interactions between the essential response regulator RpaB and cyanobacterial circadian clock output. PNAS 112:2198-203
17. Garces RG,Wu N, GillonW, Pai EF. 2004. Anabaena circadian clock proteins KaiA and KaiB reveal a potential common binding site to their partner KaiC. EMBO J. 23:1688-98
18. Gontero B, Maberly S. 2012. An intrinsically disordered protein, CP12: jack of all trades and master of the Calvin cycle. Biochem. Soc. Trans. 40:995-99
19. GonzeD, RousselM,Goldbeter A. 2002. Amodel for the enhancement of fitness in cyanobacteria based on resonance of a circadian oscillator with the external light-dark cycle. J. Theor. Biol. 214:577-97
20. GrundelM, Scheunemann R, LockauW, Zilliges Y. 2012. Impaired glycogen synthesis causesmetabolic overflow reactions and affects stress responses in the cyanobacterium Synechocystis sp. PCC 6803. Microbiology 158:3032-43
21. Gutu A, O'Shea EK. 2013. Two antagonistic clock-regulated histidine kinases time the activation of circadian gene expression. Mol. Cell 50:288-94
22. Hanaoka M, Takai N, Hosokawa N, Fujiwara M, Akimoto Y, et al. 2012. RpaB, another response regulator operating circadian clock-dependent transcriptional regulation in Synechococcus elongatus PCC 7942. J. Biol. Chem. 287:26321-27
23. HanaokaM, Tanaka K. 2008. Dynamics of RpaB-promoter interaction during high light stress, revealed by chromatin immunoprecipitation (ChIP) analysis in Synechococcus elongatus PCC 7942. Plant J. 56:327-35
24. Hellweger FL. 2010. Resonating circadian clocks enhance fitness in cyanobacteria in silico. Ecol. Model. 221:1620-29
25. 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 circadian rhythm. J. Biol. Chem. 280:19127-35
26. Holtman CK, Chen Y, Sandoval P, Gonzales A, Nalty MS, et al. 2005. High-throughput functional analysis of the Synechococcus elongatus PCC 7942 genome. DNA Res. 12:103-15
27. Holtzendorff J, Partensky F, Mella D, Lennon JF, Hess WR, Garczarek L. 2008. Genome streamlining results in loss of robustness of the circadian clock in the marine cyanobacterium Prochlorococcus marinus PCC 9511. J. Biol. Rhythm. 23:187-99
28. Hosokawa N, Kushige H, Iwasaki H. 2013. Attenuation of the posttranslational oscillator via transcription-translation feedback enhances circadian-phase shifts in Synechococcus. PNAS 110:14486-91
29. Ishiura M, Kutsuna S, Aoki S, Iwasaki H, Andersson C, et al. 1998. Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281:1519-23
30. Ito H, Mutsuda M, Murayama Y, Tomita J, Hosokawa N, et al. 2009. Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. PNAS 106:14168-73
31. Ivleva NB, Bramlett MR, Lindahl PA, Golden SS. 2005. LdpA: A component of the circadian clock senses redox state of the cell. EMBO J. 24:1202-10
32. Ivleva NB, Gao T, LiWang AC, Golden SS. 2006. Quinone sensing by the circadian input kinase of the cyanobacterial circadian clock. PNAS 103:17468-73
33. IwasakiH,Williams SB, Kitayama Y, Ishiura M, Golden SS, KondoT. 2000. AKaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223-33
34. IwaseR, Imada K, Hayashi F,Uzumaki T, MorishitaM, et al. 2005. Functionally important substructures of circadian clock protein KaiB in a unique tetramer complex. J. Biol. Chem. 280:43141-49
35. Johnson CH, Stewart PL, Egli M. 2011. The cyanobacterial circadian system: from biophysics to bioevolution. Annu. Rev. Biophys. 40:143-67
36. Kanehisa M, Goto S. 2000. KEGG: Kyoto Encyclopedia of Genes and Genomes. Nucleic Acids Res. 28:27-30
37. Katayama M, Kondo T, Xiong J, Golden SS. 2003. ldpA encodes an iron-sulfur protein involved in lightdependent modulation of the circadian period in the cyanobacterium Synechococcus elongatus PCC 7942. J. Bacteriol. 185:1415-22
38. Katayama M, Tsinoremas NF, Kondo T, Golden SS. 1999. cpmA, a gene involved in an output pathway of the cyanobacterial circadian system. J. Bacteriol. 181:3516-24
39. Kato H, Watanabe S, Nimura-Matsune K, Chibazakura T, Tozawa Y, Yoshikawa H. 2012. Exploration of a possible partnership among orphan two-component system proteins in cyanobacterium Synechococcus elongatus PCC 7942. Biosci. Biotechnol. Biochem. 76:1484-91
40. Kim YI, Vinyard DJ, Ananyev GM, Dismukes GC, Golden SS. 2012. Oxidized quinones signal onset of darkness directly to the cyanobacterial circadian oscillator. PNAS 109:17765-69
41. Knowles VL, Plaxton WC. 2003. From genome to enzyme: analysis of key glycolytic and oxidative pentose-phosphate pathway enzymes in the cyanobacterium Synechocystis sp. PCC 6803. Plant Cell Physiol. 44:758-63
42. Kondo T, Ishiura M. 1994. Circadian rhythms of cyanobacteria: monitoring the biological clocks of individual colonies by bioluminescence. J. Bacteriol. 176:1881-85
43. Kondo T, Mori T, Lebedeva NV, Aoki S, Ishiura M, Golden SS. 1997. Circadian rhythms in rapidly dividing cyanobacteria. Science 275:224-27
44. Kondo T, Strayer C, Kulkarni R, Taylor W, Ishiura M, et al. 1993. Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. PNAS 90:5672-76
45. Kondo T, Tsinoremas N, Golden S, Johnson C, Kutsuna S, Ishiura M. 1994. Circadian clock mutants of cyanobacteria. Science 266:1233-36
46. Kucho Ki, Okamoto K, Tsuchiya Y, Nomura S, Nango M, et al. 2005. Global analysis of circadian expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 187:2190-99
47. Kutsuna S, Kondo T, Aoki S, Ishiura M. 1998. A period-extender gene, pex, that extends the period of the circadian clock in the cyanobacterium Synechococcus sp. strain PCC 7942. J. Bacteriol. 180:2167-74
48. Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV, Golden SS, et al. 1995. Circadian orchestration of gene expression in cyanobacteria. Genes Dev. 9:1469-78
49. Ma P, Woelfle MA, Johnson CH. 2013. An evolutionary fitness enhancement conferred by the circadian system in cyanobacteria. Chaos Solitons Fractals 50:65-74
50. Mackey SR, Choi JS, Kitayama Y, Iwasaki H, Dong G, Golden SS. 2008. Proteins found in a CikA interaction assay link the circadian clock, metabolism, and cell division in Synechococcus elongatus. J. Bacteriol. 190:3738-46
51. Mackey SR, Ditty JL, Clerico EM, Golden SS. 2007. Detection of rhythmic bioluminescence from luciferase reporters in cyanobacteria. Methods Mol. Biol. 362:115-29
52. Mackey SR, Golden SS, Ditty JL. 2011. The itty-bitty time machine: genetics of the cyanobacterial circadian clock. Adv. Genet. 74:13-53
53. Markson JS, Piechura JR, Puszynska AM, O'Shea EK. 2013. Circadian control of global gene expression by the cyanobacterial master regulator RpaA. Cell 155:1396-408
54. Moronta-Barrios F, Espinosa J, Contreras A. 2012. In vivo features of signal transduction by the essential response regulator RpaB from Synechococcus elongatus PCC 7942. Microbiology 158:1229-37
55. Moronta-Barrios F, Espinosa J, Contreras A. 2013. Negative control of cell size in the cyanobacterium Synechococcus elongatus PCC 7942 by the essential response regulator RpaB. FEBS Lett. 587:504-9
56. Nakahira Y, Katayama M, Miyashita H, Kutsuna S, Iwasaki H, et al. 2004. Global gene repression by KaiC as a master process of prokaryotic circadian system. PNAS 101:881-85
57. Nakajima M, ImaiK, Ito H, NishiwakiT,Murayama Y, et al. 2005. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414-15
58. Nishiwaki T, Satomi Y, Nakajima M, Lee C, Kiyohara R, et al. 2004. Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. PNAS 101:13927-32
59. Ouyang Y, Andersson C, Kondo T, Golden S, Johnson C. 1998. Resonating circadian clocks enhance fitness in cyanobacteria. PNAS 95:8660-64
60. PaddockML, Boyd JS, Adin DM, Golden SS. 2013. Active output state of the Synechococcus Kai circadian oscillator. PNAS 110:E3849-57
61. Paranjpe D, Sharma V. 2005. Evolution of temporal order in living organisms. J. Circadian Rhythm. 3:7
62. PattanayakGK, Phong C, RustMJ. 2014. Rhythms in energy storage control the ability of the cyanobacterial circadian clock to reset. Curr. Biol. 24:1934-38
63. Pattanayek R, Williams DR, Pattanayek S, Xu Y, Mori T, et al. 2006. Analysis of KaiA-KaiC protein interactions in the cyano-bacterial circadian clock using hybrid structuralmethods. EMBO J. 25:2017-28
64. Petit JM, Burlet-Godinot S,Magistretti PJ, Allaman I. 2015. Glycogen metabolism and the homeostatic regulation of sleep. Metab. Brain Dis. 30:263-79
65. Rosbash M. 2009. The implications of multiple circadian clock origins. PLOS Biol. 7:e1000062
66. Rubin BE, Wetmore KM, Price MN, Diamond S, Shultzaberger RK, et al. 2015. The essential gene set of a photosynthetic organism. PNAS. In press
67. Rust MJ, Golden SS, O'Shea EK. 2011. Light-driven changes in energy metabolism directly entrain the cyanobacterial circadian oscillator. Science 331:220-23
68. Rust MJ,Markson JS, LaneWS, Fisher DS, O'Shea EK. 2007. Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318:809-12
69. Scanlan DJ, Sundaram S, Newman J, Mann NH, Carr NG. 1995. Characterization of a zwf mutant of Synechococcus sp. strain PCC 7942. J. Bacteriol. 177:2550-53
70. Schmitz O, Katayama M,Williams SB, Kondo T, Golden SS. 2000. CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science 289:765-68
71. Shestakov S, KhyenNT. 1970. Evidence for genetic transformation in blue-green alga Anacystis nidulans. Mol. Gen. Genet. 107:372-75
72. Shultzaberger RK, Boyd JS, Katsuki T, Golden SS, Greenspan RJ. 2014. Single mutations in sasA enable a simpler -cikA gene network architecture with equivalent circadian properties. PNAS 111:E5069-75
73. Shultzaberger RK, Paddock ML, Katsuki T, Greenspan RJ, Golden SS. 2015. High-throughput and quantitative approaches formeasuring circadian rhythms in cyanobacteria using bioluminescence. Methods Enzymol. 551:53-72
74. Stock AM, Robinson VL,Goudreau PN. 2000. Two-component signal transduction. Annu. Rev. Biochem. 69:183-215
75. Suzuki E, Umeda K, Nihei S, Moriya K, Ohkawa H, et al. 2007. Role of the GlgX protein in glycogen metabolism of the cyanobacterium, Synechococcus elongatus PCC 7942. Biochim. Biophys. Acta 1770:763-73
76. Sweeney BM, Borgese MB. 1989. A circadian rhythm in cell division in a prokaryote, the cyanobacterium Synechococcus WH78031. J. Phycol. 25:183-86
77. Takai N, Ikeuchi S, Manabe K, Kutsuna S. 2006. Expression of the circadian clock-related gene pex in cyanobacteria increases in darkness and is required to delay the clock. J. Biol. Rhythm. 21:235-44
78. Takai N, Nakajima M, Oyama T, Kito R, Sugita C, et al. 2006. A KaiC-associating SasA-RpaA twocomponent regulatory system as a major circadian timing mediator in cyanobacteria.PNAS103:12109-14
79. Tamoi M, Miyazaki T, Fukamizo T, Shigeoka S. 2005. The Calvin cycle in cyanobacteria is regulated by CP12 via the NAD(H)/NADP(H) ratio under light/dark conditions. Plant J. 42:504-13
80. Taniguchi Y, Katayama M, Ito R, Takai N, Kondo T, Oyama T. 2007. labA: a novel gene required for negative feedback regulation of the cyanobacterial circadian clock protein KaiC. Genes Dev. 21:60-70
81. Taniguchi Y, Nishikawa T, Kondo T, Oyama T. 2012. Overexpression of lalA, a paralog of labA, is capable of affecting both circadian gene expression and cell growth in the cyanobacterium Synechococcus elongatus PCC 7942. FEBS Lett. 586:753-59
82. Teng SW,Mukherji S,Moffitt JR, De Buyl S, O'Shea EK. 2013. Robust circadian oscillations in growing cyanobacteria require transcriptional feedback. Science 340:737-40
83. Terauchi K, Kitayama Y, Nishiwaki T, Miwa K, Murayama Y, et al. 2007. ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria. PNAS 104:16377-81
84. Tomita J, Nakajima M, Kondo T, Iwasaki H. 2005. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307:251-54
85. Tseng R, Chang YG, Bravo I, Latham R, Chaudhary A, et al. 2014. Cooperative KaiA-KaiB-KaiC interactions affect KaiB/SasA competition in the circadian clock of cyanobacteria. J. Mol. Biol. 426:389-402
86. Umetani M, Hosokawa N, Kitayama Y, Iwasaki H. 2014. Hypersensitive photic responses and intact genome-wide transcriptional control without the KaiC phosphorylation cycle in the Synechococcus circadian system. J. Bacteriol. 196:548-55
87. Vijayan V, Zuzow R, O'Shea E. 2009. Oscillations in supercoiling drive circadian gene expression in cyanobacteria. PNAS 106:22564
88. WiegardA,Dorrich AK,DeinzerHT,BeckC,WildeA, et al. 2013. Biochemical analysis of three putative KaiC clock proteins from Synechocystis sp. PCC 6803 suggests their functional divergence. Microbiology 159:948-58
89. Williams SB, Vakonakis I, Golden SS, LiWang AC. 2002. Structure and function from the circadian clock protein KaiA of Synechococcus elongatus: a potential clock input mechanism. PNAS 99:15357-62
90. Woelfle MA, Johnson CH. 2009. The adaptive value of the circadian clock system in cyanobacteria. In Bacterial Circadian Programs, ed. JL Ditty, SR Mackey, CH Johnson, pp. 205-21. Berlin: Springer
91. Woelfle MA, Ouyang Y, Phanvijhitsiri K, Johnson CH. 2004. The adaptive value of circadian clocks: an experimental assessment in cyanobacteria. Curr. Biol. 14:1481-86
92. Woelfle MA, Xu Y, Qin X, Johnson CH. 2007. Circadian rhythms of superhelical status of DNA in cyanobacteria. PNAS 104:18819-24
93. Wood TL, Bridwell-Rabb J, Kim YI, Gao T, Chang YG, et al. 2010. The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor. PNAS 107:5804-9
94. 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. PNAS 101:13933-38
95. Xu Y, Weyman PD, Umetani M, Xiong J, Qin X, et al. 2013. Circadian yin-yang regulation and its manipulation to globally reprogram gene expression. Curr. Biol. 23:2365-74
96. Yang C, Hua Q, Shimizu K. 2002. Integration of the information from gene expression and metabolic fluxes for the analysis of the regulatory mechanisms in Synechocystis. Appl.Microbiol. Biotechnol. 58:813-22
97. Yen UC, Huang TC, Yen TC. 2004. Observation of the circadian photosynthetic rhythm in cyanobacteria with a dissolved-oxygen meter. Plant Sci. 166:949-52
98. Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C, et al. 2009. Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, Prochlorococcus. PLOS ONE 4:e5135