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Abstract

For a biological oscillator to function as a circadian pacemaker that confers a fitness advantage, its timing functions must be stable in response to environmental and metabolic fluctuations. One such stability enhancer, temperature compensation, has long been a defining characteristic of these timekeepers. However, an accurate biological timekeeper must also resist changes in metabolism, and this review suggests that temperature compensation is actually a subset of a larger phenomenon, namely metabolic compensation, which maintains the frequency of circadian oscillators in response to a host of factors that impinge on metabolism and would otherwise destabilize these clocks. The circadian system of prokaryotic cyanobacteria is an illustrative model because it is composed of transcriptional and nontranscriptional oscillators that are coupled to promote resilience. Moreover, the cyanobacterial circadian program regulates gene activity and metabolic pathways, and it can be manipulated to improve the expression of bioproducts that have practical value.

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2014-06-02
2024-04-25
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Literature Cited

  1. Dunlap JC, Loros JJ, DeCoursey PJ. 1.  2004. Chronobiology: Biological Timekeeping Sunderland, MA: Sinauer406
  2. Izumo M, Johnson CH, Yamazaki S. 2.  2003. Circadian gene expression in mammalian fibroblasts revealed by real-time luminescence reporting: temperature compensation and damping. Proc. Natl. Acad. Sci. USA 100:16089–94 [Google Scholar]
  3. Reyes BA, Pendergast JS, Yamazaki S. 3.  2008. Mammalian peripheral circadian oscillators are temperature compensated. J. Biol. Rhythms 23:95–98 [Google Scholar]
  4. Ruby NF, Burns DE, Heller HC. 4.  1999. Circadian rhythms in the suprachiasmatic nucleus are temperature-compensated and phase-shifted by heat pulses in vitro. J. Neurosci. 19:8630–36 [Google Scholar]
  5. Tosini G, Menaker M. 5.  1998. The tau mutation affects temperature compensation of hamster retinal circadian oscillators. Neuroreport 9:1001–5 [Google Scholar]
  6. Pittendrigh CS.6.  1954. On the temperature independence in the clock system controlling emergence time in Drosophila. Proc. Natl. Acad. Sci. USA 40:1018–29 [Google Scholar]
  7. Pittendrigh CS.7.  1993. Temporal organization: reflections of a Darwinian clock-watcher. Annu. Rev. Physiol. 55:17–54 [Google Scholar]
  8. Hastings JW, Sweeney BM. 8.  1957. On the mechanism of temperature independence in a biological clock. Proc. Natl. Acad. Sci. USA 43:804–11 [Google Scholar]
  9. Johnson CH.9.  2010. Circadian clocks and cell division: What's the pacemaker?. Cell Cycle 9:3864–73 [Google Scholar]
  10. Mihalcescu I, Hsing W, Leibler S. 10.  2004. Resilient circadian oscillator revealed in individual cyanobacteria. Nature 430:81–85 [Google Scholar]
  11. Pittendrigh CS.11.  1960. Circadian rhythms and the circadian organization of living systems. Cold Spring Harb. Symp. Quant. Biol. 25:159–84 [Google Scholar]
  12. Sweeney BM, Hastings JW. 12.  1960. Effects of temperature upon diurnal rhythms. Cold Spring Harb. Symp. Quant. Biol. 25:87–104 [Google Scholar]
  13. Bass J. 13.  2012. Circadian topology of metabolism. Nature 491:348–56 [Google Scholar]
  14. Eckel-Mahan K, Sassone-Corsi P. 14.  2013. Metabolism and the circadian clock converge. Physiol. Rev. 93:107–35 [Google Scholar]
  15. Green CB, Takahashi JS, Bass J. 15.  2008. The meter of metabolism. Cell 134:728–42 [Google Scholar]
  16. Roenneberg T, Merrow M. 16.  1999. Circadian systems and metabolism. J. Biol. Rhythms 14:449–59 [Google Scholar]
  17. Shi S, Ansari T, McGuinness OP, Wasserman DH, Johnson CH. 17.  2013. Circadian disruption leads to insulin resistance and obesity. Curr. Biol. 23:372–81 [Google Scholar]
  18. Turek FW, Joshu C, Kohsaka A, Lin E, Ivanova G. 18.  et al. 2005. Obesity and metabolic syndrome in circadian clock mutant mice. Science 308:1043–45 [Google Scholar]
  19. Wijnen H, Young MW. 19.  2006. Interplay of circadian clocks and metabolic rhythms. Annu. Rev. Genet. 40:409–48 [Google Scholar]
  20. Xu K, DiAngelo JR, Hughes ME, Hogenesch JB, Sehgal A. 20.  2011. The circadian clock interacts with metabolic physiology to influence reproductive fitness. Cell Metab. 13:639–54 [Google Scholar]
  21. Pittendrigh CS, Caldarola PC. 21.  1973. General homeostasis of the frequency of circadian oscillations. Proc. Natl. Acad. Sci. USA 70: 2697–701
  22. Johnson CH, Golden SS, Ishiura M, Kondo T. 22.  1996. Circadian clocks in prokaryotes. Mol. Microbiol. 21:5–11 [Google Scholar]
  23. Ditty JL, Mackey SR, Johnson CH. 23.  2009. Bacterial Circadian Programs Berlin: Springer333
  24. Grobbelaar N, Huang T-C, Lin HY, Chow TJ. 24.  1986. Dinitrogen-fixing endogenous rhythm in Synechococcus RF-1. FEMS Microbiol. Lett. 37:173–77 [Google Scholar]
  25. Huang T-C, Lin R-F. 25.  2009. Circadian rhythm of Cyanothece RF-1 (Synechococcus RF-1). See Ref. 23 39–61
  26. Mitsui A, Kumazawa S, Takahashi A, Ikemoto H, Arai T. 26.  1986. Strategy by which nitrogen-fixing unicellular cyanobacteria grow photoautotrophically. Nature 323:720–22 [Google Scholar]
  27. Liu Y, Tsinoremas NF, Golden SS, Kondo T, Johnson CH. 27.  1996. Circadian expression of genes involved in the purine biosynthetic pathway of the cyanobacterium Synechococcus sp. strain PCC 7942. Mol. Microbiol. 20:1071–81 [Google Scholar]
  28. Kondo T, Strayer CA, Kulkarni RD, Taylor W, Ishiura M. 28.  et al. 1993. Circadian rhythms in prokaryotes: luciferase as a reporter of circadian gene expression in cyanobacteria. Proc. Natl. Acad. Sci. USA 90:5672–76 [Google Scholar]
  29. Ouyang Y, Andersson CR, Kondo T, Golden SS, Johnson CH. 29.  1998. Resonating circadian clocks enhance fitness in cyanobacteria. Proc. Natl. Acad. Sci. USA 95:8660–64 [Google Scholar]
  30. Woelfle MA, Ouyang Y, Phanvijhitsiri K, Johnson CH. 30.  2004. The adaptive value of circadian clocks: An experimental assessment in cyanobacteria. Curr. Biol. 14:1481–86 [Google Scholar]
  31. Nakajima M, Imai K, Ito H, Nishiwaki T, Murayama Y. 31.  et al. 2005. Reconstitution of circadian oscillation of cyanobacterial KaiC phosphorylation in vitro. Science 308:414–15 [Google Scholar]
  32. Murakami R, Mutoh R, Iwase R, Furukawa Y, Imada K. 31a.  et al. 2012. The roles of the dimeric and tetrameric structures of the clock protein KaiB in the generation of circadian oscillations in cyanobacteria. J. Biol. Chem. 287:29506–15 [Google Scholar]
  33. Liu Y, Tsinoremas NF, Johnson CH, Lebedeva NV, Golden SS. 32.  et al. 1995. Circadian orchestration of gene expression in cyanobacteria. Genes Dev. 9:1469–78 [Google Scholar]
  34. Ito H, Mutsuda M, Murayama Y, Tomita J, Hosokawa N. 33.  et al. 2009. Cyanobacterial daily life with Kai-based circadian and diurnal genome-wide transcriptional control in Synechococcus elongatus. Proc. Natl. Acad. Sci. USA 106:14168–73 [Google Scholar]
  35. Kucho K, Okamoto K, Tsuchiya Y, Nomura S, Nango M. 34.  et al. 2005. Global analysis of circadian expression in the cyanobacterium Synechocystis sp. strain PCC 6803. J. Bacteriol. 187:2190–99 [Google Scholar]
  36. Shi T, Ilikchyan I, Rabouille S, Zehr JP. 35.  2010. Genome-wide analysis of diel gene expression in the unicellular N2-fixing cyanobacterium Crocosphaera watsonii WH 8501. ISME J. 4:621–32 [Google Scholar]
  37. Vijayan V, Zuzow R, O'Shea EK. 36.  2009. Oscillations in supercoiling drive circadian gene expression in cyanobacteria. Proc. Natl. Acad. Sci. USA 106:22564–68 [Google Scholar]
  38. Xu Y, Weyman PD, Umetani M, Xiong J, Qin X. 37.  et al. 2013. Circadian yin-yang regulation and its manipulation to globally reprogram gene expression. Curr. Biol. 23:2365–74 [Google Scholar]
  39. Zinser ER, Lindell D, Johnson ZI, Futschik ME, Steglich C. 38.  et al. 2009. Choreography of the transcriptome, photophysiology, and cell cycle of a minimal photoautotroph, prochlorococcus. PLoS ONE 4:e5135 [Google Scholar]
  40. Gutu A, O'Shea EK. 39.  2013. Two antagonistic clock-regulated histidine kinases time the activation of circadian gene expression. Mol. Cell 50:288–94 [Google Scholar]
  41. Hanaoka M, Takai N, Hosokawa N, Fujiwara M, Akimoto Y. 40.  et al. 2012. RpaB, another response regulator operating circadian clock-dependent transcriptional regulation in Synechococcus elongatus PCC 7942. J. Biol. Chem. 287:26321–27 [Google Scholar]
  42. Iwasaki H, Williams SB, Kitayama Y, Ishiura M, Golden SS, Kondo T. 41.  2000. A kaiC-interacting sensory histidine kinase, SasA, necessary to sustain robust circadian oscillation in cyanobacteria. Cell 101:223–33 [Google Scholar]
  43. Takai N, Nakajima M, Oyama T, Kito R, Sugita C. 42.  et al. 2006. A KaiC-associating SasA–RpaA two-component regulatory system as a major circadian timing mediator in cyanobacteria. Proc. Natl. Acad. Sci. USA 103:12109–14 [Google Scholar]
  44. Boyd JS, Bordowitz JR, Bree AC, Golden SS. 43.  2013. An allele of the crm gene blocks cyanobacterial circadian rhythms. Proc. Natl. Acad. Sci. USA 110:13950–55 [Google Scholar]
  45. Taniguchi Y, Takai N, Katayama M, Kondo T, Oyama T. 44.  2010. Three major output pathways from the KaiABC-based oscillator cooperate to generate robust circadian kaiBC expression in cyanobacteria. Proc. Natl. Acad. Sci. USA 107:3263–68 [Google Scholar]
  46. Markson JS, Piechura JR, Puszynska AM, O'Shea EK. 44a.  2013. Circadian control of global gene expression by the cyanobacterial master regulator RpaA. Cell 155:1396–408 [Google Scholar]
  47. Schmitz O, Katayama M, Williams SB, Kondo T, Golden SS. 45.  2000. CikA, a bacteriophytochrome that resets the cyanobacterial circadian clock. Science 289:765–68 [Google Scholar]
  48. Mori T, Johnson CH. 46.  2001. Circadian programming in cyanobacteria. Semin. Cell Dev. Biol. 12:271–78 [Google Scholar]
  49. Woelfle MA, Xu Y, Qin X, Johnson CH. 47.  2007. Circadian rhythms of superhelical status of DNA in cyanobacteria. Proc. Natl. Acad. Sci. USA 104:18819–24 [Google Scholar]
  50. Smith RM, Williams SB. 48.  2006. Circadian rhythms in gene transcription imparted by chromosome compaction in the cyanobacterium Synechococcus elongatus. Proc. Natl. Acad. Sci. USA 103:8564–69 [Google Scholar]
  51. Min H, Liu Y, Johnson CH, Golden SS. 49.  2004. Phase determination of circadian gene expression in Synechococcus elongatus PCC 7942. J. Biol. Rhythms 19:103–12 [Google Scholar]
  52. Katayama M, Tsinoremas NF, Kondo T, Golden SS. 50.  1999. cpmA, a gene involved in an output pathway of the cyanobacterial circadian system. J. Bacteriol. 181:3516–24 [Google Scholar]
  53. Nakahira Y, Katayama M, Miyashita H, Kutsuna S, Iwasaki H. 51.  et al. 2004. Global gene repression by KaiC as a master process of prokaryotic circadian system. Proc. Natl. Acad. Sci. USA 101:881–85 [Google Scholar]
  54. Chabot JR, Pedraza JM, Luitel P, van Oudenaarden A. 52.  2007. Stochastic gene expression out-of-steady-state in the cyanobacterial circadian clock. Nature 450:1249–52 [Google Scholar]
  55. Amdaoud M, Vallade M, Weiss-Schaber C, Mihalcescu I. 53.  2007. Cyanobacterial clock, a stable phase oscillator with negligible intercellular coupling. Proc. Natl. Acad. Sci. USA 104:7051–56 [Google Scholar]
  56. Kondo T, Mori T, Lebedeva NV, Aoki S, Ishiura M, Golden SS. 54.  1997. Circadian rhythms in rapidly dividing cyanobacteria. Science 275:224–27 [Google Scholar]
  57. Mori T, Binder B, Johnson CH. 55.  1996. Circadian gating of cell division in cyanobacteria growing with average doubling times of less than 24 hours. Proc. Natl. Acad. Sci. USA 93:10183–88 [Google Scholar]
  58. Mackey SR, Choi JS, Kitayama Y, Iwasaki H, Dong G, Golden SS. 56.  2008. Proteins found in a CikA-interaction assay link the circadian clock, metabolism, and cell division in Synechococcus elongatus. J. Bacteriol. 190:3738–46 [Google Scholar]
  59. Dong G, Yang Q, Wang Q, Kim YI, Wood TL. 57.  et al. 2010. Elevated ATPase activity of KaiC applies a circadian checkpoint on cell division in Synechococcus elongatus. Cell 140:529–39 [Google Scholar]
  60. Aronson BD, Johnson KA, Loros JJ, Dunlap JC. 58.  1994. Negative feedback defining a circadian clock: autoregulation of the clock gene frequency. Science 263:1578–84 [Google Scholar]
  61. Hardin PE, Hall JC, Rosbash M. 59.  1990. Feedback of the Drosophila period gene product on circadian cycling of its messenger RNA levels. Nature 343:536–540 [Google Scholar]
  62. Dibner C, Sage D, Unser M, Bauer C, d'Eysmond T. 60.  et al. 2009. Circadian gene expression is resilient to large fluctuations in overall transcription rates. EMBO J. 28:123–34 [Google Scholar]
  63. Ishiura M, Kutsuna S, Aoki S, Iwasaki H, Andersson CR. 61.  et al. 1998. Expression of a gene cluster kaiABC as a circadian feedback process in cyanobacteria. Science 281:1519–23 [Google Scholar]
  64. Kitayama Y, Nishiwaki T, Terauchi K, Kondo T. 62.  2008. Dual KaiC-based oscillations constitute the circadian system of cyanobacteria. Genes Dev. 22:1513–21 [Google Scholar]
  65. Qin X, Byrne M, Xu Y, Mori T, Johnson CH. 63.  2010. Coupling of a core post-translational pacemaker to a slave transcription/translation feedback loop in a circadian system. PLoS Biol. 8:e1000394 [Google Scholar]
  66. Teng SW, Mukherji S, Moffitt JR, de Buyl S, O'Shea EK. 64.  2013. Robust circadian oscillations in growing cyanobacteria require transcriptional feedback. Science 340:737–40 [Google Scholar]
  67. Zwicker D, Lubensky DK, ten Wolde PR. 65.  2010. Robust circadian clocks from coupled protein-modification and transcription-translation cycles. Proc. Natl. Acad. Sci. USA 107:22540–45 [Google Scholar]
  68. Egli M, Johnson CH. 66.  2013. A circadian clock nanomachine that runs without transcription or translation. Curr. Opin. Neurobiol. 23:732–40 [Google Scholar]
  69. Johnson CH, Stewart PL, Egli M. 67.  2011. The cyanobacterial circadian system: from biophysics to bioevolution. Annu. Rev. Biophys. 40:143–67 [Google Scholar]
  70. 68.  Deleted in proof
  71. Mackey SR, Golden SS, Ditty JL. 69.  2011. The itty-bitty time machine genetics of the cyanobacterial circadian clock. Adv. Genet. 74:13–53 [Google Scholar]
  72. Terauchi K, Kitayama Y, Nishiwaki T, Miwa K, Murayama Y. 70.  et al. 2007. The ATPase activity of KaiC determines the basic timing for circadian clock of cyanobacteria. Proc. Natl. Acad. Sci. USA 104:16377–81 [Google Scholar]
  73. Nishiwaki T, Satomi Y, Kitayama Y, Terauchi K, Kiyohara R. 71.  et al. 2007. A sequential program of dual phosphorylation of KaiC as a basis for circadian rhythm in cyanobacteria. EMBO J. 26:4029–37 [Google Scholar]
  74. Rust MJ, Markson JS, Lane WS, Fisher DS, O'Shea EK. 72.  2007. Ordered phosphorylation governs oscillation of a three-protein circadian clock. Science 318:809–12 [Google Scholar]
  75. Murayama Y, Mukaiyama A, Imai K, Onoue Y, Tsunoda A. 73.  et al. 2011. Tracking and visualizing the circadian ticking of the cyanobacterial clock protein KaiC in solution. EMBO J. 30:68–78 [Google Scholar]
  76. Nishiwaki T, Satomi Y, Nakajima M, Lee C, Kiyohara R. 74.  et al. 2004. Role of KaiC phosphorylation in the circadian clock system of Synechococcus elongatus PCC 7942. Proc. Natl. Acad. Sci. USA 101:13927–32 [Google Scholar]
  77. Pattanayek R, Wang J, Mori T, Xu Y, Johnson CH, Egli M. 75.  2004. Visualizing a circadian clock protein: crystal structure of KaiC and functional insights. Mol. Cell 15:375–88 [Google Scholar]
  78. Pattanayek R, Mori T, Xu Y, Pattanayek S, Johnson CH, Egli M. 76.  2009. Structures of KaiC circadian clock mutant proteins: a new phosphorylation site at T426 and mechanisms of kinase, ATPase and phosphatase. PLoS ONE 4:e7529 [Google Scholar]
  79. Xu Y, Mori T, Pattanayek R, Pattanayek S, Egli M, Johnson CH. 77.  2004. Identification of key phosphorylation sites in the circadian clock protein kaic by crystallographic and mutagenetic analyses. Proc. Natl. Acad. Sci. USA 101:13933–38 [Google Scholar]
  80. Johnson CH, Egli M, Stewart PL. 78.  2008. Structural insights into a circadian oscillator. Science 322:697–701 [Google Scholar]
  81. Chang YG, Tseng R, Kuo NW, LiWang A. 79.  2012. Rhythmic ring-ring stacking drives the circadian oscillator clockwise. Proc. Natl. Acad. Sci. USA 109:16847–51 [Google Scholar]
  82. Mori T, Williams DR, Byrne MO, Qin X, Egli M. 80.  et al. 2007. Elucidating the ticking of an in vitro circadian clockwork. PLoS Biol. 5:e93 [Google Scholar]
  83. Pattanayek R, Williams DR, Pattanayek S, Xu Y, Mori T. 81.  et al. 2006. Analysis of KaiA–KaiC protein interactions in the cyano-bacterial circadian clock using hybrid structural methods. EMBO J. 25:2017–28 [Google Scholar]
  84. Pattanayek R, Williams DR, Pattanayek S, Mori T, Johnson CH. 82.  et al. 2008. Structural model of the circadian clock KaiB–KaiC complex and mechanism for modulation of KaiC phosphorylation. EMBO J. 27:1767–78 [Google Scholar]
  85. Pattanayek R, Williams DR, Rossi G, Weigand S, Mori T. 83.  et al. 2011. Combined SAXS/EM based models of the S. elongatus post-translational circadian oscillator and its interactions with the output His-kinase SasA. PLoS ONE 6:e23697 [Google Scholar]
  86. Pattanayek R, Yadagiri KK, Ohi MD, Egli M. 84.  2013. Nature of KaiB–KaiC binding in the cyanobacterial circadian oscillator. Cell Cycle 12:810–17 [Google Scholar]
  87. Snijder J, Burnley RJ, Wiegard A, Melquiond ASJ, Bonvin AMJJ. 85.  et al. 2014. Insight into cyanobacterial circadian timing from structural details of the KaiB–KaiC interaction. Proc. Natl. Acad. Sci. USA 111:1379–84 [Google Scholar]
  88. Villarreal SA, Pattanayek R, Williams DR, Mori T, Qin X. 86.  et al. 2013. CryoEM and molecular dynamics of the circadian KaiB–KaiC complex indicates KaiB monomers interact with KaiC and block ATP binding clefts. J. Mol. Biol. 425:3311–24 [Google Scholar]
  89. Kim YI, Dong G, Carruthers CW Jr, Golden SS, LiWang A. 87.  2008. The day/night switch in KaiC, a central oscillator component of the circadian clock of cyanobacteria. Proc. Natl. Acad. Sci. USA 105:12825–30 [Google Scholar]
  90. Vakonakis I, LiWang AC. 88.  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 101:10925–30 [Google Scholar]
  91. Egli M, Mori T, Pattanayek R, Xu Y, Qin X, Johnson CH. 89.  2012. Dephosphorylation of the core clock protein KaiC in the cyanobacterial KaiABC circadian oscillator proceeds via an ATP synthase mechanism. Biochemistry 51:1547–58 [Google Scholar]
  92. Nishiwaki T, Kondo T. 90.  2012. Circadian autodephosphorylation of cyanobacterial clock protein KaiC occurs via formation of ATP as intermediate. J. Biol. Chem. 287:18030–35 [Google Scholar]
  93. Tomita J, Nakajima M, Kondo T, Iwasaki H. 91.  2005. No transcription-translation feedback in circadian rhythm of KaiC phosphorylation. Science 307:251–54 [Google Scholar]
  94. Ito H, Kageyama H, Mutsuda M, Nakajima M, Oyama T, Kondo T. 92.  2007. Autonomous synchronization of the circadian KaiC phosphorylation rhythm. Nat. Struct. Mol. Biol. 14:1084–88 [Google Scholar]
  95. Akiyama S. 93.  2012. Structural and dynamic aspects of protein clocks: How can they be so slow and stable?. Cell. Mol. Life Sci. 69:2147–60 [Google Scholar]
  96. Brettschneider C, Rose RJ, Hertel S, Axmann IM, Heck AJ, Kollmann M. 94.  2010. A sequestration feedback determines dynamics and temperature entrainment of the KaiABC circadian clock. Mol. Syst. Biol. 6:389 [Google Scholar]
  97. Clodong S, Dühring U, Kronk L, Wilde A, Axmann I. 95.  et al. 2007. Functioning and robustness of a bacterial circadian clock. Mol. Syst. Biol. 3:90 [Google Scholar]
  98. Qin X, Byrne M, Mori T, Zou P, Williams DR. 96.  et al. 2010. Intermolecular associations determine the dynamics of the circadian KaiABC oscillator. Proc. Natl. Acad. Sci. USA 107:14805–10 [Google Scholar]
  99. van Zon JS, Lubensky DK, Altena PR, ten Wolde PR. 97.  2007. An allosteric model of circadian KaiC phosphorylation. Proc. Natl. Acad. Sci. USA 104:7420–25 [Google Scholar]
  100. Ozbudak EM, Thattai M, Kurtser I, Grossman AD, van Oudenaarden A. 98.  2002. Regulation of noise in the expression of a single gene. Nat. Genet. 31:69–73 [Google Scholar]
  101. Kitayama Y, Iwasaki H, Nishiwaki T, Kondo T. 99.  2003. KaiB functions as an attenuator of KaiC phosphorylation in the cyanobacterial circadian clock system. EMBO J. 22:2127–34 [Google Scholar]
  102. Eckel-Mahan KL, Patel VR, Mohney RP, Vignola KS, Baldi P, Sassone-Corsi P. 100.  2012. Coordination of the transcriptome and metabolome by the circadian clock. Proc. Natl. Acad. Sci. USA 109:5541–46 [Google Scholar]
  103. Stöckel J, Welsh EA, Liberton M, Kunnvakkam R, Aurora R, Pakrasi HB. 101.  2008. Global transcriptomic analysis of Cyanothece 51142 reveals robust diurnal oscillation of central metabolic processes. Proc. Natl. Acad. Sci. USA 105:6156–61 [Google Scholar]
  104. Hosokawa N, Hatakeyama TS, Kojima T, Kikuchi Y, Ito H, Iwasaki H. 102.  2011. Circadian transcriptional regulation by the posttranslational oscillator without de novo clock gene expression in Synechococcus. Proc. Natl. Acad. Sci. USA 108:15396–401 [Google Scholar]
  105. Yen U-C, Huang T-C, Yen T-C. 103.  2004. Observation of the circadian photosynthetic rhythm cyanobacteria with a dissolved-oxygen meter. Plant Sci. 166:949–52 [Google Scholar]
  106. Toepel J, Welsh E, Summerfield TC, Pakrasi HB, Sherman LA. 104.  2008. Differential transcriptional analysis of the cyanobacterium Cyanothece sp. strain ATCC 51142 during light-dark and continuous-light growth. J. Bacteriol. 190:3904–13 [Google Scholar]
  107. Schneegurt MA, Sherman DM, Nayar S, Sherman LA. 105.  1994. Oscillating behavior of carbohydrate granule formation and dinitrogen fixation in the cyanobacterium Cyanothece sp. strain ATCC 51142. J. Bacteriol. 176:1586–97 [Google Scholar]
  108. Sherman LA, Min H, Toepel J, Pakrasi HB. 106.  2010. Better living through Cyanothece—unicellular diazotrophic cyanobacteria with highly versatile metabolic systems. Adv. Exp. Med. Biol. 675:275–90 [Google Scholar]
  109. Červený J, Sinetova MA, Valledor L, Sherman LA, Nedbal L. 107.  2013. Ultradian metabolic rhythm in the diazotrophic cyanobacterium Cyanothece sp. ATCC 51142. Proc. Natl. Acad. Sci. USA 110:13210–15 [Google Scholar]
  110. Zhang S, Bryant DA. 108.  2011. The tricarboxylic acid cycle in cyanobacteria. Science 334:1551–53 [Google Scholar]
  111. Yang C, Hua Q, Shimizu K. 109.  2002. Metabolic flux analysis in Synechocystis using isotope distribution from 13C-labeled glucose. Metab. Eng. 4:202–16 [Google Scholar]
  112. Young JD, Shastri AA, Stephanopoulos G, Morgan JA. 110.  2011. Mapping photoautotrophic metabolism with isotopically nonstationary 13C flux analysis. Metab. Eng. 13:656–65 [Google Scholar]
  113. O'Neill JS, Reddy AB. 111.  2011. Circadian clocks in human red blood cells. Nature 469:498–503 [Google Scholar]
  114. O'Neill JS, van Ooijen G, Dixon LE, Troein C, Corellou F. 112.  et al. 2011. Circadian rhythms persist without transcription in a eukaryote. Nature 469:554–58 [Google Scholar]
  115. Edgar RS, Green EW, Zhao Y, van Ooijen G, Olmedo M. 113.  et al. 2012. Peroxiredoxins are conserved markers of circadian rhythms. Nature 485:459–64 [Google Scholar]
  116. Cheng P, He Q, He Q, Wang L, Liu Y. 114.  2005. Regulation of the Neurospora circadian clock by an RNA helicase. Genes Dev. 19:234–41 [Google Scholar]
  117. Rust MJ, Golden SS, O'Shea EK. 115.  2011. Light-driven changes in energy metabolism directly entrain the cyanobacterial circadian oscillator. Science 331:220–23 [Google Scholar]
  118. Doolittle WF. 116.  1979. The cyanobacterial genome, its expression, and the control of that expression. Adv. Microb. Physiol. 20:1–102 [Google Scholar]
  119. Xu Y, Mori T, Johnson CH. 117.  2000. Circadian clock-protein expression in cyanobacteria: rhythms and phase-setting. EMBO J. 19:3349–57 [Google Scholar]
  120. Johnson CH, Elliott JA, Foster RG. 118.  2003. Entrainment of circadian programs. Chronobiol. Int. 20:741–74 [Google Scholar]
  121. Yoshida T, Murayama Y, Ito H, Kageyama H, Kondo T. 119.  2009. Nonparametric entrainment of the in vitro circadian phosphorylation rhythm of cyanobacterial KaiC by temperature cycle. Proc. Natl. Acad. Sci. USA 106:1648–53 [Google Scholar]
  122. Boer VM, Crutchfield CA, Bradley PH, Botstein D, Rabinowitz JD. 120.  2010. Growth-limiting intracellular metabolites in yeast growing under diverse nutrient limitations. Mol. Biol. Cell. 21:198–211 [Google Scholar]
  123. Weart RB, Lee AH, Chien AC, Haeusser DP, Hill NS, Levin PA. 121.  2007. A metabolic sensor governing cell size in bacteria. Cell 130:335–47 [Google Scholar]
  124. Brinkmann K.122.  1971. Metabolic control of temperature compensation in the circadian rhythm of Euglena gracilis. Biochronometry M Menaker 567–93 Washington, DC: Natl. Acad. Sci. [Google Scholar]
  125. Sancar G, Sancar C, Brunner M. 123.  2012. Metabolic compensation of the Neurospora clock by a glucose-dependent feedback of the circadian repressor CSP1 on the core oscillator. Genes Dev. 26:2435–42 [Google Scholar]
  126. Xu Y, Ma P, Shah P, Rokas A, Liu Y, Johnson CH. 124.  2013. Non-optimal codon usage is a mechanism to achieve circadian clock conditionality. Nature 495:116–20 [Google Scholar]
  127. Liu Y, Merrow M, Loros JJ, Dunlap JC. 125.  1998. How temperature changes reset a circadian oscillator. Science 281:825–29 [Google Scholar]
  128. Morf J, Schibler U. 126.  2013. Body temperature cycles: gatekeepers of circadian clocks. Cell Cycle 12:539–40 [Google Scholar]
  129. Nagoshi E, Saini C, Bauer C, Laroche T, Naef F, Schibler U. 127.  2004. Circadian gene expression in individual fibroblasts: Cell-autonomous and self-sustained oscillators pass time to daughter cells. Cell 119:693–705 [Google Scholar]
  130. Yeom M, Pendergast JS, Ohmiya Y, Yamazaki S. 128.  2010. Circadian-independent cell mitosis in immortalized fibroblasts. Proc. Natl. Acad. Sci. USA 107:9665–70 [Google Scholar]
  131. Wood TL, Bridwell-Rabb J, Kim YI, Gao T, Chang YG. 129.  et al. 2010. The KaiA protein of the cyanobacterial circadian oscillator is modulated by a redox-active cofactor. Proc. Natl. Acad. Sci. USA 107:5804–9 [Google Scholar]
  132. Pattanayek R, Sidiqi SK, Egli M. 130.  2012. Crystal structure of the redox-active cofactor dibromothymoquinone bound to circadian clock protein KaiA and structural basis for dibromothymoquinone's ability to prevent stimulation of KaiC phosphorylation by KaiA. Biochemistry 51:8050–52 [Google Scholar]
  133. Kim YI, Vinyard DJ, Ananyev GM, Dismukes GC, Golden SS. 131.  2012. Oxidized quinones signal onset of darkness directly to the cyanobacterial circadian oscillator. Proc. Natl. Acad. Sci. USA 109:17765–69 [Google Scholar]
  134. Nakajima M, Ito H, Kondo T. 132.  2010. In vitro regulation of circadian phosphorylation rhythm of cyanobacterial clock protein KaiC by KaiA and KaiB. FEBS Lett. 584:898–902 [Google Scholar]
  135. Hosokawa N, Kushige H, Iwasaki H. 133.  2013. Attenuation of the posttranslational oscillator via transcription-translation feedback enhances circadian phase shifts in Synechococcus. Proc. Natl. Acad. Sci. USA 110:14486–91 [Google Scholar]
  136. Ducat DC, Way JC, Silver PA. 134.  2011. Engineering cyanobacteria to generate high-value products. Trends Biotechnol. 29:95–103 [Google Scholar]
  137. Rosgaard L, de Porcellinis AJ, Jacobsen JH, Frigaard NU, Sakuragi Y. 135.  2012. Bioengineering of carbon fixation, biofuels, and biochemicals in cyanobacteria and plants. J. Biotechnol. 162:134–47 [Google Scholar]
  138. Wang B, Wang J, Zhang W, Meldrum DR. 136.  2012. Application of synthetic biology in cyanobacteria and algae. Front. Microbiol. 3:344 [Google Scholar]
  139. Sheehan J.137.  2009. Engineering direct conversion of CO2 to biofuel. Nat. Biotechnol. 27:1128–29 [Google Scholar]
  140. Atsumi S, Higashide W, Liao JC. 138.  2009. Direct photosynthetic recycling of carbon dioxide to isobutyraldehyde. Nat. Biotechnol. 27:1177–80 [Google Scholar]
  141. Ducat DC, Avelar-Rivas JA, Way JC, Silver PA. 139.  2012. Rerouting carbon flux to enhance photosynthetic productivity. Appl. Environ. Microbiol. 78:2660–68 [Google Scholar]
  142. Varman AM, Xiao Y, Pakrasi HB, Tang YJ. 140.  2013. Metabolic engineering of Synechocystis sp. strain PCC 6803 for isobutanol production. Appl. Environ. Microbiol. 79:908–14 [Google Scholar]
  143. Iwasaki H, Nishiwaki T, Kitayama Y, Nakajima M, Kondo T. 141.  2002. KaiA-stimulated KaiC phosphorylation in circadian timing loops in cyanobacteria. Proc. Natl. Acad. Sci. USA 99:15788–93 [Google Scholar]
  144. Xu Y, Mori T, Johnson CH. 142.  2003. The cyanobacterial circadian clockwork: roles of KaiA, KaiB, and the kaiBC promoter in KaiC expression, phosphorylation, and degradation. EMBO J. 22:2117–26 [Google Scholar]
  145. Nikaido SS, Johnson CH. 143.  2000. Daily and circadian variation in survival from ultraviolet radiation in Chlamydomonas reinhardtii. Photochem. Photobiol. 71:758–65 [Google Scholar]
  146. Robertson JB, Davis CR, Johnson CH. 144.  2013. Visible light alters yeast metabolic rhythms by inhibiting respiration. Proc. Natl. Acad. Sci. USA 110:21130–35 [Google Scholar]
  147. Dvornyk V.145.  2009. The circadian clock gear in cyanobacteria: assembled by evolution. See Ref. 23 241–58
  148. Leipe DD, Aravind L, Grishin NV, Koonin EV. 146.  2000. The bacterial replicative helicase DnaB evolved from a RecA duplication. Genome Res. 10:5–16 [Google Scholar]
  149. Padmanabhan K, Robles MS, Westerling T, Weitz CJ. 147.  2012. Feedback regulation of transcriptional termination by the mammalian circadian clock PERIOD complex. Science 337:599–602 [Google Scholar]
  150. Dvornyk V, Vinogradova O, Nevo E. 148.  2003. Origin and evolution of circadian clock genes in prokaryotes. Proc. Natl. Acad. Sci. USA 100:2495–500 [Google Scholar]
  151. Partensky F, Hess WR, Vaulot D. 149.  1999. Prochlorococcus, a marine photosynthetic prokaryote of global significance. Microbiol. Mol. Biol. Rev. 63:106–27 [Google Scholar]
  152. Holtzendorff J, Partensky F, Mella D, Lennon JF, Hess WR, Garczarek L. 150.  2008. Genome streamlining results in loss of robustness of the circadian clock in the marine cyanobacterium Prochlorococcus marinus PC 9511. J. Biol. Rhythms 23:187–99 [Google Scholar]
  153. Axmann IM, Dühring U, Seeliger L, Arnold A, Vanselow JT. 151.  et al. 2009. Biochemical evidence for a timing mechanism in Prochlorococcus. J. Bacteriol. 191:5342–47 [Google Scholar]
  154. Mullineaux CW, Stanewsky R. 152.  2009. The rolex and the hourglass: a simplified circadian clock in Prochlorococcus?. J. Bacteriol. 191:5333–35 [Google Scholar]
  155. Kageyama H, Nishiwaki T, Nakajima M, Iwasaki H, Oyama T, Kondo T. 153.  2006. Cyanobacterial circadian pacemaker: Kai protein complex dynamics in the KaiC phosphorylation cycle in vitro. Mol. Cell 23:161–71 [Google Scholar]
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