Cyanobacterial clock, a stable phase oscillator with negligible intercellular coupling

Amdaoud, M.; Vallade, M.; Weiss-Schaber, Christoph; Mihalcescu, I.

doi:10.1073/pnas.0609315104

Cited by 52 publications

(57 citation statements)

References 22 publications

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“…These data, coupled with mathematical modeling, suggest that the TTFL is required for the generation of robust circadian oscillations specifically under conditions of rapid growth (61,62). In contrast to what is observed in eukaryotic systems, the phasing of the cyanobacterial clock is inherited from mother cell to daughter cell with negligible intercellular coupling (63,64). Combined, these results would suggest that the fidelity of cellular phase is compromised in individual cells without the TTFL.…”

Section: Regulation Of the Kai-based Oscillatormentioning

confidence: 82%

Circadian Rhythms in Cyanobacteria

Cohen

Golden

2015

Microbiol Mol Biol Rev

240

224

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SUMMARYLife on earth is subject to daily and predictable fluctuations in light intensity, temperature, and humidity created by rotation of the earth. Circadian rhythms, generated by a circadian clock, control temporal programs of cellular physiology to facilitate adaptation to daily environmental changes. Circadian rhythms are nearly ubiquitous and are found in both prokaryotic and eukaryotic organisms. Here we introduce the molecular mechanism of the circadian clock in the model cyanobacteriumSynechococcus elongatusPCC 7942. We review the current understanding of the cyanobacterial clock, emphasizing recent work that has generated a more comprehensive understanding of how the circadian oscillator becomes synchronized with the external environment and how information from the oscillator is transmitted to generate rhythms of biological activity. These results have changed how we think about the clock, shifting away from a linear model to one in which the clock is viewed as an interactive network of multifunctional components that are integrated into the context of the cell in order to pace and reset the oscillator. We conclude with a discussion of how this basic timekeeping mechanism differs in other cyanobacterial species and how information gleaned from work in cyanobacteria can be translated to understanding rhythmic phenomena in other prokaryotic systems.

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Section: Regulation Of the Kai-based Oscillatormentioning

confidence: 82%

Circadian Rhythms in Cyanobacteria

Cohen

Golden

2015

Microbiol Mol Biol Rev

240

224

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“…However, we cannot exclude the possibility that the rhythmic transcription is indirectly induced in the heterocyst by time-dependent intercellular signals from oscillators in neighboring vegetative cells. Single-cell imaging analysis in Synechococcus has demonstrated that the synchronization among cells is negligible, and instead, the intracellular timing mechanism is extremely robust and precise (39,40). In contrast, it has been suggested that in multicellular eukaryotes, cell-to-cell communication is important in synchronizing each clock cell into a robust oscillatory system at the tissue or organ level (41,42).…”

Section: Fig 2 Genome-wide Circadian Transcription Profiles Under Ll mentioning

confidence: 99%

Genome-Wide and Heterocyst-Specific Circadian Gene Expression in the Filamentous Cyanobacterium Anabaena sp. Strain PCC 7120

Kushige

Kugenuma

Matsuoka

et al. 2013

Journal of Bacteriology

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cThe filamentous, heterocystous cyanobacterium Anabaena sp. strain PCC 7120 is one of the simplest multicellular organisms that show both morphological pattern formation with cell differentiation (heterocyst formation) and circadian rhythms. Therefore, it potentially provides an excellent model in which to analyze the relationship between circadian functions and multicellularity. However, detailed cyanobacterial circadian regulation has been intensively analyzed only in the unicellular species Synechococcus elongatus. In contrast to the highest-amplitude cycle in Synechococcus, we found that none of the kai genes in Anabaena showed high-amplitude expression rhythms. Nevertheless, ϳ80 clock-controlled genes were identified. We constructed luciferase reporter strains to monitor the expression of some high-amplitude genes. The bioluminescence rhythms satisfied the three criteria for circadian oscillations and were nullified by genetic disruption of the kai gene cluster. In heterocysts, in which photosystem II is turned off, the metabolic and redox states are different from those in vegetative cells, although these conditions are thought to be important for circadian entrainment and timekeeping processes. Here, we demonstrate that circadian regulation is active in heterocysts, as shown by the finding that heterocyst-specific genes, such as all1427 and hesAB, are expressed in a robust circadian fashion exclusively without combined nitrogen.

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“…In multicellular organisms, the robustness might be explained by intercellular interactions (3,4), but it is now known that even unicellular organisms can have very stable circadian rhythms. The clock of the cyanobacterium Synechococcus elongatus, for example, has a correlation time of several months (5), even though the clocks of the different cells in a population hardly interact with one another (5,6). How circadian clocks can be so stable even at the single cell level is not understood.…”

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confidence: 99%

Robust circadian clocks from coupled protein-modification and transcription–translation cycles

Zwicker

Lubensky

Wolde

2010

Proc. Natl. Acad. Sci. U.S.A.

104

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The cyanobacterium Synechococcus elongatus uses both a protein phosphorylation cycle and a transcription-translation cycle to generate circadian rhythms that are highly robust against biochemical noise. We use stochastic simulations to analyze how these cycles interact to generate stable rhythms in growing, dividing cells. We find that a protein phosphorylation cycle by itself is robust when protein turnover is low. For high decay or dilution rates (and compensating synthesis rates), however, the phosphorylation-based oscillator loses its integrity. Circadian rhythms thus cannot be generated with a phosphorylation cycle alone when the growth rate, and consequently the rate of protein dilution, is high enough; in practice, a purely posttranslational clock ceases to function well when the cell doubling time drops below the 24-h clock period. At higher growth rates, a transcription-translation cycle becomes essential for generating robust circadian rhythms. Interestingly, although a transcription-translation cycle is necessary to sustain a phosphorylation cycle at high growth rates, a phosphorylation cycle can dramatically enhance the robustness of a transcriptiontranslation cycle at lower protein decay or dilution rates. In fact, the full oscillator built from these two tightly intertwined cycles far outperforms not just each of its two components individually, but also a hypothetical system in which the two parts are coupled as in textbook models of coupled phase oscillators. Our analysis thus predicts that both cycles are required to generate robust circadian rhythms over the full range of growth conditions.

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Cyanobacterial clock, a stable phase oscillator with negligible intercellular coupling

Cited by 52 publications

References 22 publications

Circadian Rhythms in Cyanobacteria

Circadian Rhythms in Cyanobacteria

Genome-Wide and Heterocyst-Specific Circadian Gene Expression in the Filamentous Cyanobacterium Anabaena sp. Strain PCC 7120

Robust circadian clocks from coupled protein-modification and transcription–translation cycles

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