Abstract
Circadian clocks generate reliable ~24-h rhythms despite being based on stochastic biochemical reactions. The circadian clock in Synechococcus elongatus uses a post-translational oscillator that cycles deterministically in a test tube. Because the volume of a single bacterial cell is much smaller than a macroscopic reaction, we asked how clocks in single cells function reliably. Here, we show that S. elongatus cells must express many thousands of copies of Kai proteins to effectively suppress timing errors. Stochastic modeling shows that this requirement stems from noise amplification in the post-translational feedback loop that sustains oscillations. The much smaller cyanobacterium Prochlorococcus expresses only hundreds of Kai protein copies and has a simpler, hourglass-like Kai system. We show that this timer strategy can outperform a free-running clock if internal noise is significant. This conclusion has implications for clock evolution and synthetic oscillator design, and it suggests hourglass-like behavior may be widespread in microbes.
Highlights
Circadian clocks generate reliable ~24-h rhythms despite being based on stochastic biochemical reactions
We engineered a strain of the model cyanobacterium Synechococcus elongatus PCC 7942 where the copy numbers of the Kai proteins are under experimental control
We found that P. marinus has ~700 copies of KaiC per cell (Fig. 4a and Supplementary Fig. 8), which is in the regime where the S. elongatus oscillator becomes extremely errorprone
Summary
Circadian clocks generate reliable ~24-h rhythms despite being based on stochastic biochemical reactions. The much smaller cyanobacterium Prochlorococcus expresses only hundreds of Kai protein copies and has a simpler, hourglass-like Kai system We show that this timer strategy can outperform a free-running clock if internal noise is significant. 1234567890():,; Circadian clocks are biochemical oscillators that enable organisms to anticipate the day-night cycle Their utility depends on the ability to make accurate predictions about the future[1,2] and requires precise, deterministic timing. Natural circadian clocks can be extremely precise[6,7,8] It is generally not known how biological clocks create deterministic rhythms from their stochastic components, or how the architecture of clock networks responds to the constraints of molecular noise. Our analysis supports the hypothesis that internal noise tends to disfavor free-running behavior in the Kai system, suggesting that circadian clocks are disadvantageous under some conditions
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