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The energy cost and optimal design for synchronization of coupled molecular oscillators.

ABSTRACT: A model of coupled molecular biochemical oscillators is proposed to study nonequilibrium thermodynamics of synchronization. We find that synchronization of nonequilibrium oscillators costs addition energy to drive the exchange reaction (chemical interaction) between individual oscillators. By solving the steady state of the many-body system analytically, we show that the system goes through a nonequilibrium phase transition driven by energy dissipation, and the critical energy dissipation depends on both the frequency and strength of the exchange reaction. Moreover, our study reveals the optimal design for achieving maximum synchronization with a fixed energy budget. We apply our general theory to the Kai system in Cyanobacteria circadian clock and predict a relationship between the KaiC ATPase activity and synchronization of the KaiC hexamers. The theoretical framework can be extended to study thermodynamics of collective behaviors in other extended nonequilibrium active systems.

SUBMITTER: Zhang D

PROVIDER: S-EPMC7363412 | biostudies-literature | 2020 Jan

REPOSITORIES: biostudies-literature

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The energy cost and optimal design for synchronization of coupled molecular oscillators.

Zhang Dongliang D Cao Yuansheng Y Ouyang Qi Q Tu Yuhai Y

Nature physics 20191111 1

A model of coupled molecular biochemical oscillators is proposed to study nonequilibrium thermodynamics of synchronization. We find that synchronization of nonequilibrium oscillators costs addition energy to drive the exchange reaction (chemical interaction) between individual oscillators. By solving the steady state of the many-body system analytically, we show that the system goes through a nonequilibrium phase transition driven by energy dissipation, and the critical energy dissipation depend ...[more]

PMID: 32670386

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Project description:BackgroundThe biochemical oscillator that controls periodic events during the Xenopus embryonic cell cycle is centered on the activity of CDKs, and the cell cycle is driven by a protein circuit that is centered on the cyclin-dependent protein kinase CDK1 and the anaphase-promoting complex (APC). Many studies have been conducted to confirm that the interactions in the cell cycle can produce oscillations and predict behaviors such as synchronization, but much less is known about how the various elaborations and collective behavior of the basic oscillators can affect the robustness of the system. Therefore, in this study, we investigate and model a multi-cell system of the Xenopus embryonic cell cycle oscillators that are coupled through a common complex protein, and then analyze their synchronization ability under four different external stimuli, including a constant input signal, a square-wave periodic signal, a sinusoidal signal and a noise signal.ResultsThrough bifurcation analysis and numerical simulations, we obtain synchronization intervals of the sensitive parameters in the individual oscillator and the coupling parameters in the coupled oscillators. Then, we analyze the effects of these parameters on the synchronization period and amplitude, and find interesting phenomena, e.g., there are two synchronization intervals with activation coefficient in the Hill function of the activated CDK1 that activates the Plk1, and different synchronization intervals have distinct influences on the synchronization period and amplitude. To quantify the speediness and robustness of the synchronization, we use two quantities, the synchronization time and the robustness index, to evaluate the synchronization ability. More interestingly, we find that the coupled system has an optimal signal strength that maximizes the synchronization index under different external stimuli. Simulation results also show that the ability and robustness of the synchronization for the square-wave periodic signal of cyclin synthesis is strongest in comparison to the other three different signals.ConclusionsThese results suggest that the reaction process in which the activated cyclin-CDK1 activates the Plk1 has a very important influence on the synchronization ability of the coupled system, and the square-wave periodic signal of cyclin synthesis is more conducive to the synchronization and robustness of the coupled cell-cycle oscillators. Our study provides insight into the internal mechanisms of the cell cycle system and helps to generate hypotheses for further research.

Dataset Information

The energy cost and optimal design for synchronization of coupled molecular oscillators.

Publications

The energy cost and optimal design for synchronization of coupled molecular oscillators.

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