State-space renormalization group theory of nonequilibrium reaction networks: Exact solutions for hypercubic lattices in arbitrary dimensions

Yu, Qiwei; Tu, Yuhai

doi:10.1103/physreve.105.044140

Cited by 6 publications

(6 citation statements)

References 24 publications

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“…If the true

is larger than 10, a much larger reduction in amplitude will occur for the same decrease in the [ATP]/[ADP] ratio (e.g., 51% for

). Furthermore, since our model is coarse-grained (for example, it ignores intermediate steps in the phosphotransfer between CheA and CheY), the predicted dissipation rate is smaller than that of the real system ( 35 , 36 ). Therefore, the real kinase response may be more susceptible to changes in ATP concentration than the model predicts.…”

Section: Resultsmentioning

confidence: 99%

A nonequilibrium allosteric model for receptor-kinase complexes: The role of energy dissipation in chemotaxis signaling

Hathcock,

Yu,

Mello

et al. 2023

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

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The Escherichia coli chemotaxis signaling pathway has served as a model system for the adaptive sensing of environmental signals by large protein complexes. The chemoreceptors control the kinase activity of CheA in response to the extracellular ligand concentration and adapt across a wide concentration range by undergoing methylation and demethylation. Methylation shifts the kinase response curve by orders of magnitude in ligand concentration while incurring a much smaller change in the ligand binding curve. Here, we show that the disproportionate shift in binding and kinase response is inconsistent with equilibrium allosteric models. To resolve this inconsistency, we present a nonequilibrium allosteric model that explicitly includes the dissipative reaction cycles driven by adenosine triphosphate (ATP) hydrolysis. The model successfully explains all existing joint measurements of ligand binding, receptor conformation, and kinase activity for both aspartate and serine receptors. Our results suggest that the receptor complex acts as an enzyme: Receptor methylation modulates the ON-state kinetics of the kinase (e.g., phosphorylation rate), while ligand binding controls the equilibrium balance between kinase ON/OFF states. Furthermore, sufficient energy dissipation is responsible for maintaining and enhancing the sensitivity range and amplitude of the kinase response. We demonstrate that the nonequilibrium allosteric model is broadly applicable to other sensor-kinase systems by successfully fitting previously unexplained data from the DosP bacterial oxygen-sensing system. Overall, this work provides a nonequilibrium physics perspective on cooperative sensing by large protein complexes and opens up research directions for understanding their microscopic mechanisms through simultaneous measurements and modeling of ligand binding and downstream responses.

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“…If the true

is larger than 10, a much larger reduction in amplitude will occur for the same decrease in the [ATP]/[ADP] ratio (e.g., 51% for

Section: Resultsmentioning

confidence: 99%

A nonequilibrium allosteric model for receptor-kinase complexes: The role of energy dissipation in chemotaxis signaling

Hathcock,

Yu,

Mello

et al. 2023

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

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show abstract

“…If the true G z is larger than 10, a much larger reduction in amplitude will occur for the same decrease in the [ATP]/[ADP] ratio (e.g., 51% for G z = 13). Furthermore, since our model is coarse-grained (for example, it ignores intermediate steps in the phosphotransfer between CheA and CheY), the predicted dissipation rate is smaller than that of the real system [35,36]. Therefore, the real kinase response may be more susceptible to changes in ATP concentration than the model predicts.…”

Section: Further Confirmation Of the Nonequilibrium Model: Receptor C...mentioning

confidence: 99%

Resolving the binding-kinase discrepancy in bacterial chemotaxis: A nonequilibrium allosteric model and the role of energy dissipation

Hathcock,

Yu,

Mello

et al. 2023

Preprint

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The Escherichia coli chemotaxis signaling pathway has served as a model system for studying the adaptive sensing of environmental signals by large protein complexes. The chemoreceptors control the kinase activity of CheA in response to the extracellular ligand concentration and adapt across a wide concentration range by undergoing methylation and demethylation. Methylation shifts the kinase response curve by orders of magnitude in ligand concentration while incurring a much smaller change in the ligand binding curve. Here, we show that this asymmetric shift in binding and kinase response is inconsistent with equilibrium allosteric models regardless of parameter choices. To resolve this inconsistency, we present a nonequilibrium allosteric model that explicitly includes the dissipative reaction cycles driven by ATP hydrolysis. The model successfully explains all existing measurements for both aspartate and serine receptors. Our results suggest that while ligand binding controls the equilibrium balance between the ON and OFF states of the kinase, receptor methylation modulates the kinetic properties (e.g., the phosphorylation rate) of the ON state. Furthermore, sufficient energy dissipation is necessary for maintaining and enhancing the sensitivity range and amplitude of the kinase response. We demonstrate that the nonequilibrium allosteric model is broadly applicable to other sensor-kinase systems by successfully fitting previously unexplained data from the DosP bacterial oxygen-sensing system. Overall, this work provides a new perspective on cooperative sensing by large protein complexes and opens up new research directions for understanding their microscopic mechanisms through simultaneous measurements and modeling of ligand binding and downstream responses.Significance: Adaptation in bacterial chemotaxis is carried out by receptor methylation, which shifts the kinase response curve by orders of magnitude in ligand concentration. However, the receptor-ligand binding curve is only shifted slightly by receptor methylation. We show that this discrepancy in shifts rules out the previously proposed equilibrium allosteric models for the system. We develop a nonequilibrium model that explicitly includes the phosphorylation-dephosphorylation cycle driven by ATP hydrolysis. Our model agrees with all the existing experiments and shows that while ligand binding affects the ON/OFF switching of the kinase activity, receptor methylation affects the ON-state kinetics. Our study also shows that a minimum energy dissipation is needed to maintain the observed sensitivity range and amplitude of the kinase response.

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“…Namely, it does not give the (physical) heat dissipation rate, and an alternative term "information EPR" has been proposed to differentiate it from the microscopic EPR, which has unambiguous thermodynamic interpretation [25][26][27]. The reason behind this discrepancy is that coarse-graining drastically decreases the dissipation rate [28][29][30], which means that macroscopic theories tend to dramatically underestimate the energy dissipation. Therefore, it is fundamentally important to elu-cidate the energy cost of flocking using a microscopic model, which gives the "true" heat dissipation, despite existing work using hydrodynamic approaches [31,32].…”

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confidence: 99%

Energy Cost for Flocking of Active Spins: The Cusped Dissipation Maximum at the Flocking Transition

Tu²

2022

Phys. Rev. Lett.

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We study the energy cost of flocking in the active Ising model (AIM) and show that besides the energy cost for self-propelled motion, an additional energy dissipation is required to align spins in order to maintain the flocking order. We find that this additional alignment dissipation reaches its maximum at the flocking transition point in the form of a cusp with a discontinuous first derivative with respect to the control parameter. To understand this singular behavior, we analytically solve the two-site and three-site AIM models and obtain the exact dependence of the alignment dissipation on the flocking order parameter and control parameter, which explains the cusped dissipation maximum at the flocking transition. Our results reveal a trade-off between the energy cost of the system and its performance measured by the flocking speed and sensitivity to external perturbations. This trade-off relationship provides a new perspective for understanding the dynamics of natural flocks and designing optimal artificial flocking systems.

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State-space renormalization group theory of nonequilibrium reaction networks: Exact solutions for hypercubic lattices in arbitrary dimensions

Cited by 6 publications

References 24 publications

A nonequilibrium allosteric model for receptor-kinase complexes: The role of energy dissipation in chemotaxis signaling

A nonequilibrium allosteric model for receptor-kinase complexes: The role of energy dissipation in chemotaxis signaling

Resolving the binding-kinase discrepancy in bacterial chemotaxis: A nonequilibrium allosteric model and the role of energy dissipation

Energy Cost for Flocking of Active Spins: The Cusped Dissipation Maximum at the Flocking Transition

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