Time-reversal symmetry breaking in the chemosensory array reveals a general mechanism for dissipation-enhanced cooperative sensing

David Hathcock, Qiwei Yu and Yuhai Tu ()
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David Hathcock: IBM T. J. Watson Research Center
Qiwei Yu: IBM T. J. Watson Research Center
Yuhai Tu: IBM T. J. Watson Research Center

Nature Communications, 2024, vol. 15, issue 1, 1-10

Abstract: Abstract The Escherichia coli chemoreceptors form an extensive array that achieves cooperative and adaptive sensing of extracellular signals. The receptors control the activity of histidine kinase CheA, which drives a nonequilibrium phosphorylation-dephosphorylation reaction cycle for response regulator CheY. Cooperativity and dissipation are both important aspects of chemotaxis signaling, yet their consequences have only been studied separately. Recent single-cell FRET measurements revealed that kinase activity of the array spontaneously switches between active and inactive states, with asymmetric switching times that signify time-reversal symmetry breaking in the underlying dynamics. Here, we present a nonequilibrium lattice model of the chemosensory array, which demonstrates that the observed asymmetric switching dynamics can only be explained by an interplay between the dissipative reactions within individual core units and the cooperative coupling between neighboring units. Microscopically, the switching time asymmetry originates from irreversible transition paths. The model shows that strong dissipation enables sensitive and rapid signaling response by relieving the speed-sensitivity trade-off, which can be tested by future single-cell experiments. Overall, our model provides a general framework for studying biological complexes composed of coupled subunits that are individually driven by dissipative cycles and the rich nonequilibrium physics within.

Date: 2024
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DOI: 10.1038/s41467-024-52799-0

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