Signatures of energy dissipation in bacterial chemotaxis signaling pathways

Chemotaxis signaling pathways in Escherichia coli are driven out of equilibrium by ATP hydrolysis, which enables the phosphorylation of regulator proteins that carry signals from the chemoreceptors to the motors. We show that recent experimental measurements of kinase activity exhibit signatures of this underlying energy dissipation. First, changes in receptor methylation shift kinase response curves over a disproportionately large range of ligand concentration, two orders of magnitude larger than the corresponding shift in ligand binding curves. Second, cells can spontaneously switch between active and inactive states, but the switch to inactivity takes longer, signifying time-reversal symmetry-breaking. In each case, we show that these measurements are inconsistent with equilibrium mechanisms. We develop non-equilibrium allosteric and lattice models that explain the microscopic origins of these behaviors and allow us to explore how they emerge as the system is tuned out of equilibrium. Our results indicate that strong dissipative driving plays a key role in enhancing signal fidelity and the range of adaptation in E. coli.