A multi-state dynamic process confers mechano-adaptation to a biological nanomachine

Wadhwa N, Sassi AS, Berg HC, Tu Y, Nat Comm (2022).

Abstract

Adaptation is a defining feature of living systems. The bacterial flagellar motor adapts to changes in external mechanical environment by adding or removing torque-generating stator units. However, the molecular mechanism for mechanosensitive motor remodeling remains unclear. Here, we induced stator disassembly using electrorotation, followed by the time-dependent assembly of the individual stator units into the motor. From these experiments, we extracted detailed statistics of the dwell times underlying the stochastic dynamics of stator unit binding and unbinding. The dwell time distribution contains multiple timescales, indicating the existence of multiple stator unit states. Based on these results, we propose a minimal model with four stator unit states – two bound states with different unbinding rates, a diffusive unbound state, and a recently described transiently detached state. Our minimal model quantitatively explains multiple features of the experimental data and allows us to determine the transition rates between all four states. Our experiments and modeling point towards an emergent picture for mechano-adaptive remodeling of the bacterial flagellar motor in which torque generated by bound stator units controls their effective unbinding rate by modulating the transition between the two bound states. Furthermore, the binding rate of stator units with the motor has a non-monotonic dependence on the number of bound units, likely due to two counter-acting effects of motor’s rotation on the binding process.