Spontaneous switching in a protein signalling array reveals near-critical cooperativity

Cooperative interactions within large protein assemblies are crucial for cellular information processing. However, direct observations of cooperative transitions have been limited to compact molecular assemblies. Here, we report in vivo FRET measurements of spontaneous discrete-level transitions in the activity of an entire Escherichia coli chemosensory array - an extensive membrane-associated assembly comprising thousands of molecules. Finite-size scaling analysis of the temporal statistics by a two-dimensional conformational spread model revealed nearest-neighbor coupling strengths within 3% of the Ising phase transition, indicating that chemosensory arrays are poised at criticality. We also show how E. coli exploits both static and dynamic disorder, arising from chemoreceptor mixing and sensory adaptation, respectively, to temper the near-critical dynamics. This tempering eliminates detrimental slowing of the response while retaining substantial signal gain and an ability to modulate physiologically relevant signal noise. These results identify near-critical cooperativity as a design principle for balancing the inherent tradeoff between response amplitude and response speed in higher-order signaling assemblies.