Interdependence of behavioural variability and response to small stimuli in bacteria

The chemotaxis signalling network in Escherichia coli that controls the locomotion of bacteria is a classic model system for signal transduction (1,2). This pathway modulates the behaviour of flagellar motors to propel bacteria towards sources of chemical attractants. Although this system relaxes to a steady state in response to environmental changes, the signalling events within the chemotaxis network are noisy and cause large temporal variations of the motor behaviour even in the absence of stimulus (3). That the same signalling network governs both behavioural variability and cellular response raises the question of whether these two traits are independent. Here, we experimentally establish a fluctuation-response relationship in the chemotaxis system of living bacteria. Using this relationship, we demonstrate the possibility of inferring the cellular response from the behavioural variability measured before stimulus. In monitoring the pre- and post-stimulus switching behaviour of individual bacterial motors, we found that variability scales linearly with the response time for different functioning states of the cell. This study highlights that the fundamental relationship between fluctuation and response is not constrained to physical systems at thermodynamic equilibrium (4) but is extensible to living cells (5). Such a relationship not only implies that behavioural variability and cellular response can be coupled traits, but it also provides a general framework within which we can examine how the selection of a network design shapes this interdependence.
It is standard procedure to characterize the stochastic dynamics of physical systems in thermodynamic equilibrium by measuring spontaneous fluctuations and responses to small external perturbations. Because these two distinct measurements [...]