title: Limits of feedback control in bacterial chemotaxis.
abstract: Inputs to signaling pathways can have complex statistics that depend on the environment and on the behavioral response to previous stimuli. Such behavioral feedback is particularly important in navigation. Successful navigation relies on proper coupling between sensors, which gather information during motion, and actuators, which control behavior. Because reorientation conditions future inputs, behavioral feedback can place sensors and actuators in an operational regime different from the resting state. How then can organisms maintain proper information transfer through the pathway while navigating diverse environments? In bacterial chemotaxis, robust performance is often attributed to the zero integral feedback control of the sensor, which guarantees that activity returns to resting state when the input remains constant. While this property provides sensitivity over a wide range of signal intensities, it remains unclear how other parameters such as adaptation rate and adapted activity affect chemotactic performance, especially when considering that the swimming behavior of the cell determines the input signal. We examine this issue using analytical models and simulations that incorporate recent experimental evidences about behavioral feedback and flagellar motor adaptation. By focusing on how sensory information carried by the response regulator is best utilized by the motor, we identify an operational regime that maximizes drift velocity along chemical concentration gradients for a wide range of environments and sensor adaptation rates. This optimal regime is outside the dynamic range of the motor response, but maximizes the contrast between run duration up and down gradients. In steep gradients, the feedback from chemotactic drift can push the system through a bifurcation. This creates a non-chemotactic state that traps cells unless the motor is allowed to adapt. Although motor adaptation helps, we find that as the strength of the feedback increases individual phenotypes cannot maintain the optimal operational regime in all environments, suggesting that diversity could be beneficial.
authors: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, United States of America.
authors: Yann S
authors: YS
authors: Dufour
authors: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, United States of America.
authors: Xiongfei
authors: X
authors: Fu
authors: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, United States of America.
authors: Luis
authors: L
authors: Hernandez-Nunez
authors: Department of Molecular, Cellular, and Developmental Biology, Yale University, New Haven, Connecticut, United States of America; Department of Physics, Yale University, New Haven, Connecticut, United States of America.
authors: Thierry
authors: T
authors: Emonet
mesh_terms: D001426:Bacterial Proteins; D002633:Chemotaxis / Q000502:physiology*; D019295:Computational Biology; D004926:Escherichia coli / Q000502:physiology*; D025461:Feedback, Physiological / Q000502:physiology*; D008565:Membrane Proteins; D000072236:Methyl-Accepting Chemotaxis Proteins; D008954:Models, Biological; D010641:Phenotype; D015398:Signal Transduction
chemical_list: D001426:Bacterial Proteins; D008565:Membrane Proteins; D000072236:Methyl-Accepting Chemotaxis Proteins