Singly Flagellated Pseudomonas aeruginosa Chemotaxes Efficiently by Unbiased Motor Regulation

Pseudomonas aeruginosais an opportunistic human pathogen that has long been known to chemotax. More recently, it has been established that chemotaxis is an important factor in the ability ofP. aeruginosato make biofilms. Genes that allowP. aeruginosato chemotax are homologous with genes in the paradigmatic model organism for chemotaxis,Escherichia coli However,P. aeruginosais singly flagellated andE. colihas multiple flagella. Therefore, the regulation of counterclockwise/clockwise flagellar motor bias that allowsE. colito efficiently chemotax by runs and tumbles would lead to inefficient chemotaxis byP. aeruginosa, as half of a randomly oriented population would respond to a chemoattractant gradient in the wrong sense. HowP. aeruginosaregulates flagellar rotation to achieve chemotaxis is not known. Here, we analyze the swimming trajectories of single cells in microfluidic channels and the rotations of cells tethered by their flagella to the surface of a variable-environment flow cell. We show thatP. aeruginosachemotaxes by symmetrically increasing the durations of both counterclockwise and clockwise flagellar rotations when swimming up the chemoattractant gradient and symmetrically decreasing rotation durations when swimming down the chemoattractant gradient. Unlike the case forE. coli, the counterclockwise/clockwise bias stays constant forP. aeruginosa We describeP. aeruginosa's chemotaxis using an analytical model for symmetric motor regulation. We use this model to do simulations that show that, givenP. aeruginosa's physiological constraints on motility, its distinct, symmetric regulation of motor switching optimizes chemotaxis.

Chemotaxis has long been known to strongly affect biofilm formation by the opportunistic human pathogenP. aeruginosa, whose essential chemotaxis genes have homologues inE. coli, which achieves chemotaxis by biasing the relative probability of counterclockwise and clockwise flagellar rotation. However, the physiological difference between multiflagellatedE. coliand singly flagellatedP. aeruginosaimplies that biased motor regulation should preventP. aeruginosapopulations from chemotaxing efficiently. Here, we used experiments, analytical modeling, and simulations to demonstrate thatP. aeruginosauses unbiased, symmetric regulation of the flagellar motor to maximize its chemotaxis efficiency. This mode of chemotaxis was not previously known and demonstrates a new variant of a paradigmatic signaling system in an important human pathogen.