Abstract
ABSTRACTPseudomonas aeruginosa is 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 of P. aeruginosa to make biofilms. Genes that allow P. aeruginosa to chemotax are homologous with genes in the paradigmatic model organism for chemotaxis, Escherichia coli. However, P. aeruginosa is singly flagellated and E. coli has multiple flagella. Therefore, the regulation of counterclockwise/clockwise flagellar motor bias that allows E. coli to efficiently chemotax by runs and tumbles would lead to inefficient chemotaxis by P. aeruginosa, as half of a randomly oriented population would respond to a chemoattractant gradient in the wrong sense. How P. aeruginosa regulates 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 that P. aeruginosa chemotaxes 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 for E. coli, the counterclockwise/clockwise bias stays constant for P. aeruginosa. We describe P. aeruginosa’s chemotaxis using an analytical model for symmetric motor regulation. We use this model to do simulations that show that, given P. aeruginosa’s physiological constraints on motility, its distinct, symmetric regulation of motor switching optimizes chemotaxis.
Highlights
Pseudomonas aeruginosa is an opportunistic human pathogen that has long been known to chemotax
The regulation of counterclockwise/ clockwise flagellar motor bias that allows E. coli to efficiently chemotax by runs and tumbles would lead to inefficient chemotaxis by P. aeruginosa, as half of a randomly oriented population would respond to a chemoattractant gradient in the wrong sense
We show that P. aeruginosa chemotaxes 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
Summary
P. aeruginosa swims in time-reversible, back-and-forth trajectories with little change in direction To assess the directional modulations available to P. aeruginosa, we characterized the trajectories of wild-type P. aeruginosa strain PAO1 swimming in attractant-free microfluidic channels (see Materials and Methods; see Fig. S1A in the supplemental material). The distribution of consecutively measured transit times was symmetric about zero (Fig. 2B), indicating that, on average, cells spent equal amounts of time swimming up the channel and down the channel These findings demonstrate that P. aeruginosa’s swimming motility has no intrinsic bias in direction in the absence of a chemoattractant gradient. In the absence of chemoattractant, we measured equal average angular speeds for CW and CCW rotations (see Table S2 in the supplemental material), and the CCW and CW durations were 1.36 Ϯ 1.53 s and 1.17 Ϯ 1.22 s, respectively These findings for tethered cells are consistent with our finding that swimming P. aeruginosa bacteria had the same speed for both forward and backward runs (see Fig. S4 in the supplemental material) and indicate that there is little intrinsic CW/CCW bias. When the serine concentration was stepped down, the average rotation duration decreased (Fig. 3B and D), and this decrease was monotonic with the
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