Bacterial flagellum as a propeller and as a rudder for efficient chemotaxis

Abstract

We investigate swimming and chemotactic behaviors of the polarly flagellated marine bacteria Vibrio alginolyticus in an aqueous medium. Our observations show that V. alginolyticus execute a cyclic, three-step (forward, reverse, and flick) swimming pattern that is distinctively different from the run-tumble pattern adopted by Escherichia coli. Specifically, the bacterium backtracks its forward swimming path when the motor reverses. However, upon resuming forward swimming, the flagellum flicks and a new swimming direction is selected at random. In a chemically homogeneous medium (no attractant or repellent), the consecutive forward t f and backward t b swimming times are uncorrelated. Interestingly, although t f and t b are not distributed in a Poissonian fashion, their difference Δt ¼ jt f − t b j is. Near a point source of attractant, on the other hand, t f and t b are found to be strongly correlated, and Δt obeys a bimodal distribution. These observations indicate that V. alginolyticus exploit the time-reversal symmetry of forward and backward swimming by using the time difference to regulate their chemotactic behavior. By adopting the three-step cycle, cells of V. alginolyticus are able to quickly respond to a chemical gradient as well as to localize near a point source of attractant.bacterial chemotaxis | bacterial swimming pattern E nteric bacteria, such as Escherichia coli, swim by rotating a set of flagella that forms a bundle when the flagellar motors turn in the counterclockwise (CCW) direction (1-3). The bundle falls apart when one or more motors turns in the clockwise (CW) direction, and the bacterium tumbles (4). A new swimming direction is selected upon resuming the CCW rotation of the flagellar motors. By modulating the CCW and CW intervals according to external chemical cues, the cells are able to migrate toward attractants or away from repellents (5, 6).Certain bacterial species possess a single polar flagellum with a bidirectional motor similar to E. coli. Being single polarly flagellated, low Reynolds number (Re) hydrodynamics dictates that, aside from random thermal motions, the bacterium can only backtrack its trajectory when the motor reverses. This raises an interesting question concerning how this type of cells performs chemotaxis. Studies of motility patterns of single polarly flagellated bacteria Pseudomonas citronellolis showed that the bacteria change the swimming direction by a brief reversal between two long runs. From the published trajectories (7), each reversal typically results in a small change in cell orientation, and thus several reversals appear to be necessary for a significant change in the swimming direction. Backtracking was also observed in a number of single flagellated marine bacteria such as Shewanella putrefaciens, Pseudoalteromonas haloplanktis, and Vibrio alginolyticus, which execute the so-called run-reverse steps when following attractants released from porous beads and from algae (8-10). A pioneering experiment in V. alginolyticus revealed that the timereversal s...

Bacteria can exploit a flagellar buckling instability to change direction

“…Whereas the link between a reduction in swimming speed and the disappearance of flicking was established qualitatively in the original observation of this process 4 , here a quantification of this relationship enabled the determination of the mechanism underpinning flicks. This was achieved through a reduction in the sodium concentration of the suspending medium, [Na + ] ( Fig.…”

“…from overcoiling of the flagellum has been suggested as a potential mechanism for the flick 4 . In contrast, we focus on the mechanical stability of the hook, the structure at the base of the flagellum that connects to the motor, because its bending stiffness EI (E is Young's modulus; I is the area moment of inertia) is 100-1,000 times smaller than that of the flagellar filament (Supplementary Tables S2 and S3), and because most of the deformation during a flick is confined to the base of the flagellum 4 ( Fig.…”

“…Yet, many bacteria have only a single flagellum (monotrichous), including 90% of motile marine bacteria 3 , and how they reorient has long remained unclear. Only recently has the monotrichous marine bacterium Vibrio alginolyticus been shown to exhibit the ability to turn or flick 4 by a seemingly impossible off-axis motion of its flagellum (Fig. 1a,e).…”

“…2a; Methods; ref. 4), exploiting the fact that the motor of V. alginolyticus is driven by trans-membrane sodium gradients 24 . At [Na + ] = 100 mM cells swam at 40 µm s −1 on average and regularly alternated between flicks and reversals ( Fig.…”

“…In contrast, cells have recently been reported to reorient by an average angle θ ≈ 90 • (a 'flick' 4 ) at the end of the backward run and on resuming forward swimming, on the basis of imaging at 30-100 frames s −1 (ref. 4). By imaging at up to 1,000 frames s −1 (Fig.…”