Opposite and Coordinated Rotation of Amphitrichous Flagella Governs Oriented Swimming and Reversals in a Magnetotactic Spirillum

Abstract

Current knowledge regarding the mechanism that governs flagellar motor rotation in response to environmental stimuli stems mainly from the study of monotrichous and peritrichous bacteria. Little is known about how two polar flagella, one at each cell pole of the so-called amphitrichous bacterium, are coordinated to steer the swimming. Here we fluorescently labeled the flagella of Magnetospirillum magneticum AMB-1 cells and took advantage of the magnetically controllable swimming of this bacterium to investigate flagellar rotation in moving cells. We identified three motility behaviors (runs, tumbles, and reversals) and two characteristic fluorescence patterns likely corresponding to flagella rotating in opposite directions. Each AMB-1 locomotion mode was systematically associated with particular flagellar patterns at the poles which led us to conclude that, while cell runs are allowed by the asymmetrical rotation of flagellar motors, their symmetrical rotation triggers cell tumbling. Our observations point toward a precise coordination of the two flagellar motors which can be temporarily unsynchronized during tumbling. IMPORTANCEMotility is essential for bacteria to search for optimal niches and survive. Many bacteria use one or several flagella to explore their environment. The mechanism by which bipolarly flagellated cells coordinate flagellar rotation is poorly understood. We took advantage of the genetic amenability and magnetically controlled swimming of the spirillum-shaped magnetotactic bacterium Magnetospirillum magneticum AMB-1 to correlate cell motion with flagellar rotation. We found that asymmetric rotation of the flagella (counterclockwise at the lagging pole and clockwise at the leading pole) enables cell runs whereas symmetric rotation triggers cell tumbling. Taking into consideration similar observations in spirochetes, bacteria possessing bipolar ribbons of periplasmic flagella, we propose a conserved motility paradigm for spirillum-shaped bipolarly flagellated bacteria. Mobile bacteria have developed strategies to efficiently explore their environment, in aqueous media as well as on solid surfaces (1, 2). In most cases, their movements are ensured by a highly efficient proteinaceous nanomachine, the flagellum. The flagellar apparatus comprises three main parts: the motor, the hook, and the flagellar filament. The flagellar motor, anchored in the plasma membrane, uses the proton motive force or the sodium ion gradient to power the rotation of the flagellar filament, which is connected to it through the structure called the hook (3, 4). The rotation of the motor determines the direction of flagellum rotation and, consequently, the swimming direction of the bacterium. Using that principle, chemotactic bacteria directly regulate motor rotation so as to swim toward an attractant or away from a repellent, which involves signal detection via chemoreceptors. The signal is then transmitted from the chemoreceptor to the flagellar motor through a phosphorylation-dephosphorylation cascade of dedica...

High-speed motility originates from cooperatively pushing and pulling flagella bundles in bilophotrichous bacteria

“…Their unusual motility is certainly an adaptation that represents a selective advantage that make them competitive in the highly coveted biotopes that are the oxic-anoxic interfaces [25]. Indeed, the observed geometry of this resulting swimming pattern is reminiscent of the situation recently reported for magnetospirilla [26], despite the difference in body plan. The magnetosprilla have two flagella at opposite cell poles, and a magnetic moment parallel to the flagellar axis, while the flagella of the cocci studied here are attached on one hemisphere of the cell and almost perpendicular to the magnetic moment.…”

Magnetotactic bacteria

“…Alternatively, it could be accomplished by a switch from one flagellum pushing (or alternatively pulling) the cell body to the other, if it is always the rear flagellum (respectively the front flagellum) that powers motion. The question how two flagella work together in such an organism has so far only been addressed in one study, which favors the second mechanism [33]. moment m in a (spatially homogeneous) magnetic field B is characterized by the energy…”

Distinct chemotactic behavior in the originalEscherichia coliK-12 depending on forward-and-backward swimming, not on run-tumble movements

“…Polar flagellated bacteria show flagellar polymorphic change from a normal to curly state in the single polar, flagellated species Pseudomonas spp, [47, 48] and from normal to coiled state for Rhodobacter sphaeroides [49]. A novel type of flagellar wrapping motion has recently been observed in the single polar, flagellated species Shewanella putrefaciens [11], multiple polar flagellated bacteria such as Allivibrio fischeri, Burkholderia insecticola, and P. putida [10, 50], and bipolar flagellated bacteria such as Helicobacter suis [51] and Magnetospirillum magneticus AMB-1 [52]. These bacteria reverse their direction of motion by the transition from CCW rotation of left-handed normal filaments into CW rotation of right-handed coiled filaments to escape from being trapped in structured environments.…”