Abstract
Bacteria switch only intermittently to motile planktonic lifestyles under favorable conditions. Under chronic nutrient deprivation, however, bacteria orchestrate a switch to stationary phase, conserving energy by altering metabolism and stopping motility. About two-thirds of bacteria use flagella to swim, but how bacteria deactivate this large molecular machine remains unclear. Here, we describe the previously unreported ejection of polar motors by γ-proteobacteria. We show that these bacteria eject their flagella at the base of the flagellar hook when nutrients are depleted, leaving a relic of a former flagellar motor in the outer membrane. Subtomogram averages of the full motor and relic reveal that this is an active process, as a plug protein appears in the relic, likely to prevent leakage across their outer membrane; furthermore, we show that ejection is triggered only under nutritional depletion and is independent of the filament as a possible mechanosensor. We show that filament ejection is a widespread phenomenon demonstrated by the appearance of relic structures in diverse γ-proteobacteria including Plesiomonas shigelloides, Vibrio cholerae, Vibrio fischeri, Shewanella putrefaciens, and Pseudomonas aeruginosa. While the molecular details remain to be determined, our results demonstrate a novel mechanism for bacteria to halt costly motility when nutrients become scarce.
Highlights
Many bacteria switch to a nonmotile lifestyle in stationary phase to conserve energy [1], but how this switch is accomplished is poorly understood
We describe our unexpected finding that some bacteria take the drastic measure of ejecting their flagella in response to nutrient deficiency
Bacteria continually assemble flagella as propellers—unrelated to eukaryotic flagella—rotated by rotary motors embedded in the cell; continual rotation and assembly can consume up to 3% of a bacterium’s energy
Summary
Many bacteria switch to a nonmotile lifestyle in stationary phase to conserve energy [1], but how this switch is accomplished is poorly understood. The most widespread motility device used by bacteria is the flagellum, found in approximately two-thirds of bacteria [2]. Bacterial flagellar filaments are helical propellers that extend several microns from the cell from a periplasm-spanning rotary motor; rotation of the filament by a transmembrane rotary motor exerts thrust that propels the bacterium forward. Motor torque is generated by harnessing ion flux across the inner membrane; this torque is first transmitted to a periplasm-spanning rod, to a flexible extracellular hook, and to the filament. The flagellum is vital for migration to favorable environments, sites of biofilm formation, or sites of infection, it is counterproductive for the cell to retain a functional flagellum during nutrient depletion, and stopping motility is preferable to resource exhaustion
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