Journal article

Publication year: 2019

Pages: e3000165-

Journal: PLoS Biology

Volume number: 17

Issue number: 3

ISSN: 1544-9173

eISSN: 1545-7885

Open access status: Gold

DOI Link: https://doi.org/10.1371/journal.pbio.3000165

Publisher: Public Library of Science

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 -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 -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.Author summary In the face of starvation, bacteria must minimize their energy use. Here, 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 propellersunrelated to eukaryotic flagellarotated by rotary motors embedded in the cell; continual rotation and assembly can consume up to 3% of a bacterium's energy. Using electron cryo-tomography, a technique that provides high-resolution 3D images of intact bacteria, we were surprised to find partial flagellar motors in bacterial cells that were rare when nutrients were abundant but became common when nutrients were scarce. A variety of clues led us to hypothesize that these structures were relics of motors whose flagella had been ejected, which we confirmed using a genetic approach. Curiously, flagellar relicswhich would otherwise be open portals through which the contents of the bacterial periplasm could leakwere plugged by an unidentified protein, presumably as a preservation measure. We speculate that flagellar ejection saves the bacterium from the costs of continuously assembling and rotating its flagella, as a last-ditch survival attempt. Our work provides a striking example of evolution arriving at a functional yet unintuitive solution to a problem.

Harvard Citation style: Ferreira, J., Gao, F., Rossmann, F., Nans, A., Brenzinger, S., Hosseini, R., et al. (2019) γ-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures, PLoS Biology, 17(3), Article e3000165. p. e3000165. https://doi.org/10.1371/journal.pbio.3000165

APA Citation style: Ferreira, J., Gao, F., Rossmann, F., Nans, A., Brenzinger, S., Hosseini, R., Wilson, A., Briegel, A., Thormann, K., Rosenthal, P., & Beeby, M. (2019). γ-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures. PLoS Biology. 17(3), Article e3000165, e3000165. https://doi.org/10.1371/journal.pbio.3000165