γ-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures
Josie L. Ferreira, Forson Z. Gao, Florian M. Rossmann, Andrea Nans, Susanne Brenzinger, Rohola Hosseini, Amanda Wilson, Ariane Briegel, Kai M. Thormann, Peter B. Rosenthal, Morgan Beeby
Published: March 19, 2019 https://doi.org/10.1371/journal.pbio.3000165
Source/Fonte: Phys Org - Morgan Beeby
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.
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 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. 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 relics—which would otherwise be open portals through which the contents of the bacterial periplasm could leak—were 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.
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Citation: Ferreira JL, Gao FZ, Rossmann FM, Nans A, Brenzinger S, Hosseini R, et al. (2019) γ-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures. PLoS Biol 17(3): e3000165. https://doi.org/10.1371/journal.pbio.3000165
Academic Editor: Daniel B. Kearns, Indiana University, UNITED STATES
Received: July 25, 2018; Accepted: February 8, 2019; Published: March 19, 2019
Copyright: © 2019 Ferreira et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
Data Availability: Subtomogram averages are available on EMDB (Motor: EMDB-4570. Relic: EMDB-4569).
Funding: This work was supported by a Medical Research Council grant MR/P019374/1 to MB, a Medical Research Council PhD Doctoral Training Partnership award grant number MR/K501281/1 to JLF, a Research fellowship of the German Research Foundation (DFG project number 385257318) to FMR, Grant TRR174 "Prokaryotic Cell Biology" from German Research Foundation (DFG) to KMT, Netherlands Organisation for Scientific Research (NWO) BBOL.737.016.004 to AB, a German Academy of Sciences Leopoldina (Fellowship Programme LPDS 2017-01) to SB, and NIH (AM, grants R01-GM051350 and R35-GM118108) to PBR. PBR is also supported by the Francis Crick Institute, which receives its core funding from Cancer Research UK (FC001143), the UK Medical Research Council (FC001143), and the Wellcome Trust (FC001143). The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
Competing interests: The authors have declared that no competing interests exist.
Abbreviations: CCCP, Carbonyl cyanide m-chlorophenyl hydrazone; c-di-GMP, cyclic di-GMP; CFU, colony-forming unit; ECT, electron cryo-tomography; EM, electron microscopy; FSC, Fourier Shell Correlation; OD, optical density; SEC, general secretory pathway; WT, wild-type
