γ-proteobacteria eject their polar flagella under nutrient depletion, retaining flagellar motor relic structures.


Journal

PLoS biology
ISSN: 1545-7885
Titre abrégé: PLoS Biol
Pays: United States
ID NLM: 101183755

Informations de publication

Date de publication:
03 2019
Historique:
received: 25 07 2018
accepted: 08 02 2019
entrez: 20 3 2019
pubmed: 20 3 2019
medline: 26 11 2019
Statut: epublish

Résumé

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.

Identifiants

pubmed: 30889173
doi: 10.1371/journal.pbio.3000165
pii: PBIOLOGY-D-18-00290
pmc: PMC6424402
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e3000165

Subventions

Organisme : Medical Research Council
ID : MR/K501281/1
Pays : United Kingdom
Organisme : Medical Research Council
ID : MR/P019374/1
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R01 GM051350
Pays : United States
Organisme : Wellcome Trust
ID : FC001143
Pays : United Kingdom
Organisme : NIGMS NIH HHS
ID : R35 GM118108
Pays : United States
Organisme : Medical Research Council
ID : FC001143
Pays : United Kingdom
Organisme : Cancer Research UK
ID : FC001143
Pays : United Kingdom

Commentaires et corrections

Type : CommentIn

Déclaration de conflit d'intérêts

The authors have declared that no competing interests exist.

Références

Cell. 2013 Apr 11;153(2):461-70
pubmed: 23582331
J Gen Microbiol. 1967 Feb;46(2):175-84
pubmed: 4961758
J Bacteriol. 2006 Jul;188(14):5196-203
pubmed: 16816191
J Bacteriol. 2016 Jun 13;198(13):1837-46
pubmed: 27114465
J Bacteriol. 2004 Aug;186(15):4960-71
pubmed: 15262933
Nat Commun. 2017 Jan 25;8:14276
pubmed: 28120828
Front Microbiol. 2017 Oct 04;8:1917
pubmed: 29046671
Elife. 2015 May 29;4:e06980
pubmed: 26023829
J Bacteriol. 1989 Apr;171(4):2075-82
pubmed: 2649485
Science. 2008 Jun 20;320(5883):1636-8
pubmed: 18566286
Mol Microbiol. 2015 Nov;98(4):727-42
pubmed: 26235439
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Microbiology (Reading). 2008 May;154(Pt 5):1390-1399
pubmed: 18451048
Mol Microbiol. 2012 Jan;83(2):335-50
pubmed: 22151089
Microbiology (Reading). 2005 Feb;151(Pt 2):433-438
pubmed: 15699192
Cell. 2010 Apr 2;141(1):107-16
pubmed: 20303158
J Struct Biol. 2016 Jul;195(1):93-9
pubmed: 27108186
Proc Natl Acad Sci U S A. 2013 Apr 9;110(15):6133-8
pubmed: 23530206
Appl Environ Microbiol. 2010 May;76(10):3263-74
pubmed: 20348304
Ultramicroscopy. 2006 May;106(7):587-96
pubmed: 16616422
Arch Microbiol. 1993;159(2):160-7
pubmed: 8439236
Nature. 1994 Oct 27;371(6500):752
pubmed: 7935835
Proc Natl Acad Sci U S A. 2016 Mar 29;113(13):E1917-26
pubmed: 26976588
Nat Commun. 2018 Sep 21;9(1):3840
pubmed: 30242280
PLoS Biol. 2019 Mar 19;17(3):e3000165
pubmed: 30889173
J Struct Biol. 2015 Feb;189(2):147-52
pubmed: 25528570
J Bacteriol. 1991 Jun;173(11):3564-72
pubmed: 1646201
Bioinformatics. 2013 Oct 1;29(19):2460-8
pubmed: 23958728
Nat Rev Microbiol. 2017 May;15(5):271-284
pubmed: 28163311
Curr Opin Microbiol. 2015 Dec;28:83-92
pubmed: 26476805
Science. 2017 Apr 14;356(6334):197-200
pubmed: 28408605
J Struct Biol. 2008 Mar;161(3):260-75
pubmed: 17855124
FEMS Microbiol Rev. 2000 Apr;24(2):177-91
pubmed: 10717313
Mol Microbiol. 2013 Jan;87(1):211-29
pubmed: 23190039
EMBO J. 2011 Jun 14;30(14):2972-81
pubmed: 21673657
Science. 1977 Jun 10;196(4295):1161-6
pubmed: 860134
Mol Cell. 2010 Apr 9;38(1):128-39
pubmed: 20346719
Proc Natl Acad Sci U S A. 2017 Oct 10;114(41):10966-10971
pubmed: 28973904
Genes Dev. 2007 Sep 15;21(18):2326-35
pubmed: 17761814
Sci Rep. 2017 Apr 28;7(1):1282
pubmed: 28455518
J Mol Biol. 1992 Jul 20;226(2):433-46
pubmed: 1640458
Proc Natl Acad Sci U S A. 2009 Jul 14;106(28):11582-7
pubmed: 19571004
Biophys Physicobiol. 2016 Jan 28;13:13-25
pubmed: 27924254
Cell Rep. 2016 Feb 2;14(4):679-685
pubmed: 26804901
Nucleic Acids Res. 2017 Jan 4;45(D1):D362-D368
pubmed: 27924014
Nat Methods. 2009 May;6(5):343-5
pubmed: 19363495
J Struct Biol. 1996 Jan-Feb;116(1):71-6
pubmed: 8742726
Bioinformatics. 2011 Feb 15;27(4):582-3
pubmed: 21172911
J Bacteriol. 2018 Oct 10;200(21):
pubmed: 30104237
J Struct Biol. 1997 Dec;120(3):343-52
pubmed: 9441937
J Struct Biol. 2012 Dec;180(3):519-30
pubmed: 23000701

Auteurs

Josie L Ferreira (JL)

Department of Life Sciences, Imperial College London, United Kingdom.

Forson Z Gao (FZ)

Department of Life Sciences, Imperial College London, United Kingdom.

Florian M Rossmann (FM)

Department of Life Sciences, Imperial College London, United Kingdom.
Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, Giessen, Germany.

Andrea Nans (A)

Structural Biology of Cells and Viruses Laboratory, The Francis Crick Institute, London, United Kingdom.

Susanne Brenzinger (S)

Institute of Biology, University of Leiden, Leiden, the Netherlands.

Rohola Hosseini (R)

Institute of Biology, University of Leiden, Leiden, the Netherlands.

Amanda Wilson (A)

Department of Life Sciences, Imperial College London, United Kingdom.

Ariane Briegel (A)

Institute of Biology, University of Leiden, Leiden, the Netherlands.

Kai M Thormann (KM)

Institut für Mikrobiologie und Molekularbiologie, Justus-Liebig-Universität Giessen, Giessen, Germany.

Peter B Rosenthal (PB)

Structural Biology of Cells and Viruses Laboratory, The Francis Crick Institute, London, United Kingdom.

Morgan Beeby (M)

Department of Life Sciences, Imperial College London, United Kingdom.

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