Intermembrane Crosstalk Drives Inner-membrane Protein Organization in Escherichia Coli

Overview

Journal Nat Commun

Specialty Biology

Date 2018 Mar 16

PMID 29540681

Citations 20

Authors

Patrice Rassam

Kathleen R Long

Renata Kaminska

David J Williams

Grigorios Papadakos

Christoph G Baumann

Colin Kleanthous

Affiliations

Soon will be listed here.

Abstract

Gram-negative bacteria depend on energised protein complexes that connect the two membranes of the cell envelope. However, β-barrel outer-membrane proteins (OMPs) and α-helical inner-membrane proteins (IMPs) display quite different organisation. OMPs cluster into islands that restrict their lateral mobility, while IMPs generally diffuse throughout the cell. Here, using live cell imaging of Escherichia coli, we demonstrate that when transient, energy-dependent transmembrane connections are formed, IMPs become subjugated by the inherent organisation of OMPs and that such connections impact IMP function. We show that while establishing a translocon for import, the colicin ColE9 sequesters the IMPs of the proton motive force (PMF)-linked Tol-Pal complex into islands mirroring those of colicin-bound OMPs. Through this imposed organisation, the bacteriocin subverts the outer-membrane stabilising role of Tol-Pal, blocking its recruitment to cell division sites and slowing membrane constriction. The ordering of IMPs by OMPs via an energised inter-membrane bridge represents an emerging functional paradigm in cell envelope biology.

Citing Articles

The Tol Pal system integrates maintenance of the three layered cell envelope.

Szczepaniak J, Webby M NPJ Antimicrob Resist. 2025; 2(1):46.

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Cell division cycle fluctuation of Pal concentration in Escherichia coli.

Mertens L, Liu X, Verheul J, Egan A, Vollmer W, den Blaauwen T Access Microbiol. 2024; 6(11).

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Tunable force transduction through the cell envelope.

Williams-Jones D, Webby M, Press C, Gradon J, Armstrong S, Szczepaniak J Proc Natl Acad Sci U S A. 2023; 120(47):e2306707120.

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Single-molecule dynamics show a transient lipopolysaccharide transport bridge.

Tork L, Moffatt C, Bernhardt T, Garner E, Kahne D Nature. 2023; 623(7988):814-819.

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References

Cascales E, Gavioli M, Sturgis J, Lloubes R . Proton motive force drives the interaction of the inner membrane TolA and outer membrane pal proteins in Escherichia coli. Mol Microbiol. 2000; 38(4):904-15. DOI: 10.1046/j.1365-2958.2000.02190.x. View

Bonsor D, Hecht O, Vankemmelbeke M, Sharma A, Krachler A, Housden N . Allosteric beta-propeller signalling in TolB and its manipulation by translocating colicins. EMBO J. 2009; 28(18):2846-57. PMC: 2750012. DOI: 10.1038/emboj.2009.224. View

Faure L, Fiche J, Espinosa L, Ducret A, Anantharaman V, Luciano J . The mechanism of force transmission at bacterial focal adhesion complexes. Nature. 2016; 539(7630):530-535. PMC: 5465867. DOI: 10.1038/nature20121. View

Leake M, Chandler J, Wadhams G, Bai F, Berry R, Armitage J . Stoichiometry and turnover in single, functioning membrane protein complexes. Nature. 2006; 443(7109):355-8. DOI: 10.1038/nature05135. View

Durand E, Nguyen V, Zoued A, Logger L, Pehau-Arnaudet G, Aschtgen M . Biogenesis and structure of a type VI secretion membrane core complex. Nature. 2015; 523(7562):555-60. DOI: 10.1038/nature14667. View

Vankemmelbeke M, Healy B, Moore G, Kleanthous C, Penfold C, James R . Rapid detection of colicin E9-induced DNA damage using Escherichia coli cells carrying SOS promoter-lux fusions. J Bacteriol. 2005; 187(14):4900-7. PMC: 1169509. DOI: 10.1128/JB.187.14.4900-4907.2005. View

Davidov Y, Rozen R, Smulski D, van Dyk T, Vollmer A, Elsemore D . Improved bacterial SOS promoter&Colon;lux fusions for genotoxicity detection. Mutat Res. 2001; 466(1):97-107. DOI: 10.1016/s1383-5718(99)00233-8. View

Celia H, Noinaj N, Zakharov S, Bordignon E, Botos I, Santamaria M . Structural insight into the role of the Ton complex in energy transduction. Nature. 2016; 538(7623):60-65. PMC: 5161667. DOI: 10.1038/nature19757. View

Housden N, Hopper J, Lukoyanova N, Rodriguez-Larrea D, Wojdyla J, Klein A . Intrinsically disordered protein threads through the bacterial outer-membrane porin OmpF. Science. 2013; 340(6140):1570-4. PMC: 3856478. DOI: 10.1126/science.1237864. View

10.

Noinaj N, Guillier M, Barnard T, Buchanan S . TonB-dependent transporters: regulation, structure, and function. Annu Rev Microbiol. 2010; 64:43-60. PMC: 3108441. DOI: 10.1146/annurev.micro.112408.134247. View

11.

Bisicchia P, Steel B, Mariam Debela M, Lowe J, Sherratt D . The N-terminal membrane-spanning domain of the Escherichia coli DNA translocase FtsK hexamerizes at midcell. mBio. 2013; 4(6):e00800-13. PMC: 3870252. DOI: 10.1128/mBio.00800-13. View

12.

Dosset P, Rassam P, Fernandez L, Espenel C, Rubinstein E, Margeat E . Automatic detection of diffusion modes within biological membranes using back-propagation neural network. BMC Bioinformatics. 2016; 17(1):197. PMC: 4855490. DOI: 10.1186/s12859-016-1064-z. View

13.

Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M . Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol. 2006; 2:2006.0008. PMC: 1681482. DOI: 10.1038/msb4100050. View

14.

Gerding M, Ogata Y, Pecora N, Niki H, de Boer P . The trans-envelope Tol-Pal complex is part of the cell division machinery and required for proper outer-membrane invagination during cell constriction in E. coli. Mol Microbiol. 2007; 63(4):1008-25. PMC: 4428343. DOI: 10.1111/j.1365-2958.2006.05571.x. View

15.

Egan A . Bacterial outer membrane constriction. Mol Microbiol. 2018; 107(6):676-687. DOI: 10.1111/mmi.13908. View

16.

Kleanthous C, Rassam P, Baumann C . Protein-protein interactions and the spatiotemporal dynamics of bacterial outer membrane proteins. Curr Opin Struct Biol. 2015; 35:109-15. PMC: 4684144. DOI: 10.1016/j.sbi.2015.10.007. View

17.

Tokunaga M, Imamoto N, Sakata-Sogawa K . Highly inclined thin illumination enables clear single-molecule imaging in cells. Nat Methods. 2008; 5(2):159-61. DOI: 10.1038/nmeth1171. View

18.

Uphoff S, Sherratt D, Kapanidis A . Visualizing protein-DNA interactions in live bacterial cells using photoactivated single-molecule tracking. J Vis Exp. 2014; (85). PMC: 4144692. DOI: 10.3791/51177. View

19.

Riechmann L, Holliger P . The C-terminal domain of TolA is the coreceptor for filamentous phage infection of E. coli. Cell. 1997; 90(2):351-60. DOI: 10.1016/s0092-8674(00)80342-6. View

20.

Gibson D, Smith H, Hutchison 3rd C, Venter J, Merryman C . Chemical synthesis of the mouse mitochondrial genome. Nat Methods. 2010; 7(11):901-3. DOI: 10.1038/nmeth.1515. View