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Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF

Bacteria deploy weapons to kill their neighbours during competition for resources and to aid survival within microbiomes. Colicins were the first such antibacterial system identified, yet how these bacteriocins cross the outer membrane (OM) of Escherichia coli is unknown. Here, by solving the struct...

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Autores principales: Francis, Marie‐Louise R, Webby, Melissa N, Housden, Nicholas G, Kaminska, Renata, Elliston, Emma, Chinthammit, Boonyaporn, Lukoyanova, Natalya, Kleanthous, Colin
Formato: Online Artículo Texto
Lenguaje:English
Publicado: John Wiley and Sons Inc. 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8561637/
https://www.ncbi.nlm.nih.gov/pubmed/34515361
http://dx.doi.org/10.15252/embj.2021108610
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author Francis, Marie‐Louise R
Webby, Melissa N
Housden, Nicholas G
Kaminska, Renata
Elliston, Emma
Chinthammit, Boonyaporn
Lukoyanova, Natalya
Kleanthous, Colin
author_facet Francis, Marie‐Louise R
Webby, Melissa N
Housden, Nicholas G
Kaminska, Renata
Elliston, Emma
Chinthammit, Boonyaporn
Lukoyanova, Natalya
Kleanthous, Colin
author_sort Francis, Marie‐Louise R
collection PubMed
description Bacteria deploy weapons to kill their neighbours during competition for resources and to aid survival within microbiomes. Colicins were the first such antibacterial system identified, yet how these bacteriocins cross the outer membrane (OM) of Escherichia coli is unknown. Here, by solving the structures of translocation intermediates via cryo‐EM and by imaging toxin import, we uncover the mechanism by which the Tol‐dependent nuclease colicin E9 (ColE9) crosses the bacterial OM. We show that threading of ColE9’s disordered N‐terminal domain through two pores of the trimeric porin OmpF causes the colicin to disengage from its primary receptor, BtuB, and reorganises the translocon either side of the membrane. Subsequent import of ColE9 through the lumen of a single OmpF subunit is driven by the proton‐motive force, which is delivered by the TolQ‐TolR‐TolA‐TolB assembly. Our study answers longstanding questions, such as why OmpF is a better translocator than OmpC, and reconciles the mechanisms by which both Tol‐ and Ton‐dependent bacteriocins cross the bacterial outer membrane.
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spelling pubmed-85616372021-11-12 Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF Francis, Marie‐Louise R Webby, Melissa N Housden, Nicholas G Kaminska, Renata Elliston, Emma Chinthammit, Boonyaporn Lukoyanova, Natalya Kleanthous, Colin EMBO J Articles Bacteria deploy weapons to kill their neighbours during competition for resources and to aid survival within microbiomes. Colicins were the first such antibacterial system identified, yet how these bacteriocins cross the outer membrane (OM) of Escherichia coli is unknown. Here, by solving the structures of translocation intermediates via cryo‐EM and by imaging toxin import, we uncover the mechanism by which the Tol‐dependent nuclease colicin E9 (ColE9) crosses the bacterial OM. We show that threading of ColE9’s disordered N‐terminal domain through two pores of the trimeric porin OmpF causes the colicin to disengage from its primary receptor, BtuB, and reorganises the translocon either side of the membrane. Subsequent import of ColE9 through the lumen of a single OmpF subunit is driven by the proton‐motive force, which is delivered by the TolQ‐TolR‐TolA‐TolB assembly. Our study answers longstanding questions, such as why OmpF is a better translocator than OmpC, and reconciles the mechanisms by which both Tol‐ and Ton‐dependent bacteriocins cross the bacterial outer membrane. John Wiley and Sons Inc. 2021-09-13 2021-11-02 /pmc/articles/PMC8561637/ /pubmed/34515361 http://dx.doi.org/10.15252/embj.2021108610 Text en © 2021 The Authors. Published under the terms of the CC BY 4.0 license https://creativecommons.org/licenses/by/4.0/This is an open access article under the terms of the http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) License, which permits use, distribution and reproduction in any medium, provided the original work is properly cited.
spellingShingle Articles
Francis, Marie‐Louise R
Webby, Melissa N
Housden, Nicholas G
Kaminska, Renata
Elliston, Emma
Chinthammit, Boonyaporn
Lukoyanova, Natalya
Kleanthous, Colin
Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF
title Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF
title_full Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF
title_fullStr Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF
title_full_unstemmed Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF
title_short Porin threading drives receptor disengagement and establishes active colicin transport through Escherichia coli OmpF
title_sort porin threading drives receptor disengagement and establishes active colicin transport through escherichia coli ompf
topic Articles
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8561637/
https://www.ncbi.nlm.nih.gov/pubmed/34515361
http://dx.doi.org/10.15252/embj.2021108610
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