Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect

ABSTRACT Gram-negative bacteria have a tripartite cell envelope with the cytoplasmic membrane (CM), a stress-bearing peptidoglycan (PG) layer, and the asymmetric outer membrane (OM) containing lipopolysaccharide (LPS) in the outer leaflet. Cells must tightly coordinate the growth of their complex en...

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Autores principales:	Niccolò Morè, Alessandra M. Martorana, Jacob Biboy, Christian Otten, Matthias Winkle, Carlos K. Gurnani Serrano, Alejandro Montón Silva, Lisa Atkinson, Hamish Yau, Eefjan Breukink, Tanneke den Blaauwen, Waldemar Vollmer, Alessandra Polissi
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	Escherichia coli cell envelope lipopolysaccharide peptidoglycan stress response Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/2f19b63868df4508b1af58dc5d1478a9
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spelling	oai:doaj.org-article:2f19b63868df4508b1af58dc5d1478a92021-11-15T15:55:14ZPeptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect10.1128/mBio.02729-182150-7511https://doaj.org/article/2f19b63868df4508b1af58dc5d1478a92019-02-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.02729-18https://doaj.org/toc/2150-7511ABSTRACT Gram-negative bacteria have a tripartite cell envelope with the cytoplasmic membrane (CM), a stress-bearing peptidoglycan (PG) layer, and the asymmetric outer membrane (OM) containing lipopolysaccharide (LPS) in the outer leaflet. Cells must tightly coordinate the growth of their complex envelope to maintain cellular integrity and OM permeability barrier function. The biogenesis of PG and LPS relies on specialized macromolecular complexes that span the entire envelope. In this work, we show that Escherichia coli cells are capable of avoiding lysis when the transport of LPS to the OM is compromised, by utilizing LD-transpeptidases (LDTs) to generate 3-3 cross-links in the PG. This PG remodeling program relies mainly on the activities of the stress response LDT, LdtD, together with the major PG synthase PBP1B, its cognate activator LpoB, and the carboxypeptidase PBP6a. Our data support a model according to which these proteins cooperate to strengthen the PG in response to defective OM synthesis. IMPORTANCE In Gram-negative bacteria, the outer membrane protects the cell against many toxic molecules, and the peptidoglycan layer provides protection against osmotic challenges, allowing bacterial cells to survive in changing environments. Maintaining cell envelope integrity is therefore a question of life or death for a bacterial cell. Here we show that Escherichia coli cells activate the LD-transpeptidase LdtD to introduce 3-3 cross-links in the peptidoglycan layer when the integrity of the outer membrane is compromised, and this response is required to avoid cell lysis. This peptidoglycan remodeling program is a strategy to increase the overall robustness of the bacterial cell envelope in response to defects in the outer membrane.Niccolò MorèAlessandra M. MartoranaJacob BiboyChristian OttenMatthias WinkleCarlos K. Gurnani SerranoAlejandro Montón SilvaLisa AtkinsonHamish YauEefjan BreukinkTanneke den BlaauwenWaldemar VollmerAlessandra PolissiAmerican Society for MicrobiologyarticleEscherichia colicell envelopelipopolysaccharidepeptidoglycanstress responseMicrobiologyQR1-502ENmBio, Vol 10, Iss 1 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	Escherichia coli cell envelope lipopolysaccharide peptidoglycan stress response Microbiology QR1-502
spellingShingle	Escherichia coli cell envelope lipopolysaccharide peptidoglycan stress response Microbiology QR1-502 Niccolò Morè Alessandra M. Martorana Jacob Biboy Christian Otten Matthias Winkle Carlos K. Gurnani Serrano Alejandro Montón Silva Lisa Atkinson Hamish Yau Eefjan Breukink Tanneke den Blaauwen Waldemar Vollmer Alessandra Polissi Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect
description	ABSTRACT Gram-negative bacteria have a tripartite cell envelope with the cytoplasmic membrane (CM), a stress-bearing peptidoglycan (PG) layer, and the asymmetric outer membrane (OM) containing lipopolysaccharide (LPS) in the outer leaflet. Cells must tightly coordinate the growth of their complex envelope to maintain cellular integrity and OM permeability barrier function. The biogenesis of PG and LPS relies on specialized macromolecular complexes that span the entire envelope. In this work, we show that Escherichia coli cells are capable of avoiding lysis when the transport of LPS to the OM is compromised, by utilizing LD-transpeptidases (LDTs) to generate 3-3 cross-links in the PG. This PG remodeling program relies mainly on the activities of the stress response LDT, LdtD, together with the major PG synthase PBP1B, its cognate activator LpoB, and the carboxypeptidase PBP6a. Our data support a model according to which these proteins cooperate to strengthen the PG in response to defective OM synthesis. IMPORTANCE In Gram-negative bacteria, the outer membrane protects the cell against many toxic molecules, and the peptidoglycan layer provides protection against osmotic challenges, allowing bacterial cells to survive in changing environments. Maintaining cell envelope integrity is therefore a question of life or death for a bacterial cell. Here we show that Escherichia coli cells activate the LD-transpeptidase LdtD to introduce 3-3 cross-links in the peptidoglycan layer when the integrity of the outer membrane is compromised, and this response is required to avoid cell lysis. This peptidoglycan remodeling program is a strategy to increase the overall robustness of the bacterial cell envelope in response to defects in the outer membrane.
format	article
author	Niccolò Morè Alessandra M. Martorana Jacob Biboy Christian Otten Matthias Winkle Carlos K. Gurnani Serrano Alejandro Montón Silva Lisa Atkinson Hamish Yau Eefjan Breukink Tanneke den Blaauwen Waldemar Vollmer Alessandra Polissi
author_facet	Niccolò Morè Alessandra M. Martorana Jacob Biboy Christian Otten Matthias Winkle Carlos K. Gurnani Serrano Alejandro Montón Silva Lisa Atkinson Hamish Yau Eefjan Breukink Tanneke den Blaauwen Waldemar Vollmer Alessandra Polissi
author_sort	Niccolò Morè
title	Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect
title_short	Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect
title_full	Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect
title_fullStr	Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect
title_full_unstemmed	Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect
title_sort	peptidoglycan remodeling enables <named-content content-type="genus-species">escherichia</named-content><named-content content-type="genus-species"> coli</named-content> to survive severe outer membrane assembly defect
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/2f19b63868df4508b1af58dc5d1478a9
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Peptidoglycan Remodeling Enables <named-content content-type="genus-species">Escherichia</named-content><named-content content-type="genus-species"> coli</named-content> To Survive Severe Outer Membrane Assembly Defect

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