Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival

ABSTRACT Bacterial biofilm communities are associated with profound physiological changes that lead to novel properties compared to the properties of individual (planktonic) bacteria. The study of biofilm-associated phenotypes is an essential step toward control of deleterious effects of pathogenic...

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Autores principales:	Sabina Chalabaev, Ashwini Chauhan, Alexey Novikov, Pavithra Iyer, Magdalena Szczesny, Christophe Beloin, Martine Caroff, Jean-Marc Ghigo
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2014
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/8bdbaa43b97f40158e4deea764d5a07c
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spelling	oai:doaj.org-article:8bdbaa43b97f40158e4deea764d5a07c2021-11-15T15:47:21ZBiofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival10.1128/mBio.01116-142150-7511https://doaj.org/article/8bdbaa43b97f40158e4deea764d5a07c2014-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01116-14https://doaj.org/toc/2150-7511ABSTRACT Bacterial biofilm communities are associated with profound physiological changes that lead to novel properties compared to the properties of individual (planktonic) bacteria. The study of biofilm-associated phenotypes is an essential step toward control of deleterious effects of pathogenic biofilms. Here we investigated lipopolysaccharide (LPS) structural modifications in Escherichia coli biofilm bacteria, and we showed that all tested commensal and pathogenic E. coli biofilm bacteria display LPS modifications corresponding to an increased level of incorporation of palmitate acyl chain (palmitoylation) into lipid A compared to planktonic bacteria. Genetic analysis showed that lipid A palmitoylation in biofilms is mediated by the PagP enzyme, which is regulated by the histone-like protein repressor H-NS and the SlyA regulator. While lipid A palmitoylation does not influence bacterial adhesion, it weakens inflammatory response and enhances resistance to some antimicrobial peptides. Moreover, we showed that lipid A palmitoylation increases in vivo survival of biofilm bacteria in a clinically relevant model of catheter infection, potentially contributing to biofilm tolerance to host immune defenses. The widespread occurrence of increased lipid A palmitoylation in biofilms formed by all tested bacteria suggests that it constitutes a new biofilm-associated phenotype in Gram-negative bacteria. IMPORTANCE Bacterial communities called biofilms display characteristic properties compared to isolated (planktonic) bacteria, suggesting that some molecules could be more particularly produced under biofilm conditions. We investigated biofilm-associated modifications occurring in the lipopolysaccharide (LPS), a major component of all Gram-negative bacterial outer membrane. We showed that all tested commensal and pathogenic biofilm bacteria display high incorporation of a palmitate acyl chain into the lipid A part of LPS. This lipid A palmitoylation is mediated by the PagP enzyme, whose expression in biofilm is controlled by the regulatory proteins H-NS and SlyA. We also showed that lipid A palmitoylation in biofilm bacteria reduces host inflammatory response and enhances their survival in an animal model of biofilm infections. While these results provide new insights into the biofilm lifestyle, they also suggest that the level of lipid A palmitoylation could be used as an indicator to monitor the development of biofilm infections on medical surfaces.Sabina ChalabaevAshwini ChauhanAlexey NovikovPavithra IyerMagdalena SzczesnyChristophe BeloinMartine CaroffJean-Marc GhigoAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 5, Iss 4 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Sabina Chalabaev Ashwini Chauhan Alexey Novikov Pavithra Iyer Magdalena Szczesny Christophe Beloin Martine Caroff Jean-Marc Ghigo Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival
description	ABSTRACT Bacterial biofilm communities are associated with profound physiological changes that lead to novel properties compared to the properties of individual (planktonic) bacteria. The study of biofilm-associated phenotypes is an essential step toward control of deleterious effects of pathogenic biofilms. Here we investigated lipopolysaccharide (LPS) structural modifications in Escherichia coli biofilm bacteria, and we showed that all tested commensal and pathogenic E. coli biofilm bacteria display LPS modifications corresponding to an increased level of incorporation of palmitate acyl chain (palmitoylation) into lipid A compared to planktonic bacteria. Genetic analysis showed that lipid A palmitoylation in biofilms is mediated by the PagP enzyme, which is regulated by the histone-like protein repressor H-NS and the SlyA regulator. While lipid A palmitoylation does not influence bacterial adhesion, it weakens inflammatory response and enhances resistance to some antimicrobial peptides. Moreover, we showed that lipid A palmitoylation increases in vivo survival of biofilm bacteria in a clinically relevant model of catheter infection, potentially contributing to biofilm tolerance to host immune defenses. The widespread occurrence of increased lipid A palmitoylation in biofilms formed by all tested bacteria suggests that it constitutes a new biofilm-associated phenotype in Gram-negative bacteria. IMPORTANCE Bacterial communities called biofilms display characteristic properties compared to isolated (planktonic) bacteria, suggesting that some molecules could be more particularly produced under biofilm conditions. We investigated biofilm-associated modifications occurring in the lipopolysaccharide (LPS), a major component of all Gram-negative bacterial outer membrane. We showed that all tested commensal and pathogenic biofilm bacteria display high incorporation of a palmitate acyl chain into the lipid A part of LPS. This lipid A palmitoylation is mediated by the PagP enzyme, whose expression in biofilm is controlled by the regulatory proteins H-NS and SlyA. We also showed that lipid A palmitoylation in biofilm bacteria reduces host inflammatory response and enhances their survival in an animal model of biofilm infections. While these results provide new insights into the biofilm lifestyle, they also suggest that the level of lipid A palmitoylation could be used as an indicator to monitor the development of biofilm infections on medical surfaces.
format	article
author	Sabina Chalabaev Ashwini Chauhan Alexey Novikov Pavithra Iyer Magdalena Szczesny Christophe Beloin Martine Caroff Jean-Marc Ghigo
author_facet	Sabina Chalabaev Ashwini Chauhan Alexey Novikov Pavithra Iyer Magdalena Szczesny Christophe Beloin Martine Caroff Jean-Marc Ghigo
author_sort	Sabina Chalabaev
title	Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival
title_short	Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival
title_full	Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival
title_fullStr	Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival
title_full_unstemmed	Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival
title_sort	biofilms formed by gram-negative bacteria undergo increased lipid a palmitoylation, enhancing <italic toggle="yes">in vivo</italic> survival
publisher	American Society for Microbiology
publishDate	2014
url	https://doaj.org/article/8bdbaa43b97f40158e4deea764d5a07c
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Biofilms Formed by Gram-Negative Bacteria Undergo Increased Lipid A Palmitoylation, Enhancing <italic toggle="yes">In Vivo</italic> Survival

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