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Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro

External signals are crucial for bacteria to sense their immediate environment and fine-tune gene expression accordingly. The foodborne pathogen Listeria monocytogenes senses a range of environmental cues in order to activate or deactivate the virulence-inducing transcriptional factor PrfA during tr...

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Autores principales: Villoria Recio, Miguel, Lee, Bo-Hyung, Lillebæk, Eva Maria Sternkopf, Kallipolitis, Birgitte H., Gahan, Cormac G. M., Ingmer, Hanne, Larsen, Marianne Halberg
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744463/
https://www.ncbi.nlm.nih.gov/pubmed/33343529
http://dx.doi.org/10.3389/fmicb.2020.588906
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author Villoria Recio, Miguel
Lee, Bo-Hyung
Lillebæk, Eva Maria Sternkopf
Kallipolitis, Birgitte H.
Gahan, Cormac G. M.
Ingmer, Hanne
Larsen, Marianne Halberg
author_facet Villoria Recio, Miguel
Lee, Bo-Hyung
Lillebæk, Eva Maria Sternkopf
Kallipolitis, Birgitte H.
Gahan, Cormac G. M.
Ingmer, Hanne
Larsen, Marianne Halberg
author_sort Villoria Recio, Miguel
collection PubMed
description External signals are crucial for bacteria to sense their immediate environment and fine-tune gene expression accordingly. The foodborne pathogen Listeria monocytogenes senses a range of environmental cues in order to activate or deactivate the virulence-inducing transcriptional factor PrfA during transition between infectious and saprophytic lifecycles. Chitin is an abundant biopolymer formed from linked β-(1–4)-N-acetyl-D-glucosamine residues associated with fungi, the exoskeleton of insects and often incorporated into foods as a thickener or stabilizer. L. monocytogenes evolved to hydrolyse chitin, presumably, to facilitate nutrient acquisition from competitive environments such as soil where the polymer is abundant. Since mammals do not produce chitin, we reasoned that the polymer could serve as an environmental signal contributing to repression of L. monocytogenes PrfA-dependent expression. This study shows a significant downregulation of the core PrfA-regulon during virulence-inducing conditions in vitro in the presence of chitin. Our data suggest this phenomenon occurs through a mechanism that differs from PTS-transport of oligosaccharides generated from either degradation or chitinase-mediated hydrolysis of the polymer. Importantly, an indication that chitin can repress virulence expression of a constitutively active PrfA(∗) mutant is shown, possibly mediated via a post-translational modification inhibiting PrfA(∗) activity. To our knowledge, this is the first time that chitin is reported as a molecule with anti-virulence properties against a pathogenic bacterium. Thus, our findings identify chitin as a signal which may downregulate the virulence potential of the pathogen and may provide an alternative approach toward reducing disease risk.
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spelling pubmed-77444632020-12-18 Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro Villoria Recio, Miguel Lee, Bo-Hyung Lillebæk, Eva Maria Sternkopf Kallipolitis, Birgitte H. Gahan, Cormac G. M. Ingmer, Hanne Larsen, Marianne Halberg Front Microbiol Microbiology External signals are crucial for bacteria to sense their immediate environment and fine-tune gene expression accordingly. The foodborne pathogen Listeria monocytogenes senses a range of environmental cues in order to activate or deactivate the virulence-inducing transcriptional factor PrfA during transition between infectious and saprophytic lifecycles. Chitin is an abundant biopolymer formed from linked β-(1–4)-N-acetyl-D-glucosamine residues associated with fungi, the exoskeleton of insects and often incorporated into foods as a thickener or stabilizer. L. monocytogenes evolved to hydrolyse chitin, presumably, to facilitate nutrient acquisition from competitive environments such as soil where the polymer is abundant. Since mammals do not produce chitin, we reasoned that the polymer could serve as an environmental signal contributing to repression of L. monocytogenes PrfA-dependent expression. This study shows a significant downregulation of the core PrfA-regulon during virulence-inducing conditions in vitro in the presence of chitin. Our data suggest this phenomenon occurs through a mechanism that differs from PTS-transport of oligosaccharides generated from either degradation or chitinase-mediated hydrolysis of the polymer. Importantly, an indication that chitin can repress virulence expression of a constitutively active PrfA(∗) mutant is shown, possibly mediated via a post-translational modification inhibiting PrfA(∗) activity. To our knowledge, this is the first time that chitin is reported as a molecule with anti-virulence properties against a pathogenic bacterium. Thus, our findings identify chitin as a signal which may downregulate the virulence potential of the pathogen and may provide an alternative approach toward reducing disease risk. Frontiers Media S.A. 2020-12-03 /pmc/articles/PMC7744463/ /pubmed/33343529 http://dx.doi.org/10.3389/fmicb.2020.588906 Text en Copyright © 2020 Villoria Recio, Lee, Lillebæk, Kallipolitis, Gahan, Ingmer and Larsen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Villoria Recio, Miguel
Lee, Bo-Hyung
Lillebæk, Eva Maria Sternkopf
Kallipolitis, Birgitte H.
Gahan, Cormac G. M.
Ingmer, Hanne
Larsen, Marianne Halberg
Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro
title Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro
title_full Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro
title_fullStr Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro
title_full_unstemmed Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro
title_short Chitin Attenuates Expression of Listeria monocytogenes Virulence Genes in vitro
title_sort chitin attenuates expression of listeria monocytogenes virulence genes in vitro
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7744463/
https://www.ncbi.nlm.nih.gov/pubmed/33343529
http://dx.doi.org/10.3389/fmicb.2020.588906
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