Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.

We characterized key components and major targets of the c-di-GMP signaling pathways in the foodborne pathogen Listeria monocytogenes, identified a new c-di-GMP-inducible exopolysaccharide responsible for motility inhibition, cell aggregation, and enhanced tolerance to disinfectants and desiccation,...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Li-Hong Chen, Volkan K Köseoğlu, Zehra T Güvener, Tanya Myers-Morales, Joseph M Reed, Sarah E F D'Orazio, Kurt W Miller, Mark Gomelsky
Formato:	article
Lenguaje:	EN
Publicado:	Public Library of Science (PLoS) 2014
Materias:	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
Acceso en línea:	https://doaj.org/article/520c5f84accf48f09422a49585babf72
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:520c5f84accf48f09422a49585babf72
record_format	dspace
spelling	oai:doaj.org-article:520c5f84accf48f09422a49585babf722021-11-25T05:46:12ZCyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.1553-73661553-737410.1371/journal.ppat.1004301https://doaj.org/article/520c5f84accf48f09422a49585babf722014-08-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/25101646/?tool=EBIhttps://doaj.org/toc/1553-7366https://doaj.org/toc/1553-7374We characterized key components and major targets of the c-di-GMP signaling pathways in the foodborne pathogen Listeria monocytogenes, identified a new c-di-GMP-inducible exopolysaccharide responsible for motility inhibition, cell aggregation, and enhanced tolerance to disinfectants and desiccation, and provided first insights into the role of c-di-GMP signaling in listerial virulence. Genome-wide genetic and biochemical analyses of c-di-GMP signaling pathways revealed that L. monocytogenes has three GGDEF domain proteins, DgcA (Lmo1911), DgcB (Lmo1912) and DgcC (Lmo2174), that possess diguanylate cyclase activity, and three EAL domain proteins, PdeB (Lmo0131), PdeC (Lmo1914) and PdeD (Lmo0111), that possess c-di-GMP phosphodiesterase activity. Deletion of all phosphodiesterase genes (ΔpdeB/C/D) or expression of a heterologous diguanylate cyclase stimulated production of a previously unknown exopolysaccharide. The synthesis of this exopolysaccharide was attributed to the pssA-E (lmo0527-0531) gene cluster. The last gene of the cluster encodes the fourth listerial GGDEF domain protein, PssE, that functions as an I-site c-di-GMP receptor essential for exopolysaccharide synthesis. The c-di-GMP-inducible exopolysaccharide causes cell aggregation in minimal medium and impairs bacterial migration in semi-solid agar, however, it does not promote biofilm formation on abiotic surfaces. The exopolysaccharide also greatly enhances bacterial tolerance to commonly used disinfectants as well as desiccation, which may contribute to survival of L. monocytogenes on contaminated food products and in food-processing facilities. The exopolysaccharide and another, as yet unknown c-di-GMP-dependent target, drastically decrease listerial invasiveness in enterocytes in vitro, and lower pathogen load in the liver and gallbladder of mice infected via an oral route, which suggests that elevated c-di-GMP levels play an overall negative role in listerial virulence.Li-Hong ChenVolkan K KöseoğluZehra T GüvenerTanya Myers-MoralesJoseph M ReedSarah E F D'OrazioKurt W MillerMark GomelskyPublic Library of Science (PLoS)articleImmunologic diseases. AllergyRC581-607Biology (General)QH301-705.5ENPLoS Pathogens, Vol 10, Iss 8, p e1004301 (2014)
institution	DOAJ
collection	DOAJ
language	EN
topic	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5
spellingShingle	Immunologic diseases. Allergy RC581-607 Biology (General) QH301-705.5 Li-Hong Chen Volkan K Köseoğlu Zehra T Güvener Tanya Myers-Morales Joseph M Reed Sarah E F D'Orazio Kurt W Miller Mark Gomelsky Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.
description	We characterized key components and major targets of the c-di-GMP signaling pathways in the foodborne pathogen Listeria monocytogenes, identified a new c-di-GMP-inducible exopolysaccharide responsible for motility inhibition, cell aggregation, and enhanced tolerance to disinfectants and desiccation, and provided first insights into the role of c-di-GMP signaling in listerial virulence. Genome-wide genetic and biochemical analyses of c-di-GMP signaling pathways revealed that L. monocytogenes has three GGDEF domain proteins, DgcA (Lmo1911), DgcB (Lmo1912) and DgcC (Lmo2174), that possess diguanylate cyclase activity, and three EAL domain proteins, PdeB (Lmo0131), PdeC (Lmo1914) and PdeD (Lmo0111), that possess c-di-GMP phosphodiesterase activity. Deletion of all phosphodiesterase genes (ΔpdeB/C/D) or expression of a heterologous diguanylate cyclase stimulated production of a previously unknown exopolysaccharide. The synthesis of this exopolysaccharide was attributed to the pssA-E (lmo0527-0531) gene cluster. The last gene of the cluster encodes the fourth listerial GGDEF domain protein, PssE, that functions as an I-site c-di-GMP receptor essential for exopolysaccharide synthesis. The c-di-GMP-inducible exopolysaccharide causes cell aggregation in minimal medium and impairs bacterial migration in semi-solid agar, however, it does not promote biofilm formation on abiotic surfaces. The exopolysaccharide also greatly enhances bacterial tolerance to commonly used disinfectants as well as desiccation, which may contribute to survival of L. monocytogenes on contaminated food products and in food-processing facilities. The exopolysaccharide and another, as yet unknown c-di-GMP-dependent target, drastically decrease listerial invasiveness in enterocytes in vitro, and lower pathogen load in the liver and gallbladder of mice infected via an oral route, which suggests that elevated c-di-GMP levels play an overall negative role in listerial virulence.
format	article
author	Li-Hong Chen Volkan K Köseoğlu Zehra T Güvener Tanya Myers-Morales Joseph M Reed Sarah E F D'Orazio Kurt W Miller Mark Gomelsky
author_facet	Li-Hong Chen Volkan K Köseoğlu Zehra T Güvener Tanya Myers-Morales Joseph M Reed Sarah E F D'Orazio Kurt W Miller Mark Gomelsky
author_sort	Li-Hong Chen
title	Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.
title_short	Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.
title_full	Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.
title_fullStr	Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.
title_full_unstemmed	Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.
title_sort	cyclic di-gmp-dependent signaling pathways in the pathogenic firmicute listeria monocytogenes.
publisher	Public Library of Science (PLoS)
publishDate	2014
url	https://doaj.org/article/520c5f84accf48f09422a49585babf72
work_keys_str_mv	AT lihongchen cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT volkankkoseoglu cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT zehratguvener cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT tanyamyersmorales cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT josephmreed cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT sarahefdorazio cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT kurtwmiller cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes AT markgomelsky cyclicdigmpdependentsignalingpathwaysinthepathogenicfirmicutelisteriamonocytogenes
_version_	1718414457051283456

Cyclic di-GMP-dependent signaling pathways in the pathogenic Firmicute Listeria monocytogenes.

Ejemplares similares