Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host

Many bacteria build biofilm matrices using a conserved exopolysaccharide named PGA or PNAG (poly-β-1,6-N-acetyl-D-glucosamine). Interestingly, while E. coli and other members of the family Enterobacteriaceae encode the pgaABCD operon responsible for PGA synthesis, Salmonella lacks it. The evolutiona...

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Autores: Echeverz Sarasúa, Maite, García Martínez, Begoña, Sabalza Baztán, Amaia, Valle Turrillas, Jaione, Gabaldón Estevan, Juan Antonio, Solano Goñi, Cristina, Lasa Uzcudun, Íñigo
Tipo de recurso: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Institución:Universidad Pública de Navarra
Repositorio:Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
OAI Identifier:oai:academica-e.unavarra.es:2454/30537
Acceso en línea:https://hdl.handle.net/2454/30537
Access Level:acceso abierto
Palabra clave:PGA exopolysaccharide
Salmonella
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spelling Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the hostEcheverz Sarasúa, MaiteGarcía Martínez, BegoñaSabalza Baztán, AmaiaValle Turrillas, JaioneGabaldón Estevan, Juan AntonioSolano Goñi, CristinaLasa Uzcudun, ÍñigoPGA exopolysaccharideSalmonellaMany bacteria build biofilm matrices using a conserved exopolysaccharide named PGA or PNAG (poly-β-1,6-N-acetyl-D-glucosamine). Interestingly, while E. coli and other members of the family Enterobacteriaceae encode the pgaABCD operon responsible for PGA synthesis, Salmonella lacks it. The evolutionary force driving this difference remains to be determined. Here, we report that Salmonella lost the pgaABCD operon after the divergence of Salmonella and Citrobacter clades, and previous to the diversification of the currently sequenced Salmonella strains. Reconstitution of the PGA machinery endows Salmonella with the capacity to produce PGA in a cyclic dimeric GMP (c-di-GMP) dependent manner. Outside the host, the PGA polysaccharide does not seem to provide any significant benefit to Salmonella: resistance against chlorine treatment, ultraviolet light irradiation, heavy metal stress and phage infection remained the same as in a strain producing cellulose, the main biofilm exopolysaccharide naturally produced by Salmonella. In contrast, PGA production proved to be deleterious to Salmonella survival inside the host, since it increased susceptibility to bile salts and oxidative stress, and hindered the capacity of S. Enteritidis to survive inside macrophages and to colonize extraintestinal organs, including the gallbladder. Altogether, our observations indicate that PGA is an antivirulence factor whose loss may have been a necessary event during Salmonella speciation to permit survival inside the host.This work was supported by the Spanish Ministry of Economy and Competitiveness grants BIO2014-53530-R and SAF2014-56716-REDT. JV was supported by Ramon y Cajal (RYC-2009-03948) contract from the Spanish Ministry of Economy and Competitiveness.PLOSIdAB. Instituto de Agrobiotecnología / Agrobioteknologiako Institutua2017info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionapplication/pdfhttps://hdl.handle.net/2454/30537reponame:Academica-e. Repositorio Institucional de la Universidad Pública de Navarrainstname:Universidad Pública de NavarraInglésinfo:eu-repo/grantAgreement/MINECO//BIO2014-53530-Rinfo:eu-repo/grantAgreement/MINECO//SAF2014-56716-REDT© 2017 Echeverz et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.https://creativecommons.org/licenses/by/4.0/info:eu-repo/semantics/openAccessoai:academica-e.unavarra.es:2454/305372026-06-17T12:41:47Z
dc.title.none.fl_str_mv Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
title Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
spellingShingle Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
Echeverz Sarasúa, Maite
PGA exopolysaccharide
Salmonella
title_short Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
title_full Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
title_fullStr Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
title_full_unstemmed Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
title_sort Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the host
dc.creator.none.fl_str_mv Echeverz Sarasúa, Maite
García Martínez, Begoña
Sabalza Baztán, Amaia
Valle Turrillas, Jaione
Gabaldón Estevan, Juan Antonio
Solano Goñi, Cristina
Lasa Uzcudun, Íñigo
author Echeverz Sarasúa, Maite
author_facet Echeverz Sarasúa, Maite
García Martínez, Begoña
Sabalza Baztán, Amaia
Valle Turrillas, Jaione
Gabaldón Estevan, Juan Antonio
Solano Goñi, Cristina
Lasa Uzcudun, Íñigo
author_role author
author2 García Martínez, Begoña
Sabalza Baztán, Amaia
Valle Turrillas, Jaione
Gabaldón Estevan, Juan Antonio
Solano Goñi, Cristina
Lasa Uzcudun, Íñigo
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv IdAB. Instituto de Agrobiotecnología / Agrobioteknologiako Institutua
dc.subject.none.fl_str_mv PGA exopolysaccharide
Salmonella
topic PGA exopolysaccharide
Salmonella
description Many bacteria build biofilm matrices using a conserved exopolysaccharide named PGA or PNAG (poly-β-1,6-N-acetyl-D-glucosamine). Interestingly, while E. coli and other members of the family Enterobacteriaceae encode the pgaABCD operon responsible for PGA synthesis, Salmonella lacks it. The evolutionary force driving this difference remains to be determined. Here, we report that Salmonella lost the pgaABCD operon after the divergence of Salmonella and Citrobacter clades, and previous to the diversification of the currently sequenced Salmonella strains. Reconstitution of the PGA machinery endows Salmonella with the capacity to produce PGA in a cyclic dimeric GMP (c-di-GMP) dependent manner. Outside the host, the PGA polysaccharide does not seem to provide any significant benefit to Salmonella: resistance against chlorine treatment, ultraviolet light irradiation, heavy metal stress and phage infection remained the same as in a strain producing cellulose, the main biofilm exopolysaccharide naturally produced by Salmonella. In contrast, PGA production proved to be deleterious to Salmonella survival inside the host, since it increased susceptibility to bile salts and oxidative stress, and hindered the capacity of S. Enteritidis to survive inside macrophages and to colonize extraintestinal organs, including the gallbladder. Altogether, our observations indicate that PGA is an antivirulence factor whose loss may have been a necessary event during Salmonella speciation to permit survival inside the host.
publishDate 2017
dc.date.none.fl_str_mv 2017
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv https://hdl.handle.net/2454/30537
url https://hdl.handle.net/2454/30537
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv info:eu-repo/grantAgreement/MINECO//BIO2014-53530-R
info:eu-repo/grantAgreement/MINECO//SAF2014-56716-REDT
dc.rights.none.fl_str_mv https://creativecommons.org/licenses/by/4.0/
info:eu-repo/semantics/openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by/4.0/
eu_rights_str_mv openAccess
dc.format.none.fl_str_mv application/pdf
dc.publisher.none.fl_str_mv PLOS
publisher.none.fl_str_mv PLOS
dc.source.none.fl_str_mv reponame:Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
instname:Universidad Pública de Navarra
instname_str Universidad Pública de Navarra
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collection Academica-e. Repositorio Institucional de la Universidad Pública de Navarra
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