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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Detalhes bibliográficos
Autores: Echeverz, Maite, García, Begoña, Sabalza, Amaia, Valle Turrillas, Jaione, Gabaldón, Toni, Solano Goñi, Cristina, Lasa, Íñigo
Formato: artículo
Estado:Versión publicada
Fecha de publicación:2017
País:España
Recursos:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/244718
Acesso em linha:http://hdl.handle.net/10261/244718
Access Level:acceso abierto
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spelling Lack of the PGA exopolysaccharide in Salmonella as an adaptive trait for survival in the hostEcheverz, MaiteGarcía, BegoñaSabalza, AmaiaValle Turrillas, JaioneGabaldón, ToniSolano Goñi, CristinaLasa, ÍñigoMany 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.[Author summary] During bacterial evolution, specific traits that optimize the organism’s fitness are selected. The production of exopolysaccharides is widespread among bacteria in which they play a protective shielding role as main constituents of biofilms. In contrast to closely related siblings, Salmonella has lost the capacity to produce the exopolysaccharide PGA. Our study reveals that Salmonella lost pga genes, and that the driving force for such a loss may have been the detrimental impact that PGA has during Salmonella invasion of internal organs where it augments the susceptibility to bile salts and oxygen radicals, reducing bacterial survival inside macrophages and rendering Salmonella avirulent. These results suggest that gene-loss has played an important role during Salmonella evolution.This work was supported by the Spanish Ministry of Economy and Competitiveness grants BIO2014-53530-R and SAF2014-56716-REDT (http://www.mineco.gob.es/portal/site/mineco/?lang_choosen=en). JV was supported by Ramon y Cajal (RYC-2009-03948) contract from the Spanish Ministry of Economy and Competitiveness.Public Library of ScienceMinisterio de Economía y Competitividad (España)Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]2021202120172021info:eu-repo/semantics/articlehttp://purl.org/coar/resource_type/c_6501Publisher's versioninfo:eu-repo/semantics/publishedVersionhttp://hdl.handle.net/10261/244718reponame:DIGITAL.CSIC. Repositorio Institucional del CSICinstname:Consejo Superior de Investigaciones Científicas (CSIC)Inglés#PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE##PLACEHOLDER_PARENT_METADATA_VALUE#info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BIO2014-53530-Rinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/SAF2014-56716-REDTinfo:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RYC-2009-03948http://doi.org/10.1371/journal. pgen.1006816Síinfo:eu-repo/semantics/openAccessoai:digital.csic.es:10261/2447182026-05-22T06:33:51Z
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, Maite
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, Maite
García, Begoña
Sabalza, Amaia
Valle Turrillas, Jaione
Gabaldón, Toni
Solano Goñi, Cristina
Lasa, Íñigo
author Echeverz, Maite
author_facet Echeverz, Maite
García, Begoña
Sabalza, Amaia
Valle Turrillas, Jaione
Gabaldón, Toni
Solano Goñi, Cristina
Lasa, Íñigo
author_role author
author2 García, Begoña
Sabalza, Amaia
Valle Turrillas, Jaione
Gabaldón, Toni
Solano Goñi, Cristina
Lasa, Íñigo
author2_role author
author
author
author
author
author
dc.contributor.none.fl_str_mv Ministerio de Economía y Competitividad (España)
Consejo Superior de Investigaciones Científicas [https://ror.org/02gfc7t72]
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
2021
2021
2021
dc.type.none.fl_str_mv info:eu-repo/semantics/article
http://purl.org/coar/resource_type/c_6501
Publisher's version
info:eu-repo/semantics/publishedVersion
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/10261/244718
url http://hdl.handle.net/10261/244718
dc.language.none.fl_str_mv Inglés
language_invalid_str_mv Inglés
dc.relation.none.fl_str_mv #PLACEHOLDER_PARENT_METADATA_VALUE#
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#PLACEHOLDER_PARENT_METADATA_VALUE#
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/BIO2014-53530-R
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/SAF2014-56716-REDT
info:eu-repo/grantAgreement/AEI/Plan Estatal de Investigación Científica y Técnica y de Innovación 2017-2020/RYC-2009-03948
http://doi.org/10.1371/journal. pgen.1006816
Sí
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
eu_rights_str_mv openAccess
dc.publisher.none.fl_str_mv Public Library of Science
publisher.none.fl_str_mv Public Library of Science
dc.source.none.fl_str_mv reponame:DIGITAL.CSIC. Repositorio Institucional del CSIC
instname:Consejo Superior de Investigaciones Científicas (CSIC)
instname_str Consejo Superior de Investigaciones Científicas (CSIC)
reponame_str DIGITAL.CSIC. Repositorio Institucional del CSIC
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