Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi

ABSTRACT Expression of capsular polysaccharides is a variable trait often associated with more-virulent forms of a bacterial species. For example, typhoid fever is caused by the capsulated Salmonella enterica serovar Typhi, while nontyphoidal Salmonella serovars associated with gastroenteritis are n...

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Autores principales:	Robert W. Crawford, Tamding Wangdi, Alanna M. Spees, Mariana N. Xavier, Renée M. Tsolis, Andreas J. Bäumler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2013
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/0d43b5ed8a194d1a869c0c88057b3cc4
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spelling	oai:doaj.org-article:0d43b5ed8a194d1a869c0c88057b3cc42021-11-15T15:43:08ZLoss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi10.1128/mBio.00232-132150-7511https://doaj.org/article/0d43b5ed8a194d1a869c0c88057b3cc42013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00232-13https://doaj.org/toc/2150-7511ABSTRACT Expression of capsular polysaccharides is a variable trait often associated with more-virulent forms of a bacterial species. For example, typhoid fever is caused by the capsulated Salmonella enterica serovar Typhi, while nontyphoidal Salmonella serovars associated with gastroenteritis are noncapsulated. Here we show that optimization of the immune evasive properties conferred by the virulence-associated (Vi) capsular polysaccharide involved an additional alteration to the cell envelope of S. Typhi, namely inactivation of the fepE gene, encoding the regulator of very-long O-antigen chains. Introduction of the capsule-encoding viaB locus into the nontyphoidal S. enterica serovar Typhimurium reduced complement deposition in vitro and intestinal inflammation in a mouse colitis model. However, both phenotypes were markedly enhanced when the viaB locus was introduced into an S. Typhimurium fepE mutant, which lacks very-long O-antigen chains. Collectively, these data suggest that during the evolution of the S. Typhi lineage, loss of very-long O-antigen chains by pseudogene formation was an adaptation to maximize the anti-inflammatory properties of the Vi capsular polysaccharide. IMPORTANCE Genomic comparison illustrates that acquisition of virulence factors by horizontal gene transfer is an important contributor to the evolution of enteric pathogens. Acquisition of complex virulence traits commonly involves horizontal transfer of a large gene cluster, and integration of the gene cluster into the host genome results in the formation of a pathogenicity island. Acquisition of the virulence-associated (Vi) capsular polysaccharide encoded by SPI7 (Salmonella pathogenicity island 7) was accompanied in the human-adapted Salmonella enterica serovar Typhi by inactivation of the fepE gene, encoding the regulator of very-long O-antigen chains. We show that the resulting loss of very-long O-antigen chains was an important mechanism for maximizing immune evasion mediated by the Vi capsular polysaccharide. These data suggest that successful incorporation of a capsular polysaccharide requires changes in the cell envelope of the hosting pathogen.Robert W. CrawfordTamding WangdiAlanna M. SpeesMariana N. XavierRenée M. TsolisAndreas J. BäumlerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 4, Iss 4 (2013)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Robert W. Crawford Tamding Wangdi Alanna M. Spees Mariana N. Xavier Renée M. Tsolis Andreas J. Bäumler Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi
description	ABSTRACT Expression of capsular polysaccharides is a variable trait often associated with more-virulent forms of a bacterial species. For example, typhoid fever is caused by the capsulated Salmonella enterica serovar Typhi, while nontyphoidal Salmonella serovars associated with gastroenteritis are noncapsulated. Here we show that optimization of the immune evasive properties conferred by the virulence-associated (Vi) capsular polysaccharide involved an additional alteration to the cell envelope of S. Typhi, namely inactivation of the fepE gene, encoding the regulator of very-long O-antigen chains. Introduction of the capsule-encoding viaB locus into the nontyphoidal S. enterica serovar Typhimurium reduced complement deposition in vitro and intestinal inflammation in a mouse colitis model. However, both phenotypes were markedly enhanced when the viaB locus was introduced into an S. Typhimurium fepE mutant, which lacks very-long O-antigen chains. Collectively, these data suggest that during the evolution of the S. Typhi lineage, loss of very-long O-antigen chains by pseudogene formation was an adaptation to maximize the anti-inflammatory properties of the Vi capsular polysaccharide. IMPORTANCE Genomic comparison illustrates that acquisition of virulence factors by horizontal gene transfer is an important contributor to the evolution of enteric pathogens. Acquisition of complex virulence traits commonly involves horizontal transfer of a large gene cluster, and integration of the gene cluster into the host genome results in the formation of a pathogenicity island. Acquisition of the virulence-associated (Vi) capsular polysaccharide encoded by SPI7 (Salmonella pathogenicity island 7) was accompanied in the human-adapted Salmonella enterica serovar Typhi by inactivation of the fepE gene, encoding the regulator of very-long O-antigen chains. We show that the resulting loss of very-long O-antigen chains was an important mechanism for maximizing immune evasion mediated by the Vi capsular polysaccharide. These data suggest that successful incorporation of a capsular polysaccharide requires changes in the cell envelope of the hosting pathogen.
format	article
author	Robert W. Crawford Tamding Wangdi Alanna M. Spees Mariana N. Xavier Renée M. Tsolis Andreas J. Bäumler
author_facet	Robert W. Crawford Tamding Wangdi Alanna M. Spees Mariana N. Xavier Renée M. Tsolis Andreas J. Bäumler
author_sort	Robert W. Crawford
title	Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi
title_short	Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi
title_full	Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi
title_fullStr	Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi
title_full_unstemmed	Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi
title_sort	loss of very-long o-antigen chains optimizes capsule-mediated immune evasion by <named-content content-type="genus-species">salmonella enterica</named-content> serovar typhi
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/0d43b5ed8a194d1a869c0c88057b3cc4
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Loss of Very-Long O-Antigen Chains Optimizes Capsule-Mediated Immune Evasion by <named-content content-type="genus-species">Salmonella enterica</named-content> Serovar Typhi

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