Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion

ABSTRACT Salmonella enterica serovar Typhimurium can cross the epithelial barrier using either the invasion-associated type III secretion system (T3SS-1) or a T3SS-1-independent mechanism that remains poorly characterized. Here we show that flagellum-mediated motility supported a T3SS-1-independent...

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Autores principales:	Fabian Rivera-Chávez, Christopher A. Lopez, Lillian F. Zhang, Lucía García-Pastor, Alfredo Chávez-Arroyo, Kristen L. Lokken, Renée M. Tsolis, Sebastian E. Winter, Andreas J. Bäumler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/11b2dad8eed5433db76d3ef18a19d813
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spelling	oai:doaj.org-article:11b2dad8eed5433db76d3ef18a19d8132021-11-15T15:50:18ZEnergy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion10.1128/mBio.00960-162150-7511https://doaj.org/article/11b2dad8eed5433db76d3ef18a19d8132016-09-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00960-16https://doaj.org/toc/2150-7511ABSTRACT Salmonella enterica serovar Typhimurium can cross the epithelial barrier using either the invasion-associated type III secretion system (T3SS-1) or a T3SS-1-independent mechanism that remains poorly characterized. Here we show that flagellum-mediated motility supported a T3SS-1-independent pathway for entering ileal Peyer’s patches in the mouse model. Flagellum-dependent invasion of Peyer’s patches required energy taxis toward nitrate, which was mediated by the methyl-accepting chemotaxis protein (MCP) Tsr. Generation of nitrate in the intestinal lumen required inducible nitric oxide synthase (iNOS), which was synthesized constitutively in the mucosa of the terminal ileum but not in the jejunum, duodenum, or cecum. Tsr-mediated invasion of ileal Peyer’s patches was abrogated in mice deficient for Nos2, the gene encoding iNOS. We conclude that Tsr-mediated energy taxis enables S. Typhimurium to migrate toward the intestinal epithelium by sensing host-derived nitrate, thereby contributing to invasion of Peyer’s patches. IMPORTANCE Nontyphoidal Salmonella serovars, such as S. enterica serovar Typhimurium, are a common cause of gastroenteritis in immunocompetent individuals but can also cause bacteremia in immunocompromised individuals. While the invasion-associated type III secretion system (T3SS-1) is important for entry, S. Typhimurium strains lacking a functional T3SS-1 can still cross the intestinal epithelium and cause a disseminated lethal infection in mice. Here we observed that flagellum-mediated motility and chemotaxis contributed to a T3SS-1-independent pathway for invasion and systemic dissemination to the spleen. This pathway required the methyl-accepting chemotaxis protein (MCP) Tsr and energy taxis toward host-derived nitrate, which we found to be generated by inducible nitric oxide synthase (iNOS) in the ileal mucosa prior to infection. Collectively, our data suggest that S. Typhimurium enhances invasion by actively migrating toward the intestinal epithelium along a gradient of host-derived nitrate emanating from the mucosal surface of the ileum.Fabian Rivera-ChávezChristopher A. LopezLillian F. ZhangLucía García-PastorAlfredo Chávez-ArroyoKristen L. LokkenRenée M. TsolisSebastian E. WinterAndreas J. BäumlerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 4 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Fabian Rivera-Chávez Christopher A. Lopez Lillian F. Zhang Lucía García-Pastor Alfredo Chávez-Arroyo Kristen L. Lokken Renée M. Tsolis Sebastian E. Winter Andreas J. Bäumler Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion
description	ABSTRACT Salmonella enterica serovar Typhimurium can cross the epithelial barrier using either the invasion-associated type III secretion system (T3SS-1) or a T3SS-1-independent mechanism that remains poorly characterized. Here we show that flagellum-mediated motility supported a T3SS-1-independent pathway for entering ileal Peyer’s patches in the mouse model. Flagellum-dependent invasion of Peyer’s patches required energy taxis toward nitrate, which was mediated by the methyl-accepting chemotaxis protein (MCP) Tsr. Generation of nitrate in the intestinal lumen required inducible nitric oxide synthase (iNOS), which was synthesized constitutively in the mucosa of the terminal ileum but not in the jejunum, duodenum, or cecum. Tsr-mediated invasion of ileal Peyer’s patches was abrogated in mice deficient for Nos2, the gene encoding iNOS. We conclude that Tsr-mediated energy taxis enables S. Typhimurium to migrate toward the intestinal epithelium by sensing host-derived nitrate, thereby contributing to invasion of Peyer’s patches. IMPORTANCE Nontyphoidal Salmonella serovars, such as S. enterica serovar Typhimurium, are a common cause of gastroenteritis in immunocompetent individuals but can also cause bacteremia in immunocompromised individuals. While the invasion-associated type III secretion system (T3SS-1) is important for entry, S. Typhimurium strains lacking a functional T3SS-1 can still cross the intestinal epithelium and cause a disseminated lethal infection in mice. Here we observed that flagellum-mediated motility and chemotaxis contributed to a T3SS-1-independent pathway for invasion and systemic dissemination to the spleen. This pathway required the methyl-accepting chemotaxis protein (MCP) Tsr and energy taxis toward host-derived nitrate, which we found to be generated by inducible nitric oxide synthase (iNOS) in the ileal mucosa prior to infection. Collectively, our data suggest that S. Typhimurium enhances invasion by actively migrating toward the intestinal epithelium along a gradient of host-derived nitrate emanating from the mucosal surface of the ileum.
format	article
author	Fabian Rivera-Chávez Christopher A. Lopez Lillian F. Zhang Lucía García-Pastor Alfredo Chávez-Arroyo Kristen L. Lokken Renée M. Tsolis Sebastian E. Winter Andreas J. Bäumler
author_facet	Fabian Rivera-Chávez Christopher A. Lopez Lillian F. Zhang Lucía García-Pastor Alfredo Chávez-Arroyo Kristen L. Lokken Renée M. Tsolis Sebastian E. Winter Andreas J. Bäumler
author_sort	Fabian Rivera-Chávez
title	Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion
title_short	Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion
title_full	Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion
title_fullStr	Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion
title_full_unstemmed	Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion
title_sort	energy taxis toward host-derived nitrate supports a <italic toggle="yes">salmonella</italic> pathogenicity island 1-independent mechanism of invasion
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/11b2dad8eed5433db76d3ef18a19d813
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Energy Taxis toward Host-Derived Nitrate Supports a <italic toggle="yes">Salmonella</italic> Pathogenicity Island 1-Independent Mechanism of Invasion

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