Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration

ABSTRACT Treatment with streptomycin enhances the growth of human commensal Escherichia coli isolates in the mouse intestine, suggesting that the resident microbial community (microbiota) can inhibit the growth of invading microbes, a phenomenon known as “colonization resistance.” However, the preci...

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Autores principales:	Alanna M. Spees, Tamding Wangdi, Christopher A. Lopez, Dawn D. Kingsbury, Mariana N. Xavier, Sebastian E. Winter, 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/5dbd0960cb4647b995e9e6b187a5c991
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spelling	oai:doaj.org-article:5dbd0960cb4647b995e9e6b187a5c9912021-11-15T15:43:09ZStreptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration10.1128/mBio.00430-132150-7511https://doaj.org/article/5dbd0960cb4647b995e9e6b187a5c9912013-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00430-13https://doaj.org/toc/2150-7511ABSTRACT Treatment with streptomycin enhances the growth of human commensal Escherichia coli isolates in the mouse intestine, suggesting that the resident microbial community (microbiota) can inhibit the growth of invading microbes, a phenomenon known as “colonization resistance.” However, the precise mechanisms by which streptomycin treatment lowers colonization resistance remain obscure. Here we show that streptomycin treatment rendered mice more susceptible to the development of chemically induced colitis, raising the possibility that the antibiotic might lower colonization resistance by changing mucosal immune responses rather than by preventing microbe-microbe interactions. Investigation of the underlying mechanism revealed a mild inflammatory infiltrate in the cecal mucosa of streptomycin-treated mice, which was accompanied by elevated expression of Nos2, the gene that encodes inducible nitric oxide synthase. In turn, this inflammatory response enhanced the luminal growth of E. coli by nitrate respiration in a Nos2-dependent fashion. These data identify low-level intestinal inflammation as one of the factors responsible for the loss of resistance to E. coli colonization after streptomycin treatment. IMPORTANCE Our intestine is host to a complex microbial community that confers benefits by educating the immune system and providing niche protection. Perturbation of intestinal communities by streptomycin treatment lowers “colonization resistance” through unknown mechanisms. Here we show that streptomycin increases the inflammatory tone of the intestinal mucosa, thereby making the bowel more susceptible to dextran sulfate sodium treatment and boosting the Nos2-dependent growth of commensal Escherichia coli by nitrate respiration. These data point to the generation of alternative electron acceptors as a by-product of the inflammatory host response as an important factor responsible for lowering resistance to colonization by facultative anaerobic bacteria such as E. coli.Alanna M. SpeesTamding WangdiChristopher A. LopezDawn D. KingsburyMariana N. XavierSebastian E. WinterRenée 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 Alanna M. Spees Tamding Wangdi Christopher A. Lopez Dawn D. Kingsbury Mariana N. Xavier Sebastian E. Winter Renée M. Tsolis Andreas J. Bäumler Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration
description	ABSTRACT Treatment with streptomycin enhances the growth of human commensal Escherichia coli isolates in the mouse intestine, suggesting that the resident microbial community (microbiota) can inhibit the growth of invading microbes, a phenomenon known as “colonization resistance.” However, the precise mechanisms by which streptomycin treatment lowers colonization resistance remain obscure. Here we show that streptomycin treatment rendered mice more susceptible to the development of chemically induced colitis, raising the possibility that the antibiotic might lower colonization resistance by changing mucosal immune responses rather than by preventing microbe-microbe interactions. Investigation of the underlying mechanism revealed a mild inflammatory infiltrate in the cecal mucosa of streptomycin-treated mice, which was accompanied by elevated expression of Nos2, the gene that encodes inducible nitric oxide synthase. In turn, this inflammatory response enhanced the luminal growth of E. coli by nitrate respiration in a Nos2-dependent fashion. These data identify low-level intestinal inflammation as one of the factors responsible for the loss of resistance to E. coli colonization after streptomycin treatment. IMPORTANCE Our intestine is host to a complex microbial community that confers benefits by educating the immune system and providing niche protection. Perturbation of intestinal communities by streptomycin treatment lowers “colonization resistance” through unknown mechanisms. Here we show that streptomycin increases the inflammatory tone of the intestinal mucosa, thereby making the bowel more susceptible to dextran sulfate sodium treatment and boosting the Nos2-dependent growth of commensal Escherichia coli by nitrate respiration. These data point to the generation of alternative electron acceptors as a by-product of the inflammatory host response as an important factor responsible for lowering resistance to colonization by facultative anaerobic bacteria such as E. coli.
format	article
author	Alanna M. Spees Tamding Wangdi Christopher A. Lopez Dawn D. Kingsbury Mariana N. Xavier Sebastian E. Winter Renée M. Tsolis Andreas J. Bäumler
author_facet	Alanna M. Spees Tamding Wangdi Christopher A. Lopez Dawn D. Kingsbury Mariana N. Xavier Sebastian E. Winter Renée M. Tsolis Andreas J. Bäumler
author_sort	Alanna M. Spees
title	Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration
title_short	Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration
title_full	Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration
title_fullStr	Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration
title_full_unstemmed	Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration
title_sort	streptomycin-induced inflammation enhances <named-content content-type="genus-species">escherichia coli</named-content> gut colonization through nitrate respiration
publisher	American Society for Microbiology
publishDate	2013
url	https://doaj.org/article/5dbd0960cb4647b995e9e6b187a5c991
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Streptomycin-Induced Inflammation Enhances <named-content content-type="genus-species">Escherichia coli</named-content> Gut Colonization Through Nitrate Respiration

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