Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration

ABSTRACT Information on how emerging pathogens can invade and persist and spread within host populations remains sparse. In the 1980s, a multidrug-resistant Salmonella enterica serotype Typhimurium clone lysogenized by a bacteriophage carrying the sopE virulence gene caused an epidemic among cattle...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Christopher A. Lopez, Sebastian E. Winter, Fabian Rivera-Chávez, Mariana N. Xavier, Victor Poon, Sean-Paul Nuccio, Renée M. Tsolis, Andreas J. Bäumler
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2012
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/a4eefda001b3435fade47546c140fa28
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:a4eefda001b3435fade47546c140fa28
record_format	dspace
spelling	oai:doaj.org-article:a4eefda001b3435fade47546c140fa282021-11-15T15:39:02ZPhage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration10.1128/mBio.00143-122150-7511https://doaj.org/article/a4eefda001b3435fade47546c140fa282012-07-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00143-12https://doaj.org/toc/2150-7511ABSTRACT Information on how emerging pathogens can invade and persist and spread within host populations remains sparse. In the 1980s, a multidrug-resistant Salmonella enterica serotype Typhimurium clone lysogenized by a bacteriophage carrying the sopE virulence gene caused an epidemic among cattle and humans in Europe. Here we show that phage-mediated horizontal transfer of the sopE gene enhances the production of host-derived nitrate, an energetically highly valuable electron acceptor, in a mouse colitis model. In turn, nitrate fuels a bloom of S. Typhimurium in the gut lumen through anaerobic nitrate respiration while suppressing genes for the utilization of energetically inferior electron acceptors such as tetrathionate. Through this mechanism, horizontal transfer of sopE can enhance the fitness of S. Typhimurium, resulting in its significantly increased abundance in the feces. IMPORTANCE During gastroenteritis, Salmonella enterica serotype Typhimurium can use tetrathionate respiration to edge out competing microbes in the gut lumen. However, the concept that tetrathionate respiration confers a growth benefit in the inflamed gut is not broadly applicable to other host-pathogen combinations because tetrathionate respiration is a signature trait used to differentiate Salmonella serotypes from most other members of the family Enterobacteriaceae. Here we show that by acquiring the phage-carried sopE gene, S. Typhimurium can drive the host to generate an additional respiratory electron acceptor, nitrate. Nitrate suppresses genes for the utilization of energetically inferior electron acceptors such as tetrathionate while enhancing the luminal growth of S. Typhimurium through anaerobic nitrate respiration. Pathways for anaerobic nitrate respiration are widely conserved among members of the family Enterobacteriaceae, thereby making our observations relevant to other enteric pathogens whose relative abundance in the intestinal lumen increases during infection.Christopher A. LopezSebastian E. WinterFabian Rivera-ChávezMariana N. XavierVictor PoonSean-Paul NuccioRenée M. TsolisAndreas J. BäumlerAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 3, Iss 3 (2012)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Christopher A. Lopez Sebastian E. Winter Fabian Rivera-Chávez Mariana N. Xavier Victor Poon Sean-Paul Nuccio Renée M. Tsolis Andreas J. Bäumler Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration
description	ABSTRACT Information on how emerging pathogens can invade and persist and spread within host populations remains sparse. In the 1980s, a multidrug-resistant Salmonella enterica serotype Typhimurium clone lysogenized by a bacteriophage carrying the sopE virulence gene caused an epidemic among cattle and humans in Europe. Here we show that phage-mediated horizontal transfer of the sopE gene enhances the production of host-derived nitrate, an energetically highly valuable electron acceptor, in a mouse colitis model. In turn, nitrate fuels a bloom of S. Typhimurium in the gut lumen through anaerobic nitrate respiration while suppressing genes for the utilization of energetically inferior electron acceptors such as tetrathionate. Through this mechanism, horizontal transfer of sopE can enhance the fitness of S. Typhimurium, resulting in its significantly increased abundance in the feces. IMPORTANCE During gastroenteritis, Salmonella enterica serotype Typhimurium can use tetrathionate respiration to edge out competing microbes in the gut lumen. However, the concept that tetrathionate respiration confers a growth benefit in the inflamed gut is not broadly applicable to other host-pathogen combinations because tetrathionate respiration is a signature trait used to differentiate Salmonella serotypes from most other members of the family Enterobacteriaceae. Here we show that by acquiring the phage-carried sopE gene, S. Typhimurium can drive the host to generate an additional respiratory electron acceptor, nitrate. Nitrate suppresses genes for the utilization of energetically inferior electron acceptors such as tetrathionate while enhancing the luminal growth of S. Typhimurium through anaerobic nitrate respiration. Pathways for anaerobic nitrate respiration are widely conserved among members of the family Enterobacteriaceae, thereby making our observations relevant to other enteric pathogens whose relative abundance in the intestinal lumen increases during infection.
format	article
author	Christopher A. Lopez Sebastian E. Winter Fabian Rivera-Chávez Mariana N. Xavier Victor Poon Sean-Paul Nuccio Renée M. Tsolis Andreas J. Bäumler
author_facet	Christopher A. Lopez Sebastian E. Winter Fabian Rivera-Chávez Mariana N. Xavier Victor Poon Sean-Paul Nuccio Renée M. Tsolis Andreas J. Bäumler
author_sort	Christopher A. Lopez
title	Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration
title_short	Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration
title_full	Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration
title_fullStr	Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration
title_full_unstemmed	Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration
title_sort	phage-mediated acquisition of a type iii secreted effector protein boosts growth of <italic toggle="yes">salmonella</italic> by nitrate respiration
publisher	American Society for Microbiology
publishDate	2012
url	https://doaj.org/article/a4eefda001b3435fade47546c140fa28
work_keys_str_mv	AT christopheralopez phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT sebastianewinter phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT fabianriverachavez phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT mariananxavier phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT victorpoon phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT seanpaulnuccio phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT reneemtsolis phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration AT andreasjbaumler phagemediatedacquisitionofatypeiiisecretedeffectorproteinboostsgrowthofitalictoggleyessalmonellaitalicbynitraterespiration
_version_	1718427784424980480

Phage-Mediated Acquisition of a Type III Secreted Effector Protein Boosts Growth of <italic toggle="yes">Salmonella</italic> by Nitrate Respiration

Ejemplares similares