Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence

ABSTRACT The biogeography of the gut is diverse in its longitudinal axis, as well as within specific microenvironments. Differential oxygenation and nutrient composition drive the membership of microbial communities in these habitats. Moreover, enteric pathogens can orchestrate further modifications...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Kimberly M. Carlson-Banning, Vanessa Sperandio
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2016
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d695abcb8c63483bb38b9b01ae5768c2
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:d695abcb8c63483bb38b9b01ae5768c2
record_format	dspace
spelling	oai:doaj.org-article:d695abcb8c63483bb38b9b01ae5768c22021-11-15T15:50:15ZCatabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence10.1128/mBio.01852-162150-7511https://doaj.org/article/d695abcb8c63483bb38b9b01ae5768c22016-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01852-16https://doaj.org/toc/2150-7511ABSTRACT The biogeography of the gut is diverse in its longitudinal axis, as well as within specific microenvironments. Differential oxygenation and nutrient composition drive the membership of microbial communities in these habitats. Moreover, enteric pathogens can orchestrate further modifications to gain a competitive advantage toward host colonization. These pathogens are versatile and adept when exploiting the human colon. They expertly navigate complex environmental cues and interkingdom signaling to colonize and infect their hosts. Here we demonstrate how enterohemorrhagic Escherichia coli (EHEC) uses three sugar-sensing transcription factors, Cra, KdpE, and FusR, to exquisitely regulate the expression of virulence factors associated with its type III secretion system (T3SS) when exposed to various oxygen concentrations. We also explored the effect of mucin-derived nonpreferred carbon sources on EHEC growth and expression of virulence genes. Taken together, the results show that EHEC represses the expression of its T3SS when oxygen is absent, mimicking the largely anaerobic lumen, and activates its T3SS when oxygen is available through Cra. In addition, when EHEC senses mucin-derived sugars heavily present in the O-linked and N-linked glycans of the large intestine, virulence gene expression is initiated. Sugars derived from pectin, a complex plant polysaccharide digested in the large intestine, also increased virulence gene expression. Not only does EHEC sense host- and microbiota-derived interkingdom signals, it also uses oxygen availability and mucin-derived sugars liberated by the microbiota to stimulate expression of the T3SS. This precision in gene regulation allows EHEC to be an efficient pathogen with an extremely low infectious dose. IMPORTANCE Enteric pathogens have to be crafty when interpreting multiple environmental cues to successfully establish themselves within complex and diverse gut microenvironments. Differences in oxygen tension and nutrient composition determine the biogeography of the gut microbiota and provide unique niches that can be exploited by enteric pathogens. EHEC is an enteric pathogen that colonizes the colon and causes outbreaks of bloody diarrhea and hemolytic-uremic syndrome worldwide. It has a very low infectious dose, which requires it to be an extremely effective pathogen. Hence, here we show that EHEC senses multiple sugar sources and oxygen levels to optimally control the expression of its virulence repertoire. This exquisite regulatory control equips EHEC to sense different intestinal compartments to colonize the host.Kimberly M. Carlson-BanningVanessa SperandioAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 7, Iss 6 (2016)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Kimberly M. Carlson-Banning Vanessa Sperandio Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence
description	ABSTRACT The biogeography of the gut is diverse in its longitudinal axis, as well as within specific microenvironments. Differential oxygenation and nutrient composition drive the membership of microbial communities in these habitats. Moreover, enteric pathogens can orchestrate further modifications to gain a competitive advantage toward host colonization. These pathogens are versatile and adept when exploiting the human colon. They expertly navigate complex environmental cues and interkingdom signaling to colonize and infect their hosts. Here we demonstrate how enterohemorrhagic Escherichia coli (EHEC) uses three sugar-sensing transcription factors, Cra, KdpE, and FusR, to exquisitely regulate the expression of virulence factors associated with its type III secretion system (T3SS) when exposed to various oxygen concentrations. We also explored the effect of mucin-derived nonpreferred carbon sources on EHEC growth and expression of virulence genes. Taken together, the results show that EHEC represses the expression of its T3SS when oxygen is absent, mimicking the largely anaerobic lumen, and activates its T3SS when oxygen is available through Cra. In addition, when EHEC senses mucin-derived sugars heavily present in the O-linked and N-linked glycans of the large intestine, virulence gene expression is initiated. Sugars derived from pectin, a complex plant polysaccharide digested in the large intestine, also increased virulence gene expression. Not only does EHEC sense host- and microbiota-derived interkingdom signals, it also uses oxygen availability and mucin-derived sugars liberated by the microbiota to stimulate expression of the T3SS. This precision in gene regulation allows EHEC to be an efficient pathogen with an extremely low infectious dose. IMPORTANCE Enteric pathogens have to be crafty when interpreting multiple environmental cues to successfully establish themselves within complex and diverse gut microenvironments. Differences in oxygen tension and nutrient composition determine the biogeography of the gut microbiota and provide unique niches that can be exploited by enteric pathogens. EHEC is an enteric pathogen that colonizes the colon and causes outbreaks of bloody diarrhea and hemolytic-uremic syndrome worldwide. It has a very low infectious dose, which requires it to be an extremely effective pathogen. Hence, here we show that EHEC senses multiple sugar sources and oxygen levels to optimally control the expression of its virulence repertoire. This exquisite regulatory control equips EHEC to sense different intestinal compartments to colonize the host.
format	article
author	Kimberly M. Carlson-Banning Vanessa Sperandio
author_facet	Kimberly M. Carlson-Banning Vanessa Sperandio
author_sort	Kimberly M. Carlson-Banning
title	Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence
title_short	Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence
title_full	Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence
title_fullStr	Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence
title_full_unstemmed	Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence
title_sort	catabolite and oxygen regulation of enterohemorrhagic <named-content content-type="genus-species">escherichia coli</named-content> virulence
publisher	American Society for Microbiology
publishDate	2016
url	https://doaj.org/article/d695abcb8c63483bb38b9b01ae5768c2
work_keys_str_mv	AT kimberlymcarlsonbanning cataboliteandoxygenregulationofenterohemorrhagicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentvirulence AT vanessasperandio cataboliteandoxygenregulationofenterohemorrhagicnamedcontentcontenttypegenusspeciesescherichiacolinamedcontentvirulence
_version_	1718427489320042496

Catabolite and Oxygen Regulation of Enterohemorrhagic <named-content content-type="genus-species">Escherichia coli</named-content> Virulence

Ejemplares similares