Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein

ABSTRACT The HUαE38K, V42L mutant of the bacterial histone-like protein HU causes a major change in the transcription profile of the commensal organism Escherichia coli K-12 (Kar S, Edgar R, Adhya S, Proc. Natl. Acad. Sci. U. S. A. 102:16397–16402, 2005). Among the upregulated genes are several rela...

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Autores principales:	Preeti Koli, Sudhanshu Sudan, David Fitzgerald, Sankar Adhya, Sudeshna Kar
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Lenguaje:	EN
Publicado:	American Society for Microbiology 2011
Materias:	Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/855346676f54430897e7c96236b49420
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spelling	oai:doaj.org-article:855346676f54430897e7c96236b494202021-11-15T15:38:57ZConversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein10.1128/mBio.00182-112150-7511https://doaj.org/article/855346676f54430897e7c96236b494202011-11-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00182-11https://doaj.org/toc/2150-7511ABSTRACT The HUαE38K, V42L mutant of the bacterial histone-like protein HU causes a major change in the transcription profile of the commensal organism Escherichia coli K-12 (Kar S, Edgar R, Adhya S, Proc. Natl. Acad. Sci. U. S. A. 102:16397–16402, 2005). Among the upregulated genes are several related to pathogenic interactions with mammalian cells, as evidenced by the expression of curli fibers, Ivy, and hemolysin E. When E. coli K-12/ HUαE38K, V42L was added to Int-407 cells, there was host cell invasion, phagosomal disruption, and intracellular replication. The invasive trait was also retained in a murine ileal loop model and intestinal explant assays. In addition to invasion, the internalized bacteria caused a novel subversion of host cell apoptosis through modification and regulation of the BH3-only proteins BimEL and Puma. Changes in the transcription profile were attributed to positive supercoiling of DNA leading to the altered availability of relevant promoters. Using the E. coli K-12/HUαE38K, V42L variant as a model, we propose that traditional commensal E. coli can adopt an invasive lifestyle through reprogramming its cellular transcription, without gross genetic changes. IMPORTANCE Escherichia coli K-12 is well established as a benign laboratory strain and a human intestinal commensal. Recent evidences, however, indicate that the typical noninvasive nature of resident E. coli can be reversed under specific circumstances even in the absence of any major genomic flux. We previously engineered an E. coli strain with a mutant histone-like protein, HU, which exhibited significant changes in nucleoid organization and global transcription. Here we showed that the changes induced by the mutant HU have critical functional consequences: from a strict extracellular existence, the mutant E. coli adopts an almost obligate intracellular lifestyle. The internalized E. coli exhibits many of the prototypical characteristics of traditional intracellular bacteria, like phagosomal escape, intracellular replication, and subversion of host cell apoptosis. We suggest that E. coli K-12 can switch between widely divergent lifestyles in relation to mammalian host cells by reprogramming its cellular transcription program and without gross changes in its genomic content.Preeti KoliSudhanshu SudanDavid FitzgeraldSankar AdhyaSudeshna KarAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 2, Iss 5 (2011)
institution	DOAJ
collection	DOAJ
language	EN
topic	Microbiology QR1-502
spellingShingle	Microbiology QR1-502 Preeti Koli Sudhanshu Sudan David Fitzgerald Sankar Adhya Sudeshna Kar Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein
description	ABSTRACT The HUαE38K, V42L mutant of the bacterial histone-like protein HU causes a major change in the transcription profile of the commensal organism Escherichia coli K-12 (Kar S, Edgar R, Adhya S, Proc. Natl. Acad. Sci. U. S. A. 102:16397–16402, 2005). Among the upregulated genes are several related to pathogenic interactions with mammalian cells, as evidenced by the expression of curli fibers, Ivy, and hemolysin E. When E. coli K-12/ HUαE38K, V42L was added to Int-407 cells, there was host cell invasion, phagosomal disruption, and intracellular replication. The invasive trait was also retained in a murine ileal loop model and intestinal explant assays. In addition to invasion, the internalized bacteria caused a novel subversion of host cell apoptosis through modification and regulation of the BH3-only proteins BimEL and Puma. Changes in the transcription profile were attributed to positive supercoiling of DNA leading to the altered availability of relevant promoters. Using the E. coli K-12/HUαE38K, V42L variant as a model, we propose that traditional commensal E. coli can adopt an invasive lifestyle through reprogramming its cellular transcription, without gross genetic changes. IMPORTANCE Escherichia coli K-12 is well established as a benign laboratory strain and a human intestinal commensal. Recent evidences, however, indicate that the typical noninvasive nature of resident E. coli can be reversed under specific circumstances even in the absence of any major genomic flux. We previously engineered an E. coli strain with a mutant histone-like protein, HU, which exhibited significant changes in nucleoid organization and global transcription. Here we showed that the changes induced by the mutant HU have critical functional consequences: from a strict extracellular existence, the mutant E. coli adopts an almost obligate intracellular lifestyle. The internalized E. coli exhibits many of the prototypical characteristics of traditional intracellular bacteria, like phagosomal escape, intracellular replication, and subversion of host cell apoptosis. We suggest that E. coli K-12 can switch between widely divergent lifestyles in relation to mammalian host cells by reprogramming its cellular transcription program and without gross changes in its genomic content.
format	article
author	Preeti Koli Sudhanshu Sudan David Fitzgerald Sankar Adhya Sudeshna Kar
author_facet	Preeti Koli Sudhanshu Sudan David Fitzgerald Sankar Adhya Sudeshna Kar
author_sort	Preeti Koli
title	Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein
title_short	Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein
title_full	Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein
title_fullStr	Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein
title_full_unstemmed	Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein
title_sort	conversion of commensal <named-content content-type="genus-species">escherichia coli</named-content> k-12 to an invasive form via expression of a mutant histone-like protein
publisher	American Society for Microbiology
publishDate	2011
url	https://doaj.org/article/855346676f54430897e7c96236b49420
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Conversion of Commensal <named-content content-type="genus-species">Escherichia coli</named-content> K-12 to an Invasive Form via Expression of a Mutant Histone-Like Protein

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