Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli

Summary: Propionic acid (PA) is a bacterium-derived intestinal antimicrobial and immune modulator used widely in food production and agriculture. Passage of Crohn’s disease-associated adherent-invasive Escherichia coli (AIEC) through a murine model, in which intestinal PA levels are increased to mim...

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Main Authors: Michael J. Ormsby, Síle A. Johnson, Nuria Carpena, Lynsey M. Meikle, Robert J. Goldstone, Anne McIntosh, Hannah M. Wessel, Heather E. Hulme, Ceilidh C. McConnachie, James P.R. Connolly, Andrew J. Roe, Conor Hasson, Joseph Boyd, Eamonn Fitzgerald, Konstantinos Gerasimidis, Douglas Morrison, Georgina L. Hold, Richard Hansen, Daniel Walker, David G.E. Smith, Daniel M. Wall
Format: Article
Language:English
Published: Elsevier 2020-02-01
Series:Cell Reports
Online Access:http://www.sciencedirect.com/science/article/pii/S2211124720301030
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author Michael J. Ormsby
Síle A. Johnson
Nuria Carpena
Lynsey M. Meikle
Robert J. Goldstone
Anne McIntosh
Hannah M. Wessel
Heather E. Hulme
Ceilidh C. McConnachie
James P.R. Connolly
Andrew J. Roe
Conor Hasson
Joseph Boyd
Eamonn Fitzgerald
Konstantinos Gerasimidis
Douglas Morrison
Georgina L. Hold
Richard Hansen
Daniel Walker
David G.E. Smith
Daniel M. Wall
spellingShingle Michael J. Ormsby
Síle A. Johnson
Nuria Carpena
Lynsey M. Meikle
Robert J. Goldstone
Anne McIntosh
Hannah M. Wessel
Heather E. Hulme
Ceilidh C. McConnachie
James P.R. Connolly
Andrew J. Roe
Conor Hasson
Joseph Boyd
Eamonn Fitzgerald
Konstantinos Gerasimidis
Douglas Morrison
Georgina L. Hold
Richard Hansen
Daniel Walker
David G.E. Smith
Daniel M. Wall
Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli
Cell Reports
author_facet Michael J. Ormsby
Síle A. Johnson
Nuria Carpena
Lynsey M. Meikle
Robert J. Goldstone
Anne McIntosh
Hannah M. Wessel
Heather E. Hulme
Ceilidh C. McConnachie
James P.R. Connolly
Andrew J. Roe
Conor Hasson
Joseph Boyd
Eamonn Fitzgerald
Konstantinos Gerasimidis
Douglas Morrison
Georgina L. Hold
Richard Hansen
Daniel Walker
David G.E. Smith
Daniel M. Wall
author_sort Michael J. Ormsby
title Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli
title_short Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli
title_full Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli
title_fullStr Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli
title_full_unstemmed Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coli
title_sort propionic acid promotes the virulent phenotype of crohn’s disease-associated adherent-invasive escherichia coli
publisher Elsevier
series Cell Reports
issn 2211-1247
publishDate 2020-02-01
description Summary: Propionic acid (PA) is a bacterium-derived intestinal antimicrobial and immune modulator used widely in food production and agriculture. Passage of Crohn’s disease-associated adherent-invasive Escherichia coli (AIEC) through a murine model, in which intestinal PA levels are increased to mimic the human intestine, leads to the recovery of AIEC with significantly increased virulence. Similar phenotypic changes are observed outside the murine model when AIEC is grown in culture with PA as the sole carbon source; such PA exposure also results in AIEC that persists at 20-fold higher levels in vivo. RNA sequencing identifies an upregulation of genes involved in biofilm formation, stress response, metabolism, membrane integrity, and alternative carbon source utilization. PA exposure also increases virulence in a number of E. coli isolates from Crohn’s disease patients. Removal of PA is sufficient to reverse these phenotypic changes. Our data indicate that exposure to PA results in AIEC resistance and increased virulence in its presence. : The short chain fatty acid propionic acid is a bacterium-derived human intestinal antimicrobial and immune modulator used widely in Western food production and agriculture. Here, Ormsby et al. demonstrate that exposure to propionic acid induces virulence-associated phenotypic changes in Crohn’s disease-associated adherent-invasive Escherichia coli (AIEC). Keywords: adherent-invasive E. coli, Crohn's disease, short chain fatty acid, propionic acid
url http://www.sciencedirect.com/science/article/pii/S2211124720301030
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spelling doaj-c67d7647d1fe4b1ebd8cd8c4b45171352020-11-25T02:27:39ZengElsevierCell Reports2211-12472020-02-0130722972305.e5Propionic Acid Promotes the Virulent Phenotype of Crohn’s Disease-Associated Adherent-Invasive Escherichia coliMichael J. Ormsby0Síle A. Johnson1Nuria Carpena2Lynsey M. Meikle3Robert J. Goldstone4Anne McIntosh5Hannah M. Wessel6Heather E. Hulme7Ceilidh C. McConnachie8James P.R. Connolly9Andrew J. Roe10Conor Hasson11Joseph Boyd12Eamonn Fitzgerald13Konstantinos Gerasimidis14Douglas Morrison15Georgina L. Hold16Richard Hansen17Daniel Walker18David G.E. Smith19Daniel M. Wall20Institute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Biological Chemistry, Biophysics and Bioengineering, Heriot-Watt University, Edinburgh EH14 4AS, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UK; Institute for Cell and Molecular Biosciences, Newcastle University, Newcastle-upon-Tyne NE2 4HH, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKHuman Nutrition, School of Medicine, College of Medical Veterinary and Life Sciences, University of Glasgow, Glasgow Royal Infirmary, Glasgow G31 2ER, UKScottish Universities Environmental Research Centre, University of Glasgow, Glasgow G75 0QF, UKMicrobiome Research Centre, St George and Sutherland Clinical School, University of New South Wales, Sydney, NSW, AustraliaDepartment of Paediatric Gastroenterology, Hepatology and Nutrition, Royal Hospital for Children, 1345 Govan Road, Glasgow G51 4TF, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UKInstitute of Biological Chemistry, Biophysics and Bioengineering, Heriot-Watt University, Edinburgh EH14 4AS, UKInstitute of Infection, Immunity and Inflammation, College of Medical, Veterinary and Life Sciences, Sir Graeme Davies Building, University of Glasgow, Glasgow G12 8TA, UK; Corresponding authorSummary: Propionic acid (PA) is a bacterium-derived intestinal antimicrobial and immune modulator used widely in food production and agriculture. Passage of Crohn’s disease-associated adherent-invasive Escherichia coli (AIEC) through a murine model, in which intestinal PA levels are increased to mimic the human intestine, leads to the recovery of AIEC with significantly increased virulence. Similar phenotypic changes are observed outside the murine model when AIEC is grown in culture with PA as the sole carbon source; such PA exposure also results in AIEC that persists at 20-fold higher levels in vivo. RNA sequencing identifies an upregulation of genes involved in biofilm formation, stress response, metabolism, membrane integrity, and alternative carbon source utilization. PA exposure also increases virulence in a number of E. coli isolates from Crohn’s disease patients. Removal of PA is sufficient to reverse these phenotypic changes. Our data indicate that exposure to PA results in AIEC resistance and increased virulence in its presence. : The short chain fatty acid propionic acid is a bacterium-derived human intestinal antimicrobial and immune modulator used widely in Western food production and agriculture. Here, Ormsby et al. demonstrate that exposure to propionic acid induces virulence-associated phenotypic changes in Crohn’s disease-associated adherent-invasive Escherichia coli (AIEC). Keywords: adherent-invasive E. coli, Crohn's disease, short chain fatty acid, propionic acidhttp://www.sciencedirect.com/science/article/pii/S2211124720301030