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

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

doi:10.1016/j.celrep.2020.01.078

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

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. SmithDaniel M. Wall

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Abstract

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.

Original language	English
Pages (from-to)	2297-2305.e5
Number of pages	15
Journal	Cell Reports
Volume	30
Issue number	7
DOIs	https://doi.org/10.1016/j.celrep.2020.01.078
Publication status	Published - 18 Feb 2020

Keywords

Crohn's disease
adherent-invasive E. coli
propionic acid
short chain fatty acid

ASJC Scopus subject areas

General Biochemistry,Genetics and Molecular Biology

UN SDGs

This output contributes to the following UN Sustainable Development Goals (SDGs)

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Ormsby, M. J., Johnson, S. A., Carpena, N., Meikle, L. M., Goldstone, R. J., McIntosh, A., Wessel, H. M., Hulme, H. E., McConnachie, C. C., Connolly, J. P. R., Roe, A. J., Hasson, C., Boyd, J., Fitzgerald, E., Gerasimidis, K., Morrison, D., Hold, G. L., Hansen, R., Walker, D., ... Wall, D. M. (2020). Propionic Acid Promotes the Virulent Phenotype of Crohn's Disease-Associated Adherent-Invasive Escherichia coli. Cell Reports, 30(7), 2297-2305.e5. https://doi.org/10.1016/j.celrep.2020.01.078

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title = "Propionic Acid Promotes the Virulent Phenotype of Crohn's Disease-Associated Adherent-Invasive Escherichia coli",

abstract = "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.",

keywords = "Crohn's disease, adherent-invasive E. coli, propionic acid, short chain fatty acid",

author = "Ormsby, {Michael J.} and Johnson, {S{\'i}le A.} and Nuria Carpena and Meikle, {Lynsey M.} and Goldstone, {Robert J.} and Anne McIntosh and Wessel, {Hannah M.} and Hulme, {Heather E.} and McConnachie, {Ceilidh C.} and Connolly, {James P. R.} and Roe, {Andrew J.} and Conor Hasson and Joseph Boyd and Eamonn Fitzgerald and Konstantinos Gerasimidis and Douglas Morrison and Hold, {Georgina L.} and Richard Hansen and Daniel Walker and Smith, {David G. E.} and Wall, {Daniel M.}",

year = "2020",

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day = "18",

doi = "10.1016/j.celrep.2020.01.078",

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Ormsby, MJ, Johnson, SA, Carpena, N, Meikle, LM, Goldstone, RJ, McIntosh, A, Wessel, HM, Hulme, HE, McConnachie, CC, Connolly, JPR, Roe, AJ, Hasson, C, Boyd, J, Fitzgerald, E, Gerasimidis, K, Morrison, D, Hold, GL, Hansen, R, Walker, D, Smith, DGE & Wall, DM 2020, 'Propionic Acid Promotes the Virulent Phenotype of Crohn's Disease-Associated Adherent-Invasive Escherichia coli', Cell Reports, vol. 30, no. 7, pp. 2297-2305.e5. https://doi.org/10.1016/j.celrep.2020.01.078

TY - JOUR

T1 - Propionic Acid Promotes the Virulent Phenotype of Crohn's Disease-Associated Adherent-Invasive Escherichia coli

AU - Ormsby, Michael J.

AU - Johnson, Síle A.

AU - Carpena, Nuria

AU - Meikle, Lynsey M.

AU - Goldstone, Robert J.

AU - McIntosh, Anne

AU - Wessel, Hannah M.

AU - Hulme, Heather E.

AU - McConnachie, Ceilidh C.

AU - Connolly, James P. R.

AU - Roe, Andrew J.

AU - Hasson, Conor

AU - Boyd, Joseph

AU - Fitzgerald, Eamonn

AU - Gerasimidis, Konstantinos

AU - Morrison, Douglas

AU - Hold, Georgina L.

AU - Hansen, Richard

AU - Walker, Daniel

AU - Smith, David G. E.

AU - Wall, Daniel M.

PY - 2020/2/18

Y1 - 2020/2/18

N2 - 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.

AB - 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.

KW - Crohn's disease

KW - adherent-invasive E. coli

KW - propionic acid

KW - short chain fatty acid

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DO - 10.1016/j.celrep.2020.01.078

M3 - Article

C2 - 32075765

SN - 2211-1247

VL - 30

SP - 2297-2305.e5

JO - Cell Reports

JF - Cell Reports

IS - 7

ER -

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

Abstract

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UN SDGs

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David George Emslie Smith

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

Abstract

Keywords

ASJC Scopus subject areas

UN SDGs

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David George Emslie Smith

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