The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota

ABSTRACT An increasing number of human beings from developed countries are colonized by Escherichia coli strains producing colibactin, a genotoxin suspected to be associated with the development of colorectal cancers. Deoxynivalenol (DON) is the most prevalent mycotoxin that contaminates staple food...

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Autores principales: Delphine Payros, Ulrich Dobrindt, Patricia Martin, Thomas Secher, Ana Paula F. L. Bracarense, Michèle Boury, Joelle Laffitte, Philippe Pinton, Eric Oswald, Isabelle P. Oswald
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Publicado: American Society for Microbiology 2017
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spelling oai:doaj.org-article:87218569696a422a83360c9f371f24282021-11-15T15:50:59ZThe Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota10.1128/mBio.00007-172150-7511https://doaj.org/article/87218569696a422a83360c9f371f24282017-05-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.00007-17https://doaj.org/toc/2150-7511ABSTRACT An increasing number of human beings from developed countries are colonized by Escherichia coli strains producing colibactin, a genotoxin suspected to be associated with the development of colorectal cancers. Deoxynivalenol (DON) is the most prevalent mycotoxin that contaminates staple food—especially cereal products—in Europe and North America. This study investigates the effect of the food contaminant DON on the genotoxicity of the E. coli strains producing colibactin. In vitro, intestinal epithelial cells were coexposed to DON and E. coli producing colibactin. In vivo, newborn rats colonized at birth with E. coli producing colibactin were fed a DON-contaminated diet. Intestinal DNA damage was estimated by the phosphorylation of histone H2AX. DON exacerbates the genotoxicity of the E. coli producing colibactin in a time- and dose-dependent manner in vitro. Although DON had no effect on the composition of the gut microbiota, and especially on the number of E. coli, a significant increase in DNA damage was observed in intestinal epithelial cells of animals colonized by E. coli strains producing colibactin and coexposed to DON compared to animals colonized with E. coli strains unable to produce colibactin or animals exposed only to DON. In conclusion, our data demonstrate that the genotoxicity of E. coli strains producing colibactin, increasingly present in the microbiota of asymptomatic human beings, is modulated by the presence of DON in the diet. This raises questions about the synergism between food contaminants and gut microbiota with regard to intestinal carcinogenesis. IMPORTANCE An increasing number of human beings from developed countries are colonized by Escherichia coli strains producing colibactin, a genotoxin suspected to be associated with the development of colorectal cancers. Deoxynivalenol (DON) is the most prevalent mycotoxin that contaminates staple food—especially cereal products—in Europe and North America. Our in vitro and in vivo results demonstrate that the intestinal DNA damage induced by colibactin-producing E. coli strains was exacerbated by the presence of DON in the diet. This raises questions about the synergism between food contaminants and gut microbiota with regard to intestinal carcinogenesis.Delphine PayrosUlrich DobrindtPatricia MartinThomas SecherAna Paula F. L. BracarenseMichèle BouryJoelle LaffittePhilippe PintonEric OswaldIsabelle P. OswaldAmerican Society for MicrobiologyarticleMicrobiologyQR1-502ENmBio, Vol 8, Iss 2 (2017)
institution DOAJ
collection DOAJ
language EN
topic Microbiology
QR1-502
spellingShingle Microbiology
QR1-502
Delphine Payros
Ulrich Dobrindt
Patricia Martin
Thomas Secher
Ana Paula F. L. Bracarense
Michèle Boury
Joelle Laffitte
Philippe Pinton
Eric Oswald
Isabelle P. Oswald
The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota
description ABSTRACT An increasing number of human beings from developed countries are colonized by Escherichia coli strains producing colibactin, a genotoxin suspected to be associated with the development of colorectal cancers. Deoxynivalenol (DON) is the most prevalent mycotoxin that contaminates staple food—especially cereal products—in Europe and North America. This study investigates the effect of the food contaminant DON on the genotoxicity of the E. coli strains producing colibactin. In vitro, intestinal epithelial cells were coexposed to DON and E. coli producing colibactin. In vivo, newborn rats colonized at birth with E. coli producing colibactin were fed a DON-contaminated diet. Intestinal DNA damage was estimated by the phosphorylation of histone H2AX. DON exacerbates the genotoxicity of the E. coli producing colibactin in a time- and dose-dependent manner in vitro. Although DON had no effect on the composition of the gut microbiota, and especially on the number of E. coli, a significant increase in DNA damage was observed in intestinal epithelial cells of animals colonized by E. coli strains producing colibactin and coexposed to DON compared to animals colonized with E. coli strains unable to produce colibactin or animals exposed only to DON. In conclusion, our data demonstrate that the genotoxicity of E. coli strains producing colibactin, increasingly present in the microbiota of asymptomatic human beings, is modulated by the presence of DON in the diet. This raises questions about the synergism between food contaminants and gut microbiota with regard to intestinal carcinogenesis. IMPORTANCE An increasing number of human beings from developed countries are colonized by Escherichia coli strains producing colibactin, a genotoxin suspected to be associated with the development of colorectal cancers. Deoxynivalenol (DON) is the most prevalent mycotoxin that contaminates staple food—especially cereal products—in Europe and North America. Our in vitro and in vivo results demonstrate that the intestinal DNA damage induced by colibactin-producing E. coli strains was exacerbated by the presence of DON in the diet. This raises questions about the synergism between food contaminants and gut microbiota with regard to intestinal carcinogenesis.
format article
author Delphine Payros
Ulrich Dobrindt
Patricia Martin
Thomas Secher
Ana Paula F. L. Bracarense
Michèle Boury
Joelle Laffitte
Philippe Pinton
Eric Oswald
Isabelle P. Oswald
author_facet Delphine Payros
Ulrich Dobrindt
Patricia Martin
Thomas Secher
Ana Paula F. L. Bracarense
Michèle Boury
Joelle Laffitte
Philippe Pinton
Eric Oswald
Isabelle P. Oswald
author_sort Delphine Payros
title The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota
title_short The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota
title_full The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota
title_fullStr The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota
title_full_unstemmed The Food Contaminant Deoxynivalenol Exacerbates the Genotoxicity of Gut Microbiota
title_sort food contaminant deoxynivalenol exacerbates the genotoxicity of gut microbiota
publisher American Society for Microbiology
publishDate 2017
url https://doaj.org/article/87218569696a422a83360c9f371f2428
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