Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models

Enterotoxigenic Escherichia coli (ETEC) is one of the most common causes of acute traveler’s diarrhea. Adhesins and enterotoxins constitute the major ETEC virulence traits. With the dramatic increase in antibiotic resistance, probiotics are considered a wholesome alternative to prevent or treat ETEC...

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Main Authors: Charlène Roussel, Kim De Paepe, Wessam Galia, Jana de Bodt, Sandrine Chalancon, Sylvain Denis, Françoise Leriche, Pascal Vandekerkove, Nathalie Ballet, Stéphanie Blanquet-Diot, Tom Van de Wiele
Format: Article
Language:English
Published: Taylor & Francis Group 2021-01-01
Series:Gut Microbes
Subjects:
Online Access:http://dx.doi.org/10.1080/19490976.2021.1953246
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spelling doaj-79a5bced629246d18e44f4381c59b4f52021-09-06T14:06:26ZengTaylor & Francis GroupGut Microbes1949-09761949-09842021-01-0113110.1080/19490976.2021.19532461953246Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut modelsCharlène Roussel0Kim De Paepe1Wessam Galia2Jana de Bodt3Sandrine Chalancon4Sylvain Denis5Françoise Leriche6Pascal Vandekerkove7Nathalie Ballet8Stéphanie Blanquet-DiotTom Van de Wiele9Université Clermont Auvergne, UMR UCA-INRA 454 MEDIS, Microbiology Digestive Environment and HealthGhent UniversityUMR 5557 Microbial Ecology, Research Group On Bacterial Opportunistic Pathogens And Environment, CNRS, VetAgro SupGhent UniversityUniversité Clermont Auvergne, UMR UCA-INRA 454 MEDIS, Microbiology Digestive Environment and HealthUniversité Clermont Auvergne, UMR UCA-INRA 454 MEDIS, Microbiology Digestive Environment and HealthUnité De Recherche Fromagère, VetAgro SupLesaffre International, Lesaffre GroupLesaffre International, Lesaffre GroupGhent UniversityEnterotoxigenic Escherichia coli (ETEC) is one of the most common causes of acute traveler’s diarrhea. Adhesins and enterotoxins constitute the major ETEC virulence traits. With the dramatic increase in antibiotic resistance, probiotics are considered a wholesome alternative to prevent or treat ETEC infections. Here, we examined the antimicrobial properties of the probiotic Saccharomyces cerevisiae CNCM I-3856 against ETEC H10407 pathogenesis upon co-administration in the TNO gastrointestinal Model (TIM-1), simulating the physicochemical and enzymatic conditions of the human upper digestive tract and preventive treatment in the Mucosal Simulator of the Human Intestinal Microbial Ecosystem (M-SHIME), integrating microbial populations of the ileum and ascending colon. Interindividual variability was assessed by separate M-SHIME experiments with microbiota from six human individuals. The probiotic did not affect ETEC survival along the digestive tract. However, ETEC pathogenicity was significantly reduced: enterotoxin encoding virulence genes were repressed, especially in the TIM-1 system, and a lower enterotoxin production was noted. M-SHIME experiments revealed that 18-days probiotic treatment stimulate the growth of Bifidobacterium and Lactobacillus in different gut regions (mucosal and luminal, ileum and ascending colon) while a stronger metabolic activity was noted in terms of short-chain fatty acids (acetate, propionate, and butyrate) and ethanol production. Moreover, the probiotic pre-treated microbiota displayed a higher robustness in composition following ETEC challenge compared to the control condition. We thus demonstrated the multi-inhibitory properties of the probiotic S. cerevisiae CNCM I-3856 against ETEC in the overall simulated human digestive tract, regardless of the inherent variability across individuals in the M-SHIME.http://dx.doi.org/10.1080/19490976.2021.1953246probioticsaccharomyces cerevisiaefoodborne pathogenetec; virulenceenterotoxinantagonism effectgut microbiota
collection DOAJ
language English
format Article
sources DOAJ
author Charlène Roussel
Kim De Paepe
Wessam Galia
Jana de Bodt
Sandrine Chalancon
Sylvain Denis
Françoise Leriche
Pascal Vandekerkove
Nathalie Ballet
Stéphanie Blanquet-Diot
Tom Van de Wiele
spellingShingle Charlène Roussel
Kim De Paepe
Wessam Galia
Jana de Bodt
Sandrine Chalancon
Sylvain Denis
Françoise Leriche
Pascal Vandekerkove
Nathalie Ballet
Stéphanie Blanquet-Diot
Tom Van de Wiele
Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models
Gut Microbes
probiotic
saccharomyces cerevisiae
foodborne pathogen
etec; virulence
enterotoxin
antagonism effect
gut microbiota
author_facet Charlène Roussel
Kim De Paepe
Wessam Galia
Jana de Bodt
Sandrine Chalancon
Sylvain Denis
Françoise Leriche
Pascal Vandekerkove
Nathalie Ballet
Stéphanie Blanquet-Diot
Tom Van de Wiele
author_sort Charlène Roussel
title Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models
title_short Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models
title_full Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models
title_fullStr Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models
title_full_unstemmed Multi-targeted properties of the probiotic saccharomyces cerevisiae CNCM I-3856 against enterotoxigenic escherichia coli (ETEC) H10407 pathogenesis across human gut models
title_sort multi-targeted properties of the probiotic saccharomyces cerevisiae cncm i-3856 against enterotoxigenic escherichia coli (etec) h10407 pathogenesis across human gut models
publisher Taylor & Francis Group
series Gut Microbes
issn 1949-0976
1949-0984
publishDate 2021-01-01
description Enterotoxigenic Escherichia coli (ETEC) is one of the most common causes of acute traveler’s diarrhea. Adhesins and enterotoxins constitute the major ETEC virulence traits. With the dramatic increase in antibiotic resistance, probiotics are considered a wholesome alternative to prevent or treat ETEC infections. Here, we examined the antimicrobial properties of the probiotic Saccharomyces cerevisiae CNCM I-3856 against ETEC H10407 pathogenesis upon co-administration in the TNO gastrointestinal Model (TIM-1), simulating the physicochemical and enzymatic conditions of the human upper digestive tract and preventive treatment in the Mucosal Simulator of the Human Intestinal Microbial Ecosystem (M-SHIME), integrating microbial populations of the ileum and ascending colon. Interindividual variability was assessed by separate M-SHIME experiments with microbiota from six human individuals. The probiotic did not affect ETEC survival along the digestive tract. However, ETEC pathogenicity was significantly reduced: enterotoxin encoding virulence genes were repressed, especially in the TIM-1 system, and a lower enterotoxin production was noted. M-SHIME experiments revealed that 18-days probiotic treatment stimulate the growth of Bifidobacterium and Lactobacillus in different gut regions (mucosal and luminal, ileum and ascending colon) while a stronger metabolic activity was noted in terms of short-chain fatty acids (acetate, propionate, and butyrate) and ethanol production. Moreover, the probiotic pre-treated microbiota displayed a higher robustness in composition following ETEC challenge compared to the control condition. We thus demonstrated the multi-inhibitory properties of the probiotic S. cerevisiae CNCM I-3856 against ETEC in the overall simulated human digestive tract, regardless of the inherent variability across individuals in the M-SHIME.
topic probiotic
saccharomyces cerevisiae
foodborne pathogen
etec; virulence
enterotoxin
antagonism effect
gut microbiota
url http://dx.doi.org/10.1080/19490976.2021.1953246
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