Enterobacteriaceae are essential for the modulation of colitis severity by fungi

Abstract Background Host-microbe balance maintains intestinal homeostasis and strongly influences inflammatory conditions such as inflammatory bowel diseases (IBD). Here we focused on bacteria-fungi interactions and their implications on intestinal inflammation, a poorly understood area. Methods Dex...

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Main Authors: Bruno Sovran, Julien Planchais, Sarah Jegou, Marjolene Straube, Bruno Lamas, Jane Mea Natividad, Allison Agus, Louise Dupraz, Jérémy Glodt, Grégory Da Costa, Marie-Laure Michel, Philippe Langella, Mathias L. Richard, Harry Sokol
Format: Article
Language:English
Published: BMC 2018-09-01
Series:Microbiome
Subjects:
Online Access:http://link.springer.com/article/10.1186/s40168-018-0538-9
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spelling doaj-279c3f8e97ed47df8032f9222eef52de2020-11-25T02:52:07ZengBMCMicrobiome2049-26182018-09-016111610.1186/s40168-018-0538-9Enterobacteriaceae are essential for the modulation of colitis severity by fungiBruno Sovran0Julien Planchais1Sarah Jegou2Marjolene Straube3Bruno Lamas4Jane Mea Natividad5Allison Agus6Louise Dupraz7Jérémy Glodt8Grégory Da Costa9Marie-Laure Michel10Philippe Langella11Mathias L. Richard12Harry Sokol13Micalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclaySorbonne Universités, École Normale Supérieure, CNRS, INSERM, APHP Laboratoire des Biomolécules (LBM)Sorbonne Universités, École Normale Supérieure, CNRS, INSERM, APHP Laboratoire des Biomolécules (LBM)Micalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayMicalis Institute, INRA, AgroParisTech, Université Paris-SaclayAbstract Background Host-microbe balance maintains intestinal homeostasis and strongly influences inflammatory conditions such as inflammatory bowel diseases (IBD). Here we focused on bacteria-fungi interactions and their implications on intestinal inflammation, a poorly understood area. Methods Dextran sodium sulfate (DSS)-induced colitis was assessed in mice treated with vancomycin (targeting gram-positive bacteria) or colistin (targeting Enterobacteriaceae) and supplemented with either Saccharomyces boulardii CNCM I-745 or Candida albicans. Inflammation severity as well as bacterial and fungal microbiota compositions was monitored. Results While S. boulardii improved DSS-induced colitis and C. albicans worsened it in untreated settings, antibiotic treatment strongly modified DSS susceptibility and effects of fungi on colitis. Vancomycin-treated mice were fully protected from colitis, while colistin-treated mice retained colitis phenotype but were not affected anymore by administration of fungi. Antibacterial treatments not only influenced bacterial populations but also had indirect effects on fungal microbiota. Correlations between bacterial and fungal relative abundance were dramatically decreased in colistin-treated mice compared to vancomycin-treated and control mice, suggesting that colistin-sensitive bacteria are involved in interactions with fungi. Restoration of the Enterobacteriaceae population by administrating colistin-resistant Escherichia coli reestablished both beneficial effects of S. boulardii and pathogenic effects of C. albicans on colitis severity. This effect was at least partly mediated by an improved gut colonization by fungi. Conclusions Fungal colonization of the gut is affected by the Enterobacteriaceae population, indirectly modifying effects of mycobiome on the host. This finding provides new insights into the role of inter-kingdom functional interactions in intestinal physiopathology and potentially in IBD.http://link.springer.com/article/10.1186/s40168-018-0538-9EnterobacteriaceaeS. boulardii CNCM I-745C. albicansColitisMicrobiotaFungi
collection DOAJ
language English
format Article
sources DOAJ
author Bruno Sovran
Julien Planchais
Sarah Jegou
Marjolene Straube
Bruno Lamas
Jane Mea Natividad
Allison Agus
Louise Dupraz
Jérémy Glodt
Grégory Da Costa
Marie-Laure Michel
Philippe Langella
Mathias L. Richard
Harry Sokol
spellingShingle Bruno Sovran
Julien Planchais
Sarah Jegou
Marjolene Straube
Bruno Lamas
Jane Mea Natividad
Allison Agus
Louise Dupraz
Jérémy Glodt
Grégory Da Costa
Marie-Laure Michel
Philippe Langella
Mathias L. Richard
Harry Sokol
Enterobacteriaceae are essential for the modulation of colitis severity by fungi
Microbiome
Enterobacteriaceae
S. boulardii CNCM I-745
C. albicans
Colitis
Microbiota
Fungi
author_facet Bruno Sovran
Julien Planchais
Sarah Jegou
Marjolene Straube
Bruno Lamas
Jane Mea Natividad
Allison Agus
Louise Dupraz
Jérémy Glodt
Grégory Da Costa
Marie-Laure Michel
Philippe Langella
Mathias L. Richard
Harry Sokol
author_sort Bruno Sovran
title Enterobacteriaceae are essential for the modulation of colitis severity by fungi
title_short Enterobacteriaceae are essential for the modulation of colitis severity by fungi
title_full Enterobacteriaceae are essential for the modulation of colitis severity by fungi
title_fullStr Enterobacteriaceae are essential for the modulation of colitis severity by fungi
title_full_unstemmed Enterobacteriaceae are essential for the modulation of colitis severity by fungi
title_sort enterobacteriaceae are essential for the modulation of colitis severity by fungi
publisher BMC
series Microbiome
issn 2049-2618
publishDate 2018-09-01
description Abstract Background Host-microbe balance maintains intestinal homeostasis and strongly influences inflammatory conditions such as inflammatory bowel diseases (IBD). Here we focused on bacteria-fungi interactions and their implications on intestinal inflammation, a poorly understood area. Methods Dextran sodium sulfate (DSS)-induced colitis was assessed in mice treated with vancomycin (targeting gram-positive bacteria) or colistin (targeting Enterobacteriaceae) and supplemented with either Saccharomyces boulardii CNCM I-745 or Candida albicans. Inflammation severity as well as bacterial and fungal microbiota compositions was monitored. Results While S. boulardii improved DSS-induced colitis and C. albicans worsened it in untreated settings, antibiotic treatment strongly modified DSS susceptibility and effects of fungi on colitis. Vancomycin-treated mice were fully protected from colitis, while colistin-treated mice retained colitis phenotype but were not affected anymore by administration of fungi. Antibacterial treatments not only influenced bacterial populations but also had indirect effects on fungal microbiota. Correlations between bacterial and fungal relative abundance were dramatically decreased in colistin-treated mice compared to vancomycin-treated and control mice, suggesting that colistin-sensitive bacteria are involved in interactions with fungi. Restoration of the Enterobacteriaceae population by administrating colistin-resistant Escherichia coli reestablished both beneficial effects of S. boulardii and pathogenic effects of C. albicans on colitis severity. This effect was at least partly mediated by an improved gut colonization by fungi. Conclusions Fungal colonization of the gut is affected by the Enterobacteriaceae population, indirectly modifying effects of mycobiome on the host. This finding provides new insights into the role of inter-kingdom functional interactions in intestinal physiopathology and potentially in IBD.
topic Enterobacteriaceae
S. boulardii CNCM I-745
C. albicans
Colitis
Microbiota
Fungi
url http://link.springer.com/article/10.1186/s40168-018-0538-9
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