Cargando…

A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis

BACKGROUND: The intestinal microbiota plays a crucial role in the maintenance of gut homeostasis. Changes in crosstalk between the intestinal epithelial cells, immune cells and the microbiota are critically involved in the development of inflammatory bowel disease. In the experimental mouse model, t...

Descripción completa

Detalles Bibliográficos
Autores principales: Charlet, Rogatien, Bortolus, Clovis, Barbet, Melissandre, Sendid, Boualem, Jawhara, Samir
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6276212/
https://www.ncbi.nlm.nih.gov/pubmed/30524506
http://dx.doi.org/10.1186/s13099-018-0277-2
_version_ 1783377969728716800
author Charlet, Rogatien
Bortolus, Clovis
Barbet, Melissandre
Sendid, Boualem
Jawhara, Samir
author_facet Charlet, Rogatien
Bortolus, Clovis
Barbet, Melissandre
Sendid, Boualem
Jawhara, Samir
author_sort Charlet, Rogatien
collection PubMed
description BACKGROUND: The intestinal microbiota plays a crucial role in the maintenance of gut homeostasis. Changes in crosstalk between the intestinal epithelial cells, immune cells and the microbiota are critically involved in the development of inflammatory bowel disease. In the experimental mouse model, the development of colitis induced by dextran sulfate sodium (DSS) promotes overgrowth of the opportunistic yeast pathogen Candida glabrata. Conversely, fungal colonization aggravates inflammatory parameters. In the present study, we explored the effect of C. glabrata colonization on the diversity of the gut microbiota in a DSS-induced colitis model, and determined the impact of soluble β-glucans on C. glabrata-host interactions. RESULTS: Mice were administered a single inoculum of C. glabrata and were exposed to DSS treatment for 2 weeks in order to induce acute colitis. For β-glucan treatment, mice were administered with soluble β-glucans purified from C. glabrata (3 mg per mouse), orally and daily, for 5 days, starting on day 1. The number of C. glabrata colonies and changes in microbiota diversity were assessed in freshly collected stool samples from each tagged mouse, using traditional culture methods based on agar plates. An increase in Escherichia coli and Enterococcus faecalis populations and a reduction in Lactobacillus johnsonii and Bacteroides thetaiotaomicron were observed during colitis development. This decrease in L. johnsonii was significantly accentuated by C. glabrata overgrowth. Oral administration of β-glucans to mice decreased the overgrowth of aerobic bacteria and IL-1β expression while L. johnsonii and B. thetaiotaomicron populations increased significantly. β-glucan treatment increased IL-10 production via PPARγ sensing, promoting the attenuation of colitis and C. glabrata elimination. CONCLUSIONS: This study shows that the colonic inflammation alters the microbial balance, while β-glucan treatment increases the anaerobic bacteria and promotes colitis attenuation and C. glabrata elimination.
format Online
Article
Text
id pubmed-6276212
institution National Center for Biotechnology Information
language English
publishDate 2018
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-62762122018-12-06 A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis Charlet, Rogatien Bortolus, Clovis Barbet, Melissandre Sendid, Boualem Jawhara, Samir Gut Pathog Research BACKGROUND: The intestinal microbiota plays a crucial role in the maintenance of gut homeostasis. Changes in crosstalk between the intestinal epithelial cells, immune cells and the microbiota are critically involved in the development of inflammatory bowel disease. In the experimental mouse model, the development of colitis induced by dextran sulfate sodium (DSS) promotes overgrowth of the opportunistic yeast pathogen Candida glabrata. Conversely, fungal colonization aggravates inflammatory parameters. In the present study, we explored the effect of C. glabrata colonization on the diversity of the gut microbiota in a DSS-induced colitis model, and determined the impact of soluble β-glucans on C. glabrata-host interactions. RESULTS: Mice were administered a single inoculum of C. glabrata and were exposed to DSS treatment for 2 weeks in order to induce acute colitis. For β-glucan treatment, mice were administered with soluble β-glucans purified from C. glabrata (3 mg per mouse), orally and daily, for 5 days, starting on day 1. The number of C. glabrata colonies and changes in microbiota diversity were assessed in freshly collected stool samples from each tagged mouse, using traditional culture methods based on agar plates. An increase in Escherichia coli and Enterococcus faecalis populations and a reduction in Lactobacillus johnsonii and Bacteroides thetaiotaomicron were observed during colitis development. This decrease in L. johnsonii was significantly accentuated by C. glabrata overgrowth. Oral administration of β-glucans to mice decreased the overgrowth of aerobic bacteria and IL-1β expression while L. johnsonii and B. thetaiotaomicron populations increased significantly. β-glucan treatment increased IL-10 production via PPARγ sensing, promoting the attenuation of colitis and C. glabrata elimination. CONCLUSIONS: This study shows that the colonic inflammation alters the microbial balance, while β-glucan treatment increases the anaerobic bacteria and promotes colitis attenuation and C. glabrata elimination. BioMed Central 2018-12-03 /pmc/articles/PMC6276212/ /pubmed/30524506 http://dx.doi.org/10.1186/s13099-018-0277-2 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Charlet, Rogatien
Bortolus, Clovis
Barbet, Melissandre
Sendid, Boualem
Jawhara, Samir
A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
title A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
title_full A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
title_fullStr A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
title_full_unstemmed A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
title_short A decrease in anaerobic bacteria promotes Candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
title_sort decrease in anaerobic bacteria promotes candida glabrata overgrowth while β-glucan treatment restores the gut microbiota and attenuates colitis
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6276212/
https://www.ncbi.nlm.nih.gov/pubmed/30524506
http://dx.doi.org/10.1186/s13099-018-0277-2
work_keys_str_mv AT charletrogatien adecreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT bortolusclovis adecreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT barbetmelissandre adecreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT sendidboualem adecreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT jawharasamir adecreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT charletrogatien decreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT bortolusclovis decreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT barbetmelissandre decreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT sendidboualem decreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis
AT jawharasamir decreaseinanaerobicbacteriapromotescandidaglabrataovergrowthwhilebglucantreatmentrestoresthegutmicrobiotaandattenuatescolitis