Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model

ABSTRACT Inflammatory bowel disease (IBD) has become a global public health problem. Although the pathogenesis of the disease is unknown, a potential association between the gut microbiota and inflammatory signatures has been established. Probiotics, especially Lactobacillus or Bifidobacterium, are...

Full description

Bibliographic Details
Main Authors: Limin Xu, Bingdong Liu, Liujing Huang, Ze Li, Yanbo Cheng, Ye Tian, Guihua Pan, Huijun Li, Yinlan Xu, Weidong Wu, Zongbin Cui, Liwei Xie
Format: Article
Language:English
Published: American Society for Microbiology 2022-08-01
Series:Microbiology Spectrum
Subjects:
Online Access:https://journals.asm.org/doi/10.1128/spectrum.00657-22
_version_ 1811188268933316608
author Limin Xu
Bingdong Liu
Liujing Huang
Ze Li
Yanbo Cheng
Ye Tian
Guihua Pan
Huijun Li
Yinlan Xu
Weidong Wu
Zongbin Cui
Liwei Xie
author_facet Limin Xu
Bingdong Liu
Liujing Huang
Ze Li
Yanbo Cheng
Ye Tian
Guihua Pan
Huijun Li
Yinlan Xu
Weidong Wu
Zongbin Cui
Liwei Xie
author_sort Limin Xu
collection DOAJ
description ABSTRACT Inflammatory bowel disease (IBD) has become a global public health problem. Although the pathogenesis of the disease is unknown, a potential association between the gut microbiota and inflammatory signatures has been established. Probiotics, especially Lactobacillus or Bifidobacterium, are orally taken as food supplements or microbial drugs by patients with IBD or gastrointestinal disorders due to their safety, efficacy, and power to restore the gut microenvironment. In the current study, we investigated the comprehensive effects of probiotic bacterial consortia consisting of Lactobacillus reuteri, Lactobacillus gasseri, Lactobacillus acidophilus (Lactobacillus spp.), and Bifidobacterium lactis (Bifidobacterium spp.) or their metabolites in a dextran sodium sulfate (DSS)-induced colitis mouse model. Our data demonstrate that probiotic consortia not only ameliorate the disease phenotype but also restore the composition and structure of the gut microbiota. Moreover, the effect of probiotic consortia is better than that of any single probiotic strain. The results also demonstrate that mixed fermentation metabolites are capable of ameliorating the symptoms of gut inflammation. However, the administration of metabolites is not as effective as probiotic consortia with respect to phenotypic characteristics, such as body weight, disease activity index (DAI), and histological score. In addition, mixed metabolites led only to changes in intestinal flora composition. In summary, probiotic consortia and metabolites could exert protective roles in the DSS-induced colitis mouse model by reducing inflammation and regulating microbial dysbiosis. These findings from the current study provide support for the development of probiotic-based microbial products as an alternative therapeutic strategy for IBD. IMPORTANCE IBD is a chronic nonspecific inflammatory disease. IBD is characterized by a wide range of lesions, often involving the entire colon, and is characterized mainly by ulcers and erosions of the colonic mucosa. In the present study, we investigated the efficacy of probiotics on the recovery of gut inflammation and the restoration of gut microecology. We demonstrate that probiotic consortia have a superior effect in inhibiting inflammation and accelerating recovery compared with the effects observed in the control group or groups administered with a single strain. These results support the utilization of probiotic consortia as an alternative therapeutic approach to treat IBD.
first_indexed 2024-04-11T14:17:12Z
format Article
id doaj.art-5ea93af78f2e455e9b62da04d0af2679
institution Directory Open Access Journal
issn 2165-0497
language English
last_indexed 2024-04-11T14:17:12Z
publishDate 2022-08-01
publisher American Society for Microbiology
record_format Article
series Microbiology Spectrum
spelling doaj.art-5ea93af78f2e455e9b62da04d0af26792022-12-22T04:19:14ZengAmerican Society for MicrobiologyMicrobiology Spectrum2165-04972022-08-0110410.1128/spectrum.00657-22Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse ModelLimin Xu0Bingdong Liu1Liujing Huang2Ze Li3Yanbo Cheng4Ye Tian5Guihua Pan6Huijun Li7Yinlan Xu8Weidong Wu9Zongbin Cui10Liwei Xie11School of Public Health, Xinxiang Medical University, Xinxiang, ChinaState Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, ChinaState Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, ChinaSchool of Public Health, Xinxiang Medical University, Xinxiang, ChinaState Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, ChinaState Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, ChinaState Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, ChinaSchool of Public Health, Xinxiang Medical University, Xinxiang, ChinaSchool of Public Health, Xinxiang Medical University, Xinxiang, ChinaSchool of Public Health, Xinxiang Medical University, Xinxiang, ChinaState Key Laboratory of Applied Microbiology Southern China, Guangdong Provincial Key Laboratory of Microbial Culture Collection and Application, Guangdong Open Laboratory of Applied Microbiology, Institute of Microbiology, Guangdong Academy of Sciences, Guangzhou, ChinaSchool of Public Health, Xinxiang Medical University, Xinxiang, ChinaABSTRACT Inflammatory bowel disease (IBD) has become a global public health problem. Although the pathogenesis of the disease is unknown, a potential association between the gut microbiota and inflammatory signatures has been established. Probiotics, especially Lactobacillus or Bifidobacterium, are orally taken as food supplements or microbial drugs by patients with IBD or gastrointestinal disorders due to their safety, efficacy, and power to restore the gut microenvironment. In the current study, we investigated the comprehensive effects of probiotic bacterial consortia consisting of Lactobacillus reuteri, Lactobacillus gasseri, Lactobacillus acidophilus (Lactobacillus spp.), and Bifidobacterium lactis (Bifidobacterium spp.) or their metabolites in a dextran sodium sulfate (DSS)-induced colitis mouse model. Our data demonstrate that probiotic consortia not only ameliorate the disease phenotype but also restore the composition and structure of the gut microbiota. Moreover, the effect of probiotic consortia is better than that of any single probiotic strain. The results also demonstrate that mixed fermentation metabolites are capable of ameliorating the symptoms of gut inflammation. However, the administration of metabolites is not as effective as probiotic consortia with respect to phenotypic characteristics, such as body weight, disease activity index (DAI), and histological score. In addition, mixed metabolites led only to changes in intestinal flora composition. In summary, probiotic consortia and metabolites could exert protective roles in the DSS-induced colitis mouse model by reducing inflammation and regulating microbial dysbiosis. These findings from the current study provide support for the development of probiotic-based microbial products as an alternative therapeutic strategy for IBD. IMPORTANCE IBD is a chronic nonspecific inflammatory disease. IBD is characterized by a wide range of lesions, often involving the entire colon, and is characterized mainly by ulcers and erosions of the colonic mucosa. In the present study, we investigated the efficacy of probiotics on the recovery of gut inflammation and the restoration of gut microecology. We demonstrate that probiotic consortia have a superior effect in inhibiting inflammation and accelerating recovery compared with the effects observed in the control group or groups administered with a single strain. These results support the utilization of probiotic consortia as an alternative therapeutic approach to treat IBD.https://journals.asm.org/doi/10.1128/spectrum.00657-22inflammatory bowel diseaseprobiotic consortiametabolitesLactobacillus
spellingShingle Limin Xu
Bingdong Liu
Liujing Huang
Ze Li
Yanbo Cheng
Ye Tian
Guihua Pan
Huijun Li
Yinlan Xu
Weidong Wu
Zongbin Cui
Liwei Xie
Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model
Microbiology Spectrum
inflammatory bowel disease
probiotic consortia
metabolites
Lactobacillus
title Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model
title_full Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model
title_fullStr Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model
title_full_unstemmed Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model
title_short Probiotic Consortia and Their Metabolites Ameliorate the Symptoms of Inflammatory Bowel Diseases in a Colitis Mouse Model
title_sort probiotic consortia and their metabolites ameliorate the symptoms of inflammatory bowel diseases in a colitis mouse model
topic inflammatory bowel disease
probiotic consortia
metabolites
Lactobacillus
url https://journals.asm.org/doi/10.1128/spectrum.00657-22
work_keys_str_mv AT liminxu probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT bingdongliu probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT liujinghuang probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT zeli probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT yanbocheng probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT yetian probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT guihuapan probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT huijunli probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT yinlanxu probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT weidongwu probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT zongbincui probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel
AT liweixie probioticconsortiaandtheirmetabolitesamelioratethesymptomsofinflammatoryboweldiseasesinacolitismousemodel