Bacteroides uniformis degrades β-glucan to promote Lactobacillus johnsonii improving indole-3-lactic acid levels in alleviating colitis

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Reviewed Marked as Reviewed by Svetlana up on 2024-11-5
study design
Citation
PMID PubMed identifier for scientific articles.
DOI Digital object identifier for electronic documents.
URI
Authors
Zhang S, Nie Q, Sun Y, Zuo S, Chen C, Li S, Yang J, Hu J, Zhou X, Yu Y, Huang P, Lian L, Xie M, Nie S
Journal
Microbiome
Year
2024
Keywords:
Bacteroides uniformis, Lactobacillus johnsonii, β-glucan, Aryl hydrocarbon receptor, Cross-feeding, Indole-3-lactic acid, Inflammatory bowel disease, Nicotinamide
BACKGROUND: Intake of dietary fiber is associated with a reduced risk of inflammatory bowel disease. β-Glucan (BG), a bioactive dietary fiber, has potential health-promoting effects on intestinal functions; however, the underlying mechanism remains unclear. Here, we explore the role of BG in ameliorating colitis by modulating key bacteria and metabolites, confirmed by multiple validation experiments and loss-of-function studies, and reveal a novel bacterial cross-feeding interaction. RESULTS: BG intervention ameliorates colitis and reverses Lactobacillus reduction in colitic mice, and Lactobacillus abundance was significantly negatively correlated with the severity of colitis. It was confirmed by further studies that Lactobacillus johnsonii was the most significantly enriched Lactobacillus spp. Multi-omics analysis revealed that L. johnsonii produced abundant indole-3-lactic acid (ILA) leading to the activation of aryl hydrocarbon receptor (AhR) responsible for the mitigation of colitis. Interestingly, L. johnsonii cannot utilize BG but requires a cross-feeding with Bacteroides uniformis, which degrades BG and produces nicotinamide (NAM) to promote the growth of L. johnsonii. A proof-of-concept study confirmed that BG increases L. johnsonii and B. uniformis abundance and ILA levels in healthy individuals. CONCLUSIONS: These findings demonstrate the mechanism by which BG ameliorates colitis via L. johnsonii-ILA-AhR axis and reveal the important cross-feeding interaction between L. johnsonii and B. uniformis. Video Abstract.

Experiment 1


Reviewed Marked as Reviewed by Svetlana up on 2024-11-5

Curated date: 2024/10/11

Curator: Appleeyes

Revision editor(s): Appleeyes, Svetlana up

Subjects

Location of subjects
China
Host species Species from which microbiome was sampled. Contact us to have more species added.
Mus musculus
Body site Anatomical site where microbial samples were extracted from according to the Uber Anatomy Ontology
Feces Cow dung,Cow pat,Droppings,Dung,Excrement,Excreta,Faeces,Fecal material,Fecal matter,Fewmet,Frass,Guano,Matières fécales@fr,Merde@fr,Ordure,Partie de la merde@fr,Piece of shit,Porción de mierda@es,Portion of dung,Portion of excrement,Portion of faeces,Portion of fecal material,Portion of fecal matter,Portion of feces,Portion of guano,Portion of scat,Portionem cacas,Scat,Spoor,Spraint,Stool,Teil der fäkalien@de,Feces,feces
Condition The experimental condition / phenotype studied according to the Experimental Factor Ontology
Colitis Colitides,colitis,colitis (disease),colon inflammation,inflammation of colon,Colitis
Group 0 name Corresponds to the control (unexposed) group for case-control studies
DSS group
Group 1 name Corresponds to the case (exposed) group for case-control studies
BG + DSS group
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Mice treated with β-glucan (BG) alongside dextran sulfate sodium (DSS) to study the potential therapeutic effects of BG on DSS-induced colitis.
Group 0 sample size Number of subjects in the control (unexposed) group
6
Group 1 sample size Number of subjects in the case (exposed) group
6

Lab analysis

Sequencing type
16S
16S variable region One or more hypervariable region(s) of the bacterial 16S gene
V4
Sequencing platform Manufacturer and experimental platform used for quantifying microbial abundance
Illumina

Statistical Analysis

Data transformation Data transformation applied to microbial abundance measurements prior to differential abundance testing (if any).
relative abundances
Statistical test
LEfSe
Significance threshold p-value or FDR threshold used for differential abundance testing (if any)
0.05
MHT correction Have statistical tests be corrected for multiple hypothesis testing (MHT)?
Yes
LDA Score above Threshold for the linear discriminant analysis (LDA) score for studies using the popular LEfSe tool
2

Alpha Diversity

Shannon Estimator of species richness and species evenness: more weight on species richness
unchanged
Chao1 Abundance-based estimator of species richness
unchanged

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-11-5

Curated date: 2024/10/25

Curator: Appleeyes

Revision editor(s): Appleeyes

Source: figure 2d

Description: Comparison of relative abundance of bacteria between DSS and BG + DSS group was calculated by linear discriminant analysis effect size (LEfSe). Taxa meeting an LDA score threshold > 2.0 is shown.

Abundance in Group 1: increased abundance in BG + DSS group

NCBI Quality ControlLinks
Bacilli
Bacteroides uniformis
Lactobacillaceae
Lactobacillales
Lactobacillus
Porphyromonadaceae

Revision editor(s): Appleeyes

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-11-5

Curated date: 2024/10/25

Curator: Appleeyes

Revision editor(s): Appleeyes

Source: figure 2d

Description: Comparison of relative abundance of bacteria between DSS and BG + DSS group was calculated by linear discriminant analysis effect size (LEfSe). Taxa meeting an LDA score threshold > 2.0 is shown.

Abundance in Group 1: decreased abundance in BG + DSS group

NCBI Quality ControlLinks
Clostridia
Coriobacteriaceae
Coriobacteriales
Coriobacteriia
Lachnospiraceae
Actinomycetota

Revision editor(s): Appleeyes

Experiment 2


Reviewed Marked as Reviewed by Svetlana up on 2024-11-5

Curated date: 2024/10/16

Curator: Appleeyes

Revision editor(s): Appleeyes

Differences from previous experiment shown

Subjects

Group 0 name Corresponds to the control (unexposed) group for case-control studies
0-h fermented samples
Group 1 name Corresponds to the case (exposed) group for case-control studies
24-h fermented samples
Group 1 definition Diagnostic criteria applied to define the specific condition / phenotype represented in the case (exposed) group
Samples taken 24 hours after the intervention has been administered.
Group 0 sample size Number of subjects in the control (unexposed) group
3
Group 1 sample size Number of subjects in the case (exposed) group
3

Lab analysis

Statistical Analysis

Signature 1

Reviewed Marked as Reviewed by Svetlana up on 2024-11-5

Curated date: 2024/10/25

Curator: Appleeyes

Revision editor(s): Appleeyes

Source: figure 2i

Description: Comparison of relative abundance of bacteria between 0 and 24 h in the fermented sample by LEfSe.

Abundance in Group 1: increased abundance in 24-h fermented samples

NCBI Quality ControlLinks
Allobaculum
Bacilli
Bacteroides
Bacteroides uniformis
Bifidobacteriaceae
Bifidobacterium
Bifidobacterium pseudolongum
Lactobacillaceae
Lactobacillales
Lactobacillus
Parabacteroides
Parabacteroides distasonis

Revision editor(s): Appleeyes

Signature 2

Reviewed Marked as Reviewed by Svetlana up on 2024-11-5

Curated date: 2024/10/25

Curator: Appleeyes

Revision editor(s): Appleeyes

Source: figure 2i

Description: Comparison of relative abundance of bacteria between 0 and 24 h in the fermented sample by LEfSe.

Abundance in Group 1: decreased abundance in 24-h fermented samples

NCBI Quality ControlLinks
Bacteroidales
Bacteroides acidifaciens
Bacteroides ovatus
Bacteroidia
Bilophila
Desulfovibrio
Mucispirillum
Mucispirillum schaedleri
Odoribacter
Streptococcus
Turicibacter
Bacteroidota

Revision editor(s): Appleeyes