Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice

The antibiotic-induced intestinal injury (AIJ) is associated with diarrhoea and gastrointestinal discomfort. However, the pathological intestinal mechanisms and related side effects associated with antibiotic use/misuse may be counteracted by probiotics. This study aims to evaluate the effect and th...

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Main Authors: C. Pirozzi, N. Opallo, L. Coretti, A. Lama, C. Annunziata, F. Comella, S. Melini, E. Buommino, M.P. Mollica, G. Aviello, G. Mattace Raso, F. Lembo, R. Meli
Format: Article
Language:English
Published: Elsevier 2023-07-01
Series:Biomedicine & Pharmacotherapy
Subjects:
Online Access:http://www.sciencedirect.com/science/article/pii/S0753332223006509
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author C. Pirozzi
N. Opallo
L. Coretti
A. Lama
C. Annunziata
F. Comella
S. Melini
E. Buommino
M.P. Mollica
G. Aviello
G. Mattace Raso
F. Lembo
R. Meli
author_facet C. Pirozzi
N. Opallo
L. Coretti
A. Lama
C. Annunziata
F. Comella
S. Melini
E. Buommino
M.P. Mollica
G. Aviello
G. Mattace Raso
F. Lembo
R. Meli
author_sort C. Pirozzi
collection DOAJ
description The antibiotic-induced intestinal injury (AIJ) is associated with diarrhoea and gastrointestinal discomfort. However, the pathological intestinal mechanisms and related side effects associated with antibiotic use/misuse may be counteracted by probiotics. This study aims to evaluate the effect and the protective mechanisms of a probiotic formulation containing Alkalihalobacillus clausii (formerly Bacillus clausii; BC) spores in an experimental model of AIJ. C57/Bl6J mice were orally challenged with a high dose of ceftriaxone for five days along with BC treatment which lasted up to the 15th day. Our results showed the beneficial effect of the probiotic in preserving colonic integrity and limiting tissue inflammation and immune cell infiltration in AIJ mice. BC increased tight junction expression and regulated the unbalanced production of colonic pro- and anti-inflammatory cytokines, converging toward the full resolution of the intestinal damage. These findings were supported by the histological evaluation of the intestinal mucosa, suggesting a potential restoration of mucus production. Notably, BC treatment increased gene transcription of the secretory products responsible for epithelium repair and mucus synthesis and normalized the expression of antimicrobial peptides involved in immune activation. Reconstruction of complex and diverse gut microbiota in antibiotic-induced dysbiosis was recorded upon BC supplementation. Specifically, the expansion of A. clausii, Prevotella rara and Eubacterium ruminatium drove intestinal microbiota rebalance by primarily impacting Bacteroidota members. Taken together, our data indicate that BC administration alleviates AIJ by multiple converging mechanisms leading to restoring gut integrity and homeostasis and reshaping microbiota composition.
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spelling doaj.art-82fb808dd251469f9d6feffb946c8d672023-05-23T04:21:19ZengElsevierBiomedicine & Pharmacotherapy0753-33222023-07-01163114860Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in miceC. Pirozzi0N. Opallo1L. Coretti2A. Lama3C. Annunziata4F. Comella5S. Melini6E. Buommino7M.P. Mollica8G. Aviello9G. Mattace Raso10F. Lembo11R. Meli12Department of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, Italy; Task Force on Microbiome Studies, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, Italy; Task Force on Microbiome Studies, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Biology, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, Italy; Correspondence to: Department of Pharmacy, School of Medicine, University of Naples Federico II, Via Domenico Montesano, 49, 80131 Naples, Italy.Department of Pharmacy, School of Medicine, University of Naples Federico II, Naples, Italy; Task Force on Microbiome Studies, University of Naples Federico II, Naples, ItalyDepartment of Pharmacy, School of Medicine, University of Naples Federico II, Naples, ItalyThe antibiotic-induced intestinal injury (AIJ) is associated with diarrhoea and gastrointestinal discomfort. However, the pathological intestinal mechanisms and related side effects associated with antibiotic use/misuse may be counteracted by probiotics. This study aims to evaluate the effect and the protective mechanisms of a probiotic formulation containing Alkalihalobacillus clausii (formerly Bacillus clausii; BC) spores in an experimental model of AIJ. C57/Bl6J mice were orally challenged with a high dose of ceftriaxone for five days along with BC treatment which lasted up to the 15th day. Our results showed the beneficial effect of the probiotic in preserving colonic integrity and limiting tissue inflammation and immune cell infiltration in AIJ mice. BC increased tight junction expression and regulated the unbalanced production of colonic pro- and anti-inflammatory cytokines, converging toward the full resolution of the intestinal damage. These findings were supported by the histological evaluation of the intestinal mucosa, suggesting a potential restoration of mucus production. Notably, BC treatment increased gene transcription of the secretory products responsible for epithelium repair and mucus synthesis and normalized the expression of antimicrobial peptides involved in immune activation. Reconstruction of complex and diverse gut microbiota in antibiotic-induced dysbiosis was recorded upon BC supplementation. Specifically, the expansion of A. clausii, Prevotella rara and Eubacterium ruminatium drove intestinal microbiota rebalance by primarily impacting Bacteroidota members. Taken together, our data indicate that BC administration alleviates AIJ by multiple converging mechanisms leading to restoring gut integrity and homeostasis and reshaping microbiota composition.http://www.sciencedirect.com/science/article/pii/S0753332223006509Antibiotic-induced dysbiosisColon damageProbioticGut microbiotaImmunityInflammation
spellingShingle C. Pirozzi
N. Opallo
L. Coretti
A. Lama
C. Annunziata
F. Comella
S. Melini
E. Buommino
M.P. Mollica
G. Aviello
G. Mattace Raso
F. Lembo
R. Meli
Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice
Biomedicine & Pharmacotherapy
Antibiotic-induced dysbiosis
Colon damage
Probiotic
Gut microbiota
Immunity
Inflammation
title Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice
title_full Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice
title_fullStr Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice
title_full_unstemmed Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice
title_short Alkalihalobacillus clausii (formerly Bacillus clausii) spores lessen antibiotic-induced intestinal injury and reshape gut microbiota composition in mice
title_sort alkalihalobacillus clausii formerly bacillus clausii spores lessen antibiotic induced intestinal injury and reshape gut microbiota composition in mice
topic Antibiotic-induced dysbiosis
Colon damage
Probiotic
Gut microbiota
Immunity
Inflammation
url http://www.sciencedirect.com/science/article/pii/S0753332223006509
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