Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health

Abstract Background Altered gut microbiota has emerged as a major contributing factor to the etiology of chronic conditions in humans. Antibiotic exposure, historically dating back to the mass production of penicillin in the early 1940s, has been proposed as a primary contributor to the cumulative a...

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Main Authors: Yumin Han, Teh Min Teng, Juwon Han, Heenam Stanley Kim
Format: Article
Language:English
Published: BMC 2025-02-01
Series:Microbiome
Subjects:
Online Access:https://doi.org/10.1186/s40168-024-02023-4
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author Yumin Han
Teh Min Teng
Juwon Han
Heenam Stanley Kim
author_facet Yumin Han
Teh Min Teng
Juwon Han
Heenam Stanley Kim
author_sort Yumin Han
collection DOAJ
description Abstract Background Altered gut microbiota has emerged as a major contributing factor to the etiology of chronic conditions in humans. Antibiotic exposure, historically dating back to the mass production of penicillin in the early 1940s, has been proposed as a primary contributor to the cumulative alteration of microbiota over generations. However, the mechanistic link between the antibiotics-altered microbiota and chronic conditions remains unclear. Results In this study, we discovered that variants of the key beneficial gut microbe, Akkermansia muciniphila, were selected upon exposure to penicillin. These variants had mutations in the promoter of a TEM-type β-lactamase gene or pur genes encoding the de novo purine biosynthesis pathway, and they exhibited compromised abilities to mitigate host obesity in a murine model. Notably, variants of A. muciniphila are prevalent in the human microbiome worldwide. Conclusions These findings highlight a previously unknown mechanism through which antibiotics influence host health by affecting the beneficial capacities of the key gut microbes. Furthermore, the global prevalence of A. muciniphila variants raises the possibility that these variants contribute to global epidemics of chronic conditions, warranting further investigations in human populations. Video Abstract
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issn 2049-2618
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spelling doaj-art-eaa98c4242234e4889b8e9615264d54e2025-02-09T12:46:46ZengBMCMicrobiome2049-26182025-02-0113111510.1186/s40168-024-02023-4Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic healthYumin Han0Teh Min Teng1Juwon Han2Heenam Stanley Kim3Division of Biosystems & Biomedical Sciences, College of Health SciencesDivision of Biosystems & Biomedical Sciences, College of Health SciencesDivision of Biosystems & Biomedical Sciences, College of Health SciencesDivision of Biosystems & Biomedical Sciences, College of Health SciencesAbstract Background Altered gut microbiota has emerged as a major contributing factor to the etiology of chronic conditions in humans. Antibiotic exposure, historically dating back to the mass production of penicillin in the early 1940s, has been proposed as a primary contributor to the cumulative alteration of microbiota over generations. However, the mechanistic link between the antibiotics-altered microbiota and chronic conditions remains unclear. Results In this study, we discovered that variants of the key beneficial gut microbe, Akkermansia muciniphila, were selected upon exposure to penicillin. These variants had mutations in the promoter of a TEM-type β-lactamase gene or pur genes encoding the de novo purine biosynthesis pathway, and they exhibited compromised abilities to mitigate host obesity in a murine model. Notably, variants of A. muciniphila are prevalent in the human microbiome worldwide. Conclusions These findings highlight a previously unknown mechanism through which antibiotics influence host health by affecting the beneficial capacities of the key gut microbes. Furthermore, the global prevalence of A. muciniphila variants raises the possibility that these variants contribute to global epidemics of chronic conditions, warranting further investigations in human populations. Video Abstracthttps://doi.org/10.1186/s40168-024-02023-4Akkermansia muciniphilaGut microbiomeAntibiotic resistancePersistenceTEM-type β-lactamaseThe de novo purine biosynthesis pathway
spellingShingle Yumin Han
Teh Min Teng
Juwon Han
Heenam Stanley Kim
Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health
Microbiome
Akkermansia muciniphila
Gut microbiome
Antibiotic resistance
Persistence
TEM-type β-lactamase
The de novo purine biosynthesis pathway
title Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health
title_full Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health
title_fullStr Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health
title_full_unstemmed Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health
title_short Antibiotic-associated changes in Akkermansia muciniphila alter its effects on host metabolic health
title_sort antibiotic associated changes in akkermansia muciniphila alter its effects on host metabolic health
topic Akkermansia muciniphila
Gut microbiome
Antibiotic resistance
Persistence
TEM-type β-lactamase
The de novo purine biosynthesis pathway
url https://doi.org/10.1186/s40168-024-02023-4
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