Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner

Abstract Competition among bacteria for carbohydrates is pivotal for colonization resistance (CR). However, the impact of Western-style diets on CR remains unclear. Here we show how the competition between Klebsiella oxytoca and Klebsiella pneumoniae is modulated by consuming one of three Western-st...

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Main Authors: Éva d. H. Almási, Lea Eisenhard, Lisa Osbelt, Till Robin Lesker, Anna C. Vetter, Nele Knischewski, Agata Anna Bielecka, Achim Gronow, Uthayakumar Muthukumarasamy, Marie Wende, Caroline Tawk, Meina Neumann-Schaal, Mark Brönstrup, Till Strowig
Format: Article
Language:English
Published: Nature Portfolio 2025-01-01
Series:Nature Communications
Online Access:https://doi.org/10.1038/s41467-024-55800-y
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author Éva d. H. Almási
Lea Eisenhard
Lisa Osbelt
Till Robin Lesker
Anna C. Vetter
Nele Knischewski
Agata Anna Bielecka
Achim Gronow
Uthayakumar Muthukumarasamy
Marie Wende
Caroline Tawk
Meina Neumann-Schaal
Mark Brönstrup
Till Strowig
author_facet Éva d. H. Almási
Lea Eisenhard
Lisa Osbelt
Till Robin Lesker
Anna C. Vetter
Nele Knischewski
Agata Anna Bielecka
Achim Gronow
Uthayakumar Muthukumarasamy
Marie Wende
Caroline Tawk
Meina Neumann-Schaal
Mark Brönstrup
Till Strowig
author_sort Éva d. H. Almási
collection DOAJ
description Abstract Competition among bacteria for carbohydrates is pivotal for colonization resistance (CR). However, the impact of Western-style diets on CR remains unclear. Here we show how the competition between Klebsiella oxytoca and Klebsiella pneumoniae is modulated by consuming one of three Western-style diets characterized by high-starch, high-sucrose, or high-fat/high-sucrose content. In vivo competition experiments in ampicillin-treated mice reveal that K. oxytoca promotes K. pneumoniae decolonization on all dietary backgrounds. However, mice on the high-fat/high-sucrose diet show reduced pathogen clearance. Microbiome analysis reveals that the combination of Western-style diets and ampicillin treatment synergize in microbiome impairment, particularly noticeable in the presence of high dietary fat content. The diet-independent degradation of ampicillin in the gut lumen by K. oxytoca beta-lactamases facilitates rapid commensal outgrowth, which is required for subsequent pathogen clearance. Our findings provide insights into how diet modulates functional microbiome recovery and K. oxytoca-mediated pathogen elimination from the gut.
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spelling doaj-art-47713110ee6348f7b06a39af661bc7a12025-01-12T12:30:09ZengNature PortfolioNature Communications2041-17232025-01-0116111310.1038/s41467-024-55800-yKlebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent mannerÉva d. H. Almási0Lea Eisenhard1Lisa Osbelt2Till Robin Lesker3Anna C. Vetter4Nele Knischewski5Agata Anna Bielecka6Achim Gronow7Uthayakumar Muthukumarasamy8Marie Wende9Caroline Tawk10Meina Neumann-Schaal11Mark Brönstrup12Till Strowig13Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Chemical Biology, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Bacterial Metabolomics, Leibniz Institute DSMZ-German Collection of Microorganisms and Cell CulturesDepartment of Chemical Biology, Helmholtz Centre for Infection Research (HZI)Department of Microbial Immune Regulation, Helmholtz Centre for Infection Research (HZI)Abstract Competition among bacteria for carbohydrates is pivotal for colonization resistance (CR). However, the impact of Western-style diets on CR remains unclear. Here we show how the competition between Klebsiella oxytoca and Klebsiella pneumoniae is modulated by consuming one of three Western-style diets characterized by high-starch, high-sucrose, or high-fat/high-sucrose content. In vivo competition experiments in ampicillin-treated mice reveal that K. oxytoca promotes K. pneumoniae decolonization on all dietary backgrounds. However, mice on the high-fat/high-sucrose diet show reduced pathogen clearance. Microbiome analysis reveals that the combination of Western-style diets and ampicillin treatment synergize in microbiome impairment, particularly noticeable in the presence of high dietary fat content. The diet-independent degradation of ampicillin in the gut lumen by K. oxytoca beta-lactamases facilitates rapid commensal outgrowth, which is required for subsequent pathogen clearance. Our findings provide insights into how diet modulates functional microbiome recovery and K. oxytoca-mediated pathogen elimination from the gut.https://doi.org/10.1038/s41467-024-55800-y
spellingShingle Éva d. H. Almási
Lea Eisenhard
Lisa Osbelt
Till Robin Lesker
Anna C. Vetter
Nele Knischewski
Agata Anna Bielecka
Achim Gronow
Uthayakumar Muthukumarasamy
Marie Wende
Caroline Tawk
Meina Neumann-Schaal
Mark Brönstrup
Till Strowig
Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner
Nature Communications
title Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner
title_full Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner
title_fullStr Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner
title_full_unstemmed Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner
title_short Klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet-dependent manner
title_sort klebsiella oxytoca facilitates microbiome recovery via antibiotic degradation and restores colonization resistance in a diet dependent manner
url https://doi.org/10.1038/s41467-024-55800-y
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