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...
Saved in:
Main Authors: | , , , , , , , , , , , , , |
---|---|
Format: | Article |
Language: | English |
Published: |
Nature Portfolio
2025-01-01
|
Series: | Nature Communications |
Online Access: | https://doi.org/10.1038/s41467-024-55800-y |
Tags: |
Add Tag
No Tags, Be the first to tag this record!
|
_version_ | 1841544505220661248 |
---|---|
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. |
format | Article |
id | doaj-art-47713110ee6348f7b06a39af661bc7a1 |
institution | Kabale University |
issn | 2041-1723 |
language | English |
publishDate | 2025-01-01 |
publisher | Nature Portfolio |
record_format | Article |
series | Nature Communications |
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 |
work_keys_str_mv | AT evadhalmasi klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT leaeisenhard klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT lisaosbelt klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT tillrobinlesker klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT annacvetter klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT neleknischewski klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT agataannabielecka klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT achimgronow klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT uthayakumarmuthukumarasamy klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT mariewende klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT carolinetawk klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT meinaneumannschaal klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT markbronstrup klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner AT tillstrowig klebsiellaoxytocafacilitatesmicrobiomerecoveryviaantibioticdegradationandrestorescolonizationresistanceinadietdependentmanner |