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Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics

Novel approaches to combating antibiotic resistance are needed given the ever-continuing rise of antibiotic resistance and the scarce discovery of new antibiotics. Little is known about the colonization dynamics and the role of intrinsic plant-food characteristics in this process. We sought to deter...

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Autores principales: Maeusli, Marlène, Skandalis, Nicholas, Lee, Bosul, Lu, Peggy, Miller, Sarah, Yan, Jun, Talyansky, Yuli, Li, Rachel, Reyna, Zeferino, Guerrero, Noel, Ulhaq, Amber, Slarve, Matthew, Theologidis, Ioannis, Spellberg, Brad, Luna, Brian
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241499/
https://www.ncbi.nlm.nih.gov/pubmed/35582906
http://dx.doi.org/10.1128/msphere.00071-22
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author Maeusli, Marlène
Skandalis, Nicholas
Lee, Bosul
Lu, Peggy
Miller, Sarah
Yan, Jun
Talyansky, Yuli
Li, Rachel
Reyna, Zeferino
Guerrero, Noel
Ulhaq, Amber
Slarve, Matthew
Theologidis, Ioannis
Spellberg, Brad
Luna, Brian
author_facet Maeusli, Marlène
Skandalis, Nicholas
Lee, Bosul
Lu, Peggy
Miller, Sarah
Yan, Jun
Talyansky, Yuli
Li, Rachel
Reyna, Zeferino
Guerrero, Noel
Ulhaq, Amber
Slarve, Matthew
Theologidis, Ioannis
Spellberg, Brad
Luna, Brian
author_sort Maeusli, Marlène
collection PubMed
description Novel approaches to combating antibiotic resistance are needed given the ever-continuing rise of antibiotic resistance and the scarce discovery of new antibiotics. Little is known about the colonization dynamics and the role of intrinsic plant-food characteristics in this process. We sought to determine whether plant fiber could alter colonization dynamics by antibiotic-resistant bacteria in the gut. We determined that ingestion of antibiotics in mice markedly enhanced gut colonization by a pathogenic extended-spectrum beta-lactamase-producing Escherichia coli strain of human origin, E. coli JJ1886 (ST131-H30Rx). Furthermore, ingestion of soluble acacia fiber before and after antibiotic exposure significantly reduced pathogenic E. coli colonization. 16S rRNA analysis and ex vivo cocultures demonstrated that fiber protected the microbiome by serving as a prebiotic, which induced native gut E. coli to inhibit pathogenic E. coli via colicin M. Fiber may be a useful prebiotic with which to administer antibiotics to protect human and livestock gut microbiomes against colonization from antibiotic-resistant, pathogenic bacteria. IMPORTANCE A One Health-based strategy—the concept that human health and animal health are interconnected with the environment—is necessary to determine the drivers of antibiotic resistance from food to the clinic. Moreover, humans can ingest antibiotic-resistant bacteria on food and asymptomatically, or “silently,” carry such bacteria in the gut long before they develop an opportunistic extraintestinal infection. Here, we determined that fiber-rich foods, in particular acacia fiber, may be a new, promising, and inexpensive prebiotic to administer with antibiotics to protect the mammalian (i.e., human and livestock) gut against such colonization by antibiotic-resistant, pathogenic bacteria.
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spelling pubmed-92414992022-06-30 Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics Maeusli, Marlène Skandalis, Nicholas Lee, Bosul Lu, Peggy Miller, Sarah Yan, Jun Talyansky, Yuli Li, Rachel Reyna, Zeferino Guerrero, Noel Ulhaq, Amber Slarve, Matthew Theologidis, Ioannis Spellberg, Brad Luna, Brian mSphere Research Article Novel approaches to combating antibiotic resistance are needed given the ever-continuing rise of antibiotic resistance and the scarce discovery of new antibiotics. Little is known about the colonization dynamics and the role of intrinsic plant-food characteristics in this process. We sought to determine whether plant fiber could alter colonization dynamics by antibiotic-resistant bacteria in the gut. We determined that ingestion of antibiotics in mice markedly enhanced gut colonization by a pathogenic extended-spectrum beta-lactamase-producing Escherichia coli strain of human origin, E. coli JJ1886 (ST131-H30Rx). Furthermore, ingestion of soluble acacia fiber before and after antibiotic exposure significantly reduced pathogenic E. coli colonization. 16S rRNA analysis and ex vivo cocultures demonstrated that fiber protected the microbiome by serving as a prebiotic, which induced native gut E. coli to inhibit pathogenic E. coli via colicin M. Fiber may be a useful prebiotic with which to administer antibiotics to protect human and livestock gut microbiomes against colonization from antibiotic-resistant, pathogenic bacteria. IMPORTANCE A One Health-based strategy—the concept that human health and animal health are interconnected with the environment—is necessary to determine the drivers of antibiotic resistance from food to the clinic. Moreover, humans can ingest antibiotic-resistant bacteria on food and asymptomatically, or “silently,” carry such bacteria in the gut long before they develop an opportunistic extraintestinal infection. Here, we determined that fiber-rich foods, in particular acacia fiber, may be a new, promising, and inexpensive prebiotic to administer with antibiotics to protect the mammalian (i.e., human and livestock) gut against such colonization by antibiotic-resistant, pathogenic bacteria. American Society for Microbiology 2022-05-18 /pmc/articles/PMC9241499/ /pubmed/35582906 http://dx.doi.org/10.1128/msphere.00071-22 Text en Copyright © 2022 Maeusli et al. https://creativecommons.org/licenses/by/4.0/This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Research Article
Maeusli, Marlène
Skandalis, Nicholas
Lee, Bosul
Lu, Peggy
Miller, Sarah
Yan, Jun
Talyansky, Yuli
Li, Rachel
Reyna, Zeferino
Guerrero, Noel
Ulhaq, Amber
Slarve, Matthew
Theologidis, Ioannis
Spellberg, Brad
Luna, Brian
Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics
title Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics
title_full Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics
title_fullStr Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics
title_full_unstemmed Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics
title_short Acacia Fiber Protects the Gut from Extended-Spectrum Beta-Lactamase (ESBL)-Producing Escherichia coli Colonization Enabled by Antibiotics
title_sort acacia fiber protects the gut from extended-spectrum beta-lactamase (esbl)-producing escherichia coli colonization enabled by antibiotics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9241499/
https://www.ncbi.nlm.nih.gov/pubmed/35582906
http://dx.doi.org/10.1128/msphere.00071-22
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