Gut microbiome signatures of nursing home residents carrying Enterobacteria producing extended-spectrum [beta]-lactamases

Background The prevalence of extended beta-lactamase producing Enterobacteriaceae (ESBL-E) has been constantly increasing over the last few decades. These microorganisms that have acquired broad antibiotic resistance are now common human pathogens. Changes in the gut microbiome, induced by antibioti...

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Published inAntimicrobial resistance & infection control Vol. 9; no. 1
Main Authors Le Bastard, Quentin, Chapelet, Guillaume, Birgand, Gabriel, Hillmann, Benjamin M, Javaudin, François, Hayatgheib, Niki, Bourigault, Céline, Bemer, Pascale, De Decker, Laure, Batard, Eric, Lepelletier, Didier, Montassier, Emmanuel
Format Journal Article
LanguageEnglish
Published BioMed Central Ltd 14.07.2020
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ISSN2047-2994
2047-2994
DOI10.1186/s13756-020-00773-y

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Abstract Background The prevalence of extended beta-lactamase producing Enterobacteriaceae (ESBL-E) has been constantly increasing over the last few decades. These microorganisms that have acquired broad antibiotic resistance are now common human pathogens. Changes in the gut microbiome, induced by antibiotics or other drugs, enable expansion of these microorganisms, but the mechanisms are not yet fully understood. Objectives The main objective was to identify specific bacteria and functional pathways and genes characterizing the gut microbiome of nursing home residents carrying ESBL-E, using metagenomics. Subjects and methods We included 144 residents living in two different nursing homes. All fecal samples were screened for ESBL-E and gut microbiome was characterized using shallow shotgun metagenomic DNA sequencing. Results Ten nursing home residents were colonized by ESBL-E, namely Escherichia coli, Klebsiella pneumoniae and Enterobacter cloacae species, and were compared to non-carriers. We found that ESBL-E carriers had an alteration in within-sample diversity. Using a bootstrap algorithm, we found that the gut microbiome of ESBL-E carriers was depleted in butyrate-producing species, enriched in succinate-producing species and enriched in pathways involved in intracellular pH homeostasis compared to non-carriers individuals. Several energy metabolism pathways were overrepresented in ESBL-E carriers suggesting a greater ability to metabolize multiple microbiota and mucus layer-derived nutrients. Conclusions The gut microbiome of ESBL-E carriers in nursing homes harbors specific taxonomic and functional characteristics, conferring an environment that enables Enterobacteriaceae expansion. Here we describe new functional features associated with ESBL-E carriage that could help us to elucidate the complex interactions leading to colonization persistence in the human gut microbiota. Keywords: Microbiome, Antibiotic resistance, Enterobacteriaceae, Metabolome
AbstractList Background The prevalence of extended beta-lactamase producing Enterobacteriaceae (ESBL-E) has been constantly increasing over the last few decades. These microorganisms that have acquired broad antibiotic resistance are now common human pathogens. Changes in the gut microbiome, induced by antibiotics or other drugs, enable expansion of these microorganisms, but the mechanisms are not yet fully understood. Objectives The main objective was to identify specific bacteria and functional pathways and genes characterizing the gut microbiome of nursing home residents carrying ESBL-E, using metagenomics. Subjects and methods We included 144 residents living in two different nursing homes. All fecal samples were screened for ESBL-E and gut microbiome was characterized using shallow shotgun metagenomic DNA sequencing. Results Ten nursing home residents were colonized by ESBL-E, namely Escherichia coli, Klebsiella pneumoniae and Enterobacter cloacae species, and were compared to non-carriers. We found that ESBL-E carriers had an alteration in within-sample diversity. Using a bootstrap algorithm, we found that the gut microbiome of ESBL-E carriers was depleted in butyrate-producing species, enriched in succinate-producing species and enriched in pathways involved in intracellular pH homeostasis compared to non-carriers individuals. Several energy metabolism pathways were overrepresented in ESBL-E carriers suggesting a greater ability to metabolize multiple microbiota and mucus layer-derived nutrients. Conclusions The gut microbiome of ESBL-E carriers in nursing homes harbors specific taxonomic and functional characteristics, conferring an environment that enables Enterobacteriaceae expansion. Here we describe new functional features associated with ESBL-E carriage that could help us to elucidate the complex interactions leading to colonization persistence in the human gut microbiota. Keywords: Microbiome, Antibiotic resistance, Enterobacteriaceae, Metabolome
The prevalence of extended beta-lactamase producing Enterobacteriaceae (ESBL-E) has been constantly increasing over the last few decades. These microorganisms that have acquired broad antibiotic resistance are now common human pathogens. Changes in the gut microbiome, induced by antibiotics or other drugs, enable expansion of these microorganisms, but the mechanisms are not yet fully understood. The main objective was to identify specific bacteria and functional pathways and genes characterizing the gut microbiome of nursing home residents carrying ESBL-E, using metagenomics. We included 144 residents living in two different nursing homes. All fecal samples were screened for ESBL-E and gut microbiome was characterized using shallow shotgun metagenomic DNA sequencing. Ten nursing home residents were colonized by ESBL-E, namely Escherichia coli, Klebsiella pneumoniae and Enterobacter cloacae species, and were compared to non-carriers. We found that ESBL-E carriers had an alteration in within-sample diversity. Using a bootstrap algorithm, we found that the gut microbiome of ESBL-E carriers was depleted in butyrate-producing species, enriched in succinate-producing species and enriched in pathways involved in intracellular pH homeostasis compared to non-carriers individuals. Several energy metabolism pathways were overrepresented in ESBL-E carriers suggesting a greater ability to metabolize multiple microbiota and mucus layer-derived nutrients. The gut microbiome of ESBL-E carriers in nursing homes harbors specific taxonomic and functional characteristics, conferring an environment that enables Enterobacteriaceae expansion. Here we describe new functional features associated with ESBL-E carriage that could help us to elucidate the complex interactions leading to colonization persistence in the human gut microbiota.
Audience Academic
Author Hayatgheib, Niki
Batard, Eric
Montassier, Emmanuel
Hillmann, Benjamin M
Bemer, Pascale
Bourigault, Céline
Birgand, Gabriel
De Decker, Laure
Lepelletier, Didier
Le Bastard, Quentin
Chapelet, Guillaume
Javaudin, François
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DOI 10.1186/s13756-020-00773-y
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Snippet Background The prevalence of extended beta-lactamase producing Enterobacteriaceae (ESBL-E) has been constantly increasing over the last few decades. These...
The prevalence of extended beta-lactamase producing Enterobacteriaceae (ESBL-E) has been constantly increasing over the last few decades. These microorganisms...
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SubjectTerms Antibiotics
Bacteria
Beta lactamases
DNA sequencing
Escherichia coli
Microbial drug resistance
Microbiota (Symbiotic organisms)
Nursing home patients
Nursing homes
Physiological aspects
Title Gut microbiome signatures of nursing home residents carrying Enterobacteria producing extended-spectrum [beta]-lactamases
Volume 9
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