Gut microbiome signatures of nursing home residents carrying Enterobacteria producing extended-spectrum β-lactamases

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.

Long-term gut colonization with ESBL-producingEscherichia coliin participants without known risk factors from the southeastern United States

“…Alpha and beta diversity analysis suggests that ESBL-E carriage was not associated with substantially different gut microbiome composition or diversity, consistent with the results of other studies (68, 69). However, pairwise analysis identified multiple taxa with significantly different abundance in carriers and non-carriers.…”

Fecal Microbiome Features Associated with Extended-Spectrum β-Lactamase-Producing Enterobacterales Carriage in Dairy Heifers

“…and Bacteroidales spp. were more abundant in the ESBL-PE carrier group and, therefore, could be considered as a potential marker for ESBL-PE carriers, as was suggested previously [12,16]. Lysinibacillus, Ruminococcaceae and Treponema were more abundant in the noncarrier group and may also serve as potential markers.…”

“…In a more recent study from Thailand, where ESBL-PE colonization is high, the most notable difference was that the phylum Bacteroidetes was more abundant in ESBL-PE noncarriers [ 15 ]. In a study carried out in France, taxonomic and functional differences were also observed between the microbiome of ESBL-PE carriers versus noncarriers, including lower diversity in ESBL carriers than noncarriers [ 16 ]. Intestinal colonization is recognized as a key risk factor regarding ESBL-PE dissemination.…”

Bridging gut microbiota composition with extended-spectrum beta-lactamase Enterobacteriales faecal carriage in critically ill patients (microbe cohort study)

“…The same comparison in the Amerindian Wayampi community showed that ESBL-E faecal carriers had a lower gut bacteriobiota α-diversity than non-carriers while taxa belonging to the genera Desulfovibrio and Oscillospira (Ruminococcaceae) were associated with the absence of ESBL-E faecal carriage and Prevotella was associated with ESBL-E faecal carriage [ 19 ]. Comparison of gut bacteriobiota between ESBL-E faecal carriers and non-carriers, not in the community but in nursing home residents, found a decreased α-diversity in ESBL-E faecal carriers with a depletion in butyrate-producing bacterial species and an enrichment in succinate-producing bacterial species [ 20 ]. While the impact of microbiota on MDRO is mediated by indirect mechanisms including local and systemic immune activation and by direct mechanisms including competition for nutrients between species composing the microbiota and direct toxicity, none of these studies took ESBL-E bacterial species into account.…”