A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes

ABSTRACT Roux-en-Y gastric bypass (RYGB) is an effective weight loss surgery, resulting in a characteristic increase of fecal Gammaproteobacteria. The contribution of this compositional change to metabolic benefits of RYGB is currently debatable. Therefore, this study employed 16S rRNA gene sequenci...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Zhigang Liu, Isabelle Coales, Nicholas Penney, Julie A. K. McDonald, Jutarop Phetcharaburanin, Florian Seyfried, Jia V. Li
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2020
Materias:	fecal microbiota transplantation antibiotic effect gut microbiota metabolomics weight loss surgery Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/02c1e006a9a04f28bff0656a1aa7b9c5
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:02c1e006a9a04f28bff0656a1aa7b9c5
record_format	dspace
spelling	oai:doaj.org-article:02c1e006a9a04f28bff0656a1aa7b9c52021-12-02T18:15:46ZA Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes10.1128/mSystems.01047-202379-5077https://doaj.org/article/02c1e006a9a04f28bff0656a1aa7b9c52020-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSystems.01047-20https://doaj.org/toc/2379-5077ABSTRACT Roux-en-Y gastric bypass (RYGB) is an effective weight loss surgery, resulting in a characteristic increase of fecal Gammaproteobacteria. The contribution of this compositional change to metabolic benefits of RYGB is currently debatable. Therefore, this study employed 16S rRNA gene sequencing and metabolic profiling to monitor the dynamic colonization of the RYGB microbial consortium and their metabolic impact on the host. Eleven Wistar rats received vancomycin and enrofloxacin, followed by fecal microbiota transplantation (FMT) of cecal slurry obtained from either RYGB- or sham-operated rats. Urine and feces from the microbiota recipients (RYGB microbiota recipients [RYGBr], n = 6; sham microbiota recipients [SHAMr], n = 5) were collected pre- and post-antibiotics and 1, 3, 6, 9, and 16 days post-FMT. No significant differences in body weight and food intake were observed between RYGBr and SHAMr. While neither group reached the community richness of that of their donors, by day 6, both groups reached the richness and diversity of that prior to antibiotic treatment. However, the typical signature of RYGB microbiome—increased Enterobacteriaceae—was not replicated in these recipients after two consecutive FMT, suggesting that the environmental changes induced by the anatomical rearrangements of RYGB could be key for sustaining such a consortium. The transplanted bacteria did not induce the same metabolic signature of urine and feces as those previously reported in RYGB-operated rats. Future work is required to explore environmental factors that shape the RYGB microbiota in order to further investigate the metabolic functions of the RYGB microbiota, thereby teasing out the mechanisms of the RYGB surgery. IMPORTANCE Roux-en-Y gastric bypass (RYGB) surgery results in a long-term gut bacterial shift toward Gammaproteobacteria in both patients and rodents. The contribution of this compositional shift, or the RYGB bacterial consortium, to the metabolic benefit of the surgery remains debatable. It is unclear how well these bacteria colonize in an anatomically normal gut. This is a fundamental question in both defining the function of the RYGB microbiota and evaluating its potential as a nonsurgical treatment for obesity. We monitored the dynamic colonization of the RYGB bacterial consortium and observed that while approximately one-third of the bacterial taxa from the RYGB donor colonized in the gut of the nonoperated recipients, Gammaproteobacteria were unable to colonize for longer than 3 days. The study highlighted that a successful long-term colonization of Gammaproteobacteria-rich RYGB microbiota in nonsurgical animals requires key environmental factors that may be dictated by the intestinal anatomical modification by the surgery itself.Zhigang LiuIsabelle CoalesNicholas PenneyJulie A. K. McDonaldJutarop PhetcharaburaninFlorian SeyfriedJia V. LiAmerican Society for Microbiologyarticlefecal microbiota transplantationantibiotic effectgut microbiotametabolomicsweight loss surgeryMicrobiologyQR1-502ENmSystems, Vol 5, Iss 6 (2020)
institution	DOAJ
collection	DOAJ
language	EN
topic	fecal microbiota transplantation antibiotic effect gut microbiota metabolomics weight loss surgery Microbiology QR1-502
spellingShingle	fecal microbiota transplantation antibiotic effect gut microbiota metabolomics weight loss surgery Microbiology QR1-502 Zhigang Liu Isabelle Coales Nicholas Penney Julie A. K. McDonald Jutarop Phetcharaburanin Florian Seyfried Jia V. Li A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
description	ABSTRACT Roux-en-Y gastric bypass (RYGB) is an effective weight loss surgery, resulting in a characteristic increase of fecal Gammaproteobacteria. The contribution of this compositional change to metabolic benefits of RYGB is currently debatable. Therefore, this study employed 16S rRNA gene sequencing and metabolic profiling to monitor the dynamic colonization of the RYGB microbial consortium and their metabolic impact on the host. Eleven Wistar rats received vancomycin and enrofloxacin, followed by fecal microbiota transplantation (FMT) of cecal slurry obtained from either RYGB- or sham-operated rats. Urine and feces from the microbiota recipients (RYGB microbiota recipients [RYGBr], n = 6; sham microbiota recipients [SHAMr], n = 5) were collected pre- and post-antibiotics and 1, 3, 6, 9, and 16 days post-FMT. No significant differences in body weight and food intake were observed between RYGBr and SHAMr. While neither group reached the community richness of that of their donors, by day 6, both groups reached the richness and diversity of that prior to antibiotic treatment. However, the typical signature of RYGB microbiome—increased Enterobacteriaceae—was not replicated in these recipients after two consecutive FMT, suggesting that the environmental changes induced by the anatomical rearrangements of RYGB could be key for sustaining such a consortium. The transplanted bacteria did not induce the same metabolic signature of urine and feces as those previously reported in RYGB-operated rats. Future work is required to explore environmental factors that shape the RYGB microbiota in order to further investigate the metabolic functions of the RYGB microbiota, thereby teasing out the mechanisms of the RYGB surgery. IMPORTANCE Roux-en-Y gastric bypass (RYGB) surgery results in a long-term gut bacterial shift toward Gammaproteobacteria in both patients and rodents. The contribution of this compositional shift, or the RYGB bacterial consortium, to the metabolic benefit of the surgery remains debatable. It is unclear how well these bacteria colonize in an anatomically normal gut. This is a fundamental question in both defining the function of the RYGB microbiota and evaluating its potential as a nonsurgical treatment for obesity. We monitored the dynamic colonization of the RYGB bacterial consortium and observed that while approximately one-third of the bacterial taxa from the RYGB donor colonized in the gut of the nonoperated recipients, Gammaproteobacteria were unable to colonize for longer than 3 days. The study highlighted that a successful long-term colonization of Gammaproteobacteria-rich RYGB microbiota in nonsurgical animals requires key environmental factors that may be dictated by the intestinal anatomical modification by the surgery itself.
format	article
author	Zhigang Liu Isabelle Coales Nicholas Penney Julie A. K. McDonald Jutarop Phetcharaburanin Florian Seyfried Jia V. Li
author_facet	Zhigang Liu Isabelle Coales Nicholas Penney Julie A. K. McDonald Jutarop Phetcharaburanin Florian Seyfried Jia V. Li
author_sort	Zhigang Liu
title	A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
title_short	A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
title_full	A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
title_fullStr	A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
title_full_unstemmed	A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
title_sort	subset of roux-en-y gastric bypass bacterial consortium colonizes the gut of nonsurgical rats without inducing host-microbe metabolic changes
publisher	American Society for Microbiology
publishDate	2020
url	https://doaj.org/article/02c1e006a9a04f28bff0656a1aa7b9c5
work_keys_str_mv	AT zhigangliu asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT isabellecoales asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT nicholaspenney asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT julieakmcdonald asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT jutaropphetcharaburanin asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT florianseyfried asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT jiavli asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT zhigangliu subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT isabellecoales subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT nicholaspenney subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT julieakmcdonald subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT jutaropphetcharaburanin subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT florianseyfried subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges AT jiavli subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
_version_	1718378313667313664

A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes

Ejemplares similares