Cargando…

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

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 me...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Zhigang, Coales, Isabelle, Penney, Nicholas, McDonald, Julie A. K., Phetcharaburanin, Jutarop, Seyfried, Florian, Li, Jia V.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: American Society for Microbiology 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579838/
https://www.ncbi.nlm.nih.gov/pubmed/33293406
http://dx.doi.org/10.1128/mSystems.01047-20
_version_ 1784596504526192640
author Liu, Zhigang
Coales, Isabelle
Penney, Nicholas
McDonald, Julie A. K.
Phetcharaburanin, Jutarop
Seyfried, Florian
Li, Jia V.
author_facet Liu, Zhigang
Coales, Isabelle
Penney, Nicholas
McDonald, Julie A. K.
Phetcharaburanin, Jutarop
Seyfried, Florian
Li, Jia V.
author_sort Liu, Zhigang
collection PubMed
description 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 Online
Article
Text
id pubmed-8579838
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher American Society for Microbiology
record_format MEDLINE/PubMed
spelling pubmed-85798382021-11-10 A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes Liu, Zhigang Coales, Isabelle Penney, Nicholas McDonald, Julie A. K. Phetcharaburanin, Jutarop Seyfried, Florian Li, Jia V. mSystems Research Article 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. American Society for Microbiology 2020-12-08 /pmc/articles/PMC8579838/ /pubmed/33293406 http://dx.doi.org/10.1128/mSystems.01047-20 Text en Copyright © 2020 Liu 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
Liu, Zhigang
Coales, Isabelle
Penney, Nicholas
McDonald, Julie A. K.
Phetcharaburanin, Jutarop
Seyfried, Florian
Li, Jia V.
A Subset of Roux-en-Y Gastric Bypass Bacterial Consortium Colonizes the Gut of Nonsurgical Rats without Inducing Host-Microbe Metabolic Changes
title 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_short 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
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8579838/
https://www.ncbi.nlm.nih.gov/pubmed/33293406
http://dx.doi.org/10.1128/mSystems.01047-20
work_keys_str_mv AT liuzhigang asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT coalesisabelle asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT penneynicholas asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT mcdonaldjulieak asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT phetcharaburaninjutarop asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT seyfriedflorian asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT lijiav asubsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT liuzhigang subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT coalesisabelle subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT penneynicholas subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT mcdonaldjulieak subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT phetcharaburaninjutarop subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT seyfriedflorian subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges
AT lijiav subsetofrouxenygastricbypassbacterialconsortiumcolonizesthegutofnonsurgicalratswithoutinducinghostmicrobemetabolicchanges