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Metagenomic reconstructions of gut microbial metabolism in weanling pigs

BACKGROUND: The piglets’ transition from milk to solid feed induces a succession of bacterial communities, enhancing the hosts’ ability to harvest energy from dietary carbohydrates. To reconstruct microbial carbohydrate metabolism in weanling pigs, this study combined 16S rRNA gene sequencing (n = 1...

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Autores principales: Wang, Weilan, Hu, Huifeng, Zijlstra, Ruurd T., Zheng, Jinshui, Gänzle, Michael G.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436221/
https://www.ncbi.nlm.nih.gov/pubmed/30914068
http://dx.doi.org/10.1186/s40168-019-0662-1
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author Wang, Weilan
Hu, Huifeng
Zijlstra, Ruurd T.
Zheng, Jinshui
Gänzle, Michael G.
author_facet Wang, Weilan
Hu, Huifeng
Zijlstra, Ruurd T.
Zheng, Jinshui
Gänzle, Michael G.
author_sort Wang, Weilan
collection PubMed
description BACKGROUND: The piglets’ transition from milk to solid feed induces a succession of bacterial communities, enhancing the hosts’ ability to harvest energy from dietary carbohydrates. To reconstruct microbial carbohydrate metabolism in weanling pigs, this study combined 16S rRNA gene sequencing (n = 191) and shotgun metagenomics (n = 72). RESULTS: Time and wheat content in feed explained most of the variation of the microbiota as assessed by 16S rRNA gene sequencing in weanling pigs. De novo metagenomic binning reconstructed 360 high-quality genomes that represented 11 prokaryotic and 1 archaeal phylum. Analysis of carbohydrate metabolism in these genomes revealed that starch fermentation is carried out by a consortium of Firmicutes expressing extracellular α-(1 → 4)-glucan branching enzyme (GH13) and Bacteroidetes expressing periplasmic neopullulanase (GH13) and α-glucosidase (GH97). Fructans were degraded by extracellular GH32 enzymes from Bacteriodetes and Lactobacillus. Lactose fermentation by β-galactosidases (GH2 and GH42) was identified in Firmicutes. In conclusion, the assembly of 360 high-quality genomes as the first metagenomic reference for swine intestinal microbiota allowed identification of key microbial contributors to degradation of starch, fructans, and lactose. CONCLUSIONS: Microbial consortia that are responsible for degradation of these glycans differ substantially from the microbial consortia that degrade the same glycans in humans. Our study thus enables improvement of feeding models with higher feed efficiency and better pathogen control for weanling pigs. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0662-1) contains supplementary material, which is available to authorized users.
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spelling pubmed-64362212019-04-08 Metagenomic reconstructions of gut microbial metabolism in weanling pigs Wang, Weilan Hu, Huifeng Zijlstra, Ruurd T. Zheng, Jinshui Gänzle, Michael G. Microbiome Research BACKGROUND: The piglets’ transition from milk to solid feed induces a succession of bacterial communities, enhancing the hosts’ ability to harvest energy from dietary carbohydrates. To reconstruct microbial carbohydrate metabolism in weanling pigs, this study combined 16S rRNA gene sequencing (n = 191) and shotgun metagenomics (n = 72). RESULTS: Time and wheat content in feed explained most of the variation of the microbiota as assessed by 16S rRNA gene sequencing in weanling pigs. De novo metagenomic binning reconstructed 360 high-quality genomes that represented 11 prokaryotic and 1 archaeal phylum. Analysis of carbohydrate metabolism in these genomes revealed that starch fermentation is carried out by a consortium of Firmicutes expressing extracellular α-(1 → 4)-glucan branching enzyme (GH13) and Bacteroidetes expressing periplasmic neopullulanase (GH13) and α-glucosidase (GH97). Fructans were degraded by extracellular GH32 enzymes from Bacteriodetes and Lactobacillus. Lactose fermentation by β-galactosidases (GH2 and GH42) was identified in Firmicutes. In conclusion, the assembly of 360 high-quality genomes as the first metagenomic reference for swine intestinal microbiota allowed identification of key microbial contributors to degradation of starch, fructans, and lactose. CONCLUSIONS: Microbial consortia that are responsible for degradation of these glycans differ substantially from the microbial consortia that degrade the same glycans in humans. Our study thus enables improvement of feeding models with higher feed efficiency and better pathogen control for weanling pigs. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s40168-019-0662-1) contains supplementary material, which is available to authorized users. BioMed Central 2019-03-26 /pmc/articles/PMC6436221/ /pubmed/30914068 http://dx.doi.org/10.1186/s40168-019-0662-1 Text en © The Author(s). 2019 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Wang, Weilan
Hu, Huifeng
Zijlstra, Ruurd T.
Zheng, Jinshui
Gänzle, Michael G.
Metagenomic reconstructions of gut microbial metabolism in weanling pigs
title Metagenomic reconstructions of gut microbial metabolism in weanling pigs
title_full Metagenomic reconstructions of gut microbial metabolism in weanling pigs
title_fullStr Metagenomic reconstructions of gut microbial metabolism in weanling pigs
title_full_unstemmed Metagenomic reconstructions of gut microbial metabolism in weanling pigs
title_short Metagenomic reconstructions of gut microbial metabolism in weanling pigs
title_sort metagenomic reconstructions of gut microbial metabolism in weanling pigs
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6436221/
https://www.ncbi.nlm.nih.gov/pubmed/30914068
http://dx.doi.org/10.1186/s40168-019-0662-1
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