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Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model

Ruminant animals possess a characteristic four-compartment stomach (rumen, reticulum, omasum, and abomasum) that is specialized for pre-intestinal digestion of plant materials. Of these four compartments, the rumen is the largest. The rumen’s diverse microbial community has been well studied. Howeve...

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Autores principales: Lei, Yu, Zhang, Ke, Guo, Mengmeng, Li, Guanwei, Li, Chao, Li, Bibo, Yang, Yuxin, Chen, Yulin, Wang, Xiaolong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6104157/
https://www.ncbi.nlm.nih.gov/pubmed/30158908
http://dx.doi.org/10.3389/fmicb.2018.01846
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author Lei, Yu
Zhang, Ke
Guo, Mengmeng
Li, Guanwei
Li, Chao
Li, Bibo
Yang, Yuxin
Chen, Yulin
Wang, Xiaolong
author_facet Lei, Yu
Zhang, Ke
Guo, Mengmeng
Li, Guanwei
Li, Chao
Li, Bibo
Yang, Yuxin
Chen, Yulin
Wang, Xiaolong
author_sort Lei, Yu
collection PubMed
description Ruminant animals possess a characteristic four-compartment stomach (rumen, reticulum, omasum, and abomasum) that is specialized for pre-intestinal digestion of plant materials. Of these four compartments, the rumen is the largest. The rumen’s diverse microbial community has been well studied. However, the current understanding of microbial profiles in the reticulum, omasum and abomasum are lacking. In the present study, fluid samples from the reticulum, omasum, and abomasum of goats at 3, 7, 14, 21, 28, 42, and 56 days after birth, as well as the negative controls (NC) used for microbial DNA extraction, were subjected to 16S rRNA sequencing. By filtering operational taxonomic units (OTUs) in NC, distinct temporal distributions of microbes were observed in the different compartments, we showed that the OTUs in control samples had a large effect to the samples with low microbial density. In addition, Proteobacteria gradually decreased with age from days 3 to 56 in all three compartments, and the relative abundance of Bacteroidetes increased from 24.15% (Day 3) to 52.03% (Day 56) in abomasum. Network analysis revealed that Prevotellaceae_UGG-03 and Rikenellaceae_RC9 were positively correlated with Prevotella_1, lending support to the well understood fact that cellulose is well digested in compound stomachs prior to the rumen. Pathway analysis revealed that gene expression in abomasum at Day 3 were primarily related to Glycolysis/Gluconeogenesis and Pyruvate metabolism, suggesting that colostrum digestion is the dominant function of the abomasum at an early age. These findings combined with other recent rumen microbiota data show that the microbiome landscape represents three distinct stages in ruminant stomachs. The first stage is to gain access to external microorganisms at Day 0–14, the secondary stage is for microbial transition at Day 14–28, and the third stage is for exogenous and endogenous microbial colonization beyond Day 28 of age. Our results provide insight into microbiota dynamics in ruminant stomachs, and will facilitate efforts for the maintenance of gastrointestinal balance and intervention with starter diets in juvenile ruminants during early development.
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spelling pubmed-61041572018-08-29 Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model Lei, Yu Zhang, Ke Guo, Mengmeng Li, Guanwei Li, Chao Li, Bibo Yang, Yuxin Chen, Yulin Wang, Xiaolong Front Microbiol Microbiology Ruminant animals possess a characteristic four-compartment stomach (rumen, reticulum, omasum, and abomasum) that is specialized for pre-intestinal digestion of plant materials. Of these four compartments, the rumen is the largest. The rumen’s diverse microbial community has been well studied. However, the current understanding of microbial profiles in the reticulum, omasum and abomasum are lacking. In the present study, fluid samples from the reticulum, omasum, and abomasum of goats at 3, 7, 14, 21, 28, 42, and 56 days after birth, as well as the negative controls (NC) used for microbial DNA extraction, were subjected to 16S rRNA sequencing. By filtering operational taxonomic units (OTUs) in NC, distinct temporal distributions of microbes were observed in the different compartments, we showed that the OTUs in control samples had a large effect to the samples with low microbial density. In addition, Proteobacteria gradually decreased with age from days 3 to 56 in all three compartments, and the relative abundance of Bacteroidetes increased from 24.15% (Day 3) to 52.03% (Day 56) in abomasum. Network analysis revealed that Prevotellaceae_UGG-03 and Rikenellaceae_RC9 were positively correlated with Prevotella_1, lending support to the well understood fact that cellulose is well digested in compound stomachs prior to the rumen. Pathway analysis revealed that gene expression in abomasum at Day 3 were primarily related to Glycolysis/Gluconeogenesis and Pyruvate metabolism, suggesting that colostrum digestion is the dominant function of the abomasum at an early age. These findings combined with other recent rumen microbiota data show that the microbiome landscape represents three distinct stages in ruminant stomachs. The first stage is to gain access to external microorganisms at Day 0–14, the secondary stage is for microbial transition at Day 14–28, and the third stage is for exogenous and endogenous microbial colonization beyond Day 28 of age. Our results provide insight into microbiota dynamics in ruminant stomachs, and will facilitate efforts for the maintenance of gastrointestinal balance and intervention with starter diets in juvenile ruminants during early development. Frontiers Media S.A. 2018-08-15 /pmc/articles/PMC6104157/ /pubmed/30158908 http://dx.doi.org/10.3389/fmicb.2018.01846 Text en Copyright © 2018 Lei, Zhang, Guo, Li, Li, Li, Yang, Chen and Wang. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Lei, Yu
Zhang, Ke
Guo, Mengmeng
Li, Guanwei
Li, Chao
Li, Bibo
Yang, Yuxin
Chen, Yulin
Wang, Xiaolong
Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model
title Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model
title_full Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model
title_fullStr Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model
title_full_unstemmed Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model
title_short Exploring the Spatial-Temporal Microbiota of Compound Stomachs in a Pre-weaned Goat Model
title_sort exploring the spatial-temporal microbiota of compound stomachs in a pre-weaned goat model
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6104157/
https://www.ncbi.nlm.nih.gov/pubmed/30158908
http://dx.doi.org/10.3389/fmicb.2018.01846
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