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Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency

Rumen microbiome composition and functionality is linked to animal feed efficiency, particularly for bovine ruminants. To investigate this in sheep, we compared rumen bacterial and archaeal populations (and predicted metabolic processes) of sheep divergent for the feed efficiency trait feed conversi...

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Autores principales: McLoughlin, Steven, Spillane, Charles, Claffey, Noel, Smith, Paul E., O’Rourke, Tommy, Diskin, Michael G., Waters, Sinéad M.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7477290/
https://www.ncbi.nlm.nih.gov/pubmed/32983009
http://dx.doi.org/10.3389/fmicb.2020.01981
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author McLoughlin, Steven
Spillane, Charles
Claffey, Noel
Smith, Paul E.
O’Rourke, Tommy
Diskin, Michael G.
Waters, Sinéad M.
author_facet McLoughlin, Steven
Spillane, Charles
Claffey, Noel
Smith, Paul E.
O’Rourke, Tommy
Diskin, Michael G.
Waters, Sinéad M.
author_sort McLoughlin, Steven
collection PubMed
description Rumen microbiome composition and functionality is linked to animal feed efficiency, particularly for bovine ruminants. To investigate this in sheep, we compared rumen bacterial and archaeal populations (and predicted metabolic processes) of sheep divergent for the feed efficiency trait feed conversion ratio (FCR). In our study 50 Texel cross Scottish Blackface (TXSB) ram lambs were selected from an original cohort of 200 lambs. From these, 26 were further selected for experimentation based on their extreme FCR (High Feed Efficiency, HFE = 13; Low Feed Efficiency, LFE = 13). Animals were fed a 95% concentrate diet ad libitum over 36 days. 16S rRNA amplicon sequencing was used to investigate the rumen bacterial and archaeal communities in the liquid and solid rumen fractions of sheep divergent for FCR. Weighted UniFrac distances separated HFE and LFE archaea communities from the liquid rumen fraction (Permanova, P < 0.05), with greater variation observed for the LFE cohort (Permdisp, P < 0.05). LFE animals exhibited greater Shannon and Simpson diversity indices, which was significant for the liquid rumen fraction (P < 0.05). Methanobrevibacter olleyae (in liquid and solid fractions) and Methanobrevibacter millerae (liquid fraction) were differentially abundant, and increased in the LFE cohort (P.adj < 0.05), while Methanobrevibacter wolinii (liquid fraction) was increased in the HFE cohort (P.adj < 0.05). This suggests that methanogenic archaea may be responsible for a potential loss of energy for the LFE cohort. Bacterial community composition (Permanova, P > 0.1) and diversity (P > 0.1) was not affected by the FCR phenotype. Only the genus Prevotella 1 was differentially abundant between HFE and LFE cohorts. Although no major compositional shifts of bacterial populations were identified amongst the feed efficient cohorts (FDR > 0.05), correlation analysis identified putative drivers of feed efficiency with Ruminococcaceae UCG-014 (liquid, rho = −0.53; solid, rho = −0.56) and Olsenella (solid, rho = −0.40) exhibiting significant negative association with FCR (P < 0.05). Bifidobacterium and Megasphaera showed significant positive correlations with ADG. Major cellulolytic bacteria Fibrobacter (liquid, rho = 0.43) and Ruminococcus 1 (liquid, rho = 0.41; solid, rho = 41) correlated positively with FCR (P < 0.05). Our study provides evidence that feed efficiency in sheep is likely influenced by compositional changes to the archaeal community, and abundance changes of specific bacteria, rather than major overall shifts within the rumen microbiome.
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spelling pubmed-74772902020-09-26 Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency McLoughlin, Steven Spillane, Charles Claffey, Noel Smith, Paul E. O’Rourke, Tommy Diskin, Michael G. Waters, Sinéad M. Front Microbiol Microbiology Rumen microbiome composition and functionality is linked to animal feed efficiency, particularly for bovine ruminants. To investigate this in sheep, we compared rumen bacterial and archaeal populations (and predicted metabolic processes) of sheep divergent for the feed efficiency trait feed conversion ratio (FCR). In our study 50 Texel cross Scottish Blackface (TXSB) ram lambs were selected from an original cohort of 200 lambs. From these, 26 were further selected for experimentation based on their extreme FCR (High Feed Efficiency, HFE = 13; Low Feed Efficiency, LFE = 13). Animals were fed a 95% concentrate diet ad libitum over 36 days. 16S rRNA amplicon sequencing was used to investigate the rumen bacterial and archaeal communities in the liquid and solid rumen fractions of sheep divergent for FCR. Weighted UniFrac distances separated HFE and LFE archaea communities from the liquid rumen fraction (Permanova, P < 0.05), with greater variation observed for the LFE cohort (Permdisp, P < 0.05). LFE animals exhibited greater Shannon and Simpson diversity indices, which was significant for the liquid rumen fraction (P < 0.05). Methanobrevibacter olleyae (in liquid and solid fractions) and Methanobrevibacter millerae (liquid fraction) were differentially abundant, and increased in the LFE cohort (P.adj < 0.05), while Methanobrevibacter wolinii (liquid fraction) was increased in the HFE cohort (P.adj < 0.05). This suggests that methanogenic archaea may be responsible for a potential loss of energy for the LFE cohort. Bacterial community composition (Permanova, P > 0.1) and diversity (P > 0.1) was not affected by the FCR phenotype. Only the genus Prevotella 1 was differentially abundant between HFE and LFE cohorts. Although no major compositional shifts of bacterial populations were identified amongst the feed efficient cohorts (FDR > 0.05), correlation analysis identified putative drivers of feed efficiency with Ruminococcaceae UCG-014 (liquid, rho = −0.53; solid, rho = −0.56) and Olsenella (solid, rho = −0.40) exhibiting significant negative association with FCR (P < 0.05). Bifidobacterium and Megasphaera showed significant positive correlations with ADG. Major cellulolytic bacteria Fibrobacter (liquid, rho = 0.43) and Ruminococcus 1 (liquid, rho = 0.41; solid, rho = 41) correlated positively with FCR (P < 0.05). Our study provides evidence that feed efficiency in sheep is likely influenced by compositional changes to the archaeal community, and abundance changes of specific bacteria, rather than major overall shifts within the rumen microbiome. Frontiers Media S.A. 2020-08-25 /pmc/articles/PMC7477290/ /pubmed/32983009 http://dx.doi.org/10.3389/fmicb.2020.01981 Text en Copyright © 2020 McLoughlin, Spillane, Claffey, Smith, O’Rourke, Diskin and Waters. 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
McLoughlin, Steven
Spillane, Charles
Claffey, Noel
Smith, Paul E.
O’Rourke, Tommy
Diskin, Michael G.
Waters, Sinéad M.
Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency
title Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency
title_full Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency
title_fullStr Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency
title_full_unstemmed Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency
title_short Rumen Microbiome Composition Is Altered in Sheep Divergent in Feed Efficiency
title_sort rumen microbiome composition is altered in sheep divergent in feed efficiency
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7477290/
https://www.ncbi.nlm.nih.gov/pubmed/32983009
http://dx.doi.org/10.3389/fmicb.2020.01981
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