Identification of Rumen Microbial Genes Involved in Pathways Linked to Appetite, Growth, and Feed Conversion Efficiency in Cattle

Joana Lima; Marc D. Auffret; Robert D. Stewart; Richard J. Dewhurst; Carol-Anne Duthie; Timothy J. Snelling; Alan W. Walker; Tom C. Freeman; Mick Watson; Rainer Roehe

doi:10.3389/fgene.2019.00701

Identification of Rumen Microbial Genes Involved in Pathways Linked to Appetite, Growth, and Feed Conversion Efficiency in Cattle

Joana Lima (Corresponding Author), Marc D. Auffret, Robert D. Stewart, Richard J. Dewhurst, Carol-Anne Duthie, Timothy J. Snelling, Alan W. Walker, Tom C. Freeman, Mick Watson, Rainer Roehe (Corresponding Author)

The Rowett Institute of Nutrition and Health

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Abstract

The rumen microbiome is essential for the biological processes involved in the conversion of feed into nutrients that can be utilized by the host animal. In the present research the influence of the rumen microbiome on feed conversion efficiency, growth rate and appetite of beef cattle was investigated using metagenomic data. Our aim was to explore the associations between microbial genes and functional pathways, to shed light on the influence of bacterial enzyme expression on host phenotypes. Two groups of cattle were selected on the basis of their high and low feed conversion ratio. Microbial DNA was extracted from rumen samples and the relative abundances of microbial genes were determined via shotgun metagenomic sequencing. Using partial least squares analyses, we identified sets of 20, 14, 17 and 18 microbial genes whose relative abundances explained 63%, 65%, 66% and 73% of the variation of feed conversion efficiency, average daily weight gain, residual feed intake and daily feed intake, respectively. The microbial genes associated with each of these traits were mostly different, but highly correlated traits such as feed conversion ratio and growth rate showed some overlapping genes. Consistently with this result, distinct clusters of a co-abundance network were enriched with microbial genes identified to be related with feed conversion ratio and growth rate or daily feed intake and residual feed intake. Microbial genes encoding for proteins related to cell wall biosynthesis, hemicellulose and cellulose degradation and host-microbiome cross talk (e.g. aguA, ptb, K01188 and murD) were associated with feed conversion ratio and/or average daily gain. Genes related to vitamin B12 biosynthesis, environmental information processing and bacterial mobility (e.g. cobD, tolC and fliN) were associated with residual feed intake and/or daily feed intake. This research highlights the association of the microbiome with feed conversion processes, influencing growth rate and appetite, and it emphasizes the opportunity to use relative abundances of microbial genes in the prediction of these performance traits, with potential implementation in animal breeding programs and dietary interventions.

Original language	English
Article number	701
Journal	Frontiers in Genetics
Volume	10
DOIs	https://doi.org/10.3389/fgene.2019.00701
Publication status	Published - 8 Aug 2019

Bibliographical note

The project was supported by grants from the Biotechnology and Biological Sciences Research Council (BBSRC BB/N01720X/1 and BB/N016742/1) and by the Scottish Government (RESAS Division) as part of the 2016–2021 commission. The research is based on data from experiments funded by the Scottish Government as part of the 2011–2016 commission, Agriculture and Horticulture Development Board (AHDB) Beef & Lamb, Quality Meat Scotland (QMS), and Department for Environment Food & Rural Affairs (Defra).

Keywords

Feed conversion efficiency
Appetite
Metagenomics
Rumen microbiome
Microbial gene networks
PROTEIN
ESCHERICHIA-COLI
MECHANISMS
microbial gene networks
BEEF-CATTLE
DAIRY
rumen microbiome
PHENOTYPIC RELATIONSHIPS
PROPIONATE
CHALLENGE
metagenomics
CHAIN FATTY-ACIDS
BIOSYNTHESIS
feed conversion efficiency
appetite

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Copyright © 2019 Lima, Auffret, Stewart, Dewhurst, Duthie, Snelling, Walker, Freeman, Watson and Roehe. 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. https://creativecommons.org/licenses/by/4.0/
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Cite this

@article{cde659d756424cda875b7e7e490ebf8e,

title = "Identification of Rumen Microbial Genes Involved in Pathways Linked to Appetite, Growth, and Feed Conversion Efficiency in Cattle",

abstract = "The rumen microbiome is essential for the biological processes involved in the conversion of feed into nutrients that can be utilized by the host animal. In the present research the influence of the rumen microbiome on feed conversion efficiency, growth rate and appetite of beef cattle was investigated using metagenomic data. Our aim was to explore the associations between microbial genes and functional pathways, to shed light on the influence of bacterial enzyme expression on host phenotypes. Two groups of cattle were selected on the basis of their high and low feed conversion ratio. Microbial DNA was extracted from rumen samples and the relative abundances of microbial genes were determined via shotgun metagenomic sequencing. Using partial least squares analyses, we identified sets of 20, 14, 17 and 18 microbial genes whose relative abundances explained 63%, 65%, 66% and 73% of the variation of feed conversion efficiency, average daily weight gain, residual feed intake and daily feed intake, respectively. The microbial genes associated with each of these traits were mostly different, but highly correlated traits such as feed conversion ratio and growth rate showed some overlapping genes. Consistently with this result, distinct clusters of a co-abundance network were enriched with microbial genes identified to be related with feed conversion ratio and growth rate or daily feed intake and residual feed intake. Microbial genes encoding for proteins related to cell wall biosynthesis, hemicellulose and cellulose degradation and host-microbiome cross talk (e.g. aguA, ptb, K01188 and murD) were associated with feed conversion ratio and/or average daily gain. Genes related to vitamin B12 biosynthesis, environmental information processing and bacterial mobility (e.g. cobD, tolC and fliN) were associated with residual feed intake and/or daily feed intake. This research highlights the association of the microbiome with feed conversion processes, influencing growth rate and appetite, and it emphasizes the opportunity to use relative abundances of microbial genes in the prediction of these performance traits, with potential implementation in animal breeding programs and dietary interventions.",

keywords = "Feed conversion efficiency, Appetite, Metagenomics, Rumen microbiome, Microbial gene networks, PROTEIN, ESCHERICHIA-COLI, MECHANISMS, microbial gene networks, BEEF-CATTLE, DAIRY, rumen microbiome, PHENOTYPIC RELATIONSHIPS, PROPIONATE, CHALLENGE, metagenomics, CHAIN FATTY-ACIDS, BIOSYNTHESIS, feed conversion efficiency, appetite",

author = "Joana Lima and Auffret, {Marc D.} and Stewart, {Robert D.} and Dewhurst, {Richard J.} and Carol-Anne Duthie and Snelling, {Timothy J.} and Walker, {Alan W.} and Freeman, {Tom C.} and Mick Watson and Rainer Roehe",

note = "The project was supported by grants from the Biotechnology and Biological Sciences Research Council (BBSRC BB/N01720X/1 and BB/N016742/1) and by the Scottish Government (RESAS Division) as part of the 2016–2021 commission. The research is based on data from experiments funded by the Scottish Government as part of the 2011–2016 commission, Agriculture and Horticulture Development Board (AHDB) Beef & Lamb, Quality Meat Scotland (QMS), and Department for Environment Food & Rural Affairs (Defra). ",

year = "2019",

month = aug,

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doi = "10.3389/fgene.2019.00701",

language = "English",

volume = "10",

journal = "Frontiers in Genetics",

publisher = "Frontiers Media S.A.",

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T1 - Identification of Rumen Microbial Genes Involved in Pathways Linked to Appetite, Growth, and Feed Conversion Efficiency in Cattle

AU - Lima, Joana

AU - Auffret, Marc D.

AU - Stewart, Robert D.

AU - Dewhurst, Richard J.

AU - Duthie, Carol-Anne

AU - Snelling, Timothy J.

AU - Walker, Alan W.

AU - Freeman, Tom C.

AU - Watson, Mick

AU - Roehe, Rainer

N1 - The project was supported by grants from the Biotechnology and Biological Sciences Research Council (BBSRC BB/N01720X/1 and BB/N016742/1) and by the Scottish Government (RESAS Division) as part of the 2016–2021 commission. The research is based on data from experiments funded by the Scottish Government as part of the 2011–2016 commission, Agriculture and Horticulture Development Board (AHDB) Beef & Lamb, Quality Meat Scotland (QMS), and Department for Environment Food & Rural Affairs (Defra).

PY - 2019/8/8

Y1 - 2019/8/8

N2 - The rumen microbiome is essential for the biological processes involved in the conversion of feed into nutrients that can be utilized by the host animal. In the present research the influence of the rumen microbiome on feed conversion efficiency, growth rate and appetite of beef cattle was investigated using metagenomic data. Our aim was to explore the associations between microbial genes and functional pathways, to shed light on the influence of bacterial enzyme expression on host phenotypes. Two groups of cattle were selected on the basis of their high and low feed conversion ratio. Microbial DNA was extracted from rumen samples and the relative abundances of microbial genes were determined via shotgun metagenomic sequencing. Using partial least squares analyses, we identified sets of 20, 14, 17 and 18 microbial genes whose relative abundances explained 63%, 65%, 66% and 73% of the variation of feed conversion efficiency, average daily weight gain, residual feed intake and daily feed intake, respectively. The microbial genes associated with each of these traits were mostly different, but highly correlated traits such as feed conversion ratio and growth rate showed some overlapping genes. Consistently with this result, distinct clusters of a co-abundance network were enriched with microbial genes identified to be related with feed conversion ratio and growth rate or daily feed intake and residual feed intake. Microbial genes encoding for proteins related to cell wall biosynthesis, hemicellulose and cellulose degradation and host-microbiome cross talk (e.g. aguA, ptb, K01188 and murD) were associated with feed conversion ratio and/or average daily gain. Genes related to vitamin B12 biosynthesis, environmental information processing and bacterial mobility (e.g. cobD, tolC and fliN) were associated with residual feed intake and/or daily feed intake. This research highlights the association of the microbiome with feed conversion processes, influencing growth rate and appetite, and it emphasizes the opportunity to use relative abundances of microbial genes in the prediction of these performance traits, with potential implementation in animal breeding programs and dietary interventions.

AB - The rumen microbiome is essential for the biological processes involved in the conversion of feed into nutrients that can be utilized by the host animal. In the present research the influence of the rumen microbiome on feed conversion efficiency, growth rate and appetite of beef cattle was investigated using metagenomic data. Our aim was to explore the associations between microbial genes and functional pathways, to shed light on the influence of bacterial enzyme expression on host phenotypes. Two groups of cattle were selected on the basis of their high and low feed conversion ratio. Microbial DNA was extracted from rumen samples and the relative abundances of microbial genes were determined via shotgun metagenomic sequencing. Using partial least squares analyses, we identified sets of 20, 14, 17 and 18 microbial genes whose relative abundances explained 63%, 65%, 66% and 73% of the variation of feed conversion efficiency, average daily weight gain, residual feed intake and daily feed intake, respectively. The microbial genes associated with each of these traits were mostly different, but highly correlated traits such as feed conversion ratio and growth rate showed some overlapping genes. Consistently with this result, distinct clusters of a co-abundance network were enriched with microbial genes identified to be related with feed conversion ratio and growth rate or daily feed intake and residual feed intake. Microbial genes encoding for proteins related to cell wall biosynthesis, hemicellulose and cellulose degradation and host-microbiome cross talk (e.g. aguA, ptb, K01188 and murD) were associated with feed conversion ratio and/or average daily gain. Genes related to vitamin B12 biosynthesis, environmental information processing and bacterial mobility (e.g. cobD, tolC and fliN) were associated with residual feed intake and/or daily feed intake. This research highlights the association of the microbiome with feed conversion processes, influencing growth rate and appetite, and it emphasizes the opportunity to use relative abundances of microbial genes in the prediction of these performance traits, with potential implementation in animal breeding programs and dietary interventions.

KW - Feed conversion efficiency

KW - Appetite

KW - Metagenomics

KW - Rumen microbiome

KW - Microbial gene networks

KW - PROTEIN

KW - ESCHERICHIA-COLI

KW - MECHANISMS

KW - microbial gene networks

KW - BEEF-CATTLE

KW - DAIRY

KW - rumen microbiome

KW - PHENOTYPIC RELATIONSHIPS

KW - PROPIONATE

KW - CHALLENGE

KW - metagenomics

KW - CHAIN FATTY-ACIDS

KW - BIOSYNTHESIS

KW - feed conversion efficiency

KW - appetite

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U2 - 10.3389/fgene.2019.00701

DO - 10.3389/fgene.2019.00701

M3 - Article

C2 - 31440274

VL - 10

JO - Frontiers in Genetics

JF - Frontiers in Genetics

M1 - 701

ER -

Identification of Rumen Microbial Genes Involved in Pathways Linked to Appetite, Growth, and Feed Conversion Efficiency in Cattle

Abstract

Bibliographical note

Keywords

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