Cargando…

The rumen microbiome inhibits methane formation through dietary choline supplementation

Enteric fermentation from ruminants is a primary source of anthropogenic methane emission. This study aims to add another approach for methane mitigation by manipulation of the rumen microbiome. Effects of choline supplementation on methane formation were quantified in vitro using the Rumen Simulati...

Descripción completa

Detalles Bibliográficos
Autores principales: Li, Yang, Kreuzer, Michael, Clayssen, Quentin, Ebert, Marc-Olivier, Ruscheweyh, Hans-Joachim, Sunagawa, Shinichi, Kunz, Carmen, Attwood, Graeme, Amelchanka, Sergej, Terranova, Melissa
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group UK 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8571420/
https://www.ncbi.nlm.nih.gov/pubmed/34741032
http://dx.doi.org/10.1038/s41598-021-01031-w
_version_ 1784595017855139840
author Li, Yang
Kreuzer, Michael
Clayssen, Quentin
Ebert, Marc-Olivier
Ruscheweyh, Hans-Joachim
Sunagawa, Shinichi
Kunz, Carmen
Attwood, Graeme
Amelchanka, Sergej
Terranova, Melissa
author_facet Li, Yang
Kreuzer, Michael
Clayssen, Quentin
Ebert, Marc-Olivier
Ruscheweyh, Hans-Joachim
Sunagawa, Shinichi
Kunz, Carmen
Attwood, Graeme
Amelchanka, Sergej
Terranova, Melissa
author_sort Li, Yang
collection PubMed
description Enteric fermentation from ruminants is a primary source of anthropogenic methane emission. This study aims to add another approach for methane mitigation by manipulation of the rumen microbiome. Effects of choline supplementation on methane formation were quantified in vitro using the Rumen Simulation Technique. Supplementing 200 mM of choline chloride or choline bicarbonate reduced methane emissions by 97–100% after 15 days. Associated with the reduction of methane formation, metabolomics analysis revealed high post-treatment concentrations of ethanol, which likely served as a major hydrogen sink. Metagenome sequencing showed that the methanogen community was almost entirely lost, and choline-utilizing bacteria that can produce either lactate, ethanol or formate as hydrogen sinks were enriched. The taxa most strongly associated with methane mitigation were Megasphaera elsdenii and Denitrobacterium detoxificans, both capable of consuming lactate, which is an intermediate product and hydrogen sink. Accordingly, choline metabolism promoted the capability of bacteria to utilize alternative hydrogen sinks leading to a decline of hydrogen as a substrate for methane formation. However, fermentation of fibre and total organic matter could not be fully maintained with choline supplementation, while amino acid deamination and ethanolamine catabolism produced excessive ammonia, which would reduce feed efficiency and adversely affect live animal performance.
format Online
Article
Text
id pubmed-8571420
institution National Center for Biotechnology Information
language English
publishDate 2021
publisher Nature Publishing Group UK
record_format MEDLINE/PubMed
spelling pubmed-85714202021-11-09 The rumen microbiome inhibits methane formation through dietary choline supplementation Li, Yang Kreuzer, Michael Clayssen, Quentin Ebert, Marc-Olivier Ruscheweyh, Hans-Joachim Sunagawa, Shinichi Kunz, Carmen Attwood, Graeme Amelchanka, Sergej Terranova, Melissa Sci Rep Article Enteric fermentation from ruminants is a primary source of anthropogenic methane emission. This study aims to add another approach for methane mitigation by manipulation of the rumen microbiome. Effects of choline supplementation on methane formation were quantified in vitro using the Rumen Simulation Technique. Supplementing 200 mM of choline chloride or choline bicarbonate reduced methane emissions by 97–100% after 15 days. Associated with the reduction of methane formation, metabolomics analysis revealed high post-treatment concentrations of ethanol, which likely served as a major hydrogen sink. Metagenome sequencing showed that the methanogen community was almost entirely lost, and choline-utilizing bacteria that can produce either lactate, ethanol or formate as hydrogen sinks were enriched. The taxa most strongly associated with methane mitigation were Megasphaera elsdenii and Denitrobacterium detoxificans, both capable of consuming lactate, which is an intermediate product and hydrogen sink. Accordingly, choline metabolism promoted the capability of bacteria to utilize alternative hydrogen sinks leading to a decline of hydrogen as a substrate for methane formation. However, fermentation of fibre and total organic matter could not be fully maintained with choline supplementation, while amino acid deamination and ethanolamine catabolism produced excessive ammonia, which would reduce feed efficiency and adversely affect live animal performance. Nature Publishing Group UK 2021-11-05 /pmc/articles/PMC8571420/ /pubmed/34741032 http://dx.doi.org/10.1038/s41598-021-01031-w Text en © The Author(s) 2021 https://creativecommons.org/licenses/by/4.0/Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licence, and indicate if changes were made. The images or other third party material in this article are included in the article's Creative Commons licence, unless indicated otherwise in a credit line to the material. If material is not included in the article's Creative Commons licence and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this licence, visit http://creativecommons.org/licenses/by/4.0/ (https://creativecommons.org/licenses/by/4.0/) .
spellingShingle Article
Li, Yang
Kreuzer, Michael
Clayssen, Quentin
Ebert, Marc-Olivier
Ruscheweyh, Hans-Joachim
Sunagawa, Shinichi
Kunz, Carmen
Attwood, Graeme
Amelchanka, Sergej
Terranova, Melissa
The rumen microbiome inhibits methane formation through dietary choline supplementation
title The rumen microbiome inhibits methane formation through dietary choline supplementation
title_full The rumen microbiome inhibits methane formation through dietary choline supplementation
title_fullStr The rumen microbiome inhibits methane formation through dietary choline supplementation
title_full_unstemmed The rumen microbiome inhibits methane formation through dietary choline supplementation
title_short The rumen microbiome inhibits methane formation through dietary choline supplementation
title_sort rumen microbiome inhibits methane formation through dietary choline supplementation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8571420/
https://www.ncbi.nlm.nih.gov/pubmed/34741032
http://dx.doi.org/10.1038/s41598-021-01031-w
work_keys_str_mv AT liyang therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT kreuzermichael therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT clayssenquentin therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT ebertmarcolivier therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT ruscheweyhhansjoachim therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT sunagawashinichi therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT kunzcarmen therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT attwoodgraeme therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT amelchankasergej therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT terranovamelissa therumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT liyang rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT kreuzermichael rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT clayssenquentin rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT ebertmarcolivier rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT ruscheweyhhansjoachim rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT sunagawashinichi rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT kunzcarmen rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT attwoodgraeme rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT amelchankasergej rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation
AT terranovamelissa rumenmicrobiomeinhibitsmethaneformationthroughdietarycholinesupplementation