Methanogenesis inhibition remodels microbial fermentation and stimulates acetogenesis in ruminants.

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Autores principales: Ni, Gaofeng, Wang, Min, Walker, Nicola, Muetzel, Stefan, Schmidt, Oliver, Fischer, André, Stemmler, René T, Leung, Pok Man, Zhang, Xiumin, Li, Qiushuang, Jain, Surbhi, Jespersen, Marion, Grinter, Rhys, Archer, Stephen D J, Pacheco, David, Lowe, Katherine, Pope, Phillip B, Müller, Volker, Pitta, Dipti W, Janssen, Peter H, Watson, Mick, Attwood, Graeme T, Ver Loren van Themaat, Emiel, Kindermann, Maik, Greening, Chris
Formato: Artículo científico
Lenguaje:en
Publicado: Proceedings of the National Academy of Sciences of the United States of America 2025
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author Ni, Gaofeng
Wang, Min
Walker, Nicola
Muetzel, Stefan
Schmidt, Oliver
Fischer, André
Stemmler, René T
Leung, Pok Man
Zhang, Xiumin
Li, Qiushuang
Jain, Surbhi
Jespersen, Marion
Grinter, Rhys
Archer, Stephen D J
Pacheco, David
Lowe, Katherine
Pope, Phillip B
Müller, Volker
Pitta, Dipti W
Janssen, Peter H
Watson, Mick
Attwood, Graeme T
Ver Loren van Themaat, Emiel
Kindermann, Maik
Greening, Chris
author_facet Ni, Gaofeng
Wang, Min
Walker, Nicola
Muetzel, Stefan
Schmidt, Oliver
Fischer, André
Stemmler, René T
Leung, Pok Man
Zhang, Xiumin
Li, Qiushuang
Jain, Surbhi
Jespersen, Marion
Grinter, Rhys
Archer, Stephen D J
Pacheco, David
Lowe, Katherine
Pope, Phillip B
Müller, Volker
Pitta, Dipti W
Janssen, Peter H
Watson, Mick
Attwood, Graeme T
Ver Loren van Themaat, Emiel
Kindermann, Maik
Greening, Chris
Ni, Gaofeng
Wang, Min
Walker, Nicola
Muetzel, Stefan
Schmidt, Oliver
Fischer, André
Stemmler, René T
Leung, Pok Man
Zhang, Xiumin
Li, Qiushuang
Jain, Surbhi
Jespersen, Marion
Grinter, Rhys
Archer, Stephen D J
Pacheco, David
Lowe, Katherine
Pope, Phillip B
Müller, Volker
Pitta, Dipti W
Janssen, Peter H
Watson, Mick
Attwood, Graeme T
Ver Loren van Themaat, Emiel
Kindermann, Maik
Greening, Chris
collection PubMed - marine biology
contents Methanogenesis inhibition remodels microbial fermentation and stimulates acetogenesis in ruminants. Ni, Gaofeng Wang, Min Walker, Nicola Muetzel, Stefan Schmidt, Oliver Fischer, André Stemmler, René T Leung, Pok Man Zhang, Xiumin Li, Qiushuang Jain, Surbhi Jespersen, Marion Grinter, Rhys Archer, Stephen D J Pacheco, David Lowe, Katherine Pope, Phillip B Müller, Volker Pitta, Dipti W Janssen, Peter H Watson, Mick Attwood, Graeme T Ver Loren van Themaat, Emiel Kindermann, Maik Greening, Chris Animals Methane Fermentation Rumen Cattle Gastrointestinal Microbiome Propanols Animal Feed Ruminants Microbiota Fatty Acids, Volatile Rumen microbiota enable ruminants to grow on fibrous plant materials, but also produce methane, driving 5% of global greenhouse gas emissions and leading to a loss of gross energy content. Methanogenesis inhibitors such as 3-nitrooxypropanol (3-NOP) decrease methane emissions in ruminants when supplemented in feed. Yet we lack a system-wide, species-resolved understanding of how the rumen microbiota remodels following inhibition and how this influences animal production. Here, we conducted a large-scale trial with 51 dairy calves to analyze microbiota responses to 3-NOP, pairing host performance, emissions, and nutritional profiles with genome-resolved metagenomic and metatranscriptomic data. 3-NOP supplementation decreased methane emissions by 62%, modulated short-chain fatty acid and H levels, and did not affect dietary intake or animal performance. We created a rumen microbial genome catalogue (27,884 genomes) that mapped to the meta-omic data at high rates. There was a strong reduction of methanogens and stimulation of reductive acetogens, primarily uncultivated lineages such as " Faecousia." However, there was a shift in major fermentative communities away from acetate production in response to hydrogen gas accumulation. In vitro incubations recapitulated these results and showed an enrichment of acetate from reductive acetogenesis. Altogether, the divergent responses of the fermentative and hydrogenotrophic communities lead to net hydrogen build-up and limit potential productivity gains from methane reduction. By linking ruminant greenhouse gas emissions and productivity to specific microbial species, this study emphasizes the importance of microbiota-wide analysis for optimizing methane mitigation strategies and identifies promising strategies to simultaneously reduce emissions while increasing animal production.
format Artículo científico
id pubmed_41052332
institution PubMed
language en
publishDate 2025
publisher Proceedings of the National Academy of Sciences of the United States of America
record_format pubmed
spellingShingle Methanogenesis inhibition remodels microbial fermentation and stimulates acetogenesis in ruminants.
Ni, Gaofeng
Wang, Min
Walker, Nicola
Muetzel, Stefan
Schmidt, Oliver
Fischer, André
Stemmler, René T
Leung, Pok Man
Zhang, Xiumin
Li, Qiushuang
Jain, Surbhi
Jespersen, Marion
Grinter, Rhys
Archer, Stephen D J
Pacheco, David
Lowe, Katherine
Pope, Phillip B
Müller, Volker
Pitta, Dipti W
Janssen, Peter H
Watson, Mick
Attwood, Graeme T
Ver Loren van Themaat, Emiel
Kindermann, Maik
Greening, Chris
Animals
Methane
Fermentation
Rumen
Cattle
Gastrointestinal Microbiome
Propanols
Animal Feed
Ruminants
Microbiota
Fatty Acids, Volatile
Methanogenesis inhibition remodels microbial fermentation and stimulates acetogenesis in ruminants. Ni, Gaofeng Wang, Min Walker, Nicola Muetzel, Stefan Schmidt, Oliver Fischer, André Stemmler, René T Leung, Pok Man Zhang, Xiumin Li, Qiushuang Jain, Surbhi Jespersen, Marion Grinter, Rhys Archer, Stephen D J Pacheco, David Lowe, Katherine Pope, Phillip B Müller, Volker Pitta, Dipti W Janssen, Peter H Watson, Mick Attwood, Graeme T Ver Loren van Themaat, Emiel Kindermann, Maik Greening, Chris Animals Methane Fermentation Rumen Cattle Gastrointestinal Microbiome Propanols Animal Feed Ruminants Microbiota Fatty Acids, Volatile Rumen microbiota enable ruminants to grow on fibrous plant materials, but also produce methane, driving 5% of global greenhouse gas emissions and leading to a loss of gross energy content. Methanogenesis inhibitors such as 3-nitrooxypropanol (3-NOP) decrease methane emissions in ruminants when supplemented in feed. Yet we lack a system-wide, species-resolved understanding of how the rumen microbiota remodels following inhibition and how this influences animal production. Here, we conducted a large-scale trial with 51 dairy calves to analyze microbiota responses to 3-NOP, pairing host performance, emissions, and nutritional profiles with genome-resolved metagenomic and metatranscriptomic data. 3-NOP supplementation decreased methane emissions by 62%, modulated short-chain fatty acid and H levels, and did not affect dietary intake or animal performance. We created a rumen microbial genome catalogue (27,884 genomes) that mapped to the meta-omic data at high rates. There was a strong reduction of methanogens and stimulation of reductive acetogens, primarily uncultivated lineages such as " Faecousia." However, there was a shift in major fermentative communities away from acetate production in response to hydrogen gas accumulation. In vitro incubations recapitulated these results and showed an enrichment of acetate from reductive acetogenesis. Altogether, the divergent responses of the fermentative and hydrogenotrophic communities lead to net hydrogen build-up and limit potential productivity gains from methane reduction. By linking ruminant greenhouse gas emissions and productivity to specific microbial species, this study emphasizes the importance of microbiota-wide analysis for optimizing methane mitigation strategies and identifies promising strategies to simultaneously reduce emissions while increasing animal production.
title Methanogenesis inhibition remodels microbial fermentation and stimulates acetogenesis in ruminants.
topic Animals
Methane
Fermentation
Rumen
Cattle
Gastrointestinal Microbiome
Propanols
Animal Feed
Ruminants
Microbiota
Fatty Acids, Volatile
url https://pubmed.ncbi.nlm.nih.gov/41052332/