Methanogenesis inhibition remodels microbial fermentation and stimulates acetogenesis in ruminants
Abstract
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 2 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 “ Candidatus 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.
Article Details
Journal Info
Proceedings of the National Academy of Sciences
National Academy of Sciences
Authors (25)
Gaofeng Ni
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Min Wang
Nicola Walker
Animal Nutrition and Health, dsm-firmenich
Stefan Muetzel
Grasslands Research Centre, AgResearch Limited
Oliver Schmidt
Department of Arctic and Marine Biology, Faculty of Biosciences, Fisheries and Economics, Universitetet i Tromsø -The Arctic University of Norway
Andre Fischer
René T. Stemmler
Chemical and Process Sciences, dsm-firmenich
Pok Man Leung
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Xiumin Zhang
State Key Laboratory of Forage Breeding-by-Design and Utilization, Institute of Subtropical Agriculture, Chinese Academy of Sciences
Qiushuang Li
State Key Laboratory of Forage Breeding-by-Design and Utilization, Institute of Subtropical Agriculture, Chinese Academy of Sciences
Surbhi Jain
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Marion Jespersen
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Rhys Grinter
Department of Microbiology, Biomedicine Discovery Institute, Monash University
Stephen D. J. Archer
Grasslands Research Centre, AgResearch Limited
David Pacheco
Grasslands Research Centre, AgResearch Limited
Katherine Lowe
Grasslands Research Centre, AgResearch Limited
Phillip B. Pope
Centre for Microbiome Research, School of Biomedical Sciences, Faculty of Health, Queensland University of Technology
Volker Müller
Department of Molecular Microbiology and Bioenergetics, Institute of Molecular Biosciences, Johann Wolfgang Goethe University
Dipti W. Pitta
Department of Clinical Studies, School of Veterinary Medicine, University of Pennsylvania
Peter H. Janssen
Grasslands Research Centre, AgResearch Limited
Mick Watson
Data Science and Research, dsm-firmenich
Graeme T. Attwood
Grasslands Research Centre, AgResearch Limited
Emiel Ver Loren van Themaat
Data Science and Research, dsm-firmenich
Maik Kindermann
Animal Nutrition and Health, dsm-firmenich
Chris Greening