Abstract

Mitigation of greenhouse gas emissions is relevant for reducing the environmental impact of ruminant production. In this study, the rumen microbiome from Holstein cows was characterized through a combination of 16S rRNA gene and shotgun metagenomic sequencing. Methane production (CH4) and dry matter intake (DMI) were individually measured over 4–6 weeks to calculate the CH4 yield (CH4y = CH4/DMI) per cow. We implemented a combination of clustering, multivariate and mixed model analyses to identify a set of operational taxonomic unit (OTU) jointly associated with CH4y and the structure of ruminal microbial communities. Three ruminotype clusters (R1, R2 and R3) were identified, and R2 was associated with higher CH4y. The taxonomic composition on R2 had lower abundance of Succinivibrionaceae and Methanosphaera, and higher abundance of Ruminococcaceae, Christensenellaceae and Lachnospiraceae. Metagenomic data confirmed the lower abundance of Succinivibrionaceae and Methanosphaera in R2 and identified genera (Fibrobacter and unclassified Bacteroidales) not highlighted by metataxonomic analysis. In addition, the functional metagenomic analysis revealed that samples classified in cluster R2 were overrepresented by genes coding for KEGG modules associated with methanogenesis, including a significant relative abundance of the methyl‐coenzyme M reductase enzyme. Based on the cluster assignment, we applied a sparse partial least‐squares discriminant analysis at the taxonomic and functional levels. In addition, we implemented a sPLS regression model using the phenotypic variation of CH4y. By combining these two approaches, we identified 86 discriminant bacterial OTUs, notably including families linked to CH4 emission such as Succinivibrionaceae, Ruminococcaceae, Christensenellaceae, Lachnospiraceae and Rikenellaceae. These selected OTUs explained 24% of the CH4y phenotypic variance, whereas the host genome contribution was ~14%. In summary, we identified rumen microbial biomarkers associated with the methane production of dairy cows; these biomarkers could be used for targeted methane‐reduction selection programmes in the dairy cattle industry provided they are heritable.

Highlights

  • Cattle have the remarkable ability to digest and transform non‐edible plant cell wall components into high‐quality proteins for human consumption

  • Our results confirm the link between the structure of the ruminal bacterial community and CH4 emission

  • We identified 86 operational taxonomic unit (OTU) simultaneously linked to CH4y emission and the ruminal bacterial community structure

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Summary

Introduction

Cattle have the remarkable ability to digest and transform non‐edible plant cell wall components into high‐quality proteins for human consumption. Exploring the abundance and composition of microbial communities in the gastrointestinal tract of cattle in relation to the host genome is of great interest for quantifying animal variability in feed digestibility and enteric CH4 emission (Huws et al, 2018; Leahy et al, 2013; Li et al, 2019). Pioneering rumen‐engineering studies have suggested that microbial communities are highly resilient and host‐specific (Cole, 1991; Weimer, 2015) These latter properties make it difficult to manipulate the ruminal microbial community, they enable the analysis of the covariation of these ecosystems with host performance and jointly selecting both host genome and microbiome variants

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