iMeta | Genome and transcriptome to uncover the host-microbiome interactions in rumen methanogenesis

RESEARCH ARTICLE
Open Access
Integrating genome- and transcriptome-wide association studies to uncover the host-microbiome interactions in bovine rumen methanogenesis
Wei Wang, Zhenyu Wei, Zhuohui Li, Jianrong Ren, Yanliang Song, Jingyi Xu, Anguo Liu, Xinmei Li, Manman Li, Huimei Fan, Liangliang Jin, Zhannur Niyazbekova, Wen Wang, Yuanpeng Gao, Yu Jiang, Junhu Yao, Fuyong Li, Shengru Wu, Yu Wang … See fewer authors
First published: 03 September 2024 doi.org/10.100...
Wei Wang, Zhenyu Wei, and Zhuohui Li contributed equally to this study.
Abstract
The ruminal microbiota generates biogenic methane in ruminants. However, the role of host genetics in modifying ruminal microbiota-mediated methane emissions remains mysterious, which has severely hindered the emission control of this notorious greenhouse gas. Here, we uncover the host genetic basis of rumen microorganisms by genome- and transcriptome-wide association studies with matched genome, rumen transcriptome, and microbiome data from a cohort of 574 Holstein cattle. Heritability estimation revealed that approximately 70% of microbial taxa had significant heritability, but only 43 genetic variants with significant association with 22 microbial taxa were identified through a genome-wide association study (GWAS). In contrast, the transcriptome-wide association study (TWAS) of rumen microbiota detected 28,260 significant gene-microbe associations, involving 210 taxa and 4652 unique genes. On average, host genetic factors explained approximately 28% of the microbial abundance variance, while rumen gene expression explained 43%. In addition, we highlighted that TWAS exhibits a strong advantage in detecting gene expression and phenotypic trait associations in direct effector organs. For methanogenic archaea, only one significant signal was detected by GWAS, whereas the TWAS obtained 1703 significant associated host genes. By combining multiple correlation analyses based on these host TWAS genes, rumen microbiota, and volatile fatty acids, we observed that substrate hydrogen metabolism is an essential factor linking host-microbe interactions in methanogenesis. Overall, these findings provide valuable guidelines for mitigating methane emissions through genetic regulation and microbial management strategies in ruminants.
Graphical Abstract
We systematically evaluated the relationship between host and microorganisms using matched host genome, rumen transcriptome, and microbiome data from a cohort of 574 Holstein cattle. The associations between rumen gene expression and rumen microbiota abundance via transcriptome-wide association study (TWAS) may provide more molecular markers at the gene level, which bridge the host-microbe interactions. Methanogens belonging to Methanobrevibacter genus are common hydrogenotrophic methanogenic archaea, which usually utilize hydrogen (H2) and carbon dioxide (CO2) produced from microbial fermentation as substrates to produce methane (CH4). By combining multiple correlation analyses based on host TWAS genes, rumen microbiota, and volatile fatty acids, we illustrated that host-microbe interactions in the hydrogenotrophic methanogenesis pathway are possibly involved in substrate hydrogen metabolism and transport. This study broadens our insights into the potential mechanisms of host-microbe interactions in rumen methanogenesis.
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Highlights
Using large-scale matched samples, we reveal the impact of host genetics variants and rumen gene expressions on rumen microbiota in Holstein cattle.
Host genetic factors average explained approximately 28% of the microbial abundance variance, whereas rumen gene expression explained 43%.
The transcriptome-wide association study is a promising method for exploring the associations between gene expression and complex phenotypes in direct effector organs.
Host-microbial interactions in bovine rumen methanogenesis are possibly involved in substrate hydrogen metabolism and transport.