Host Genetic Effects and Phenotypic Landscapes of Rumen Bacterial Enterotypes in a Large Sheep Population

Population stratification based on gut microbiota composition has revealed several enterotypes in humans and animals, providing valuable tools for studying the gut microbiota landscape, which is crucial for animal health and production. However, knowledge about rumen enterotype identification in sheep, its influencing factors, and its association with growth performance and host genetics remains limited. Here, we investigated host genetic effects and phenotypic landscapes of rumen bacterial enterotypes in a large sheep population. Ruminal contents from 1150 healthy sheep were analyzed using 16S rRNA gene sequencing and genus-level clustering, complemented by extensive phenotypic data covering 47 traits spanning growth, feed efficiency, meat yield, and ruminal fermentation, along with whole-genome resequencing data. We identified two distinct enterotypes: Enterotype 1 (E1), a mixture of multiple genera, and Enterotype 2 (E2), dominated by Prevotella. E2 sheep exhibit superior growth and meat production performance, but lower feed efficiency and increased fat deposition. Two-part beta-regression models and co-occurrence network analyses revealed the extensive impact of enterotypes on microbial community structure, with E1 displaying a higher frequency of unique bacterial interactions. The estimated heritability of the enterotype was 0.47, and a GWAS identified five key genetic markers associated with rumen enterotype, localized to two candidate genes: CHODL and ENPP6. These markers significantly influence 58 ruminal bacterial genera, including key taxa and driving genus. Overall, our data provide new insights into sheep rumen-enterotype characteristics, contributing to a better understanding of microbial interactions that are crucial for improving ruminant growth performance.