Host genetic regulation of specific functional groups in the rumen microbiome of dairy cows: Implications for lactation trait

Abstract

Introduction: Ruminants play a pivotal role in our society by transforming non-consumable substances from industrial by-products and plant fibers into valuable resources such as meat and milk. This remarkable conversion ability is primarily attributed to the rumen microbiota, which is influenced by various factors, including diet, climate, and geographical location. In recent years, increasing research has shown that host factors (breed, genetic variation, etc.) also play vital roles in shaping rumen microbial composition and function in cattle.

Objective: This study aims to provide a theoretical basis and an opportunity for further investigating the regulation of lactation traits in dairy cows through host genetics and the interaction with the rumen microbiota.

Method: To investigate the interactions between host genotype, rumen microbiota, and animal phenotype, we curated and analyzed the dairy herd improvement data, single nucleotide polymorphisms (SNPs) genotypes, and 16S rumen microbiota data from 1,169 Holstein dairy cows. Heritability and microbiability estimation, along with genome-wide association studies, were performed to identify candidate microorganisms and host genetic loci.

Result: We identified thirty-one heritable taxa, whose functions were predominantly enriched in carbohydrate metabolism and energy metabolism. The genome-wide association study revealed that nine heritable bacteria were significantly associated with forty-three SNPs. Functional genes located within or near these SNPs were primarily associated with rumen epithelial development. Additionally, these nine heritable bacteria were primarily annotated as complex polysaccharide degraders and butyrate producers, such as Fibrobacter sp900143055 and Pseudoruminococcus massiliensis, which showed significant associations with milk yield and milk fat percentage. Compared to previous studies, we newly discovered the existence of a high heritability of Olsenella umbonate, Butyrivibrio hungatei, among others.

Conclusion: This study identified thirty-one heritable bacterial taxa in Holstein dairy cows' rumen microbiota, with nine showing significant associations with forty-three SNPs related to rumen epithelial development. The discovery of novel heritable species and their correlations with lactation traits provides valuable insights for future breeding strategies aimed at improving dairy cattle productivity through the manipulation of host genetics and rumen microbiota.

Keywords: Dairy cows; Genome-wide association studies; Heritability; Microbiability; Rumen microbiota.

Graphical abstract

Fig. 1

Compositional profile of rumen bacterial communities in Holstein dairy cow. From the outer to inner circles are: percentage of identified phyla; heatmap of mean relative abundance at phylum level; line of mean relative abundance at genus level; heatmap of prevalence at species level; venn of core and non_core rumen bacteria.

Fig. 2

Heritable rumen bacteria and proportion of core and non-core bacteria in heritable bacteria. (A) Heritability of 31 heritable bacteria, 25 heritable bacteria were noncore bacteria and 6 heritable bacteria were core bacteria. (B) The Venn diagram of heritability between noncore bacteria and core bacteria.

Fig. 3

Manhattan of single nucleotide polymorphism loci for heritable rumen bacterial taxa.

Fig. 4

Predicted functions of heritable and non-heritable bacteria. (A) Predicted functions by PICRUSt2 software of heritable bacteria and nonheritable bacteria. (i) KEGG pathways in level 2. (ii) KEGG pathways in level 3. (B) KEGG pathways with different relative abundance between heritable bacteria and nonheritable bacteria.

Fig. 5

Microbiability and mean microbiability for three lactation traits with heritable and non-heritable bacteria and correlation analysis between heritable bacteria and host lactation traits. Twenty six of 31 heritable bacteria were associated with at least one lactation trait. Of these 26 heritable bacteria, 22 were core bacteria and 4 were noncore bacteria.