Multi-omics reveals effects of several rumen bacteria on reproductive performance of sheep

Mounting evidence indicates that the rumen microbiota plays a crucial role in the reproductive health of sheep. However, the potential beneficial effects of rumen microbiota on lambing performance in sheep across different stages of the reproductive cycle and the precise mechanisms underlying these effects remain unclear. We aimed to elucidate the rumen microbial regulatory network underlying differences in reproductive performance in sheep by integrating multi-stage metagenomics and metabolomics. No significant difference was observed in the ruminal microbial α-diversity between sheep with high and low litter size. However, significant stage-specific segregation was observed in their community structures. We identified a cohort of key species strongly associated with litter size. These included Asaia bogorensis, Methanolobus zinderi, Erwinia gerundensis, Marinobacter sp. BSs20148, and Lactobacillus amylolyticus enriched during pregnancy; Rhizobium gallicum, Aeromonas caviae, Pseudolysobacter antarcticus, Mucilaginibacter rubeus, Thermococcus paralvinellae, and Janthinobacterium svalbardensis enriched during lactation; Pseudomonas mandelii, Gordonia sp. HY186, Arachidicoccus sp. BS20, Mesotoga prima, Acidovorax ebreus, Donacia cinerea, and Salmonella enterica enriched during estrus. Host plasma metabolomics analysis further revealed an enrichment of a set of core metabolites in the blood of high-fertility sheep, including Inositol, 2-Linoleoylglycerol, lysophosphatidylcholines and neuromodulatory substances such as tyramine and sphingosine-1-phosphate. We constructed stage-specific “rumen microbe-rumen metabolite-plasma metabolite” regulatory axes. These results suggest the influence of the rumen microbiome on plasma metabolic profiles and subsequent fertility outcomes in sheep. We elucidate the dynamic mechanism by which the rumen microbiota in high-fertility sheep is associated with superior reproductive performance through stage-adaptive community succession and functional remodeling, which in turn may modulate the host’s neuroendocrine and lipid metabolic profiles. These findings provide a new perspective for understanding the regulation of fertility in ruminants and lay a theoretical foundation for improving reproductive efficiency through nutritional strategies targeting the rumen microbiota.