Rumen microbes affect the somatic cell counts of dairy cows by modulating glutathione metabolism

ABSTRACT Healthy mammary glands are essential for high-quality milk production in the dairy industry. The relationship between somatic cell counts (SCCs), rumen fermentation, and microbiota interactions remains unclear. This study integrated physiological indicators, high-throughput 16S rRNA gene sequencing, and metagenomics data analysis to investigate the mechanisms linking rumen microbes and mastitis and to evaluate the changes in milk production and serum cytokine levels in cows with low (L-SCC) and high (H-SCC) somatic cell counts. Compared with the L-SCC group, the H-SCC group exhibited significantly lower lactose and fat contents in milk, reduced rumen fermentation product levels, and increased abundances of Bacteroidetes, Firmicutes, Lachnospiraceae , Prevotella , and Rumiclostridium. Elevated serum levels of IgG2, IgM, IL-1β, IL-6, and TNF-ɑ in the H-SCC group indicated inflammation and rumen microbiota dysbiosis. Functional analysis of microbial communities revealed significant enrichment in pathways related to glutathione metabolism, thyroid hormone synthesis, hypertrophic cardiomyopathy (HCM), the phosphotransferase system (PTS), the P53 signaling pathway, and the Jak-STAT signaling pathway. Correlation network analysis showed that changes in bacterial families, such as Rikenellaceae, Muribaculaceae, and Prevotellaceae , were associated with cytokines, rumen fermentation, and milk quality. The study highlights the interaction between rumen microbiota homeostasis and mammary gland health, indicating that rumen fermentation status influences serum inflammation and milk quality. Modulating rumen fermentation to enhance mammary gland immune function presents a viable strategy for sustainable dairy industry development with long-lived, highly productive cows. IMPORTANCE High somatic cell counts (SCCs) are a key biomarker of mastitis and are associated with decreased milk production and significant economic losses in dairy farming. This study systematically examines the relationship between elevated SCCs, rumen microbial dysbiosis, and host inflammatory responses, shedding light on the intricate interplay between microbial ecosystems and host physiology. The findings highlight the potential for microbiota-targeted interventions to reduce inflammation, improve milk composition, and enhance dairy cow productivity. Rather than presuming a direct causative link between SCC-associated dysbiosis and inflammation, this research focuses on their interdependent dynamics, offering a nuanced understanding of the complex biological mechanisms involved. This work advances knowledge of host-microbiota interactions in livestock, providing practical insights for the development of innovative strategies to manage mastitis and improve overall herd health. By adhering to One Health principles, this study underscores the significance of sustainable agricultural practices that prioritize animal welfare, environmental stewardship, and food security. These findings establish a robust foundation for future research into microbiota-driven solutions aimed at enhancing the health and productivity of dairy cattle.