{"title":"Rumen microbes affect the somatic cell counts of dairy cows by modulating glutathione metabolism.","authors":"Hua Zhang, Tianhang Lu, Shijiao Guo, Tianying He, Min-Kyoung Shin, Chaochao Luo, Jinjin Tong, Yinhua Zhang","doi":"10.1128/msystems.01093-24","DOIUrl":null,"url":null,"abstract":"<p><p>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, <i>Lachnospiraceae</i>, <i>Prevotella</i>, 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 <i>Rikenellaceae, Muribaculaceae,</i> and <i>Prevotellaceae</i>, 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.IMPORTANCEHigh 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.</p>","PeriodicalId":18819,"journal":{"name":"mSystems","volume":" ","pages":"e0109324"},"PeriodicalIF":5.0000,"publicationDate":"2025-03-19","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":null,"platform":"Semanticscholar","paperid":null,"PeriodicalName":"mSystems","FirstCategoryId":"99","ListUrlMain":"https://doi.org/10.1128/msystems.01093-24","RegionNum":2,"RegionCategory":"生物学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"MICROBIOLOGY","Score":null,"Total":0}
引用次数: 0
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.IMPORTANCEHigh 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.
mSystemsBiochemistry, Genetics and Molecular Biology-Biochemistry
CiteScore
10.50
自引率
3.10%
发文量
308
审稿时长
13 weeks
期刊介绍:
mSystems™ will publish preeminent work that stems from applying technologies for high-throughput analyses to achieve insights into the metabolic and regulatory systems at the scale of both the single cell and microbial communities. The scope of mSystems™ encompasses all important biological and biochemical findings drawn from analyses of large data sets, as well as new computational approaches for deriving these insights. mSystems™ will welcome submissions from researchers who focus on the microbiome, genomics, metagenomics, transcriptomics, metabolomics, proteomics, glycomics, bioinformatics, and computational microbiology. mSystems™ will provide streamlined decisions, while carrying on ASM''s tradition of rigorous peer review.