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Dietary Supplementation of Inulin Ameliorates Subclinical Mastitis via Regulation of Rumen Microbial Community and Metabolites in Dairy Cows.

ABSTRACT: Subclinical mastitis (SCM) is one of the highly infectious diseases in dairy cows with the characteristics of high incidence and nonvisible clinical symptoms. The gastrointestinal microbiota is closely related to mastitis. Inulin is a prebiotic fiber with functions in improving intestinal microbial communities and enhancing the host's immunity. However, the impact of dietary inulin on the rumen inner environment remains unknown. The current study investigated whether inulin could relieve SCM by affecting the profiles of ruminal bacterial and metabolites in dairy cows. Inulin inclusion rates were 0, 100, 200, 300, and 400 g/day per cow, respectively. Inulin increased milk yield, milk protein, and lactose and reduced the somatic cell counts (SCC) in milk. In serum, the concentration of proinflammatory cytokines, such as interleukin-6 (IL-6), IL-8, tumor necrosis factor α (TNF-α), and malondialdehyde (MDA) were decreased, and IL-4 and superoxide dismutase (SOD) were increased. Meanwhile, inulin increased the concentration of propionate, butyrate, and lactic acid (LA), while it decreased NH₃-N in rumen. The propionate- and butyrate-producing bacteria (e.g., Prevotella and Butyrivibrio) and several beneficial commensal bacteria (e.g., Muribaculaceae and Bifidobacterium) as well as metabolites related to energy and amino acid metabolism (e.g., melibiose and l-glutamate) were increased. However, several proinflammatory bacteria (e.g., Clostridia UCG-014, Streptococcus, and Escherichia-Shigella) were decreased, accompanied by the downregulation of lipid proinflammatory metabolites, for example, ceramide(d18:0/15:0) [Cer(d18:0/15:0)] and 17-phenyl-18,19,20-trinor-prostaglandin E₂. In the current study, the above indicators showed the best response in the 300 g/day inulin group. Overall, dietary supplementation of inulin could alleviate inflammatory responses in cows with SCM through improving the rumen inner environment. IMPORTANCE The correlation between mastitis and the gastrointestinal microbiome in dairy cows has been demonstrated. Regulating the profile of rumen microorganisms may contribute to remission of subclinical mastitis (SCM). Supplementation of inulin in the diets of cows with SCM could increase the abundance of short-chain fatty acid (SCFA)-producing bacteria and beneficial commensal bacteria in rumen and meanwhile the levels of amino acids and energy metabolism. Conversely, the abundance of ruminal bacteria and metabolites with proinflammatory effects were decreased. Our study suggests that the improvement of the rumen internal environment by inulin supplementation could ameliorate inflammatory responses during SCM in dairy cows and thus improve lactation performance and milk quality. Our results provide a theoretical basis for regulation measures of SCM in dairy cows.

SUBMITTER: Wang Y

PROVIDER: S-EPMC8557905 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:BackgroundDue to the high prevalence and complex etiology, bovine mastitis (BM) is one of the most important diseases to compromise dairy cow health and milk quality. The shift in milk compositions has been widely investigated during mastitis, but recent studies suggested that gastrointestinal microorganism also has a crucial effect on the inflammation of other peripheral tissues and organs, including the mammary gland. However, research focused on the variation of rumen inner-environment during mastitis is still limited. Therefore, the ruminal microbial profiles, metabolites, and milk compositions in cows with different udder health conditions were compared in the present study. Furthermore, the correlations between udder health status and ruminal conditions were investigated. Based on the somatic cell counts (SCC), California mastitis test (CMT) parameters and clinical symptoms of mastitis, 60 lactating Holstein dairy cows with similar body conditions (excepted for the udder health condition) were randomly divided into 3 groups (n = 20 per group) including the healthy (H) group, the subclinical mastitis (SM) group and the clinical mastitis (CM) group. Lactation performance and rumen fermentation parameters were recorded. And rumen microbiota and metabolites were also analyzed via 16S rRNA amplicon sequencing and untargeted metabolomics, respectively.ResultsAs the degree of mastitis increased, rumen lactic acid (LA) (P < 0.01), acetate, propionate, butyrate, valerate (P < 0.001), and total volatile fatty acids (TVFAs) (P < 0.01) concentrations were significantly decreased. In the rumen of CM cows, the significantly increased bacteria related to intestinal and oral inflammation, such as Lachnospiraceae (FDR-adjusted P = 0.039), Moraxella (FDR-adjusted P = 0.011) and Neisseriaceae (FDR-adjusted P = 0.036), etc., were accompanied by a significant increase in 12-oxo-20-dihydroxy-leukotriene B4 (FDR-adjusted P = 5.97 × 10- 9) and 10beta-hydroxy-6beta-isobutyrylfuranoeremophilane (FDR-adjusted P = 3.88 × 10- 10). Meanwhile, in the rumen of SM cows, the Ruminiclostridium_9 (FDR-adjusted P = 0.042) and Enterorhabdus (FDR-adjusted P = 0.043) were increased along with increasing methenamine (FDR-adjusted P = 6.95 × 10- 6), 5-hydroxymethyl-2-furancarboxaldehyde (5-HMF) (FDR-adjusted P = 2.02 × 10- 6) and 6-methoxymellein (FDR-adjusted P = 2.57 × 10- 5). The short-chain fatty acids (SCFAs)-producing bacteria and probiotics in rumen, including Prevoterotoella_1 (FDR-adjusted P = 0.045) and Bifidobacterium (FDR-adjusted P = 0.035), etc., were significantly reduced, with decreasing 2-phenylbutyric acid (2-PBA) (FDR-adjusted P = 4.37 × 10- 6).ConclusionThe results indicated that there was a significant shift in the ruminal microflora and metabolites associated with inflammation and immune responses during CM. Moreover, in the rumen of cows affected by SM, the relative abundance of several opportunistic pathogens and the level of metabolites which could produce antibacterial compounds or had a competitive inhibitory effect were all increased.

Project description:This study investigated the effects of inulin on rumen fermentation parameters, ruminal microbiome and metabolites, as well as lactation performance and serum indexes in dairy cows. Sixteen Holstein dairy cows with similar body conditions were randomly divided into 2 groups (n = 8 per group), with inulin addition at 0 and 200 g/d per cow. The experiment lasted for 6 weeks, including a 1-week adaptation period and a 5-week treatment period. At the end of the experimental period, the milk, serum and rumen fluid were sampled and analyzed. The microbiome and metabolome in the rumen fluid were analyzed via 16S rRNA sequencing and untargeted metabolomics, respectively. The results showed that supplementation with inulin (200 g/d per cow) increased the milk yield (P = 0.001), milk protein (P = 0.032), lactose rate (P = 0.004) and proportion of saturated fatty acids (SFA) in milk (P < 0.001), but decreased the proportion of unsaturated fatty acids (USFA) (P = 0.041). Rumen pH (P = 0.040) and the concentration of NH3-N (P = 0.024) were decreased; however, acetate (P < 0.001), propionate (P = 0.003), butyrate (P < 0.001) and lactic acid (LA) (P = 0.043) were increased. The total cholesterol (TC) (P = 0.008) and triglycerides (TG) (P = 0.01) in serum were also reduced. Additionally, inulin addition elevated the relative abundance of several beneficial symbiotic and short-chain fatty acid (SCFA)-producing bacteria, such as Muribaculaceae (false discovery rate [FDR]-adjusted P < 0.01), Acetitomaculum (FDR-adjusted P = 0.043), and Butyrivibrio (FDR-adjusted P = 0.036), while elevating the levels of L-lysine (FDR-adjusted P = 4.24 × 10-3), L-proline (FDR-adjusted P = 0.0158), and L-phenylalanine (FDR-adjusted P = 0.027). In contrast, several pathogens and ruminal bacteria abundant in high-fat diets, such as Escherichia-Shigella (FDR-adjusted P = 0.022), Erysipelotrichaceae __UCG-004 (FDR-adjusted P < 0.01) and RF39 (FDR-adjusted P = 0.042) were decreased along with the reduction of lysophosphatidylcholine (LysoPC) (18:1 (9Z)) (FDR-adjusted P = 1.03 × 10-3), LysoPC (16:0) (FDR-adjusted P = 0.0108), LysoPC (18:2 (9Z, 12Z)) (FDR-adjusted P = 1.65 × 10-3) and 8-methylnonenoate. In conclusion, dietary inulin supplementation could increase the relative abundance of commensal microbiota and SCFA-producing bacteria, upregulate amino acidmetabolism and downregulate lipid metabolism in the rumen of dairy cows, which might further improve lactation performance and the level of serum lipids.

Project description:The microbial ecosystem in the udders of dairy cows directly influences the flavor and quality of milk. However, to our knowledge, no published research has analyzed the complex relationship between the udder microbiome and its associated metabolism in animals with subclinical mastitis. We identified the bacterial species and measured relative population numbers in the milk of cows with subclinical Streptococcus agalactiae mastitis (GBS) and compared this information to that from the milk of healthy cows. Metabolite profiles were determined to investigate correlations between the milk microbiota and metabolic factors in healthy vs. GBS dairy cows. Six milk samples from GBS cows and six from healthy cows were subjected to 16S rRNA gene sequencing to identify the microbial species using a MiSeq high-throughput sequencing apparatus. The metabolites present in the milk were identified by gas chromatography time-of-flight mass spectrometry. Both principal component analysis and orthogonal partial least squares discriminant analysis indicated that the metabolites were well-separated from each other in the milk samples from the two groups. GBS dramatically altered microbial diversity, and the GBS group had significantly fewer Proteobacteria, Actinobacteria, and Acidobacteria than the CON group, with greater relative abundance of Firmicutes (p < 0.01). Several bacterial genera, such as Streptococcus, were significantly more abundant in milk from the GBS group than in milk from the CON group, and there was a tendency for greater abundance of Turicibacter (p = 0.07) and Enterococcus spp. (p = 0.07) in the GBS group. The levels of five milk metabolites were significantly higher in the GBS group than in the CON group: phenylpyruvic acid, the homogentisic acid: 4-hydroxyphenylpyruvic acid ratio, the xanthine: guanine ratio, uridine and glycerol. Metabolic pathway analysis of the different metabolites revealed that the following were enriched in both groups: galactose metabolism; pentose and glucuronate interconversion; starch and sucrose metabolism; alanine, aspartate and glutamate metabolism; arginine biosynthesis; citrate cycle (TCA cycle); D-glutamine and D-glutamate metabolism; and the neomycin, kanamycin, and gentamicin biosynthesis pathways. Several typical metabolites were highly correlated with specific ruminal bacteria, such as Streptococcaceae, Lachnospiraceae, Lactobacillaceae and Corynebacteriaceae, demonstrating the functional correlations between the milk microbiome and associated metabolites. These findings revealed that the milk microbiota and metabolite profiles were significantly different between the two groups of cows, raising the question of whether the microbiota associated with the bovine mammary gland could be related to mammary gland health. There was also a relationship between milk quality and the presence of spoilage bacteria. Other bacterial taxa should be investigated, as related information may provide insights into how perturbations in milk metabolomics profiles relate to differences in milk synthesis between healthy cows and those with subclinical mastitis.

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Dietary Supplementation of Inulin Ameliorates Subclinical Mastitis via Regulation of Rumen Microbial Community and Metabolites in Dairy Cows.

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