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Effects of ruminal pH on gene expression in the rumen epithelium, peripheral blood mononuclear cell subpopulations, and blood metabolites from Holstein calves during weaning transition.

ABSTRACT: We investigated the relationships between ruminal pH, gene expression in the rumen epithelium (RE), peripheral blood mononuclear cell subpopulations, and blood metabolites in Holstein calves during weaning transition. Calves (Weaning group, n=7) were assigned to one of two groups, and fed calf starter with forage (Forage group, n=3) or without forage (Starter group, n=4). Ruminal pH was measured continuously. Samples were collected at -1, 0, 1, and 3 weeks (blood and rumen fluid) or 3 weeks (rumen epithelium) after weaning. In the Weaning group, ruminal pH increased, and several blood metabolites increased (blood urea nitrogen [BUN], beta-hydroxybutyrate [BHB], and gamma-glutamyl transferase [GGT]) or decreased (total cholesterol [T-CHO] and phospholipid) after weaning. Ruminal pH was positively correlated with CD8⁺CD45R^- cell populations and blood metabolites (BUN, glucose, and BHB) and negatively correlated with GGT activity. The 24 hr mean ruminal pH was higher in the Forage group during weaning transition, and toll-like receptor 4 mediated signaling pathway was activated in the Starter group at 3 weeks post-weaning. The number of CD8⁺CD45R^- cells tended to be higher, and several blood metabolites (glucose, triglycerides, T-CHO, and phospholipid) were higher in the Forage group after weaning. Calves with higher ruminal pH also showed a greater energy metabolism status simultaneously with lesser hepatic disturbance enzymes in the peripheral blood. The results of our study indicate that serum GGT activity may be a plausible biomarker for predicting ruminal acidosis in Holstein calves during weaning transition.

SUBMITTER: Kim YH

PROVIDER: S-EPMC6612501 | biostudies-literature | 2019 Jun

REPOSITORIES: biostudies-literature

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Effects of ruminal pH on gene expression in the rumen epithelium, peripheral blood mononuclear cell subpopulations, and blood metabolites from Holstein calves during weaning transition.

Kim Yo-Han YH Toji Noriyuki N Kizaki Keiichiro K Takemura Kei K Kushibiki Shiro S Sato Shigeru S

The Journal of veterinary medical science 20190430 6

We investigated the relationships between ruminal pH, gene expression in the rumen epithelium (RE), peripheral blood mononuclear cell subpopulations, and blood metabolites in Holstein calves during weaning transition. Calves (Weaning group, n=7) were assigned to one of two groups, and fed calf starter with forage (Forage group, n=3) or without forage (Starter group, n=4). Ruminal pH was measured continuously. Samples were collected at -1, 0, 1, and 3 weeks (blood and rumen fluid) or 3 weeks (rum ...[more]

PMID: 31061249

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Project description:We investigated the relationship between ruminal pH and bacteria in calves fed calf starter with and without forage during weaning transition. First, 16 Holstein bull calves were obtained from dairy farms and equipped with rumen cannulas by cannulation surgery. Then, calves (73.5 ± 4.2 kg; mean ± SE) were assigned to groups fed calf starter either with forage (HAY, n = 8) or without forage (CON, n = 8), and all calves were weaned at 8 weeks of age. Ruminal pH was measured continuously, and rumen fluid samples were collected at 7, 8, 9, and 11 weeks of age, namely -1, 0, 1, and 3 weeks after weaning, respectively, to assess volatile fatty acid concentrations and bacterial DNA. The 24-h mean ruminal pH was significantly (P < 0.05) different between the two groups. Diurnal changes in the 1-h mean ruminal pH were observed throughout the study in the HAY group; however, they were not observed at 0 and 1 weeks after weaning in the CON group. Moreover, the HAY group had significantly (P < 0.05) higher proportions of acetate and butyrate and lower proportion of propionate, and significantly (P < 0.05) lower ruminal acetate-to-propionate ratios were observed in the CON group. The ruminal bacterial diversity indices decreased after -1 week in both groups and increased at 0 and 1 weeks after weaning in the HAY and CON groups, respectively. From the 454 pyrosequencing analysis, significant differences (P < 0.05) were observed in the relative abundance of several phyla (Bacteroidetes, Actinobacteria, and Tenericutes) and one genus (Prevotella) between the two groups. From quantitative real-time PCR analysis, the HAY group had the higher copy numbers of cellulolytic bacteria (Ruminococcus flavefaciens and Ruminococcus albus) compared with the CON group. This study demonstrated that feeding of dietary forage alleviates subacute ruminal acidosis due to diurnal changes in ruminal pH. Furthermore, changes in ruminal pH affect the ruminal bacterial diversity and relative abundance, and these changes might have influenced the establishment of fermentative ruminal functions during weaning transition.

Project description:BackgroundTargeted modification of the dairy calf ruminal microbiome has been attempted through rumen fluid inoculation to alter productive phenotypes later in life. However, sustainable effects of the early life interventions have not been well studied, particularly on the metabolically active rumen microbiota and its functions. This study investigated the sustained effects of adult-derived rumen fluid inoculations in pre-weaning dairy calves on the active ruminal microbiome of post-weaned dairy calves analyzed via RNA-sequencing.ResultsTwo different adult-derived microbial inocula (bacterial- or protozoal-enriched rumen fluid; BE or PE, respectively) were administered in pre-weaned calves (3-6 weeks) followed by analyzing active rumen microbiome of post-weaned calves (9 weeks). The shared bacterial community at the genus level of 16S amplicon-seq and RNA-seq datasets was significantly different (P = 0.024), 21 out of 31 shared major bacterial genera differed in their relative abundance between the two analytic pipelines. No significant differences were found in any of the prokaryotic alpha- and beta-diversity measurements (P > 0.05), except the archaeota that differed for BE based on the Bray-Curtis dissimilarity matrix (P = 0.009). Even though the relative abundances of potentially transferred microbial and functional features from the inocula were minor, differentially abundant prokaryotic genera significantly correlated to various fermentation and animal measurements including butyrate proportion, body weight, and papillae length and counts. The overall microbial functions were affected quantitatively by BE and qualitatively by PE (P < 0.05), and this might be supported by the individual KEGG module and CAZymes profile differences. Exclusive networks between major active microbial (bacterial and archaeal genera) and functional features (KEGG modules) were determined which were differed by microbial inoculations.ConclusionsThis study demonstrated that actively transcribed microbial and functional features showed reliable connections with different fermentations and animal development responses through adult rumen fluid inoculations compared to our previous 16S amplicon sequencing results. Exclusive microbial and functional networks of the active rumen microbiome of dairy calves created by BE and PE might also be responsible for the different ruminal and animal characteristics. Further understanding of the other parts of the gastrointestinal tract (e.g., abomasum, omasum, and small intestine) using metatranscriptomics will be necessary to elucidate undetermined biological factors affected by microbial inoculations.

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Dataset Information

Effects of ruminal pH on gene expression in the rumen epithelium, peripheral blood mononuclear cell subpopulations, and blood metabolites from Holstein calves during weaning transition.

Publications

Effects of ruminal pH on gene expression in the rumen epithelium, peripheral blood mononuclear cell subpopulations, and blood metabolites from Holstein calves during weaning transition.

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