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Induction of Subacute Ruminal Acidosis Affects the Ruminal Microbiome and Epithelium.

ABSTRACT: Subacute ruminal acidosis (SARA) negatively impacts the dairy industry by decreasing dry matter intake, milk production, profitability, and increasing culling rate and death loss. Six ruminally cannulated, lactating Holstein cows were used in a replicated incomplete Latin square design to determine the effects of SARA induction on the ruminal microbiome and epithelium. Experimental periods were 10 days with days 1-3 for ad libitum intake of control diet, followed by 50% feed restriction on day 4, and ad libitum access on day 5 to the basal diet or the basal diet with an additional 10% of a 50:50 wheat/barley pellet. Based on subsequent ruminal pH, cows were grouped (SARA grouping; SG) as Non-SARA or SARA based on time <5.6 pH (0 and 3.4 h, respectively). Ruminal samples were collected on days 1 and 6 of each period prior to feeding and separated into liquid and solid fractions. Microbial DNA was extracted for bacterial analysis using 16S rRNA gene paired-end sequencing on the MiSeq Illumina platform and quantitative PCR (qPCR). Ruminal epithelium biopsies were taken on days 1 and 6 before feeding. Quantitative RT-PCR was used to determine gene expression in rumen epithelium. Bray-Curtis similarity indicated samples within the liquid fraction separated by day and coincided with an increased relative abundance of genera Prevotella, Ruminococcus, Streptococcus, and Lactobacillus on day 6 (P < 0.06). Although Firmicutes was the predominant phyla in the solid fraction, a SG × day interaction (P < 0.01) indicated a decrease on day 6 for SARA cows. In contrast, phylum Bacteroidetes increased on day 6 (P < 0.01) for SARA cows driven by greater genera Prevotella and YRC22 (P < 0.01). Streptococcus bovis and Succinivibrio dextrinosolvens populations tended to increase on day 6 but were not affected by SG. In ruminal epithelium, CLDN1 and CLDN4 expression increased on day 6 (P < 0.03) 24 h after SARA induction and a tendency for a SG × day interaction (P < 0.10) was observed for CLDN4. Overall, results indicate more rapid adaptation to an induced bout of SARA in the solid fraction ruminal microbiome compared with ruminal epithelium.

SUBMITTER: McCann JC

PROVIDER: S-EPMC4870271 | biostudies-literature | 2016

REPOSITORIES: biostudies-literature

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Induction of Subacute Ruminal Acidosis Affects the Ruminal Microbiome and Epithelium.

McCann Joshua C JC Luan Shaoyu S Cardoso Felipe C FC Derakhshani Hooman H Khafipour Ehsan E Loor Juan J JJ

Frontiers in microbiology 20160518

Subacute ruminal acidosis (SARA) negatively impacts the dairy industry by decreasing dry matter intake, milk production, profitability, and increasing culling rate and death loss. Six ruminally cannulated, lactating Holstein cows were used in a replicated incomplete Latin square design to determine the effects of SARA induction on the ruminal microbiome and epithelium. Experimental periods were 10 days with days 1-3 for ad libitum intake of control diet, followed by 50% feed restriction on day 4 ...[more]

PMID: 27242724

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Project description:Subacute ruminal acidosis (SARA) represents one of the most important digestive disorders in intensive dairy farms, and dairy cows are individually different in the severity of SARA risk. The objectives of the current study were to investigate differences in the ruminal bacterial community and metabolome in dairy cattle with different susceptibility to SARA. In the present study, 12 cows were initially enrolled in the experiment. Based on average ruminal pH, 4 cows with the lowest ruminal pH were assigned to the susceptible group (SUS, pH = 5.76, n = 4) and 4 cows with the highest ruminal pH assigned to the tolerant group (TOL, pH = 6.10, n = 4). Rumen contents from susceptible (SUS, n = 4) and tolerant (TOL, n = 4) dairy cows were collected through rumen fistula to systematically reveal the rumen microbial and metabolic alterations of dairy cows with different susceptibility to SARA using multi-omics approaches (16S and 18S rRNA gene sequencing and metabolome). The results showed that despite being fed the same diet, SUS cows had lower ruminal pH and higher concentrations of total volatile fatty acids (VFA) and propionate than TOL cows (P < 0.05). No significant differences were observed in dry matter intake, milk yield, and other milk compositions between the SUS and TOL groups (P > 0.05). The principal coordinates analysis based on the analysis of molecular variance indicated a significant difference in bacterial composition between the two groups (P = 0.01). More specifically, the relative abundance of starch-degrading bacteria (Prevotella spp.) was greater (P < 0.05), while the proportion of fiber-degrading bacteria (unclassified Ruminococcaceae spp., Ruminococcus spp., Papillibacter, and unclassified Family_XIII) was lower in the rumen of SUS cows compared with TOL cows (P < 0.05). Community analysis of protozoa showed that there were no significant differences in the diversity, richness, and community structure (P > 0.05). Metabolomics analysis revealed that the concentrations of organic acids (such as lactic acid), biogenic amines (such as histamine), and bacterial degradation products (such as hypoxanthine) were significantly higher in the SUS group compared to the TOL group (P < 0.05). These findings revealed that the higher proportion of starch-degrading bacteria/lower fiber-degrading bacteria in the rumen of SUS cows resulted in higher VFA-producing capacity, in particular propionate. This caused a disruption in metabolic homeostasis in the rumen which might be the reason for the higher susceptibility to SARA. Overall, these findings enhanced our understanding of the ruminal microbiome and metabolic changes in cows susceptible to SARA.

Project description:The demand for economic benefits has led to an increase in the proportion of high-concentrate (HC) feed in the ruminant diet, resulting in an increased incidence of subacute ruminal acidosis (SARA). During SARA, a high concentration of lipopolysaccharide (LPS) translocated in the rumen induces a systemic inflammatory response. Inflammatory diseases, such as endometritis and mastitis, are often associated with SARA; however, in sheep, the mechanism of the effect of SARA on the endometrium has rarely been reported. Therefore, the aim of this study was to investigate, for the first time, the influence of LPS translocation on endometrial tight junctions (TJs) during SARA in sheep. The results showed that LPS and TNFα levels in the ruminal fluid, serum, and endometrial tissue supernatant during SARA increased, transcription levels of TLR4, NFκB, and TNFα in the endometrium increased, the protein expression level of claudin-1 in the endometrium increased, and the protein expression level of occludin decreased. 17β-estradiol (E2) inhibits claudin-1 protein expression and promotes occludin expression, and progesterone (P4) promotes claudin-1 protein expression and inhibits occludin protein expression. E2 and P4 regulate claudin-1 and occludin protein expression through their receptor pathways. Here, we found that LPS hindered the regulatory effect of E2 and P4 on endometrial TJs by inhibiting their receptor expression. The results of this study indicate that HC feeding can cause SARA-induced LPS translocation in sheep, increase susceptibility to systemic inflammation, induce the endometrial inflammatory response, and cause endometrial epithelial TJ damage directly and/or by obstructing E2 and P4 function. LPS translocation caused by SARA has also been suggested to induce an endometrial inflammatory response, resulting in endometrial epithelial barrier damage and physiological dysfunction, which seriously affects ruminant production. Therefore, this study provides new evidence that SARA is a potential factor that induces systemic inflammation in ruminants. It provides theoretical support for research on the prevention of endometritis in ruminants.

Project description:Subacute ruminal acidosis (SARA) is a major metabolic disease in lactating dairy cows caused by the excessive intake of high-concentrate diets. Here, we investigated the synergistic responses of rumen bacteria and epithelium to high-grain (HG)-induced SARA. Eight ruminally cannulated lactating Holstein cows were randomly assigned to 2 groups for a 3-week experiment and fed either a conventional (CON) diet or an HG diet. The results showed that the HG-feeding cows had a thickened rumen epithelial papilla with edge injury and a decreased plasma β-hydroxybutyrate concentration. The 16S rRNA gene sequencing results demonstrated that HG feeding caused changes in rumen bacterial structure and composition, which further altered rumen fermentation and metabolism. Cooccurrence network analysis revealed that the distribution of the diet-sensitive bacteria responded to the treatment (CON or HG) and that all diet-sensitive amplicon sequence variants showed low to medium degrees of cooccurrence. Metabolomics analysis indicated that the endothelial permeability-increasing factor prostaglandin E1 and the polyamine synthesis by-product 5'-methylthioadenosine were enriched under HG feeding. Transcriptome analysis suggested that cholesterol biosynthesis genes were upregulated in the rumen epithelium of HG cows. The gene expression changes, coupled with more substrate being available (total volatile fatty acids), may have caused an enrichment of intracellular cholesterol and its metabolites. All of these variations could coordinately stimulate cell proliferation, increase membrane permeability, and trigger epithelial inflammation, which eventually disrupts rumen homeostasis and negatively affects cow health. IMPORTANCE Dairy cows are economically important livestock animals that supply milk for humans. The cow's rumen is a complex and symbiotic ecosystem composed of diverse microorganisms, which has evolved to digest high-fiber diets. In modern dairy production, SARA is a common health problem due to overfeeding of high-concentrate diets for an ever-increasing milk yield. Although extensive studies have been conducted on SARA, it remains unclear how HG feeding affects rumen cross talk homeostasis. Here, we identified structural and taxonomic fluctuation for the rumen bacterial community, an enrichment of certain detrimental metabolites in rumen fluid, and a general upregulation of cholesterol biosynthesis genes in the rumen epithelium of HG-feeding cows by multi-omics analysis. Based on these results, we propose a speculation to explain cellular events of coordinated rumen bacterial and epithelial adaptation to HG diets. Our work provides new insights into the exploitation of molecular regulation strategies to treat and prevent SARA.

Project description:Several ruminal cellulolytic bacteria species are sensitive to pH and could therefore be used as biomarkers to determine the risk of sub-acute ruminal acidosis (SARA) in finishing lambs. This study compared a 2-4 h post feeding ruminal pH measurement to abundances of the ruminal pH-sensitive bacteria to evaluate the risk of SARA in a herd of 120 finishing lambs. The lambs were reared in individual units for 50 days. Ruminal fluid was collected by use of an orogastric tube on day 51 2-4 h after feeding. Although the lambs were fed an identical diet, they responded differently in the abundances of four ruminal pH sensitive cellulolytic bacteria (Ruminococcus albus, Ruminococcus flavefaciens and Fibrobacter succinogenes and Butyrivibrio fibrisolvens). Lambs with the most or the least cellulolytic bacteria were then classified as either lower SARA risk (LSR, n = 10) or higher SARA risk group (HSR, n = 10), respectively. Data showed that the ruminal pH and VFA profiles were uncorrelated with the number of cellulolytic bacteria (P > 0.050). Lambs with the HSR showed lower ruminal pH (P = 0.013) and acetate to propionate ratio (P = 0.018), higher concentrations of lactate (P = 0.035) and proportion of propionate (P = 0.033) compared to those with the LSR. The DMI and ADG did not differ in LSR and HSR lambs (P > 0.050). A diversity analysis revealed significantly lower diversity in HSR lambs than in LSR (Simpson index, P = 0.004). The relative abundances of the phyla Bacteroidetes, Fibrobacteres, Verruomicrobia, and Proteobacteria were higher in LSR lambs than in HSR (P < 0.050). The abundances of several phyla including Firmicutes, Tenericutes and Actinobacteria were higher in the HSR than in the LSR group (P < 0.050). The bacterial communities of the LSR and HSR clustered separately in rumen based on the Unifrac distances, indicating distinct bacteria communities at OTU level between the LSR and HSR lambs. Overall, there was no correlation between 2 and 4 h post-feeding ruminal pH and the abundance of pH-sensitive bacteria and the amount of these bacteria could be used as a potential biomarker of SARA in lamb herd.

Project description:Simple Summary This experiment was conducted to investigate the effects of a high-dose vitamin E (VE) supplementation on rumen microorganisms and the blood metabolites of subacute ruminal acidosis (SARA) induced by a high-grain diet in dairy cows, and to explore the mechanism of action through the combined analysis of the microbiome and metabolome. Our studies indicate that a high dose of VE can alleviate a series of adverse effects caused by SARA. Abstract The aim of this trial was to assess whether the supplementation of vitamin E (VE) in high-concentrate diets could improve the fermentation and blood metabolism in the rumen of dairy cows, thereby modulating the degree of the subacute ruminal acidosis (SARA) response and improving the performance. Seven Holstein cows (four fitted with ruminal cannulas) were fed three diets (total mixed rations) during three successive periods (each lasted for 18 d): (1) the control diet (CON); (2) a high-grain (HG) diet, which was the control diet supplied with a 15% finely ground wheat diet (FGW); and (3) a high-VE diet (HGE), which was the control diet provided with a 15% FGW and 12,000 IU of VE/head per day. The results indicated that VE was able to alleviate the reduction in the dry matter intake (DMI) and milk fat yield in cows caused by HG diets. The supplementation of VE significantly reduced the levels of lipopolysaccharide (LPS), histamine (HIS), and the total volatile fatty acid (TVFA) in the rumen. The supplementation of VE observably increased the antioxidant capacity of the milk and plasma. In addition, VE markedly reduced the plasma levels of endotoxin, HIS, and pro-inflammatory factors. The supplementation of VE significantly enriched the differential metabolites of the purine metabolism, cysteine, methionine metabolism, and ABC transporter synthesis pathway in the serum. The supplementation of VE also significantly increased the relative abundance of Succiniclasticum and decreased the relative abundance of Treponema, thus reducing the production of TVFA in the rumen. In conclusion, considering that the cows in this trial had high ketone levels (BHBA > 2.3 mmol/L), we found that VE could improve the rumen fermentation and blood metabolism by modulating the relative abundance of rumen microorganisms, thereby mitigating a range of adverse effects caused by SARA.

Project description:BackgroundThe development of the rumen is an important physiological challenge for young ruminants. Previous studies have shown that starter feeding can effectively facilitate the growth and development of the rumen in ruminants. However, the mechanism through which starter feeding stimulates the development of the rumen is not clear. Here, we performed an integrated analysis in ruminal microbiota and a host transcriptomic profile in a lamb model with the intervention of starter feed to understand the ruminal microbiome-host crosstalk in stimulating the development of the ruminal epithelium.ResultsDecreased ruminal pH and increased acetate and butyrate concentrations in the rumen, followed by increasing rumen organ index, were observed in lambs supplemented with starter. Using metagenome sequencing in combination with 16S rRNA and 18S rRNA gene amplicon sequencing, the results showed the abundance of acetate-producing Mitsuokella spp., lactate-producing Sharpea spp., lactate-utilizing Megasphaera spp., and Entodinium spp. was enriched in rumen microbial communities in the starter-feed group. The abundances of genes involved in sugar degradation were decreased in starter-feed lambs, but the GH13 encoding α-amylase was obviously increased. Rumen epithelial transcriptome analysis revealed that seven differentially expressed genes, including MAPK1, PIK3CB, TNFSF10, ITGA6, SNAI2, SAV1, and DLG, related to the cell growth module were upregulated, and BAD's promotion of cell death was downregulated. Correlation analysis revealed that the increase in the concentrations of acetate and butyrate significantly correlated with the expression of these genes, which indicates acetate and butyrate likely acted as important drivers in the ruminal microbiome-host crosstalk.ConclusionsThe present study comprehensively describes the symbiotic relationship between the rumen microbiota and the host in lambs after starter feeding. Our data demonstrates that the microbiome-driven generation of acetate and butyrate mediated the growth-related genes' regulation of the growth-associated signalling pathway in the ruminal epithelium. These co-development networks regulated many physiological processes in the epithelium, including papillae morphology and rumen epithelial growth.

Dataset Information

Induction of Subacute Ruminal Acidosis Affects the Ruminal Microbiome and Epithelium.

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Induction of Subacute Ruminal Acidosis Affects the Ruminal Microbiome and Epithelium.

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