Real-time monitoring of ruminal microbiota reveals their roles in dairy goats during subacute ruminal acidosis.
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ABSTRACT:
SUBMITTER: Chen X
PROVIDER: S-EPMC8121909 | biostudies-literature | 2021 May
REPOSITORIES: biostudies-literature
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Real-time monitoring of ruminal microbiota reveals their roles in dairy goats during subacute ruminal acidosis.
Chen Xiaodong X Su Xiaodong X Li Jilong J Yang Yuntian Y Wang Peiyue P Yan Fang F Yao Junhu J Wu Shengru S
NPJ biofilms and microbiomes 20210514 1
Ruminal microbiota changes frequently with high grain diets and the occurrence of subacute ruminal acidosis (SARA). A grain-induced goat model of SARA, with durations of a significant decrease in the rumen pH value to less than 5.6 and an increase in the rumen lipopolysaccharides concentration, is constructed for real-time monitoring of bacteria alteration. Using 16 S rRNA gene sequencing, significant bacterial differences between goats from the SARA and healthy groups are identified at every ho ...[more]
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Project description:BackgroundSubacute rumen acidosis (SARA) is a common metabolic disorder in ruminants that disrupts the rumen microbiome and animal health, but diagnosis is challenging due to subtle symptoms and invasive testing requirements. This study explores the potential of the buccal (oral) microbiome as a diagnostic indicator for SARA, hypothesizing an interaction with the rumen microbiome.ResultsThe study involved 47 dairy goats, including 11 on a control diet and 36 on high-concentrate diets with increasing rumen-degradable starch. Animals were grouped based on dietary exposure and ruminal pH: Control, Low-RDS Tolerance/SARA (LRDST/LRDSS), and High-RDS Tolerance/SARA (HRDST/HRDSS). Transcriptomics of rumen epithelium showed heightened inflammatory pathway gene expression in SARA-susceptible goats compared to controls and tolerant groups. Alpha diversity of ruminal bacteria showed lower Shannon diversity in HRDSS goats compared to HRDST whereas buccal bacteria displayed significantly lower Chao1 diversity in LRDSS goats compared to HRDST. Beta diversity analyses revealed distinct patterns between SARA-affected goats and healthy controls in both ruminal and buccal microbiomes. Prevotellaceae_UCG-003 emerged as a candidate biomarker, with reduced abundance in SARA-susceptible goats in both rumen and buccal samples. Machine learning classifiers achieved high accuracy in distinguishing SARA-susceptible goats using this genus (rumen AUC = 0.807; buccal AUC = 0.779). Source tracking analysis illustrated diminished cross-population of bacteria from the buccal to rumen (2.86% to 0.25%) and vice versa (8.59% to 1.17%), signifying compromised microbial interchange in SARA-affected goats. A microbiota transplant experiment verified SARA microbiota's ability to induce pH decline, escalate inflammation-related gene expression (MAPK10, IL17B, FOSB, SPP1), disrupt microbial transfer, and reduce Prevotellaceae_UCG-003 in recipients.ConclusionOur findings highlight SARA's dual impact on ruminal and buccal microbiota, exacerbating epithelial inflammation gene expression. Shifts in the buccal microbiome, specifically reductions in Prevotellaceae_UCG-003, mirror ruminal changes and can be influenced by inter-compartmental bacterial transmission, thereby offering a non-invasive diagnostic approach for SARA.
| S-EPMC11872310 | biostudies-literature
Project description:BackgroundSubacute ruminal acidosis (SARA) is a metabolic disease in high-producing dairy cattle, and is accompanied by rumenitis. However, the mechanism of rumenitis remains unclear. Therefore, the aim of this study was to investigate the molecular mechanism of rumenitis in dairy cows with SARA.ResultsThe results showed that SARA cows displayed high concentrations of ruminal volatile fatty acids, lactic acid and lipopolysaccharide (LPS). Furthermore, the blood concentrations of LPS and acute phase proteins haptoglobin, serum amyloid-A, and LPS binding protein were significantly higher in SARA cows than in control cows. Importantly, the phosphorylation levels of nuclear factor-kappaB (NF-κB) p65, inhibitor of NF-κB (IκB), c-Jun N-terminal kinase (JNK), and extracellular signal-regulated kinase 1/2 (ERK1/2) were significantly higher in the rumen epithelium of SARA cows than those of control cows. The ruminal mRNA and protein levels of NF-κB- and mitogen-activated protein kinase (MAPK)s -regulated inflammatory cytokines, tumor necrosis factor α (TNF-α), interleukin 6 (IL-6) and interleukin 1β (IL-1β), were markedly higher in SARA cows than in control cows. Similarly, serum concentrations of TNF-α and IL-6 were also significantly higher in SARA cows.ConclusionsThese results indicate that SARA results in high concentration of ruminal LPS, which over activates the NF-κB and MAPKs inflammatory pathways and then significantly increases the expression and synthesis of pro-inflammation cytokines in the rumen epithelium, thereby partly inducing rumenitis.
| S-EPMC5909223 | biostudies-literature
Project description:The impact of a long-term subacute rumen acidosis (SARA) on the bovine epimural bacterial microbiome (BEBM) and its consequences for rumen health is poorly understood. This study aimed to investigate shifts in the BEBM during a long-term transient SARA model consisting of two concentrate-diet-induced SARA challenges separated by a 1-week challenge break. Eight cows were fed forage and varying concentrate amounts throughout the experiment. In total, 32 rumen papilla biopsies were taken for DNA isolation (4 sampling time points per cow: at the baseline before concentrate was fed, after the first SARA challenge, after the challenge break, and after the second SARA challenge). Ruminal pH was continuously monitored. The microbiome was determined using Illumina MiSeq sequencing of the 16S rRNA gene (V345 region). In total 1,215,618 sequences were obtained and clustered into 6833 operational taxonomic units (OTUs). Campylobacter and Kingella were the most abundant OTUs (16.5 and 7.1%). According to ruminal pH dynamics, the second challenge was more severe than the first challenge. Species diversity estimates and evenness increased during the challenge break compared to all other sampling time points (P < 0.05). During both SARA challenges, Kingella- and Azoarcus-OTUs decreased (0.5 and 0.4 fold-change) and a dominant Ruminobacter-OTU increased during the challenge break (18.9 fold-change; P < 0.05). qPCR confirmed SARA-related shifts. During the challenge break noticeably more OTUs increased compared to other sampling time points. Our results show that the BEBM re-establishes the baseline conditions slower after a SARA challenge than ruminal pH. Key phylotypes that were reduced during both challenges may help to establish a bacterial fingerprint to facilitate understanding effects of SARA conditions on the BEBM and their consequences for the ruminant host.
| S-EPMC4777738 | biostudies-literature
Project description:BackgroundCurrently, little is known about the effect of sodium butyrate (NaB) on oxidative stress following grain-induced sub-acute ruminal acidosis in dairy goats. In the present study, 18 lactating dairy goats implanted with a ruminal cannula and permanent indwelling catheters in the portal and hepatic veins were randomly allocated into 3 treatment groups over 20 weeks: low grain (LG, 40% grain; n = 6), high grain (HG, 60% grain; n = 6) and high grain with sodium butyrate (HG + NaB, 60% grain + NaB; n = 6).ResultsWhen added to the HG diet, NaB increased the mean ruminal pH and reduced the levels of ruminal, portal and hepatic LPS; Additionally, we observed an increase in SOD1, SOD2, SOD3, GPX1 and CAT mRNA expression, increased levels of TSOD and CAT enzyme activity as well as increased total antioxidant capacity (T-AOC) and decreased malondialdehyde (MDA) in both the liver and plasma, while GPx activity increased in the liver of goats fed the HG + NaB diet. The mRNA expression of UGT1A1, NQO1, MGST3, and Nrf2, as well as total Nrf2 protein levels were increased in goats fed the HG + NaB diet.ConclusionsOur study indicates that sodium butyrate could improve the oxidative status in sub-acute ruminal acidosis through the partial activation of Nrf2-dependent genes.
| S-EPMC6131738 | biostudies-literature
Project description: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.
| S-EPMC4870271 | biostudies-literature
Project description:Subacute ruminal acidosis (SARA) is a common metabolic disorder of high yielding dairy cows, and it is associated with dysbiosis of the rumen and gut microbiome and host inflammation. This study evaluated the impact of two postbiotics from Saccharomyces cerevisiae fermentation products (SCFP) on rumen liquid associated microbiota of lactating dairy cows subjected to repeated grain-based SARA challenges. A total of 32 rumen cannulated cows were randomly assigned to 4 treatments from 4 weeks before until 12 weeks after parturition. Treatment groups included a Control diet or diets supplemented with postbiotics (SCFPa, 14 g/d Original XPC; SCFPb-1X, 19 g/d NutriTek; SCFPb-2X, 38 g/d NutriTek, Diamond V, Cedar Rapids, IA, USA). Grain-based SARA challenges were conducted during week 5 (SARA1) and week 8 (SARA2) after parturition by replacing 20% DM of the base total mixed ration (TMR) with pellets containing 50% ground barley and 50% ground wheat. Total DNA from rumen liquid samples was subjected to V3-V4 16S rRNA gene amplicon sequencing. Characteristics of rumen microbiota were compared among treatments and SARA stages. Both SARA challenges reduced the diversity and richness of rumen liquid microbiota, altered the overall composition (β-diversity), and its predicted functionality including carbohydrates and amino acids metabolic pathways. The SARA challenges also reduced the number of significant associations among different taxa, number of hub taxa and their composition in the microbial co-occurrence networks. Supplementation with SCFP postbiotics, in particular SCFPb-2X, enhanced the robustness of the rumen microbiota. The SCFP supplemented cows had less fluctuation in relative abundances of community members when exposed to SARA challenges. The SCFP supplementation promoted the populations of lactate utilizing and fibrolytic bacteria, including members of Ruminococcaceae and Lachnospiraceae, and also increased the numbers of hub taxa during non-SARA and SARA stages. Supplementation with SCFPb-2X prevented the fluctuations in the abundances of hub taxa that were positively correlated with the acetate concentration, and α- and β-diversity metrics in rumen liquid digesta. Induction of SARA challenges reduced microbiota richness and diversity and caused fluctuations in major bacterial phyla in rumen liquid microbiota in lactating dairy cows. Supplementation of SCFP postbiotics could attenuate adverse effects of SARA on rumen liquid microbiota.
| S-EPMC11293205 | biostudies-literature
Project description:BackgroundBovine milk is an important source of nutrition for human consumption, and its quality is closely associated with the microbiota and metabolites in it. But there is limited knowledge about the milk microbiome and metabolome in cows with subacute ruminal acidosis.MethodsEight ruminally cannulated Holstein cows in mid lactation were selected for a 3-week experiment. The cows were randomly allocated into 2 groups, fed either a conventional diet (CON; 40% concentrate; dry matter basis) or a high-concentrate diet (HC; 60% concentrate; dry matter basis).ResultsThe results showed that there was a decreased milk fat percentage in the HC group compared to the CON group. The amplicon sequencing results indicated that the alpha diversity indices were not affected by the HC feeding. At the phylum level, the milk bacteria were dominated by Proteobacteria, Actinobacteria, Bacteroidetes, and Firmicutes both in the CON and HC groups. At the genus level, the HC cows displayed an improved proportion of Labrys (P = 0.015) compared with the CON cows. Results of both the principal components analysis and partial least squares of discriminant analysis of milk metabolome revealed that samples of the CON and HC groups clustered separately. A total of 31 differential metabolites were identified between the two groups. Of these, the levels of 11 metabolites decreased (α-linolenic acid, prostaglandin E2, L-lactic acid, L-malic acid, 3-hydroxysebacic acid, succinyladenosine, guanosine, pyridoxal, L-glutamic acid, hippuric acid, and trigonelline), whereas the levels of the other 20 metabolites increased in the HC group with respect to the CON group (P < 0.05).ConclusionThese results suggested that subacute ruminal acidosis less impacted the diversity and composition of milk microbiota, but altered the milk metabolic profiles, which led to the decline of the milk quality.
| S-EPMC10158360 | biostudies-literature
Project description: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.
| S-EPMC9913405 | biostudies-literature
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.
| S-EPMC8718735 | biostudies-literature
Project description:We evaluated the clinical aspects and feeding behavior of cattle with subacute ruminal acidosis (SARA) caused by short-chain fatty acids (SCFAs). Ten healthy Nelore heifers were subjected to an adjusted SARA induction protocol using citrus pulp (CP). Clinical examinations were performed at baseline and at 3, 6, 9, 12, 15, 18, and 24 h intervals after induction, with ruminal fluid, blood, and feces sampling. The animals' feeding behavior was evaluated on, before, and for 3 days after SARA by observing the animals every 5 min for 24 h. The dry matter intake (DMI) was recorded daily. The ruminal pH during SARA was always lower than baseline, with an acidotic duration of 547 ± 215 min, a minimum pH of 5.38 ± 0.16, and an average pH of 5.62 ± 0.1. SARA was mainly caused by SCFAs (maximum 118.4 ± 9.3 mmol/L), with the production of l-lactic acids (7.17 mmol/L) and d-lactic acids (0.56 mmol/L) 6 h after the experiment began. The DMI was reduced by 66% and 48% on days 1 and 2, respectively, and returned to normal levels on day 3. SARA caused a reduction in feed intake and rumination time, as well as an increase in the time spent in decubitus on days 1 and 2. These results were influenced by the ruminal pH, ruminal movement, and osmolarity. Furthermore, SARA caused different degrees of depression, which became more pronounced with higher ruminal lactic acid concentrations.
| S-EPMC7824239 | biostudies-literature