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Responsive changes of rumen microbiome and metabolome in dairy cows with different susceptibility to subacute ruminal acidosis.

ABSTRACT: 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.

SUBMITTER: Zhang T

PROVIDER: S-EPMC8718735 | biostudies-literature |

REPOSITORIES: biostudies-literature

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Project description:Effects of subacute ruminal acidosis (SARA) challenges on the bacteria in rumen fluid, cecal digesta, and feces of dairy cows were determined using 16S rRNA gene pyrosequencing and real-time quantitative PCR. Six non-lactating Holstein cows with cannulas in the rumen and cecum were used in a 3 × 3 Latin square arrangement of treatments. During the first 3 wk of each experimental period, cows received a control diet containing 70% forages on a dry matter (DM) basis. In wk 4 of each period, cows received one of three diets: (1) the control diet; (2) a diet in which 34% of the dietary DM was replaced with pellets of ground wheat and barley (GBSC); or (3) a diet in which 37% of dietary DM was replaced with pellets of ground alfalfa (APSC). Rumen fluid, cecal digesta and feces were collected on d 5 of wk 4 of each period and the composition of the bacterial community was studied. Rumen fermentation responses were reported in a companion study. Both SARA-inducing challenges resulted in similar digesta pH depressions (as shown by the companion study), and reduced bacterial richness and diversity in rumen fluid, but GBSC had the larger effect. None of the challenges affected these measures in cecal digesta, and only GBSC reduced bacterial richness and diversity in feces. Only GBSC reduced the abundance of Bacteroidetes in rumen fluid. Abundances of limited number of bacterial genera identified by 16S rRNA gene sequencing in the rumen, cecum and feces were affected by the GBSC. The APSC did not affect any of these abundances. Both challenges increased the abundances of several starch, pectin, xylan, dextrin, lactate, succinate, and sugar fermenting bacterial species in the rumen, cecum, and feces as determined by qPCR. Only GBSC increased that of Megasphaera elsdenii in the rumen. Both challenges decreased the abundance of Streptococcus bovis, and increased that of Escherichia coli, in cecal digesta and feces, with GBSC having the larger effect. These results showed that the SARA challenges caused moderate and reversible changes of the composition of the bacteria in the foregut and hindgut, with the greater changes observed during GBSC.

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.

Project description:The objective of the present study was to investigate the effects of N-carbamylglutamate (NCG) supplementation on metabolic profile and microbiota in ruminal content and feces of lactating dairy cows under heat stress (HS). Forty-eight lactating Holstein cows (154 ± 13.6 days in milk) were assigned randomly to four treatments (n = 12), to receive 0, 15, 20, or 25 g/day of commercial NCG (proportion: 97.7%) for the period of 60 days. The recorded ambient temperature-humidity index (THI) suggested that the cows were exposed to HS for almost the entire experimental period (average THI: 80.6). Samples of ruminal content and feces were collected at the end of the trial (day 60) to determine the biological effects of NCG supplementation on metabolome and microbiota using mass spectrometry-based metabolomics and 16S rRNA gene sequencing techniques, respectively. Results showed that NCG supplementation enhanced the levels of ruminal microbial protein, total volatile fatty acids (VFAs), and the molar proportion of propionate in the rumen, but lowered the ruminal pH, ammonia nitrogen (NH3-N), and the ratio of acetate to propionate. NCG at doses of 20 and 25 g/day reduced the community richness and diversity of ruminal microbiota with the decrease of Shannon and Simpson diversity. Compositions of ruminal and fecal microbiotas were altered by NCG, and the PICRUSt results revealed that metabolic pathways of the bacteria, such as amino acid metabolism, energy metabolism, and pyruvate metabolism, were enriched in NCG groups. Distinct changes in the metabolomic profile of ruminal fluid were observed between the control and NCG groups. Changes of 26 metabolites mainly involved in arginine metabolism, glutamate metabolism, and nitrogen metabolism were observed associated with NCG supplementation. These results provided new insights into the effects of NCG on metabolomic profile and microbiota in ruminal content and feces, and the optimal dose of NCG supplemented to dairy cows was 20 g/hd/day, which contributed to understanding the effects of NCG on HS in lactating dairy cows.

Project description:Rumen-protected glucose (RPG) plays an important role in alleviating the negative energy balance of dairy cows. This study used a combination of rumen microbes 16S and metabolomics to elucidate the changes of rumen microbial composition and rumen metabolites of different doses of RPG's rumen degradation part in early-lactation dairy cows. Twenty-four multiparous Holstein cows in early lactation were randomly allocated to control (CON), low-RPG (LRPG), medium-RPG (MRPG), or high-RPG (HRPG) groups in a randomized block design. The cows were fed a basal total mixed ration diet with 0, 200, 350, and 500 g of RPG per cow per day, respectively. Rumen fluid samples were analyzed using Illumina MiSeq sequencing and ultrahigh-performance liquid chromatography coupled to quadrupole time-of-flight mass spectrometry. MRPG supplementation increased bacterial richness and diversity, including increasing the relative abundance of cellulolytic bacteria, such as Ruminococcus, Lachnospiraceae_NK3A20_group, Ruminiclostridium, and Lachnospiraceae_UCG-008 MRPG significantly increased the concentrations of acetate, propionate, butyrate, and total volatile fatty acid in the rumen. Ruminal fluid metabolomics analysis showed that RPG supplementation could significantly regulate the synthesis of amino acids digested by protozoa in the rumen. Correlation analysis of the ruminal microbiome and metabolome revealed some potential relationships between major bacterial abundance and metabolite concentrations. Our analysis found that RPG supplementation of different doses can change the diversity of microorganisms in the rumen and affect the rumen fermentation pattern and microbial metabolism and that a daily supplement of 350 g of RPG might be the ideal dose.IMPORTANCE Dairy cows in early lactation are prone to a negative energy balance because their dry matter intake cannot meet the energy requirements of lactation. Rumen-protected glucose is used as an effective feed additive to alleviate the negative energy balance of dairy cows in early lactation. However, one thing that is overlooked is that people often think that rumen-protected glucose is not degraded in the rumen, thus ignoring its impact on the microorganisms in the rumen environment. Our investigation and previous experiments have found that rumen-protected glucose is partially degraded in the rumen. However, there are few reports on this subject. Therefore, we conducted research on this problem and found that rumen-protected glucose supplementation at 350 g/day can promote the development and metabolism of rumen flora. This provides a theoretical basis for the extensive application of rumen bypass glucose at a later stage.

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.

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Responsive changes of rumen microbiome and metabolome in dairy cows with different susceptibility to subacute ruminal acidosis.

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