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The response of ruminal fermentation, epithelium-associated microbiota, and epithelial barrier function to severe feed restriction in pregnant ewes.

ABSTRACT: The objective of this study was to evaluate the changes in the ruminal fermentation, epithelium-associated microbiota, and ruminal epithelial barrier function in response to severe feed restriction (SFR) in pregnant ewes. Sixteen pregnant ewes (108 d of gestation) were randomly blocked and assigned to 1 of 2 treatments: control (CON, n = 8) and SFR (n = 8). Ewes were fed a common diet with a 60:40 forage to concentrate ratio for 7-d baseline period followed by a SFR challenge period. Ewes on the SFR treatment were restricted to 30% of the base for 15 d. At the end of the experimental period, all animals were slaughtered and then ruminal contents and ruminal epithelial tissue were collected. Results showed that ruminal pH was greater in SFR group (P = 0.040) compared with CON group, while SFR decreased (P < 0.05) the concentrations of ruminal acetate, propionate, butyrate, and total volatile fatty acid. A plot of principal coordinate analysis and analysis of molecular variance revealed that the composition of ruminal epithelial bacterial communities in the CON group was distinct from that of the ruminal epithelial microbiome in the SFR animals. At the genus level, SFR increased the abundance of unclassified Neisseriaceae, Comamonas, and Papillibacter, and decreased the proportion of Howardella, Desulfobulbus, and Suttonella (P < 0.05) compared with CON group. The metagenome of ruminal epithelium-associated microbiota predicted by PICRUSt revealed that the SFR significantly affected 14 metabolic pathways, and 9 were significantly enriched in the SFR group. In particular, SFR markedly increased relative abundances of dominant gene families involved in amino acid metabolism (P = 0.003), cellular processes and signaling (P = 0.021), and lipid metabolism (P = 0.001). The real-time PCR results showed SFR decreased the mRNA expression of IL-10 (P = 0.003) and upregulated the mRNA expression of IL-6 (P = 0.003) and TLR4 (P = 0.021). The mRNA expression of Claudin-1 (P = 0.001) and ZO-1 (P = 0.009) were lower in the SFR group compared with the CON group. Generally, our data suggest that SFR decreased most ruminal fermentation parameters, altered the composition of rumen epithelium-associated microbiota, and compromised the barrier function of rumen epithelium. These findings are of great importance for understanding the alteration in the rumen function following SFR in pregnant ewes.

SUBMITTER: Hu F

PROVIDER: S-EPMC6162573 | biostudies-literature | 2018 Sep

REPOSITORIES: biostudies-literature

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The response of ruminal fermentation, epithelium-associated microbiota, and epithelial barrier function to severe feed restriction in pregnant ewes.

Hu Fan F Xue Yanfeng Y Guo Changzheng C Liu Junhua J Mao Shengyong S

Journal of animal science 20180901 10

The objective of this study was to evaluate the changes in the ruminal fermentation, epithelium-associated microbiota, and ruminal epithelial barrier function in response to severe feed restriction (SFR) in pregnant ewes. Sixteen pregnant ewes (108 d of gestation) were randomly blocked and assigned to 1 of 2 treatments: control (CON, n = 8) and SFR (n = 8). Ewes were fed a common diet with a 60:40 forage to concentrate ratio for 7-d baseline period followed by a SFR challenge period. Ewes on the ...[more]

PMID: 30272228

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Project description:BackgroundUndernutrition is a prevalent and spontaneous condition in animal production which always affects microbiota-host interaction in gastrointestinal tract. However, how undernutrition affects crosstalk homeostasis is largely unknown. Here, we discover how undernutrition affects microbial profiles and subsequently how microbial metabolism affects the signal transduction and tissue renewal in ruminal epithelium, clarifying the detrimental effect of undernutrition on ruminal homeostasis in a pregnant sheep model.ResultsSixteen pregnant ewes (115 days of gestation) were randomly and equally assigned to the control (CON) and severe feed restriction (SFR) groups. Ewes on SFR treatment were restricted to a 30% level of ad libitum feed intake while the controls were fed normally. After 15 days, all ewes were slaughtered to collect ruminal digesta for 16S rRNA gene and metagenomic sequencing and ruminal epithelium for transcriptome sequencing. Results showed that SFR diminished the levels of ruminal volatile fatty acids and microbial proteins and repressed the length, width, and surface area of ruminal papillae. The 16S rRNA gene analysis indicated that SFR altered the relative abundance of ruminal bacterial community, showing decreased bacteria about saccharide degradation (Saccharofermentans and Ruminococcus) and propionate genesis (Succiniclasticum) but increased butyrate producers (Pseudobutyrivibrio and Papillibacter). Metagenome analysis displayed that genes related to amino acid metabolism, acetate genesis, and succinate-pathway propionate production were downregulated upon SFR, while genes involved in butyrate and methane genesis and acrylate-pathway propionate production were upregulated. Transcriptome and real-time PCR analysis of ruminal epithelium showed that downregulated collagen synthesis upon SFR lowered extracellular matrix-receptor interaction, inactivated JAK3-STAT2 signaling pathway, and inhibited DNA replication and cell cycle.ConclusionsGenerally, undernutrition altered rumen bacterial community and function profile to decrease ruminal energy retention, promoted epithelial glucose and fatty acid catabolism to elevate energy supply, and inhibited the proliferation of ruminal epithelial cells. These findings provide the first insight into the systemic microbiota-host interactions that are involved in disrupting the ruminal homeostasis under a malnutrition pattern. Video Abstract.

Project description:This study investigated whether dietary metabolizable energy (ME) could generate dynamical effects on rumen fermentation, gastrointestinal tract (GIT) morphology, and microbial composition of growing ewes. A total of twenty-eight female Hu lambs were randomly allotted to two treatments with different dietary ME levels: 9.17 (FEA) and 10.41 MJ/kg (FEB). These lambs were further made ready for a 67-day feeding trial. Results showed that the molar proportions of butyrate (p = .020), iso-valerate (p = .028), and valerate (p = .005) were significantly higher in the FEB group than those in the FEA group. The results of the GIT morphologic properties showed that the villus height (VH) (p = .005) was significantly higher and crypt depth was significantly deeper (CD) (p = .005) in the duodenum and that the rumen papillary height (PH) was significantly higher (p = .020) in FEB group compared with the FEA group. High-throughput sequencing results showed that 1826 operational taxonomic units (OTUs) were obtained and that the OTU number (p = .039), the ACE (p = .035), and Chao1 indices (p = .005) were lower in the FEB group. Moreover, 76 genera belonging to 21 phyla were detected in all samples; the relative abundance of Papillibacter (p = .036) and Flexilinea (p = .046) was significantly lower in the high energy group, whereas the relative abundance of unidentified Lachnospiraceae (p = .019), Acetitomaculum (p = .029), unidentified Veillonellaceae (p = .017), Anaerovibrio (p = .005), and Succinivibrio (p = .035) was significantly higher in the FEB group at the genus level. Furthermore, the relative abundance of genes and metabolic pathways were predicted by PICRUSt. The relative abundance of gene families related to carbohydrate metabolism was particularly higher (p = .027) in the FEB group. In summary, these results reveal that the dietary energy levels altered the composition and function of rumen microbiota and GIT morphology in growing female Hu sheep and provide a reference for optimizing diet formula and 10.41MJ/kg of ME level has been recommended in the growing period.

Project description:Differences in chickens' feed intake may be the underlying factor influencing feed-efficiency (FE)-associated variation in intestinal microbiota and physiology. In chickens eating the same amount of feed, quantitative feed restriction may create similar intestinal conditions and help clarify this cause-and-effect relationship. This study investigated the effect of ad libitum versus restrictive feeding (85% of ad libitum) on ileal and cecal microbiota, concentrations of short-chain fatty acids, visceral organ size, intestinal morphology, permeability, and expression of genes related to nutrient uptake, barrier function, and innate immune response in broiler chickens with divergent residual feed intake (RFI; metric for FE). On day 30 posthatch, 28 low-RFI (good FE) and 29 high-RFI (poor FE) chickens across both feeding-level groups (n?=?112) were selected. Supervised multigroup data integration and relevance network analyses showed that especially Lactobacillus (negative) in ileal digesta, Turicibacter (positive) in cecal digesta, and Enterobacteriaceae (positive) in both intestinal segments depended on chicken's feed intake, whereas the level of Anaerotruncus in cecal digesta was most discriminative for high RFI. Moreover, shallower crypts and fewer goblet cells in ceca indicated host-related energy-saving mechanisms with low RFI, whereas greater tissue resistance suggested a stronger jejunal barrier function in low-RFI chickens. Values corresponding to feed intake level × RFI interactions indicated larger pancreas and lower levels of ileal and cecal short-chain fatty acids in restrictively fed high-RFI chickens than in the other 3 groups, suggesting host physiological adaptations to support greater energy and nutrient needs of high-RFI chickens compensating for the restricted feeding. IMPORTANCE The impact of the FE-associated differences in feed intake on intestinal bacterial and host physiological parameters has so far not been clarified. Understanding the underlying principles is essential for the development of cost-effective strategies to improve FE in chicken production. Under conditions of quantitative feed restriction, low- and high-RFI chickens ate the same amount of feed. Therefore, this research helps in distinguishing intestinal bacterial taxa and functions that were highly reliant on feed intake from those that were associated with physiological adaptations to RFI-associated differences in host nutritional needs and intestinal nutrient availability. This work provides a background for further research to assess manipulation of the intestinal microbiota, host physiology, and FE in chickens by dietary intervention.

Project description:There is a great interest to understand the impact of the gut microbiota on host's nutrient use and FE in chicken production. Both chicken's feed intake and gut bacterial microbiota differ between high and low-feed efficient chickens. To evaluate the impact of the feed intake level on the feed efficiency (FE)-associated variation in the chicken intestinal microbiota, differently feed efficient chickens need to eat the same amount of feed, which can be achieved by feeding chickens restrictively. Therefore, we investigated the effect of restrictive vs. ad libitum feeding on the fecal microbiome at 16 and 29 days posthatch (dph), FE and nutrient retention in chickens of low and high residual feed intake (RFI; metric for FE). Restrictively fed chickens were provided the same amount of feed which corresponded to 85% of the ad libitum fed group from 9 dph. FE was determined for the period between 9 and 30 dph and feces for nutrient retention were collected on 31 to 32 dph. From the 112 chickens (n = 56 fed ad libitum, and n = 56 fed restrictively), 14 low RFI and 15 high RFI ad libitum fed chickens, and 14 low RFI (n = 7 per sex) and 14 high RFI restrictively fed chickens were selected as the extremes in RFI and were retrospectively chosen for data analysis. Bray-Curtis dissimilarity matrices showed significant separation between time points, and feeding level groups at 29 dph for the fecal bacterial communities. Relevance networking indicated positive associations between Acinetobacter and feed intake at 16 dph, whereas at 29 dph Escherichia/Shigella and Turicibacter positively and Lactobacillus negatively correlated to chicken's feed intake. Enterobacteriaceae was indicative for low RFI at 16 dph, whereas Acinetobacter was linked to high RFI across time points. However, restrictive feeding-associated changes in the fecal microbiota were not similar in low and high RFI chickens, which may have been related to the higher nutrient retention and thus lower fecal nutrient availability in restrictively fed high RFI chickens. This may also explain the decreased RFI value in restrictively fed high RFI chickens indicating improved FE, with a stronger effect in females.

Project description:Much research on animal feed has focused on finding alternative feed ingredients that can replace conventional ones (e.g., grains and beans) to reduce feed costs. The objective of this study was to evaluate the economic, as well as nutritional value of spent coffee grounds (SCG) and Japanese mugwort (Artemisia princeps) residues (APR) as alternative feed ingredients for ruminants. We also investigated whether pre-fermentation using Lactobacillus spp. was a feasible way to increase the feed value of these by-products. Chemical analyses and an in vitro study were conducted for SCG, APR, and their pre-fermented forms. All the experimental diets for in vitro ruminal fermentation were formulated to contain a similar composition of crude protein, neutral detergent fiber and total digestible nutrients at 1x maintenance feed intake based on the dairy National Research Council (NRC). The control diet was composed of ryegrass, corn, soybean meal, whereas the treatments consisted of SCG, SCG fermented with Lactobacillus spp. (FSCG), APR, and its fermented form (FAPR). The treatment diets replaced 100 g/kg dry matter (DM) of the feed ingredients in the control. Costs were lower for the all treatments, except FAPR, than that of the control. After 24-h incubation, the NDF digestibility of the diets containing SCG and its fermented form were significantly lower than those of the other diets (P < 0.01); pre-fermentation tended to increase NDF digestibility (P = 0.07), especially for APR. Supplementation of SCG significantly decreased total gas production (ml/g DM) after 24-h fermentation in comparison with the control (P < 0.05); however, there were no significant differences between the control and the SCG or the APR diets in total gas production, as expressed per Korean Won (KRW). Diets supplemented with SCG or FSCG tended to have a higher total volatile fatty acid (VFA) concentration, expressed as per KRW, compared with the control (P = 0.06). Conversely, the fermentation process of SCG and APR significantly decreased total gas production and VFA production as expressed per KRW (P < 0.05). Because of their nutrient composition and relatively lower cost, we concluded that SCG and APR could be used as alternative feed sources, replacing conventional feed ingredients. However, pre-fermentation of agricultural by-products, such as SCG and APR, may be inappropriate for improving their nutritive considering the increase in production costs.

Project description:The rumen microbiota is vital for the health and growth performance of the host animal, mainly due to its role in the fermentation of ingested feed within the rumen. Attaining a better understanding of the development of the bacterial community and fermentation in the rumen can provide the theoretical basis for regulating feed utilization. This study analyzed the development of rumen bacteria in lambs from birth to 4 months of age using 16S-rRNA amplicon sequencing data and studied its relationship with ruminal fermentation. Serum levels of metabolites were monitored at 30, 60, 90, and 120 days of age, and the RandomForest approach was used to determine age-related changes in rumen bacteria. Levels of blood metabolites, ruminal fermentation, the rumen bacterial community and its functions were all affected by the age of the lambs (P < 0.05). Based on the Bray-Curtis distance within the age groups of the rumen microbiota, the similarity increased sharply after the lambs were weaned at 60 days of age (P < 0.05). The similarity between the samples collected from birth to 90 days of age and those collected at 120 days of age, increased after 20 days of age, reaching a maximum at 90 days vs. 120 days (P < 0.05). Some age-associated changes in the microbial genera were correlated with changes in the concentrations of volatile fatty acids and the levels of microbial crude protein in the rumen, including positive correlations between main volatile fatty acids and the genera of Prevotella 1, Lachnospiraceae NK3A20 group, Ruminococcus gauvreauii group, Ruminococcaceae UCG-014, and Ruminococcus 2 (P < 0.05). These results indicated that the microbial community and the function of rumen was not well-established before 20 days of age, so there is a degree of plasticity in the rumen bacterial community during the first 20 days of post-natal development in lambs, and this might provide an opportunity for interventions to improve rumen fermentation and, thus, increase their growth performance.

Dataset Information

The response of ruminal fermentation, epithelium-associated microbiota, and epithelial barrier function to severe feed restriction in pregnant ewes.

Publications

The response of ruminal fermentation, epithelium-associated microbiota, and epithelial barrier function to severe feed restriction in pregnant ewes.

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