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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:Ruminal microflora is closely correlated with the ruminant's diet. However, information regarding the effect of high concentrate diets on rumen microflora in yaks is lacking. In the current study, 24 healthy male yaks were randomly assigned to two groups, each fed with different diets: less concentrate (LC; concentrate: coarse = 40: 60) and high concentrate (HC; concentrate: coarse = 80: 20) diets. Subsequently, a 21-day feeding trial was performed with the yaks, and rumen fluid samples were collected and compared using 16 s rRNA sequencing. The results showed that NH3-N, total VFA, acetate, butyrate, isobutyrate, and isovalerate were significantly higher in the HC group than that in the LC group (p < 0.05), while microbial diversity and richness were significantly lower in the HC group (p < 0.05). Principal coordinate analysis indicated that rumen microflora was significantly different in LC and HC groups (p < 0.05). In the rumen, phyla Firmicutes and Bacteroidota were the most abundant bacteria, with Firmicutes being more abundant, and Bacteroidota being less abundant in the HC group than those found in the LC group. Christensenellaceae_R-7_group and Prevotella are the highest abundant ones at the genus level. The relative abundance of Acetitomaculum, Ruminococcus, and Candidatus_Saccharimonas were significantly higher in the HC group than that in the LC group (p < 0.05), while the relative abundance of Olsenella was significantly lower in the HC group than in the LC group (p < 0.05). Compared to the LC group, the relative abundance of Prevotella, Ruminococcus, and Candidatus_Saccharimonas was significantly higher in the HC group. The relative abundances of Prevotella, Prevotellaceae_UCG-003, Olsenella, Ruminococcus, Acetitomaculum, Candidatus_Saccharimonas, and NK4A214_group were correlated with ruminal fermentation parameters (p < 0.05). Furthermore, PICRUSt 2 estimation indicated that microbial genes associated with valine, leucine, and isoleucine biosynthesis were overexpressed in the rumen microflora of yaks in the HC group (p < 0.05). Conclusively, our results suggest that high concentrate diets affect the microflora composition and fermentation function in yak rumen. The present findings would provide new insights into the health of yaks under high concentrate feeding conditions and serve as a potent reference for the short-term fattening processes of yaks.

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.

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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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