Disruption of ruminal homeostasis by malnutrition involved in systemic ruminal microbiota-host interactions in a pregnan
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RESEARCH
Open Access
Disruption of ruminal homeostasis by malnutrition involved in systemic ruminal microbiota-host interactions in a pregnant sheep model Yanfeng Xue1,2†, Limei Lin1,2†, Fan Hu1,2†, Weiyun Zhu1,2 and Shengyong Mao1,2*
Abstract Background: Undernutrition 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. Results: Sixteen 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 matrixreceptor interaction, inactivated JAK3-STAT2 signaling pathway, and inhibited DNA replication and cell cycle. (Continued on next page)
* Correspondence: [email protected] † Yanfeng Xue, Limei Lin and Fan Hu contributed equally to this work. 1 Centre for Ruminant Nutrition and Feed Technology Research, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, China 2 National Center for International Research on Animal Gut Nutrition, National Experimental Teaching Demonstration Center of Animal Science, Nanjing Agricultural University, Nanjing 210095, China © The Author(s). 2020 Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons licenc
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