Gastrointestinal function in cattle: Mechanisms and the role of nutrition

Jiang, Qianming

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https://hdl.handle.net/2142/122106 Copy

Description

Title

Gastrointestinal function in cattle: Mechanisms and the role of nutrition

Author(s)

Jiang, Qianming

Issue Date

2023-11-15

Director of Research (if dissertation) or Advisor (if thesis)

Loor, Juan J

Doctoral Committee Chair(s)

Loor, Juan J

Committee Member(s)

• Cardoso, Phil
• Pan, Yuan-Xiang
• Elolimy, Ahmed

Department of Study

Animal Sciences

Discipline

Animal Sciences

Degree Granting Institution

University of Illinois at Urbana-Champaign

Degree Name

Ph.D.

Degree Level

Dissertation

Keyword(s)

rumen, intestine, amino acid, one-carbon metabolism, inflammation, RNA-sequencing, microbiome

Abstract

Transport and metabolism of amino acids (AAs) within the gastrointestinal tract (GIT) contribute to adaptations in response to physiological and environmental stressors. One-carbon metabolism (OCM) is intricately connected to AA metabolism and plays a pivotal role in enhancing antioxidant capacity. Similarly, gene and microbiome profiles in the intestinal tract of dairy cows are essential for a greater understanding of gut function. In the first study, ruminal papillae (Rum) and scrapings from the duodenum (Duo), jejunum (Jej), and ileum (Ile) were collected from 8 multiparous Holstein cows averaging 128 ± 12 d in milk and producing 39 ± 5 kg·d-1 after slaughter for profiling. Methionine adenosyl transferase 1 (MAT) activity was ~10-fold greater (P < 0.01), and cystathionine β-synthase (CBS) activity doubled in Rum vs. small intestine. Activity and mRNA abundance of betaine-homocysteine S-methyltransferase were undetectable. The mRNA abundance of serine hydroxymethyltransferase 1, 5-methyltetrahydrofolate-homocysteine methyltransferase, and MAT differed across each section (P < 0.05), and the mRNA abundance of S-adenosylhomocysteine hydrolase, betaine aldehyde dehydrogenase, and glutathione synthase was greater in Rum than small intestine (P < 0.01). In contrast, there was greater mRNA abundance of guanidinoacetate N-methyltransferase and cystathionine γ-lyase in the small intestine vs. Rum (P < 0.01). The mRNA abundance of AA transporters SLC1A5, SLC3A2, and SLC7A5 in Rum was greater than small intestine (P < 0.05). However, the mRNA abundance of AA transporters SLC1A1, SLC6A6, SLC7A8, SLC38A1, SLC38A7, and SLC43A2 in Rum was lower than small intestine (P < 0.05). Most AA concentrations were greater in the small intestine than in Rum, including Alanine, Arginine, Aspartate, Glutamine, and Methionine. Asparagine and Cysteine concentrations were greater in Rum than small intestine (P < 0.01). In the second study, we used a feed restriction (FR) challenge to address alterations in ruminal tissue OCM and anti-oxidant capacity in 7 ruminally-cannulated Angus steers (663 ± 73 kg body weight). In the first 15 days of a pre-feed restriction phase (PRE), steers had unrestricted access to feed. Subsequently, for the next 3 days (Feed Restriction Phase, FRP), steers were given only 25% of the feed they had consumed during the PRE phase. This was followed by a 15-day recovery phase (POST) during which the steers once again had unrestricted access to feed. The mRNA abundance of CBS and GCLC (P < 0.05) in OCM was downregulated by FR, and plasma IL1-β concentrations were higher (P ≤ 0.03) in FRP than PRE or POST. The mRNA abundance of the proinflammatory genes TNF, TLR2, and TLR4 in ruminal epithelium peaked (P < 0.05) at FRP and remained higher at POST. In a third study, we employed RNAseq and 16S rRNAseq techniques to investigate whether feeding a Saccharomyces cerevisiae fermentation product (SCFP) influenced the metabolism of ileum and rumen during a challenge induced by dietary FR. Multiparous cows (97.1 ± 7.6 DIM) were initially fed a control diet (CON) or CON supplemented with 19 g/d of SCFP for 9 weeks. Subsequently, they were given only 40% of their ad libitum intake, as determined from their intake 7 days before the onset of the FR challenge for 5 days. In response to SCFP, 1,696 differentially expressed genes (DEG) were identified (451 upregulated, 1,245 downregulated) in ileal tissue collected at slaughter after FR. The top DEG categories include 'cellular components': extracellular exosome, extracellular space, focal adhesion, and cell surface. 'Mucin type O-glycan biosynthesis' was the top downregulated pathway due to the downregulation of GCNT3, GALNT5, B3GNT3, GALNT18, and GALNT14. The downregulation of cell- and tissue-structure genes associated with collagen (COL6A1, COL1A1, COL4A1, COL1A2, COL6A2), laminin (LAMB2), and integrins (ITGA8, ITGA2, ITGA5). The mRNA abundance of chemokines such as CCL16, CCL21, CCL14, CXCL12, CXCL14, and cytokines such as IL33 and IL27 were downregulated by SCFP during FR. The investigation of ileal digesta revealed that SCFP supplementation tended (P = 0.07) to increase the relative abundance of Bifidobacterium animalis (P = 0.07) and Lactobacillales (P = 0.03). Certain subsets of the Firmicutes genus, members of the Bacteroidota phylum, and the Treponema genus exhibited correlations with the mRNA abundance of genes related to both ileal integrity (GCNT3, GALNT5, B3GNT3, FN1, ITGA2, LAMB2) and inflammation (AOX1, GPX8, CXCL12, CXCL14, CCL4, SAA3). In the ruminal microbiome analyses, the alpha diversity Chao 1 (P = 0.03) and Shannon indices (P = 0.05) were greater in the SCFP treatment. SCFP also increased the ruminal relative abundance of CPla_4_termite_group, Candidatus_Saccharimonas, Oribacterium, and Pirellula genus (P ≤ 0.03). Metabolomics and bacterial profiles revealed that SCFP altered microbiome metabolism in rumen. Overall, the research highlighted distinct differences in AA transport and the activity of OCM along with related pathways. The FR challenge changed OCM and antioxidant-related pathways and induced an inflammatory response in cattle. Furthermore, supplementing with SCFP reduced the inflammatory response in the ileal tissue induced by FR and exerted a regulatory influence on microbiome profiles and metabolism in both the rumen and ileum, which may potentially interact with the host (cattle). Collectively, these findings emphasize that the metabolism of the GIT varies across different sections and is modulated by nutritional factors.

Graduation Semester

2023-12

Type of Resource

Thesis

Copyright and License Information

Copyright 2023 Qianming Jiang

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