Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle
ABSTRACT: The objective of this study was to investigate changes in the composition of mucosa-associated bacterial community, the morphology of the small intestinal epithelia, and the gene expressions of junction proteins and inflammatory cytokines in the small intestines of dairy cattle fed a high-...
| Main Authors: | , , , |
|---|---|
| Format: | Article |
| Language: | English |
| Published: |
Elsevier
2022-08-01
|
| Series: | Journal of Dairy Science |
| Subjects: | |
| Online Access: | http://www.sciencedirect.com/science/article/pii/S0022030222003265 |
| _version_ | 1828451887792259072 |
|---|---|
| author | Z. Lai L. Lin J. Zhang S. Mao |
| author_facet | Z. Lai L. Lin J. Zhang S. Mao |
| author_sort | Z. Lai |
| collection | DOAJ |
| description | ABSTRACT: The objective of this study was to investigate changes in the composition of mucosa-associated bacterial community, the morphology of the small intestinal epithelia, and the gene expressions of junction proteins and inflammatory cytokines in the small intestines of dairy cattle fed a high-grain (HG) diet. A total of 12 ruminally cannulated Holstein cows in mid-lactation were randomly fed either a conventional (CON) diet (40% concentrate, dry matter basis) or an HG diet (60% concentrate, dry matter basis) for 4 wk. At the end of the feeding trial, all the cows were slaughtered and then examined for changes in the small intestinal mucosa-associated bacterial communities using 16S full-length amplicon sequencing. Furthermore, the gene expression of tight junction proteins and inflammatory cytokines in the small intestinal epithelium were studied using real-time quantitative PCR. The results of nonmetric multidimensional scaling plots showed that an HG diet altered the composition of mucosa-associated bacterial communities in the jejunum and ileum. The HG feeding only increased the numbers of operational taxonomic units in the mucosa-associated bacterial community in the jejunum. At the genus level, the HG diet increased the abundance of uncultured Succinivibrionaceae and Lachnospiraceae incertae sedis in the duodenal mucosa, whereas the proportions of Veillonella and Selenomonas increased in the jejunal mucosa. Compared with the CON group, the proportions of Acetitomaculum in both the jejunal and the ileal mucosa were higher in the HG group. Analysis via PICRUSt2 (version 2.2.0-b) suggested that the HG diet increased the abundance of genes related to biodegradation of xenobiotics in the jejunal mucosa and the abundance of genes related to immune disease in the ileal mucosa. Additionally, the group fed an HG diet had higher concentrations of lipopolysaccharides in the jejunal and ileal digesta. The HG feeding caused a downregulation of the mRNA expression of occludin and ZO-1 in the jejunal epithelium, as well as of claudin-1, claudin-4, and ZO-1 in the ileal epithelium. Moreover, the HG diet caused an increase in the mRNA expression of IL-1β, IL-2, and IFN-γ in the jejunal epithelium, but a higher expression of IL-2 and IFN-γ in the ileal epithelium. Correlation analysis revealed that the alteration of lipopolysaccharide levels and mucosa-associated bacterial community might partly contribute to changes in the expression of the epithelial cytokines in the jejunum and ileum during HG feeding. These findings suggest that microbiota residing in the small intestine provide essential health benefits to host dairy cattle. |
| first_indexed | 2024-12-10T23:44:24Z |
| format | Article |
| id | doaj.art-afadf8102741412f928c64b9ce829140 |
| institution | Directory Open Access Journal |
| issn | 0022-0302 |
| language | English |
| last_indexed | 2024-12-10T23:44:24Z |
| publishDate | 2022-08-01 |
| publisher | Elsevier |
| record_format | Article |
| series | Journal of Dairy Science |
| spelling | doaj.art-afadf8102741412f928c64b9ce8291402022-12-22T01:28:58ZengElsevierJournal of Dairy Science0022-03022022-08-01105866016615Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattleZ. Lai0L. Lin1J. Zhang2S. Mao3Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Center for Ruminant Nutrition and Feed Engineering Technology Research, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Center for Ruminant Nutrition and Feed Engineering Technology Research, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaLaboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Center for Ruminant Nutrition and Feed Engineering Technology Research, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaCorresponding author; Laboratory of Gastrointestinal Microbiology, Jiangsu Key Laboratory of Gastrointestinal Nutrition and Animal Health, Center for Ruminant Nutrition and Feed Engineering Technology Research, College of Animal Science and Technology, Nanjing Agricultural University, Nanjing 210095, ChinaABSTRACT: The objective of this study was to investigate changes in the composition of mucosa-associated bacterial community, the morphology of the small intestinal epithelia, and the gene expressions of junction proteins and inflammatory cytokines in the small intestines of dairy cattle fed a high-grain (HG) diet. A total of 12 ruminally cannulated Holstein cows in mid-lactation were randomly fed either a conventional (CON) diet (40% concentrate, dry matter basis) or an HG diet (60% concentrate, dry matter basis) for 4 wk. At the end of the feeding trial, all the cows were slaughtered and then examined for changes in the small intestinal mucosa-associated bacterial communities using 16S full-length amplicon sequencing. Furthermore, the gene expression of tight junction proteins and inflammatory cytokines in the small intestinal epithelium were studied using real-time quantitative PCR. The results of nonmetric multidimensional scaling plots showed that an HG diet altered the composition of mucosa-associated bacterial communities in the jejunum and ileum. The HG feeding only increased the numbers of operational taxonomic units in the mucosa-associated bacterial community in the jejunum. At the genus level, the HG diet increased the abundance of uncultured Succinivibrionaceae and Lachnospiraceae incertae sedis in the duodenal mucosa, whereas the proportions of Veillonella and Selenomonas increased in the jejunal mucosa. Compared with the CON group, the proportions of Acetitomaculum in both the jejunal and the ileal mucosa were higher in the HG group. Analysis via PICRUSt2 (version 2.2.0-b) suggested that the HG diet increased the abundance of genes related to biodegradation of xenobiotics in the jejunal mucosa and the abundance of genes related to immune disease in the ileal mucosa. Additionally, the group fed an HG diet had higher concentrations of lipopolysaccharides in the jejunal and ileal digesta. The HG feeding caused a downregulation of the mRNA expression of occludin and ZO-1 in the jejunal epithelium, as well as of claudin-1, claudin-4, and ZO-1 in the ileal epithelium. Moreover, the HG diet caused an increase in the mRNA expression of IL-1β, IL-2, and IFN-γ in the jejunal epithelium, but a higher expression of IL-2 and IFN-γ in the ileal epithelium. Correlation analysis revealed that the alteration of lipopolysaccharide levels and mucosa-associated bacterial community might partly contribute to changes in the expression of the epithelial cytokines in the jejunum and ileum during HG feeding. These findings suggest that microbiota residing in the small intestine provide essential health benefits to host dairy cattle.http://www.sciencedirect.com/science/article/pii/S0022030222003265high-grain feedingsmall intestinemucosa-associated bacterial communitydairy cattle |
| spellingShingle | Z. Lai L. Lin J. Zhang S. Mao Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle Journal of Dairy Science high-grain feeding small intestine mucosa-associated bacterial community dairy cattle |
| title | Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle |
| title_full | Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle |
| title_fullStr | Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle |
| title_full_unstemmed | Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle |
| title_short | Effects of high-grain diet feeding on mucosa-associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle |
| title_sort | effects of high grain diet feeding on mucosa associated bacterial community and gene expression of tight junction proteins and inflammatory cytokines in the small intestine of dairy cattle |
| topic | high-grain feeding small intestine mucosa-associated bacterial community dairy cattle |
| url | http://www.sciencedirect.com/science/article/pii/S0022030222003265 |
| work_keys_str_mv | AT zlai effectsofhighgraindietfeedingonmucosaassociatedbacterialcommunityandgeneexpressionoftightjunctionproteinsandinflammatorycytokinesinthesmallintestineofdairycattle AT llin effectsofhighgraindietfeedingonmucosaassociatedbacterialcommunityandgeneexpressionoftightjunctionproteinsandinflammatorycytokinesinthesmallintestineofdairycattle AT jzhang effectsofhighgraindietfeedingonmucosaassociatedbacterialcommunityandgeneexpressionoftightjunctionproteinsandinflammatorycytokinesinthesmallintestineofdairycattle AT smao effectsofhighgraindietfeedingonmucosaassociatedbacterialcommunityandgeneexpressionoftightjunctionproteinsandinflammatorycytokinesinthesmallintestineofdairycattle |