Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens

The intestinal microbiome is responsible for the fermentation of complex carbohydrates and orchestrates the immune system through gut microbiota-derived metabolites. In our previous study, we reported that supplementation of Enteromorpha polysaccharide (EP) and yeast glycoprotein (YG) in combination...

Full description

Bibliographic Details
Main Authors: Teketay Wassie, Bei Cheng, Tiantian Zhou, Lumin Gao, Zhuang Lu, Chunyan Xie, Xin Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2022-10-01
Series:Frontiers in Immunology
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fimmu.2022.996897/full
_version_ 1828103909028134912
author Teketay Wassie
Bei Cheng
Tiantian Zhou
Lumin Gao
Zhuang Lu
Chunyan Xie
Xin Wu
Xin Wu
author_facet Teketay Wassie
Bei Cheng
Tiantian Zhou
Lumin Gao
Zhuang Lu
Chunyan Xie
Xin Wu
Xin Wu
author_sort Teketay Wassie
collection DOAJ
description The intestinal microbiome is responsible for the fermentation of complex carbohydrates and orchestrates the immune system through gut microbiota-derived metabolites. In our previous study, we reported that supplementation of Enteromorpha polysaccharide (EP) and yeast glycoprotein (YG) in combination synergistically improved antioxidant activities, serum lipid profile, and fatty acid metabolism in chicken. However, the mechanism of action of these polysaccharides remains elusive. The present study used an integrated 16S-rRNA sequencing technology and untargeted metabolomics technique to reveal the mechanism of action of EP+YG supplementation in broiler chickens fed basal diet or diets supplemented with EP+YG (200mg/kg EP + 200mg/kg YG). The results showed that EP+YG supplementation altered the overall structure of caecal microbiota as evidenced by β diversities analysis. Besides, EP+YG supplementation changed the microbiota composition by altering the community profile at the phylum and genus levels. Furthermore, Spearman correlation analysis indicated a significant correlation between altered microbiota genera vs serum cytokine levels and microbiota genera vs volatile fatty acids production. Predicted functional analysis showed that EP+YG supplementation significantly enriched amino acid metabolism, nucleotide metabolism, glycan biosynthesis and metabolism, energy metabolism, and carbohydrate metabolism. Metabolomics analysis confirmed that EP+YG supplementation modulates a myriad of caecal metabolites by increasing some metabolites, including pyruvic acid, pyridoxine, spermidine, spermine, and dopamine, and decreasing metabolites related to lipid metabolisms such as malonic acid, oleic acid, and docosahexaenoic acid. The quantitative enrichment analysis results further showed that glycolysis/gluconeogenesis, citric acid cycle, tyrosine metabolism, glycine, serine, and threonine metabolism, and cysteine and methionine metabolism were the most important enriched pathways identified with enrichment ratio >11, whereas, fatty acid biosynthesis and biosynthesis of unsaturated fatty acids pathways were suppressed. Together, the 16S-rRNA and untargeted metabolomics results uncovered that EP+YG supplementation modulates intestinal microbiota and their metabolites, thereby influencing the important metabolism pathways, suggesting a potential feed additive.
first_indexed 2024-04-11T09:33:56Z
format Article
id doaj.art-f5ef512aa6ff4d2a97b64c8a59b7f0e7
institution Directory Open Access Journal
issn 1664-3224
language English
last_indexed 2024-04-11T09:33:56Z
publishDate 2022-10-01
publisher Frontiers Media S.A.
record_format Article
series Frontiers in Immunology
spelling doaj.art-f5ef512aa6ff4d2a97b64c8a59b7f0e72022-12-22T04:31:47ZengFrontiers Media S.A.Frontiers in Immunology1664-32242022-10-011310.3389/fimmu.2022.996897996897Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickensTeketay Wassie0Bei Cheng1Tiantian Zhou2Lumin Gao3Zhuang Lu4Chunyan Xie5Xin Wu6Xin Wu7Key Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences; National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Changsha, ChinaKey Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences; National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Changsha, ChinaKey Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences; National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Changsha, ChinaKey Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences; National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Changsha, ChinaKey Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences; National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Changsha, ChinaCollege of Bioscience and Biotechnology, Hunan Agricultural University, Changsha, ChinaKey Laboratory of Agro-ecological Processes in Subtropical Region, Institute of Subtropical Agriculture, Chinese Academy of Sciences; National Engineering Laboratory for Pollution Control and Waste Utilization in Livestock and Poultry Production, Hunan Provincial Engineering Research Center for Healthy Livestock and Poultry Production, Changsha, ChinaTianjin Institute of Industrial Biotechnology, Chinese Academy of Sciences, Tianjin, ChinaThe intestinal microbiome is responsible for the fermentation of complex carbohydrates and orchestrates the immune system through gut microbiota-derived metabolites. In our previous study, we reported that supplementation of Enteromorpha polysaccharide (EP) and yeast glycoprotein (YG) in combination synergistically improved antioxidant activities, serum lipid profile, and fatty acid metabolism in chicken. However, the mechanism of action of these polysaccharides remains elusive. The present study used an integrated 16S-rRNA sequencing technology and untargeted metabolomics technique to reveal the mechanism of action of EP+YG supplementation in broiler chickens fed basal diet or diets supplemented with EP+YG (200mg/kg EP + 200mg/kg YG). The results showed that EP+YG supplementation altered the overall structure of caecal microbiota as evidenced by β diversities analysis. Besides, EP+YG supplementation changed the microbiota composition by altering the community profile at the phylum and genus levels. Furthermore, Spearman correlation analysis indicated a significant correlation between altered microbiota genera vs serum cytokine levels and microbiota genera vs volatile fatty acids production. Predicted functional analysis showed that EP+YG supplementation significantly enriched amino acid metabolism, nucleotide metabolism, glycan biosynthesis and metabolism, energy metabolism, and carbohydrate metabolism. Metabolomics analysis confirmed that EP+YG supplementation modulates a myriad of caecal metabolites by increasing some metabolites, including pyruvic acid, pyridoxine, spermidine, spermine, and dopamine, and decreasing metabolites related to lipid metabolisms such as malonic acid, oleic acid, and docosahexaenoic acid. The quantitative enrichment analysis results further showed that glycolysis/gluconeogenesis, citric acid cycle, tyrosine metabolism, glycine, serine, and threonine metabolism, and cysteine and methionine metabolism were the most important enriched pathways identified with enrichment ratio >11, whereas, fatty acid biosynthesis and biosynthesis of unsaturated fatty acids pathways were suppressed. Together, the 16S-rRNA and untargeted metabolomics results uncovered that EP+YG supplementation modulates intestinal microbiota and their metabolites, thereby influencing the important metabolism pathways, suggesting a potential feed additive.https://www.frontiersin.org/articles/10.3389/fimmu.2022.996897/fullmicrobiotametaboliteentromorpha polysaccharideyeast glycoproteinimmunity
spellingShingle Teketay Wassie
Bei Cheng
Tiantian Zhou
Lumin Gao
Zhuang Lu
Chunyan Xie
Xin Wu
Xin Wu
Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens
Frontiers in Immunology
microbiota
metabolite
entromorpha polysaccharide
yeast glycoprotein
immunity
title Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens
title_full Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens
title_fullStr Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens
title_full_unstemmed Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens
title_short Microbiome-metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary Enteromorpha polysaccharide and Yeast glycoprotein in chickens
title_sort microbiome metabolome analysis reveals alterations in the composition and metabolism of caecal microbiota and metabolites with dietary enteromorpha polysaccharide and yeast glycoprotein in chickens
topic microbiota
metabolite
entromorpha polysaccharide
yeast glycoprotein
immunity
url https://www.frontiersin.org/articles/10.3389/fimmu.2022.996897/full
work_keys_str_mv AT teketaywassie microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT beicheng microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT tiantianzhou microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT lumingao microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT zhuanglu microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT chunyanxie microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT xinwu microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens
AT xinwu microbiomemetabolomeanalysisrevealsalterationsinthecompositionandmetabolismofcaecalmicrobiotaandmetaboliteswithdietaryenteromorphapolysaccharideandyeastglycoproteininchickens