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The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs

SIMPLE SUMMARY: Archaea is identified as the key link in the interaction between gut microbiota and host metabo-lism. Studies on human and mice have reported archaea, especially methanogenic archaea, makes an important impact on the energy harvesting capacity of the host by improving fermentation. B...

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Autores principales: Deng, Feilong, Li, Yushan, Peng, Yunjuan, Wei, Xiaoyuan, Wang, Xiaofan, Howe, Samantha, Yang, Hua, Xiao, Yingping, Li, Hua, Zhao, Jiangchao, Li, Ying
Formato: Online Artículo Texto
Lenguaje:English
Publicado: MDPI 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8300674/
https://www.ncbi.nlm.nih.gov/pubmed/34359268
http://dx.doi.org/10.3390/ani11072139
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author Deng, Feilong
Li, Yushan
Peng, Yunjuan
Wei, Xiaoyuan
Wang, Xiaofan
Howe, Samantha
Yang, Hua
Xiao, Yingping
Li, Hua
Zhao, Jiangchao
Li, Ying
author_facet Deng, Feilong
Li, Yushan
Peng, Yunjuan
Wei, Xiaoyuan
Wang, Xiaofan
Howe, Samantha
Yang, Hua
Xiao, Yingping
Li, Hua
Zhao, Jiangchao
Li, Ying
author_sort Deng, Feilong
collection PubMed
description SIMPLE SUMMARY: Archaea is identified as the key link in the interaction between gut microbiota and host metabo-lism. Studies on human and mice have reported archaea, especially methanogenic archaea, makes an important impact on the energy harvesting capacity of the host by improving fermentation. But, in pigs, the metabolic potential of archaea at different production stages are still largely unknown. Herein, we re-analyzed 276 metagenomic samples to explore the diversity, composi-tion, and potential functions of archaea in pigs. The results showed significant regional variations in archaeal composition. Furthermore, the Metacyc pathway related to hydrogen consumption (METHANOGENESIS-PWY) was only observed in archaeal reads, and archaea may be involved in carbohydrate metabolism and de novo synthesis of some kinds of essential amino acid. Overall, metagenomic re-analysis revealed that the composition and functional potential of archaea in the swine gut and suggested that archaea may make an important function in pigs. ABSTRACT: Archaea are an essential class of gut microorganisms in humans and animals. Despite the substantial progress in gut microbiome research in the last decade, most studies have focused on bacteria, and little is known about archaea in mammals. In this study, we investigated the composition, diversity, and functional potential of gut archaeal communities in pigs by re-analyzing a published metagenomic dataset including a total of 276 fecal samples from three countries: China (n = 76), Denmark (n = 100), and France (n = 100). For alpha diversity (Shannon Index) of the archaeal communities, Chinese pigs were less diverse than Danish and French pigs (p < 0.001). Consistently, Chinese pigs also possessed different archaeal community structures from the other two groups based on the Bray–Curtis distance matrix. Methanobrevibacter was the most dominant archaeal genus in Chinese pigs (44.94%) and French pigs (15.41%), while Candidatus methanomethylophilus was the most predominant in Danish pigs (15.71%). At the species level, the relative abundance of Candidatus methanomethylophilus alvus, Natrialbaceae archaeon XQ INN 246, and Methanobrevibacter gottschalkii were greatest in Danish, French, and Chinese pigs with a relative abundance of 14.32, 11.67, and 16.28%, respectively. In terms of metabolic potential, the top three pathways in the archaeal communities included the MetaCyc pathway related to the biosynthesis of L-valine, L-isoleucine, and isobutanol. Interestingly, the pathway related to hydrogen consumption (METHANOGENESIS-PWY) was only observed in archaeal reads, while the pathways participating in hydrogen production (FERMENTATION-PWY and PWY4LZ-257) were only detected in bacterial reads. Archaeal communities also possessed CAZyme gene families, with the top five being AA3, GH43, GT2, AA6, and CE9. In terms of antibiotic resistance genes (ARGs), the class of multidrug resistance was the most abundant ARG, accounting for 87.41% of archaeal ARG hits. Our study reveals the diverse composition and metabolic functions of archaea in pigs, suggesting that archaea might play important roles in swine nutrition and metabolism.
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spelling pubmed-83006742021-07-24 The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs Deng, Feilong Li, Yushan Peng, Yunjuan Wei, Xiaoyuan Wang, Xiaofan Howe, Samantha Yang, Hua Xiao, Yingping Li, Hua Zhao, Jiangchao Li, Ying Animals (Basel) Article SIMPLE SUMMARY: Archaea is identified as the key link in the interaction between gut microbiota and host metabo-lism. Studies on human and mice have reported archaea, especially methanogenic archaea, makes an important impact on the energy harvesting capacity of the host by improving fermentation. But, in pigs, the metabolic potential of archaea at different production stages are still largely unknown. Herein, we re-analyzed 276 metagenomic samples to explore the diversity, composi-tion, and potential functions of archaea in pigs. The results showed significant regional variations in archaeal composition. Furthermore, the Metacyc pathway related to hydrogen consumption (METHANOGENESIS-PWY) was only observed in archaeal reads, and archaea may be involved in carbohydrate metabolism and de novo synthesis of some kinds of essential amino acid. Overall, metagenomic re-analysis revealed that the composition and functional potential of archaea in the swine gut and suggested that archaea may make an important function in pigs. ABSTRACT: Archaea are an essential class of gut microorganisms in humans and animals. Despite the substantial progress in gut microbiome research in the last decade, most studies have focused on bacteria, and little is known about archaea in mammals. In this study, we investigated the composition, diversity, and functional potential of gut archaeal communities in pigs by re-analyzing a published metagenomic dataset including a total of 276 fecal samples from three countries: China (n = 76), Denmark (n = 100), and France (n = 100). For alpha diversity (Shannon Index) of the archaeal communities, Chinese pigs were less diverse than Danish and French pigs (p < 0.001). Consistently, Chinese pigs also possessed different archaeal community structures from the other two groups based on the Bray–Curtis distance matrix. Methanobrevibacter was the most dominant archaeal genus in Chinese pigs (44.94%) and French pigs (15.41%), while Candidatus methanomethylophilus was the most predominant in Danish pigs (15.71%). At the species level, the relative abundance of Candidatus methanomethylophilus alvus, Natrialbaceae archaeon XQ INN 246, and Methanobrevibacter gottschalkii were greatest in Danish, French, and Chinese pigs with a relative abundance of 14.32, 11.67, and 16.28%, respectively. In terms of metabolic potential, the top three pathways in the archaeal communities included the MetaCyc pathway related to the biosynthesis of L-valine, L-isoleucine, and isobutanol. Interestingly, the pathway related to hydrogen consumption (METHANOGENESIS-PWY) was only observed in archaeal reads, while the pathways participating in hydrogen production (FERMENTATION-PWY and PWY4LZ-257) were only detected in bacterial reads. Archaeal communities also possessed CAZyme gene families, with the top five being AA3, GH43, GT2, AA6, and CE9. In terms of antibiotic resistance genes (ARGs), the class of multidrug resistance was the most abundant ARG, accounting for 87.41% of archaeal ARG hits. Our study reveals the diverse composition and metabolic functions of archaea in pigs, suggesting that archaea might play important roles in swine nutrition and metabolism. MDPI 2021-07-20 /pmc/articles/PMC8300674/ /pubmed/34359268 http://dx.doi.org/10.3390/ani11072139 Text en © 2021 by the authors. https://creativecommons.org/licenses/by/4.0/Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (https://creativecommons.org/licenses/by/4.0/).
spellingShingle Article
Deng, Feilong
Li, Yushan
Peng, Yunjuan
Wei, Xiaoyuan
Wang, Xiaofan
Howe, Samantha
Yang, Hua
Xiao, Yingping
Li, Hua
Zhao, Jiangchao
Li, Ying
The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs
title The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs
title_full The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs
title_fullStr The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs
title_full_unstemmed The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs
title_short The Diversity, Composition, and Metabolic Pathways of Archaea in Pigs
title_sort diversity, composition, and metabolic pathways of archaea in pigs
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8300674/
https://www.ncbi.nlm.nih.gov/pubmed/34359268
http://dx.doi.org/10.3390/ani11072139
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