Reference gene catalog and metagenome-assembled genomes from the gut microbiome reveal the microbial composition, antibiotic resistome, and adaptability of a lignocellulose diet in the giant panda

The giant panda, a strict herbivore that feeds on bamboo, still retains a typical carnivorous digestive system. Reference catalogs of microbial genes and genomes are lacking, largely limiting the antibiotic resistome and functional exploration of the giant panda gut microbiome. Here, we integrated 1...

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Veröffentlicht in:Environmental research 2024-03, Vol.245, p.118090-118090, Article 118090
Hauptverfasser: Yang, Shengzhi, Deng, Wenwen, Li, Guo, Jin, Lei, Huang, Yan, He, Yongguo, Wu, Daifu, Li, Desheng, Zhang, Anyun, Liu, Chengxi, Li, Caiwu, Zhang, Hemin, Xu, Huailiang, Penttinen, Petri, Zhao, Ke, Zou, Likou
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container_title Environmental research
container_volume 245
creator Yang, Shengzhi
Deng, Wenwen
Li, Guo
Jin, Lei
Huang, Yan
He, Yongguo
Wu, Daifu
Li, Desheng
Zhang, Anyun
Liu, Chengxi
Li, Caiwu
Zhang, Hemin
Xu, Huailiang
Penttinen, Petri
Zhao, Ke
Zou, Likou
description The giant panda, a strict herbivore that feeds on bamboo, still retains a typical carnivorous digestive system. Reference catalogs of microbial genes and genomes are lacking, largely limiting the antibiotic resistome and functional exploration of the giant panda gut microbiome. Here, we integrated 177 fecal metagenomes of captive and wild giant pandas to construct a giant panda integrated gene catalog (GPIGC) comprised of approximately 4.5 million non-redundant genes and reconstruct 393 metagenome-assembled genomes (MAGs). Taxonomic and functional characterization of genes revealed that the captivity of the giant panda significantly changed the core microbial composition and the distribution of microbial genes. Higher abundance and prevalence of antibiotic resistance genes (ARGs) were detected in the guts of captive giant pandas, and ARG distribution was influenced by geography, for both captive and wild individuals. Escherichia, as the prevalent genus in the guts of captive giant pandas, was the main carrier of ARGs, meaning there is a high risk of ARG transmission by Escherichia. We also found that multiple mcr gene variants, conferring plasmid-mediated mobile colistin resistance, were widespread in the guts of captive and wild giant pandas. There were low proportions of carbohydrate-active enzyme (CAZyme) genes in GPIGC and MAGs compared with several omnivorous and herbivorous mammals. Many members of Clostridium MAGs were significantly enriched in the guts of adult, old and wild giant pandas. The genomes of isolates and MAGs of Clostridiaceae harbored key genes or enzymes in complete pathways for degrading lignocellulose and producing short-chain fatty acids (SCFAs), indicating the potential of these bacteria to utilize the low-nutrient bamboo diet. Overall, our data presented an exhaustive reference gene catalog and MAGs in giant panda gut and provided a comprehensive understanding of the antibiotic resistome and microbial adaptability for a high-lignocellulose diet. [Display omitted] •Captivity of giant panda changed the composition and diversity of gut microbiome.•Lifestyle and geography influenced on ARGs abundance and distribution, respectively.•Escherichia was the main carrier of ARGs in the guts of captive giant pandas.•Clostridium harbored key genes in metabolisms of lignocellulose.
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Reference catalogs of microbial genes and genomes are lacking, largely limiting the antibiotic resistome and functional exploration of the giant panda gut microbiome. Here, we integrated 177 fecal metagenomes of captive and wild giant pandas to construct a giant panda integrated gene catalog (GPIGC) comprised of approximately 4.5 million non-redundant genes and reconstruct 393 metagenome-assembled genomes (MAGs). Taxonomic and functional characterization of genes revealed that the captivity of the giant panda significantly changed the core microbial composition and the distribution of microbial genes. Higher abundance and prevalence of antibiotic resistance genes (ARGs) were detected in the guts of captive giant pandas, and ARG distribution was influenced by geography, for both captive and wild individuals. Escherichia, as the prevalent genus in the guts of captive giant pandas, was the main carrier of ARGs, meaning there is a high risk of ARG transmission by Escherichia. We also found that multiple mcr gene variants, conferring plasmid-mediated mobile colistin resistance, were widespread in the guts of captive and wild giant pandas. There were low proportions of carbohydrate-active enzyme (CAZyme) genes in GPIGC and MAGs compared with several omnivorous and herbivorous mammals. Many members of Clostridium MAGs were significantly enriched in the guts of adult, old and wild giant pandas. The genomes of isolates and MAGs of Clostridiaceae harbored key genes or enzymes in complete pathways for degrading lignocellulose and producing short-chain fatty acids (SCFAs), indicating the potential of these bacteria to utilize the low-nutrient bamboo diet. Overall, our data presented an exhaustive reference gene catalog and MAGs in giant panda gut and provided a comprehensive understanding of the antibiotic resistome and microbial adaptability for a high-lignocellulose diet. [Display omitted] •Captivity of giant panda changed the composition and diversity of gut microbiome.•Lifestyle and geography influenced on ARGs abundance and distribution, respectively.•Escherichia was the main carrier of ARGs in the guts of captive giant pandas.•Clostridium harbored key genes in metabolisms of lignocellulose.</description><identifier>ISSN: 0013-9351</identifier><identifier>EISSN: 1096-0953</identifier><identifier>DOI: 10.1016/j.envres.2023.118090</identifier><identifier>PMID: 38163545</identifier><language>eng</language><publisher>Netherlands: Elsevier Inc</publisher><subject>adults ; Ailuropoda melanoleuca ; Animals ; Anti-Bacterial Agents - pharmacology ; Antibiotic resistance ; antibiotic resistance genes ; bamboos ; carnivores ; Clostridium ; colistin ; diet ; Diet - veterinary ; digestive system ; enzymes ; Escherichia ; Gastrointestinal Microbiome - genetics ; genus ; geography ; Giant panda ; Gut microbiome ; herbivores ; Humans ; intestinal microorganisms ; Lifestyle ; Lignin ; lignocellulose ; Metagenome ; Metagenome-assembled genome ; metagenomics ; omnivores ; risk ; Ursidae</subject><ispartof>Environmental research, 2024-03, Vol.245, p.118090-118090, Article 118090</ispartof><rights>2023 Elsevier Inc.</rights><rights>Copyright © 2023 Elsevier Inc. 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Reference catalogs of microbial genes and genomes are lacking, largely limiting the antibiotic resistome and functional exploration of the giant panda gut microbiome. Here, we integrated 177 fecal metagenomes of captive and wild giant pandas to construct a giant panda integrated gene catalog (GPIGC) comprised of approximately 4.5 million non-redundant genes and reconstruct 393 metagenome-assembled genomes (MAGs). Taxonomic and functional characterization of genes revealed that the captivity of the giant panda significantly changed the core microbial composition and the distribution of microbial genes. Higher abundance and prevalence of antibiotic resistance genes (ARGs) were detected in the guts of captive giant pandas, and ARG distribution was influenced by geography, for both captive and wild individuals. Escherichia, as the prevalent genus in the guts of captive giant pandas, was the main carrier of ARGs, meaning there is a high risk of ARG transmission by Escherichia. We also found that multiple mcr gene variants, conferring plasmid-mediated mobile colistin resistance, were widespread in the guts of captive and wild giant pandas. There were low proportions of carbohydrate-active enzyme (CAZyme) genes in GPIGC and MAGs compared with several omnivorous and herbivorous mammals. Many members of Clostridium MAGs were significantly enriched in the guts of adult, old and wild giant pandas. The genomes of isolates and MAGs of Clostridiaceae harbored key genes or enzymes in complete pathways for degrading lignocellulose and producing short-chain fatty acids (SCFAs), indicating the potential of these bacteria to utilize the low-nutrient bamboo diet. Overall, our data presented an exhaustive reference gene catalog and MAGs in giant panda gut and provided a comprehensive understanding of the antibiotic resistome and microbial adaptability for a high-lignocellulose diet. 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Reference catalogs of microbial genes and genomes are lacking, largely limiting the antibiotic resistome and functional exploration of the giant panda gut microbiome. Here, we integrated 177 fecal metagenomes of captive and wild giant pandas to construct a giant panda integrated gene catalog (GPIGC) comprised of approximately 4.5 million non-redundant genes and reconstruct 393 metagenome-assembled genomes (MAGs). Taxonomic and functional characterization of genes revealed that the captivity of the giant panda significantly changed the core microbial composition and the distribution of microbial genes. Higher abundance and prevalence of antibiotic resistance genes (ARGs) were detected in the guts of captive giant pandas, and ARG distribution was influenced by geography, for both captive and wild individuals. Escherichia, as the prevalent genus in the guts of captive giant pandas, was the main carrier of ARGs, meaning there is a high risk of ARG transmission by Escherichia. We also found that multiple mcr gene variants, conferring plasmid-mediated mobile colistin resistance, were widespread in the guts of captive and wild giant pandas. There were low proportions of carbohydrate-active enzyme (CAZyme) genes in GPIGC and MAGs compared with several omnivorous and herbivorous mammals. Many members of Clostridium MAGs were significantly enriched in the guts of adult, old and wild giant pandas. The genomes of isolates and MAGs of Clostridiaceae harbored key genes or enzymes in complete pathways for degrading lignocellulose and producing short-chain fatty acids (SCFAs), indicating the potential of these bacteria to utilize the low-nutrient bamboo diet. Overall, our data presented an exhaustive reference gene catalog and MAGs in giant panda gut and provided a comprehensive understanding of the antibiotic resistome and microbial adaptability for a high-lignocellulose diet. [Display omitted] •Captivity of giant panda changed the composition and diversity of gut microbiome.•Lifestyle and geography influenced on ARGs abundance and distribution, respectively.•Escherichia was the main carrier of ARGs in the guts of captive giant pandas.•Clostridium harbored key genes in metabolisms of lignocellulose.</abstract><cop>Netherlands</cop><pub>Elsevier Inc</pub><pmid>38163545</pmid><doi>10.1016/j.envres.2023.118090</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0002-9203-9484</orcidid></addata></record>
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ispartof Environmental research, 2024-03, Vol.245, p.118090-118090, Article 118090
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source MEDLINE; ScienceDirect Journals (5 years ago - present)
subjects adults
Ailuropoda melanoleuca
Animals
Anti-Bacterial Agents - pharmacology
Antibiotic resistance
antibiotic resistance genes
bamboos
carnivores
Clostridium
colistin
diet
Diet - veterinary
digestive system
enzymes
Escherichia
Gastrointestinal Microbiome - genetics
genus
geography
Giant panda
Gut microbiome
herbivores
Humans
intestinal microorganisms
Lifestyle
Lignin
lignocellulose
Metagenome
Metagenome-assembled genome
metagenomics
omnivores
risk
Ursidae
title Reference gene catalog and metagenome-assembled genomes from the gut microbiome reveal the microbial composition, antibiotic resistome, and adaptability of a lignocellulose diet in the giant panda
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