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The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy

The characteristics of flora in the intestine of an animal, including the number and abundance of different microbial species and their functions, are closely related to the diets of the animal and affect the physical condition of the host. The Malayan pangolin (Manis javanica) is an endangered spec...

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Autores principales: Ma, Jing-E, Jiang, Hai-Ying, Li, Lin-Miao, Zhang, Xiu-Juan, Li, Guan-Yu, Li, Hui-Ming, Jin, Xue-Jun, Chen, Jin-Ping
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6265309/
https://www.ncbi.nlm.nih.gov/pubmed/30532742
http://dx.doi.org/10.3389/fmicb.2018.02793
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author Ma, Jing-E
Jiang, Hai-Ying
Li, Lin-Miao
Zhang, Xiu-Juan
Li, Guan-Yu
Li, Hui-Ming
Jin, Xue-Jun
Chen, Jin-Ping
author_facet Ma, Jing-E
Jiang, Hai-Ying
Li, Lin-Miao
Zhang, Xiu-Juan
Li, Guan-Yu
Li, Hui-Ming
Jin, Xue-Jun
Chen, Jin-Ping
author_sort Ma, Jing-E
collection PubMed
description The characteristics of flora in the intestine of an animal, including the number and abundance of different microbial species and their functions, are closely related to the diets of the animal and affect the physical condition of the host. The Malayan pangolin (Manis javanica) is an endangered species that specializes in myrmecophagy. Analyzing the microbiome in the intestine of the pangolin is imperative to protect this species. By sequencing the metagenomes of the feces of four pangolins, we constructed a non-redundant catalog of 211,868 genes representing 1,811 metagenomic species. Taxonomic annotation revealed that Bacteroidetes (49.9%), Proteobacteria (32.2%), and Firmicutes (12.6%) are the three main phyla. The annotation of gene functions identified 5,044 genes from 88 different glycoside hydrolase (GH) families in the Carbohydrate-Active enZYmes database and 114 gene modules related to chitin-degrading enzymes, corresponding to the catalytic domains of GH18 family enzymes, containing chitinase genes of classes III and V in the dataset. Fourteen gene modules corresponded to the catalytic domains of GH19 family enzymes, containing chitinase genes of classes I, II, and IV. These genes were found in 37 species belonging to four phyla: Bacteroidetes, Cyanobacteria, Firmicutes, and Proteobacteria. Moreover, when the metabolic pathways of these genes were summarized, 41,711 genes were associated with 147 unique KEGG metabolic pathways, and these genes were assigned to two Gene Ontology terms: metabolic process and catalytic activity. We also found several species that likely play roles in the digestion of cellulose and may be able to degrade chitin, including Enterobacter cloacae, Lactococcus lactis, Chitinimonas koreensis, and Chitinophaga pinensis. In addition, we identified some intestinal microflora and genes related to diseases in pangolins. Twenty-seven species were identified by STAMP analysis as differentially abundant in healthy and diseased animals: 20 species, including Cellulosilyticum lentocellum and Lactobacillus reuteri, were more abundant in healthy pangolins, while seven species, including Odoribacter splanchnicus, Marinilabilia salmonicolor, Xanthomonas citri, Xanthomonas vasicola, Oxalobacter formigenes, Prolixibacter bellariivorans, and Clostridium bolteae, were more abundant in diseased pangolins. These results will support the efforts to conserve pangolins.
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spelling pubmed-62653092018-12-07 The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy Ma, Jing-E Jiang, Hai-Ying Li, Lin-Miao Zhang, Xiu-Juan Li, Guan-Yu Li, Hui-Ming Jin, Xue-Jun Chen, Jin-Ping Front Microbiol Microbiology The characteristics of flora in the intestine of an animal, including the number and abundance of different microbial species and their functions, are closely related to the diets of the animal and affect the physical condition of the host. The Malayan pangolin (Manis javanica) is an endangered species that specializes in myrmecophagy. Analyzing the microbiome in the intestine of the pangolin is imperative to protect this species. By sequencing the metagenomes of the feces of four pangolins, we constructed a non-redundant catalog of 211,868 genes representing 1,811 metagenomic species. Taxonomic annotation revealed that Bacteroidetes (49.9%), Proteobacteria (32.2%), and Firmicutes (12.6%) are the three main phyla. The annotation of gene functions identified 5,044 genes from 88 different glycoside hydrolase (GH) families in the Carbohydrate-Active enZYmes database and 114 gene modules related to chitin-degrading enzymes, corresponding to the catalytic domains of GH18 family enzymes, containing chitinase genes of classes III and V in the dataset. Fourteen gene modules corresponded to the catalytic domains of GH19 family enzymes, containing chitinase genes of classes I, II, and IV. These genes were found in 37 species belonging to four phyla: Bacteroidetes, Cyanobacteria, Firmicutes, and Proteobacteria. Moreover, when the metabolic pathways of these genes were summarized, 41,711 genes were associated with 147 unique KEGG metabolic pathways, and these genes were assigned to two Gene Ontology terms: metabolic process and catalytic activity. We also found several species that likely play roles in the digestion of cellulose and may be able to degrade chitin, including Enterobacter cloacae, Lactococcus lactis, Chitinimonas koreensis, and Chitinophaga pinensis. In addition, we identified some intestinal microflora and genes related to diseases in pangolins. Twenty-seven species were identified by STAMP analysis as differentially abundant in healthy and diseased animals: 20 species, including Cellulosilyticum lentocellum and Lactobacillus reuteri, were more abundant in healthy pangolins, while seven species, including Odoribacter splanchnicus, Marinilabilia salmonicolor, Xanthomonas citri, Xanthomonas vasicola, Oxalobacter formigenes, Prolixibacter bellariivorans, and Clostridium bolteae, were more abundant in diseased pangolins. These results will support the efforts to conserve pangolins. Frontiers Media S.A. 2018-11-23 /pmc/articles/PMC6265309/ /pubmed/30532742 http://dx.doi.org/10.3389/fmicb.2018.02793 Text en Copyright © 2018 Ma, Jiang, Li, Zhang, Li, Li, Jin and Chen. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Microbiology
Ma, Jing-E
Jiang, Hai-Ying
Li, Lin-Miao
Zhang, Xiu-Juan
Li, Guan-Yu
Li, Hui-Ming
Jin, Xue-Jun
Chen, Jin-Ping
The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
title The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
title_full The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
title_fullStr The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
title_full_unstemmed The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
title_short The Fecal Metagenomics of Malayan Pangolins Identifies an Extensive Adaptation to Myrmecophagy
title_sort fecal metagenomics of malayan pangolins identifies an extensive adaptation to myrmecophagy
topic Microbiology
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6265309/
https://www.ncbi.nlm.nih.gov/pubmed/30532742
http://dx.doi.org/10.3389/fmicb.2018.02793
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