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A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation

BACKGROUND: The diverse microbiome present in the rumen of ruminant animals facilitates the digestion of plant-based fiber. In this study, a shotgun metagenomic analysis of the microbes adhering to plant fiber in the camel rumen was undertaken to identify the key species contributing to lignocellulo...

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Autores principales: Gharechahi, Javad, Salekdeh, Ghasem Hosseini
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2018
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6071333/
https://www.ncbi.nlm.nih.gov/pubmed/30083229
http://dx.doi.org/10.1186/s13068-018-1214-9
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author Gharechahi, Javad
Salekdeh, Ghasem Hosseini
author_facet Gharechahi, Javad
Salekdeh, Ghasem Hosseini
author_sort Gharechahi, Javad
collection PubMed
description BACKGROUND: The diverse microbiome present in the rumen of ruminant animals facilitates the digestion of plant-based fiber. In this study, a shotgun metagenomic analysis of the microbes adhering to plant fiber in the camel rumen was undertaken to identify the key species contributing to lignocellulose degradation and short chain volatile fatty acids (VFA) fermentation. RESULTS: The density of genes in the metagenome encoding glycoside hydrolases was estimated to be 25 per Mbp of assembled DNA, which is significantly greater than what has been reported in other sourced metagenomes, including cow rumen. There was also a substantial representation of sequences encoding scaffoldins, dockerins and cohesins, indicating the potential for cellulosome-mediated lignocellulose degradation. Binning of the assembled metagenome has enabled the definition of 65 high-quality genome bins which showed high diversity for lignocellulose degrading enzymes. Species associated to Bacteroidetes showed a high proportion of genes for debranching and oligosaccharide degrading enzymes, while those belonging to Firmicutes and Fibrobacteres were rich in cellulases and hemicellulases and thus these lineages were probably the key for ensuring the degradation of lignocellulose. The presence of many “polysaccharide utilization loci” (PULs) in Bacteroidetes genomes indicates their broad substrate specificity and high potential carbohydrate degradation ability. An analysis of VFA biosynthesis pathways showed that genes required for the synthesis of acetate were present in a range of species, except for Elusimicrobiota and Euryarchaeota. The production of propionate, exclusively via the succinate pathway, was carried out by species belonging to the phyla Bacteroidetes, Firmicutes, Spirochaetes and Fibrobacteres. Butyrate was generated via the butyrylCoA: acetate CoA-transferase pathway by Bacteroidetes and Lentisphaerae species, but generally via the butyrate kinase pathway by Firmicutes species. CONCLUSION: The analysis confirmed the camel rumen’s microbiome as a dense and yet largely untapped source of enzymes with the potential to be used in a range of biotechnological processes including biofuel, fine chemicals and food processing industries. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1214-9) contains supplementary material, which is available to authorized users.
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spelling pubmed-60713332018-08-06 A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation Gharechahi, Javad Salekdeh, Ghasem Hosseini Biotechnol Biofuels Research BACKGROUND: The diverse microbiome present in the rumen of ruminant animals facilitates the digestion of plant-based fiber. In this study, a shotgun metagenomic analysis of the microbes adhering to plant fiber in the camel rumen was undertaken to identify the key species contributing to lignocellulose degradation and short chain volatile fatty acids (VFA) fermentation. RESULTS: The density of genes in the metagenome encoding glycoside hydrolases was estimated to be 25 per Mbp of assembled DNA, which is significantly greater than what has been reported in other sourced metagenomes, including cow rumen. There was also a substantial representation of sequences encoding scaffoldins, dockerins and cohesins, indicating the potential for cellulosome-mediated lignocellulose degradation. Binning of the assembled metagenome has enabled the definition of 65 high-quality genome bins which showed high diversity for lignocellulose degrading enzymes. Species associated to Bacteroidetes showed a high proportion of genes for debranching and oligosaccharide degrading enzymes, while those belonging to Firmicutes and Fibrobacteres were rich in cellulases and hemicellulases and thus these lineages were probably the key for ensuring the degradation of lignocellulose. The presence of many “polysaccharide utilization loci” (PULs) in Bacteroidetes genomes indicates their broad substrate specificity and high potential carbohydrate degradation ability. An analysis of VFA biosynthesis pathways showed that genes required for the synthesis of acetate were present in a range of species, except for Elusimicrobiota and Euryarchaeota. The production of propionate, exclusively via the succinate pathway, was carried out by species belonging to the phyla Bacteroidetes, Firmicutes, Spirochaetes and Fibrobacteres. Butyrate was generated via the butyrylCoA: acetate CoA-transferase pathway by Bacteroidetes and Lentisphaerae species, but generally via the butyrate kinase pathway by Firmicutes species. CONCLUSION: The analysis confirmed the camel rumen’s microbiome as a dense and yet largely untapped source of enzymes with the potential to be used in a range of biotechnological processes including biofuel, fine chemicals and food processing industries. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s13068-018-1214-9) contains supplementary material, which is available to authorized users. BioMed Central 2018-08-02 /pmc/articles/PMC6071333/ /pubmed/30083229 http://dx.doi.org/10.1186/s13068-018-1214-9 Text en © The Author(s) 2018 Open AccessThis article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research
Gharechahi, Javad
Salekdeh, Ghasem Hosseini
A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
title A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
title_full A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
title_fullStr A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
title_full_unstemmed A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
title_short A metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
title_sort metagenomic analysis of the camel rumen’s microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation
topic Research
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6071333/
https://www.ncbi.nlm.nih.gov/pubmed/30083229
http://dx.doi.org/10.1186/s13068-018-1214-9
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