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

Javad Gharechahi, Ghasem Hosseini Salekdeh

Research output: Contribution to journalArticleResearchpeer-review

Abstract

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.

LanguageEnglish
Article number216
Pages1-19
Number of pages19
JournalBiotechnology for Biofuels
Volume11
DOIs
Publication statusPublished - 2 Aug 2018

Fingerprint

Bacteroidetes
Metagenomics
Camelus
Microbiota
Rumen
Metagenome
Fibrobacteres
Fermentation
fermentation
Volatile Fatty Acids
Genes
Degradation
degradation
Volatile fatty acids
Enzymes
Acetates
Cellulosomes
Food-Processing Industry
Coenzyme A-Transferases
Euryarchaeota

Bibliographical note

Copyright the Author(s) 2018. Version archived for private and non-commercial use with the permission of the author/s and according to publisher conditions. For further rights please contact the publisher.

Keywords

  • Camel
  • Rumen metagenome
  • Microbiome
  • Binning
  • Carbohydrate active enzymes

Cite this

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abstract = "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.",
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A metagenomic analysis of the camel rumen's microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation. / Gharechahi, Javad; Salekdeh, Ghasem Hosseini.

In: Biotechnology for Biofuels, Vol. 11, 216, 02.08.2018, p. 1-19.

Research output: Contribution to journalArticleResearchpeer-review

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T1 - A metagenomic analysis of the camel rumen's microbiome identifies the major microbes responsible for lignocellulose degradation and fermentation

AU - Gharechahi,Javad

AU - Salekdeh,Ghasem Hosseini

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Y1 - 2018/8/2

N2 - 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.

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