The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential

ABSTRACT Members of the genus Fibrobacter are cellulose-degrading bacteria and common constituents of the gastrointestinal microbiota of herbivores. Although considerable phylogenetic diversity is observed among members of this group, few functional differences explaining the distinct ecological dis...

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Autores principales: Anthony P. Neumann, Garret Suen
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Publicado: American Society for Microbiology 2018
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spelling oai:doaj.org-article:c1b5783259a94f909db313a72f6726a52021-11-15T15:22:21ZThe Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential10.1128/mSphere.00593-182379-5042https://doaj.org/article/c1b5783259a94f909db313a72f6726a52018-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mSphere.00593-18https://doaj.org/toc/2379-5042ABSTRACT Members of the genus Fibrobacter are cellulose-degrading bacteria and common constituents of the gastrointestinal microbiota of herbivores. Although considerable phylogenetic diversity is observed among members of this group, few functional differences explaining the distinct ecological distributions of specific phylotypes have been described. In this study, we sequenced and performed a comparative analysis of whole genomes from 38 novel Fibrobacter strains against the type strains for the two formally described Fibrobacter species F. succinogenes strain S85 and F. intestinalis strain NR9. Significant differences in the number of genes encoding carbohydrate-active enzyme families involved in plant cell wall polysaccharide degradation were observed among Fibrobacter phylotypes. F. succinogenes genomes were consistently enriched in genes encoding carbohydrate-active enzymes compared to those of F. intestinalis strains. Moreover, genomes of F. succinogenes phylotypes that are dominant in the rumen had significantly more genes annotated to major families involved in hemicellulose degradation (e.g., CE6, GH10, and GH43) than did the genomes of F. succinogenes phylotypes typically observed in the lower gut of large hindgut-fermenting herbivores such as horses. Genes encoding a putative urease were also identified in 12 of the Fibrobacter genomes, which were primarily isolated from hindgut-fermenting hosts. Screening for growth on urea as the sole source of nitrogen provided strong evidence that the urease was active in these strains. These results represent the strongest evidence reported to date for specific functional differences contributing to the ecology of Fibrobacter spp. in the herbivore gut. IMPORTANCE The herbivore gut microbiome is incredibly diverse, and a functional understanding of this diversity is needed to more reliably manipulate this community for specific gain, such as increased production in ruminant livestock. Microbial degraders of plant cell wall polysaccharides in the herbivore gut, particularly Fibrobacter spp., are of fundamental importance to their hosts for digestion of a diet consisting primarily of recalcitrant plant fibers. Considerable phylogenetic diversity exists among members of the genus Fibrobacter, but much of this diversity remains cryptic. Here, we used comparative genomics, applied to a diverse collection of recently isolated Fibrobacter strains, to identify a robust association between carbohydrate-active enzyme gene content and the Fibrobacter phylogeny. Our results provide the strongest evidence reported to date for functional differences among Fibrobacter phylotypes associated with either the rumen or the hindgut and emphasize the general significance of carbohydrate-active enzymes in the evolution of fiber-degrading bacteria.Anthony P. NeumannGarret SuenAmerican Society for MicrobiologyarticleFibrobactercarbohydrate-active enzymescellulosefibergenomicsgut microbiotaMicrobiologyQR1-502ENmSphere, Vol 3, Iss 6 (2018)
institution DOAJ
collection DOAJ
language EN
topic Fibrobacter
carbohydrate-active enzymes
cellulose
fiber
genomics
gut microbiota
Microbiology
QR1-502
spellingShingle Fibrobacter
carbohydrate-active enzymes
cellulose
fiber
genomics
gut microbiota
Microbiology
QR1-502
Anthony P. Neumann
Garret Suen
The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential
description ABSTRACT Members of the genus Fibrobacter are cellulose-degrading bacteria and common constituents of the gastrointestinal microbiota of herbivores. Although considerable phylogenetic diversity is observed among members of this group, few functional differences explaining the distinct ecological distributions of specific phylotypes have been described. In this study, we sequenced and performed a comparative analysis of whole genomes from 38 novel Fibrobacter strains against the type strains for the two formally described Fibrobacter species F. succinogenes strain S85 and F. intestinalis strain NR9. Significant differences in the number of genes encoding carbohydrate-active enzyme families involved in plant cell wall polysaccharide degradation were observed among Fibrobacter phylotypes. F. succinogenes genomes were consistently enriched in genes encoding carbohydrate-active enzymes compared to those of F. intestinalis strains. Moreover, genomes of F. succinogenes phylotypes that are dominant in the rumen had significantly more genes annotated to major families involved in hemicellulose degradation (e.g., CE6, GH10, and GH43) than did the genomes of F. succinogenes phylotypes typically observed in the lower gut of large hindgut-fermenting herbivores such as horses. Genes encoding a putative urease were also identified in 12 of the Fibrobacter genomes, which were primarily isolated from hindgut-fermenting hosts. Screening for growth on urea as the sole source of nitrogen provided strong evidence that the urease was active in these strains. These results represent the strongest evidence reported to date for specific functional differences contributing to the ecology of Fibrobacter spp. in the herbivore gut. IMPORTANCE The herbivore gut microbiome is incredibly diverse, and a functional understanding of this diversity is needed to more reliably manipulate this community for specific gain, such as increased production in ruminant livestock. Microbial degraders of plant cell wall polysaccharides in the herbivore gut, particularly Fibrobacter spp., are of fundamental importance to their hosts for digestion of a diet consisting primarily of recalcitrant plant fibers. Considerable phylogenetic diversity exists among members of the genus Fibrobacter, but much of this diversity remains cryptic. Here, we used comparative genomics, applied to a diverse collection of recently isolated Fibrobacter strains, to identify a robust association between carbohydrate-active enzyme gene content and the Fibrobacter phylogeny. Our results provide the strongest evidence reported to date for functional differences among Fibrobacter phylotypes associated with either the rumen or the hindgut and emphasize the general significance of carbohydrate-active enzymes in the evolution of fiber-degrading bacteria.
format article
author Anthony P. Neumann
Garret Suen
author_facet Anthony P. Neumann
Garret Suen
author_sort Anthony P. Neumann
title The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential
title_short The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential
title_full The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential
title_fullStr The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential
title_full_unstemmed The Phylogenomic Diversity of Herbivore-Associated <italic toggle="yes">Fibrobacter</italic> spp. Is Correlated to Lignocellulose-Degrading Potential
title_sort phylogenomic diversity of herbivore-associated <italic toggle="yes">fibrobacter</italic> spp. is correlated to lignocellulose-degrading potential
publisher American Society for Microbiology
publishDate 2018
url https://doaj.org/article/c1b5783259a94f909db313a72f6726a5
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