skip to main content
OSTI.GOV title logo U.S. Department of Energy
Office of Scientific and Technical Information

Title: The Phylogenomic Diversity of Herbivore-Associated Fibrobacter spp. Is Correlated to Lignocellulose-Degrading Potential

Abstract

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 themore » 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.« less

Authors:
ORCiD logo; ORCiD logo;
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States); Univ. of California, Oakland, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23)
OSTI Identifier:
1630236
Alternate Identifier(s):
OSTI ID: 1611013
Grant/Contract Number:  
AC02-05CH11231; SC0008104
Resource Type:
Journal Article: Published Article
Journal Name:
mSphere
Additional Journal Information:
Journal Name: mSphere Journal Volume: 3 Journal Issue: 6; Journal ID: ISSN 2379-5042
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English
Subject:
59 BASIC BIOLOGICAL SCIENCES; Fibrobacter; carbohydrate-active enzymes; cellulose; fiber; genomics; gut microbiota; herbivores

Citation Formats

Neumann, Anthony P., Suen, Garret, and Rodrigues, ed., Jorge M. The Phylogenomic Diversity of Herbivore-Associated Fibrobacter spp. Is Correlated to Lignocellulose-Degrading Potential. United States: N. p., 2018. Web. doi:10.1128/mSphere.00593-18.
Neumann, Anthony P., Suen, Garret, & Rodrigues, ed., Jorge M. The Phylogenomic Diversity of Herbivore-Associated Fibrobacter spp. Is Correlated to Lignocellulose-Degrading Potential. United States. doi:10.1128/mSphere.00593-18.
Neumann, Anthony P., Suen, Garret, and Rodrigues, ed., Jorge M. Wed . "The Phylogenomic Diversity of Herbivore-Associated Fibrobacter spp. Is Correlated to Lignocellulose-Degrading Potential". United States. doi:10.1128/mSphere.00593-18.
@article{osti_1630236,
title = {The Phylogenomic Diversity of Herbivore-Associated Fibrobacter spp. Is Correlated to Lignocellulose-Degrading Potential},
author = {Neumann, Anthony P. and Suen, Garret and Rodrigues, ed., Jorge M.},
abstractNote = {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.},
doi = {10.1128/mSphere.00593-18},
journal = {mSphere},
issn = {2379-5042},
number = 6,
volume = 3,
place = {United States},
year = {2018},
month = {12}
}

Journal Article:
Free Publicly Available Full Text
Publisher's Version of Record at 10.1128/mSphere.00593-18

Citation Metrics:
Cited by: 2 works
Citation information provided by
Web of Science

Save / Share:

Works referenced in this record:

Characterization and Synergistic Interactions of Fibrobacter succinogenes Glycoside Hydrolases
journal, July 2007

  • Qi, M.; Jun, H. -S.; Forsberg, C. W.
  • Applied and Environmental Microbiology, Vol. 73, Issue 19
  • DOI: 10.1128/AEM.01037-07

Catalytic and substrate-binding domains of endoglucanase 2 from Bacteroides succinogenes.
journal, January 1989


Cellulose Degradation in Anaerobic Environments
journal, October 1995


Metabolism of pectin in rumen bacteria Butyrivibrio fibrisolvens and Prevotella ruminicola
journal, December 1999


Nonhybrid, finished microbial genome assemblies from long-read SMRT sequencing data
journal, May 2013

  • Chin, Chen-Shan; Alexander, David H.; Marks, Patrick
  • Nature Methods, Vol. 10, Issue 6
  • DOI: 10.1038/nmeth.2474

Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis
journal, February 2008

  • Flint, Harry J.; Bayer, Edward A.; Rincon, Marco T.
  • Nature Reviews Microbiology, Vol. 6, Issue 2
  • DOI: 10.1038/nrmicro1817

Lignocellulose-Degrading Microbial Communities in Landfill Sites Represent a Repository of Unexplored Biomass-Degrading Diversity
journal, August 2017


Evolution of Mammals and Their Gut Microbes
journal, June 2008


Cellulolytic Streptomyces Strains Associated with Herbivorous Insects Share a Phylogenetically Linked Capacity To Degrade Lignocellulose
journal, May 2014

  • Book, Adam J.; Lewin, Gina R.; McDonald, Bradon R.
  • Applied and Environmental Microbiology, Vol. 80, Issue 15
  • DOI: 10.1128/AEM.01133-14

Degradation characteristics of isolated andin situ cell wall lucerne pectic polysaccharides by mixed ruminal microbes
journal, October 1995

  • Hatfield, R. D.; Weimer, P. J.
  • Journal of the Science of Food and Agriculture, Vol. 69, Issue 2, p. 185-196
  • DOI: 10.1002/jsfa.2740690208

Evaluating Models of Cellulose Degradation by Fibrobacter succinogenes S85
journal, December 2015


Influence of Substrates on the Surface Characteristics and Membrane Proteome of Fibrobacter succinogenes S85
journal, October 2015


A global analysis of gene expression in Fibrobacter succinogenes S85 grown on cellulose and soluble sugars at different growth rates
journal, October 2018

  • Neumann, Anthony P.; Weimer, Paul J.; Suen, Garret
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1290-x

Engineering of plant cell walls for enhanced biofuel production
journal, June 2015

  • Loqué, Dominique; Scheller, Henrik V.; Pauly, Markus
  • Current Opinion in Plant Biology, Vol. 25
  • DOI: 10.1016/j.pbi.2015.05.018

Diauxic growth of Fibrobacter succinogenes S85 on cellobiose and lactose
journal, July 2017

  • Ghali, Ines; Sofyan, Ahmad; Ohmori, Hideyuki
  • FEMS Microbiology Letters, Vol. 364, Issue 15
  • DOI: 10.1093/femsle/fnx150

BlastKOALA and GhostKOALA: KEGG Tools for Functional Characterization of Genome and Metagenome Sequences
journal, February 2016

  • Kanehisa, Minoru; Sato, Yoko; Morishima, Kanae
  • Journal of Molecular Biology, Vol. 428, Issue 4
  • DOI: 10.1016/j.jmb.2015.11.006

Complexity of the Ruminococcus flavefaciens cellulosome reflects an expansion in glycan recognition
journal, June 2016

  • Venditto, Immacolata; Luis, Ana S.; Rydahl, Maja
  • Proceedings of the National Academy of Sciences, Vol. 113, Issue 26
  • DOI: 10.1073/pnas.1601558113

A phylogenetic analysis of the phylum Fibrobacteres
journal, September 2013

  • Jewell, Kelsea A.; Scott, Jarrod J.; Adams, Sandra M.
  • Systematic and Applied Microbiology, Vol. 36, Issue 6
  • DOI: 10.1016/j.syapm.2013.04.002

The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics
journal, January 2009

  • Cantarel, B. L.; Coutinho, P. M.; Rancurel, C.
  • Nucleic Acids Research, Vol. 37, Issue Database
  • DOI: 10.1093/nar/gkn663

dbCAN: a web resource for automated carbohydrate-active enzyme annotation
journal, May 2012

  • Yin, Yanbin; Mao, Xizeng; Yang, Jincai
  • Nucleic Acids Research, Vol. 40, Issue W1
  • DOI: 10.1093/nar/gks479

Cellulose Degradation by Ruminal Microorganisms
journal, January 1992


Microbial species delineation using whole genome sequences
journal, July 2015

  • Varghese, Neha J.; Mukherjee, Supratim; Ivanova, Natalia
  • Nucleic Acids Research, Vol. 43, Issue 14
  • DOI: 10.1093/nar/gkv657

CheckM: assessing the quality of microbial genomes recovered from isolates, single cells, and metagenomes
journal, May 2015

  • Parks, Donovan H.; Imelfort, Michael; Skennerton, Connor T.
  • Genome Research, Vol. 25, Issue 7
  • DOI: 10.1101/gr.186072.114

Influence of the Composition of the Cellulolytic Flora on the Development of Hydrogenotrophic Microorganisms, Hydrogen Utilization, and Methane Production in the Rumens of Gnotobiotically Reared Lambs
journal, October 2010

  • Chaucheyras-Durand, Frédérique; Masséglia, Sébastien; Fonty, Gérard
  • Applied and Environmental Microbiology, Vol. 76, Issue 24
  • DOI: 10.1128/AEM.01784-10

Complexity of the Ruminococcus flavefaciens FD-1 cellulosome reflects an expansion of family-related protein-protein interactions
journal, February 2017

  • Israeli-Ruimy, Vered; Bule, Pedro; Jindou, Sadanari
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep42355

A Phylogenomic Analysis of the Bacterial Phylum Fibrobacteres
journal, January 2016

  • Abdul Rahman, Nurdyana; Parks, Donovan H.; Vanwonterghem, Inka
  • Frontiers in Microbiology, Vol. 6
  • DOI: 10.3389/fmicb.2015.01469

Pectinolytic enzymes of anaerobic fungi
journal, May 1995


Quantitative aspects of propionate metabolism and gluconeogenesis in sheep
journal, September 1966


RAxML version 8: a tool for phylogenetic analysis and post-analysis of large phylogenies
journal, January 2014


Prokka: rapid prokaryotic genome annotation
journal, March 2014


Fermentation of pectin and glucose, and activity of pectin-degrading enzymes in the rumen bacterium Lachnospira multiparus
journal, August 2001


The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist
journal, April 2011


How Much Do rRNA Gene Surveys Underestimate Extant Bacterial Diversity?
journal, January 2018

  • Rodriguez-R, Luis M.; Castro, Juan C.; Kyrpides, Nikos C.
  • Applied and Environmental Microbiology, Vol. 84, Issue 6
  • DOI: 10.1128/AEM.00014-18

Diversity Among Fibrobacter Isolates: Towards a Phylogenetic Classification
journal, February 1992


Observations on the Nutrition of Bacteroides Succinogenes—A Ruminal Cellulolytic Bacterium
journal, November 1959


SPAdes: A New Genome Assembly Algorithm and Its Applications to Single-Cell Sequencing
journal, May 2012

  • Bankevich, Anton; Nurk, Sergey; Antipov, Dmitry
  • Journal of Computational Biology, Vol. 19, Issue 5
  • DOI: 10.1089/cmb.2012.0021

Mutualistic Fermentative Digestion in the Gastrointestinal Tract: Diversity and Evolution
journal, April 2002


Fibrolytic capabilities of ruminal bacterium Fibrobacter succinogenes in relation to its phylogenetic grouping
journal, May 2009


Evidence for a novel mechanism of microbial cellulose degradation
journal, June 2009


Distribution and diversity of members of the bacterial phylum Fibrobacteres in environments where cellulose degradation occurs
journal, October 2014

  • Ransom-Jones, Emma; Jones, David L.; Edwards, Arwyn
  • Systematic and Applied Microbiology, Vol. 37, Issue 7
  • DOI: 10.1016/j.syapm.2014.06.001

Accelerated Profile HMM Searches
journal, October 2011


The carbohydrate-active enzymes database (CAZy) in 2013
journal, November 2013

  • Lombard, Vincent; Golaconda Ramulu, Hemalatha; Drula, Elodie
  • Nucleic Acids Research, Vol. 42, Issue D1
  • DOI: 10.1093/nar/gkt1178

A Study of Actively Cellulolytic Rod-Shaped Bacteria of the Bovine Rumen
journal, October 1954


RAxML-III: a fast program for maximum likelihood-based inference of large phylogenetic trees
journal, December 2004


Sequencing of Multiple Clostridial Genomes Related to Biomass Conversion and Biofuel Production
journal, October 2010

  • Hemme, C. L.; Mouttaki, H.; Lee, Y. -J.
  • Journal of Bacteriology, Vol. 192, Issue 24
  • DOI: 10.1128/JB.01064-10

Dendroscope 3: An Interactive Tool for Rooted Phylogenetic Trees and Networks
journal, September 2012


Transfer of Bacteroides succinogenes (Hungate) to Fibrobacter gen. nov. as Fibrobacter succinogenes comb. nov. and Description of Fibrobacter intestinalis sp. nov.
journal, October 1988

  • Montgomery, L.; Flesher, B.; Stahl, D.
  • International Journal of Systematic Bacteriology, Vol. 38, Issue 4
  • DOI: 10.1099/00207713-38-4-430

Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis
journal, January 2014

  • Christopherson, Melissa R.; Dawson, John A.; Stevenson, David M.
  • BMC Genomics, Vol. 15, Issue 1
  • DOI: 10.1186/1471-2164-15-1066

The enveomics collection: a toolbox for specialized analyses of microbial genomes and metagenomes
preprint, March 2016


Fast, scalable generation of high‐quality protein multiple sequence alignments using Clustal Omega
journal, January 2011

  • Sievers, Fabian; Wilm, Andreas; Dineen, David
  • Molecular Systems Biology, Vol. 7, Issue 1
  • DOI: 10.1038/msb.2011.75

Functional Annotation of Fibrobacter succinogenes S85 Carbohydrate Active Enzymes
journal, August 2010

  • Brumm, Phillip; Mead, David; Boyum, Julie
  • Applied Biochemistry and Biotechnology, Vol. 163, Issue 5
  • DOI: 10.1007/s12010-010-9070-5

VEGAN, a package of R functions for community ecology
journal, April 2003


Outer Membrane Proteins of Fibrobacter succinogenes with Potential Roles in Adhesion to Cellulose and in Cellulose Digestion
journal, July 2007

  • Jun, H. -S.; Qi, M.; Gong, J.
  • Journal of Bacteriology, Vol. 189, Issue 19
  • DOI: 10.1128/JB.00560-07

Polysaccharide utilization locus and CAZYme genome repertoires reveal diverse ecological adaptation of Prevotella species
journal, October 2015


Rumen microbial community composition varies with diet and host, but a core microbiome is found across a wide geographical range
journal, October 2015

  • Henderson, Gemma; Cox, Faith; Ganesh, Siva
  • Scientific Reports, Vol. 5, Issue 1
  • DOI: 10.1038/srep14567

Sporulation capability and amylosome conservation among diverse human colonic and rumen isolates of the keystone starch-degrader Ruminococcus bromii : Comparative genomics of
journal, December 2017

  • Mukhopadhya, Indrani; Moraïs, Sarah; Laverde-Gomez, Jenny
  • Environmental Microbiology, Vol. 20, Issue 1
  • DOI: 10.1111/1462-2920.14000

The Degradation and Utilization of Endogenous urea in the Gastrointestinal Tract of Ruminants: a Review
journal, June 1980

  • Kennedy, P. M.; Milligan, L. P.
  • Canadian Journal of Animal Science, Vol. 60, Issue 2
  • DOI: 10.4141/cjas80-030

Isolation and characterization of endoglucanases 1 and 2 from Bacteroides succinogenes S85.
journal, July 1988


Expansion of the enzymatic repertoire of the CAZy database to integrate auxiliary redox enzymes
journal, January 2013

  • Levasseur, Anthony; Drula, Elodie; Lombard, Vincent
  • Biotechnology for Biofuels, Vol. 6, Issue 1, Article No. 41
  • DOI: 10.1186/1754-6834-6-41

Why Don’t Ruminal Bacteria Digest Cellulose Faster?
journal, August 1996