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PMID: 19181843 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Gene-centric metagenomics of the fiber-adherent bovine rumen microbiome reveals forage specific glycoside hydrolases.

Brulc JM, Antonopoulos DA, Miller ME, Wilson MK, Yannarell AC, Dinsdale EA, Edwards RE, Frank ED, Emerson JB, Wacklin P, Coutinho PM, Henrissat B, Nelson KE, White BA

Abstract

The complex microbiome of the rumen functions as an effective system for the conversion of plant cell wall biomass to microbial protein, short chain fatty acids, and gases. As such, it provides a unique genetic resource for plant cell wall degrading microbial enzymes that could be used in the production of biofuels. The rumen and gastrointestinal tract harbor a dense and complex microbiome. To gain a greater understanding of the ecology and metabolic potential of this microbiome, we used comparative metagenomics (phylotype analysis and SEED subsystems-based annotations) to examine randomly sampled pyrosequence data from 3 fiber-adherent microbiomes and 1 pooled liquid sample (a mixture of the liquid microbiome fractions from the same bovine rumens). Even though the 3 animals were fed the same diet, the community structure, predicted phylotype, and metabolic potentials in the rumen were markedly different with respect to nutrient utilization. A comparison of the glycoside hydrolase and cellulosome functional genes revealed that in the rumen microbiome, initial colonization of fiber appears to be by organisms possessing enzymes that attack the easily available side chains of complex plant polysaccharides and not the more recalcitrant main chains, especially cellulose. Furthermore, when compared with the termite hindgut microbiome, there are fundamental differences in the glycoside hydrolase content that appear to be diet driven for either the bovine rumen (forages and legumes) or the termite hindgut (wood).

MeSH Terms
Animals Base Sequence Cattle Cellulosomes/genetics Diet Food Genomics/methods Glycoside Hydrolases/analysis,genetics Isoptera Metabolism Metabolomics/methods Metagenome Molecular Sequence Data Rumen
Chemicals
Glycoside Hydrolases
Authors & Affiliations
14 authors, click to expand affiliations / ORCID
Brulc Jennifer M
Department of Animal Sciences, University of Illinois, Urbana, IL 61801, USA.
Antonopoulos Dionysios A
Miller Margret E Berg
Wilson Melissa K
Yannarell Anthony C
Dinsdale Elizabeth A
Edwards Robert E
Frank Edward D
Emerson Joanne B
Wacklin Pirjo
Coutinho Pedro M
Henrissat Bernard
Nelson Karen E
White Bryan A
References (44)
44 references, click to expand
  1. Improved extraction of PCR-quality community DNA from digesta and fecal samples.
    Biotechniques. 2004 May;36(5):808-12 PMID: 15152600
  2. Molecular techniques for determining microbial diversity and community structure in natural environments.
    Crit Rev Microbiol. 2000;26(1):37-57 PMID: 10782339
  3. Microbiology: metagenomics.
    Nature. 2008 Sep 25;455(7212):481-3 PMID: 18818648
  4. Microbial diversity in the deep sea and the underexplored "rare biosphere".
    Proc Natl Acad Sci U S A. 2006 Aug 8;103(32):12115-20 PMID: 16880384
  5. Microbial diversity and function in soil: from genes to ecosystems.
    Curr Opin Microbiol. 2002 Jun;5(3):240-5 PMID: 12057676
  6. A molecular view of microbial diversity and the biosphere.
    Science. 1997 May 2;276(5313):734-40 PMID: 9115194
  7. Metagenomic and functional analysis of hindgut microbiota of a wood-feeding higher termite.
    Nature. 2007 Nov 22;450(7169):560-5 PMID: 18033299
  8. Genome sequencing in microfabricated high-density picolitre reactors.
    Nature. 2005 Sep 15;437(7057):376-80 PMID: 16056220
  9. Diet-dependent shifts in the bacterial population of the rumen revealed with real-time PCR.
    Appl Environ Microbiol. 2001 Jun;67(6):2766-74 PMID: 11375193
  10. An application of statistics to comparative metagenomics.
    BMC Bioinformatics. 2006 Mar 20;7:162 PMID: 16549025
  11. The subsystems approach to genome annotation and its use in the project to annotate 1000 genomes.
    Nucleic Acids Res. 2005 Oct 07;33(17):5691-702 PMID: 16214803
  12. Construction of environmental DNA libraries in Escherichia coli and screening for the presence of genes conferring utilization of 4-hydroxybutyrate.
    Appl Environ Microbiol. 1999 Sep;65(9):3901-7 PMID: 10473393
  13. Taxon-specific probes for the cellulolytic genus Fibrobacter reveal abundant and novel equine-associated populations.
    Appl Environ Microbiol. 1995 Apr;61(4):1348-51 PMID: 7538274
  14. Phylogenetic analysis of rumen bacteria by comparative sequence analysis of cloned 16S rRNA genes.
    Anaerobe. 1998 Jun;4(3):153-63 PMID: 16887636
  15. Use of phylogenetically based hybridization probes for studies of ruminal microbial ecology.
    Appl Environ Microbiol. 1988 May;54(5):1079-84 PMID: 3389805
  16. An ecological and evolutionary perspective on human-microbe mutualism and disease.
    Nature. 2007 Oct 18;449(7164):811-8 PMID: 17943117
  17. Novel microbial diversity adherent to plant biomass in the herbivore gastrointestinal tract, as revealed by ribosomal intergenic spacer analysis and rrs gene sequencing.
    Environ Microbiol. 2005 Apr;7(4):530-43 PMID: 15816930
  18. Worlds within worlds: evolution of the vertebrate gut microbiota.
    Nat Rev Microbiol. 2008 Oct;6(10):776-88 PMID: 18794915
  19. Effect of short-term chilling of rumen contents on viable bacterial numbers.
    Appl Environ Microbiol. 1980 Feb;39(2):376-81 PMID: 7377771
  20. Introducing DOTUR, a computer program for defining operational taxonomic units and estimating species richness.
    Appl Environ Microbiol. 2005 Mar;71(3):1501-6 PMID: 15746353
  21. An obesity-associated gut microbiome with increased capacity for energy harvest.
    Nature. 2006 Dec 21;444(7122):1027-31 PMID: 17183312
  22. Evolution of mammals and their gut microbes.
    Science. 2008 Jun 20;320(5883):1647-51 PMID: 18497261
  23. Development of a real-time PCR assay for monitoring anaerobic fungal and cellulolytic bacterial populations within the rumen.
    FEMS Microbiol Ecol. 2006 Dec;58(3):572-82 PMID: 17117998
  24. Comparative metagenomics reveals host specific metavirulomes and horizontal gene transfer elements in the chicken cecum microbiome.
    PLoS One. 2008 Aug 13;3(8):e2945 PMID: 18698407
  25. 16S rDNA sequencing of Ruminococcus albus and Ruminococcus flavefaciens: design of a signature probe and its application in adult sheep.
    Microbiology (Reading). 1999 Jul;145 ( Pt 7):1797-1807 PMID: 10439419
  26. Using pyrosequencing to shed light on deep mine microbial ecology.
    BMC Genomics. 2006 Mar 20;7:57 PMID: 16549033
  27. Suppressive subtractive hybridization as a tool for identifying genetic diversity in an environmental metagenome: the rumen as a model.
    Environ Microbiol. 2004 Sep;6(9):928-37 PMID: 15305918
  28. Phylogenetic analysis of the microbial populations in the wild herbivore gastrointestinal tract: insights into an unexplored niche.
    Environ Microbiol. 2003 Nov;5(11):1212-20 PMID: 14641599
  29. Comparative metagenomics of microbial communities.
    Science. 2005 Apr 22;308(5721):554-7 PMID: 15845853
  30. The Ribosomal Database Project (RDP-II): sequences and tools for high-throughput rRNA analysis.
    Nucleic Acids Res. 2005 Jan 1;33(Database issue):D294-6 PMID: 15608200
  31. Use of DNA probes to monitor nutritional effects on ruminal prokaryotes and Fibrobacter succinogenes S85.
    J Anim Sci. 1992 Jan;70(1):289-95 PMID: 1374753
  32. Phylogenetic classification of short environmental DNA fragments.
    Nucleic Acids Res. 2008 Apr;36(7):2230-9 PMID: 18285365
  33. Characterization of several Psychrobacter strains isolated from Antarctic environments and description of Psychrobacter luti sp. nov. and Psychrobacter fozii sp. nov.
    Int J Syst Evol Microbiol. 2003 Jul;53(Pt 4):1093-1100 PMID: 12892132
  34. Molecular biological access to the chemistry of unknown soil microbes: a new frontier for natural products.
    Chem Biol. 1998 Oct;5(10):R245-9 PMID: 9818143
  35. Phylogenetic analysis of archaeal 16S rRNA libraries from the rumen suggests the existence of a novel group of archaea not associated with known methanogens.
    FEMS Microbiol Lett. 2001 Jun 12;200(1):67-72 PMID: 11410351
  36. Novel polyphenol oxidase mined from a metagenome expression library of bovine rumen: biochemical properties, structural analysis, and phylogenetic relationships.
    J Biol Chem. 2006 Aug 11;281(32):22933-42 PMID: 16740638
  37. Functional metagenomic profiling of nine biomes.
    Nature. 2008 Apr 3;452(7187):629-32 PMID: 18337718
  38. Pyrosequencing enumerates and contrasts soil microbial diversity.
    ISME J. 2007 Aug;1(4):283-90 PMID: 18043639
  39. Morphological diversity of ruminal bacteriophages from sheep and cattle.
    Appl Environ Microbiol. 1988 Jun;54(6):1637-41 PMID: 3415230
  40. Comparison of microbial populations in model and natural rumens using 16S ribosomal RNA-targeted probes.
    Environ Microbiol. 2000 Dec;2(6):632-43 PMID: 11214796
  41. 16S rDNA library-based analysis of ruminal bacterial diversity.
    Antonie Van Leeuwenhoek. 2004 Oct;86(3):263-81 PMID: 15539930
  42. Phylogenetic analysis of fiber-associated rumen bacterial community and PCR detection of uncultured bacteria.
    FEMS Microbiol Lett. 2003 Dec 5;229(1):23-30 PMID: 14659538
  43. Metagenomic analysis of the human distal gut microbiome.
    Science. 2006 Jun 2;312(5778):1355-9 PMID: 16741115
  44. Novel hydrolase diversity retrieved from a metagenome library of bovine rumen microflora.
    Environ Microbiol. 2005 Dec;7(12):1996-2010 PMID: 16309396
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
1091-6490
Published
2009-02-10
Epub
2009-00-30
Pages
1948-53
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC2633212
Subset
IM
Databases
GENBANK
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