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Title: Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis

Abstract

Bacteria in the genus Ruminococcus are ubiquitous members of the mammalian gastrointestinal tract. In particular, they are important in ruminants where they digest a wide range of plant cell wall polysaccharides. For example, Ruminococcus albus 7 is a primary cellulose degrader that produces acetate usable by its bovine host. Moreover, it is one of the few organisms that ferments cellulose to form ethanol at mesophilic temperatures in vitro. The mechanism of cellulose degradation by R. albus 7 is not well-defined and is thought to involve pilin-like proteins, unique carbohydrate-binding domains, a glycocalyx, and cellulosomes. We used a combination of comparative genomics, fermentation analyses, and transcriptomics to further clarify the cellulolytic and fermentative potential of R. albus 7. A comparison of the R. albus 7 genome sequence against the genome sequences of related bacteria that either encode or do not encode cellulosomes revealed that R. albus 7 does not encode for most canonical cellulosomal components. Fermentation analysis of R. albus 7 revealed the ability to produce ethanol and acetate on a wide range of fibrous substrates in vitro. Global transcriptomic analysis of R. albus 7 grown at identical dilution rates on cellulose and cellobiose in a chemostat showed that this bacterium,more » when growing on cellulose, utilizes a carbohydrate-degrading strategy that involves increased transcription of the rare carbohydrate-binding module (CBM) family 37 domain and the tryptophan biosynthetic operon. Our data suggest that R. albus 7 does not use canonical cellulosomal components to degrade cellulose, but rather up-regulates the expression of CBM37-containing enzymes and tryptophan biosynthesis. This study contributes to a revised model of carbohydrate degradation by this key member of the rumen ecosystem.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [4];  [2];  [1]
  1. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  2. Univ. of Wisconsin, Madison, WI (United States). Dept. of Biostatistics and Medical Informatics
  3. US Dept. of Agriculture-Agricultural Research Services (USDA-ARS), Madison, WI (United States). US Dairy Forage Research Center
  4. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology; US Dept. of Agriculture-Agricultural Research Services (USDA-ARS), Madison, WI (United States). US Dairy Forage Research Center
Publication Date:
Research Org.:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER) (SC-23); National Institutes of Health (NIH); USDA
OSTI Identifier:
1454420
Grant/Contract Number:  
SC0008104; GM102756
Resource Type:
Accepted Manuscript
Journal Name:
BMC Genomics
Additional Journal Information:
Journal Volume: 15; Journal Issue: 1; Journal ID: ISSN 1471-2164
Publisher:
Springer
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; 59 BASIC BIOLOGICAL SCIENCES; Ruminococcus albus; Cellulose utilization; Ethanol production

Citation Formats

Christopherson, Melissa R., Dawson, John A., Stevenson, David M., Cunningham, Andrew C., Bramhacharya, Shanti, Weimer, Paul J., Kendziorski, Christina, and Suen, Garret. Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis. United States: N. p., 2014. Web. doi:10.1186/1471-2164-15-1066.
Christopherson, Melissa R., Dawson, John A., Stevenson, David M., Cunningham, Andrew C., Bramhacharya, Shanti, Weimer, Paul J., Kendziorski, Christina, & Suen, Garret. Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis. United States. doi:10.1186/1471-2164-15-1066.
Christopherson, Melissa R., Dawson, John A., Stevenson, David M., Cunningham, Andrew C., Bramhacharya, Shanti, Weimer, Paul J., Kendziorski, Christina, and Suen, Garret. Thu . "Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis". United States. doi:10.1186/1471-2164-15-1066. https://www.osti.gov/servlets/purl/1454420.
@article{osti_1454420,
title = {Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis},
author = {Christopherson, Melissa R. and Dawson, John A. and Stevenson, David M. and Cunningham, Andrew C. and Bramhacharya, Shanti and Weimer, Paul J. and Kendziorski, Christina and Suen, Garret},
abstractNote = {Bacteria in the genus Ruminococcus are ubiquitous members of the mammalian gastrointestinal tract. In particular, they are important in ruminants where they digest a wide range of plant cell wall polysaccharides. For example, Ruminococcus albus 7 is a primary cellulose degrader that produces acetate usable by its bovine host. Moreover, it is one of the few organisms that ferments cellulose to form ethanol at mesophilic temperatures in vitro. The mechanism of cellulose degradation by R. albus 7 is not well-defined and is thought to involve pilin-like proteins, unique carbohydrate-binding domains, a glycocalyx, and cellulosomes. We used a combination of comparative genomics, fermentation analyses, and transcriptomics to further clarify the cellulolytic and fermentative potential of R. albus 7. A comparison of the R. albus 7 genome sequence against the genome sequences of related bacteria that either encode or do not encode cellulosomes revealed that R. albus 7 does not encode for most canonical cellulosomal components. Fermentation analysis of R. albus 7 revealed the ability to produce ethanol and acetate on a wide range of fibrous substrates in vitro. Global transcriptomic analysis of R. albus 7 grown at identical dilution rates on cellulose and cellobiose in a chemostat showed that this bacterium, when growing on cellulose, utilizes a carbohydrate-degrading strategy that involves increased transcription of the rare carbohydrate-binding module (CBM) family 37 domain and the tryptophan biosynthetic operon. Our data suggest that R. albus 7 does not use canonical cellulosomal components to degrade cellulose, but rather up-regulates the expression of CBM37-containing enzymes and tryptophan biosynthesis. This study contributes to a revised model of carbohydrate degradation by this key member of the rumen ecosystem.},
doi = {10.1186/1471-2164-15-1066},
journal = {BMC Genomics},
number = 1,
volume = 15,
place = {United States},
year = {2014},
month = {12}
}

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Works referenced in this record:

Microbial Cellulose Utilization: Fundamentals and Biotechnology
journal, September 2002

  • Lynd, L. R.; Weimer, P. J.; van Zyl, W. H.
  • Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577
  • DOI: 10.1128/MMBR.66.3.506-577.2002