TY - JOUR
T1 - Unique aspects of fiber degradation by the ruminal ethanologen Ruminococcus albus 7 revealed by physiological and transcriptomic analysis
AU - Christopherson, Melissa R.
AU - Dawson, John A.
AU - Stevenson, David M.
AU - Cunningham, Andrew C.
AU - Bramhacharya, Shanti
AU - Weimer, Paul J.
AU - Kendziorski, Christina
AU - Suen, Garret
N1 - Funding Information:
This work was supported by a DOE BER Early Career Research Program Award DE–SC0008104 and funding from the Wisconsin Bioenergy Initiative to GS, an NIH award GM102756 to CK, and a USDA-Agricultural Research Service CRIS project 3655-41000-007-00D to PJW. MRC was supported by a DOE GLBRC/ BACTER Post-doctoral Research Fellowship. We thank J. M. Hackney for supplying glucomannan from Ochris tubers, P. Brumm for Soy polysaccharides, and members of the Suen lab for critical reading of the manuscript.
Publisher Copyright:
© 2014 Christopherson et al.
PY - 2014/12/4
Y1 - 2014/12/4
N2 - Background: 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. Here, we used a combination of comparative genomics, fermentation analyses, and transcriptomics to further clarify the cellulolytic and fermentative potential of R. albus 7. Results: 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. Conclusions: 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.
AB - Background: 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. Here, we used a combination of comparative genomics, fermentation analyses, and transcriptomics to further clarify the cellulolytic and fermentative potential of R. albus 7. Results: 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. Conclusions: 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.
KW - Cellulose utilization
KW - Ethanol production
KW - Ruminococcus albus
UR - http://www.scopus.com/inward/record.url?scp=84924292787&partnerID=8YFLogxK
U2 - 10.1186/1471-2164-15-1066
DO - 10.1186/1471-2164-15-1066
M3 - Article
C2 - 25477200
AN - SCOPUS:84924292787
VL - 15
JO - BMC Genomics
JF - BMC Genomics
SN - 1471-2164
IS - 1
M1 - 1066
ER -