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

被引:80
作者
Christopherson, Melissa R. [1 ]
Dawson, John A. [3 ]
Stevenson, David M. [2 ]
Cunningham, Andrew C. [1 ]
Bramhacharya, Shanti [1 ]
Weimer, Paul J. [1 ,2 ]
Kendziorski, Christina [3 ]
Suen, Garret [1 ]
机构
[1] Univ Wisconsin, Dept Bacteriol, Madison, WI 53706 USA
[2] USDA ARS, US Dairy Forage Res Ctr, Madison, WI 53706 USA
[3] Univ Wisconsin, Dept Biostat & Med Informat, Madison, WI 53706 USA
来源
BMC GENOMICS | 2014年 / 15卷
关键词
Ruminococcus albus; Cellulose utilization; Ethanol production; CARBOHYDRATE-BINDING MODULES; ALBUS; CELLULOSE; PROTEIN; FERMENTATION; ADHESION; EXPRESSION; BACTERIA; FAMILY; GENES;
D O I
10.1186/1471-2164-15-1066
中图分类号
Q81 [生物工程学(生物技术)]; Q93 [微生物学];
学科分类号
071005 ; 0836 ; 090102 ; 100705 ;
摘要
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.
引用
收藏
页数:13
相关论文
共 63 条
[1]   Differential expression analysis for sequence count data [J].
Anders, Simon ;
Huber, Wolfgang .
GENOME BIOLOGY, 2010, 11 (10)
[2]   Combined prediction of Tat and Sec signal peptides with hidden Markov models [J].
Bagos, Pantelis G. ;
Nikolaou, Elisanthi P. ;
Liakopoulos, Theodore D. ;
Tsirigos, Konstantinos D. .
BIOINFORMATICS, 2010, 26 (22) :2811-2817
[3]   Ruminococcus albus 8 mutants defective in cellulose degradation are deficient in two processive endocellulases, Cel48A and Cel9B, both of which possess a novel modular architecture [J].
Bevillard, E ;
Goodheart, DB ;
Karnati, SKR ;
Bayer, EA ;
Lamed, R ;
Miron, J ;
Nelson, KE ;
Morrison, M .
JOURNAL OF BACTERIOLOGY, 2004, 186 (01) :136-145
[4]   Ecology and Physiology of the Intestinal Tract [J].
Blaut, Michael .
BETWEEN PATHOGENICITY AND COMMENSALISM, 2013, 358 :247-272
[5]  
BRADFORD MM, 1976, ANAL BIOCHEM, V72, P248, DOI 10.1016/0003-2697(76)90527-3
[6]   The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics [J].
Cantarel, Brandi L. ;
Coutinho, Pedro M. ;
Rancurel, Corinne ;
Bernard, Thomas ;
Lombard, Vincent ;
Henrissat, Bernard .
NUCLEIC ACIDS RESEARCH, 2009, 37 :D233-D238
[7]   Effect of Phenotypic Residual Feed Intake and Dietary Forage Content on the Rumen Microbial Community of Beef Cattle [J].
Carberry, Ciara A. ;
Kenny, David A. ;
Han, Sukkyan ;
McCabe, Matthew S. ;
Waters, Sinead M. .
APPLIED AND ENVIRONMENTAL MICROBIOLOGY, 2012, 78 (14) :4949-4958
[8]   Assessment of metabolic diversity within the intestinal microbiota from healthy humans using combined molecular and cultural approaches [J].
Chassard, Christophe ;
Scott, Karen P. ;
Marquet, Perrine ;
Martin, Jennifer C. ;
Del'homme, Christophe ;
Dapoigny, Michel ;
Flint, Harry J. ;
Bernalier-Donadille, Annick .
FEMS MICROBIOLOGY ECOLOGY, 2008, 66 (03) :496-504
[9]   Feedback control of morphogenesis in fungi by aromatic alcohols [J].
Chen, H ;
Fink, GR .
GENES & DEVELOPMENT, 2006, 20 (09) :1150-1161
[10]   Improving Microbial Genome Annotations in an Integrated Database Context [J].
Chen, I-Min A. ;
Markowitz, Victor M. ;
Chu, Ken ;
Anderson, Iain ;
Mavromatis, Konstantinos ;
Kyrpides, Nikos C. ;
Ivanova, Natalia N. .
PLOS ONE, 2013, 8 (02)