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

Journal Article · · BMC Genomics
 [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

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.

Research Organization:
Univ. of Wisconsin, Madison, WI (United States)
Sponsoring Organization:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Institutes of Health (NIH); USDA
Grant/Contract Number:
SC0008104; GM102756
OSTI ID:
1454420
Journal Information:
BMC Genomics, Vol. 15, Issue 1; ISSN 1471-2164
Publisher:
SpringerCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 61 works
Citation information provided by
Web of Science

References (64)

EBSeq: an empirical Bayes hierarchical model for inference in RNA-seq experiments journal February 2013
Characterization of the Cellulolytic Complex (Cellulosome) from Ruminococcus albus journal January 2000
Design and validation of 16S rRNA probes to enumerate members of the Clostridium leptum subgroup in human faecal microbiota journal July 2005
Complete Genome of the Cellulolytic Ruminal Bacterium Ruminococcus albus 7 journal September 2011
Improving Microbial Genome Annotations in an Integrated Database Context journal February 2013
Fermentation of a Bacterial Cellulose/Xylan Composite by Mixed Ruminal Microflora:  Implications for the Role of Polysaccharide Matrix Interactions in Plant Cell Wall Biodegradability journal May 2000
Fast and accurate short read alignment with Burrows-Wheeler transform journal May 2009
Combined prediction of Tat and Sec signal peptides with hidden Markov models journal September 2010
Differential expression analysis for sequence count data journal October 2010
Populations of Select Cultured and Uncultured Bacteria in the Rumen of Sheep and the Effect of Diets and Ruminal Fractions journal January 2011
A human gut microbial gene catalogue established by metagenomic sequencing journal March 2010
Adherence of the Gram-Positive BacteriumRuminococcus albus to Cellulose and Identification of a Novel Form of Cellulose-Binding Protein Which Belongs to the Pil Family of Proteins journal November 1998
Feedback control of morphogenesis in fungi by aromatic alcohols journal May 2006
Polysaccharide utilization by gut bacteria: potential for new insights from genomic analysis journal February 2008
Colorimetric Method for Determination of Sugars and Related Substances journal March 1956
Cell Surface Enzyme Attachment Is Mediated by Family 37 Carbohydrate-Binding Modules, Unique to Ruminococcus albus journal October 2008
Salinity tolerance mechanisms of an Arctic Pelagophyte using comparative transcriptomic and gene expression analysis journal May 2022
Fermentation of Insoluble Cellulose by Continuous Cultures of Ruminococcus albus journal November 1988
Diversity and Strain Specificity of Plant Cell Wall Degrading Enzymes Revealed by the Draft Genome of Ruminococcus flavefaciens FD-1 journal August 2009
PICRUSt2 for prediction of metagenome functions journal June 2020
The leucine-rich repeat as a protein recognition motif journal December 2001
The Complete Genome Sequence of Fibrobacter succinogenes S85 Reveals a Cellulolytic and Metabolic Specialist journal April 2011
BESC knowledgebase public portal journal January 2012
Rumen Cellulosomics: Divergent Fiber-Degrading Strategies Revealed by Comparative Genome-Wide Analysis of Six Ruminococcal Strains journal July 2014
NMR study of cellulose and wheat straw degradation by Ruminococcus albus 20: Degradation of wheat straw by R. albus journal June 2008
Dominant and diet-responsive groups of bacteria within the human colonic microbiota journal August 2010
Identification of target genes conferring ethanol stress tolerance to Saccharomyces cerevisiae based on DNA microarray data analysis journal August 2007
Genome analyses highlight the different biological roles of cellulases journal January 2012
Assessment of metabolic diversity within the intestinal microbiota from healthy humans using combined molecular and cultural approaches: Metabolic diversity of gut microbiota from healthy humans journal December 2008
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 journal December 2003
An efficient algorithm for large-scale detection of protein families journal April 2002
Adhesion to cellulose by Ruminococcus albus: a combination of cellulosomes and Pil-proteins? journal April 2000
Phylogenetic diversity of bacterial communities in bovine rumen as affected by diets and microenvironments journal September 2011
Copaifera spp. oleoresins impair Toxoplasma gondii infection in both human trophoblastic cells and human placental explants journal September 2020
Noncellulosomal cohesin- and dockerin-like modules in the three domains of life journal February 2009
Kinetics of Cellulose Digestion by Fibrobacter succinogenes S85. journal January 1997
pH dynamics and bacterial community composition in the rumen of lactating dairy cows journal January 2010
Specialized cell surface structures in cellulolytic bacteria. journal August 1987
Ultrastructure and adhesion properties of Ruminococcus albus journal April 1975
Bacteria, Colonic Fermentation, and Gastrointestinal Health journal January 2012
Global Gene Expression Patterns in Clostridium thermocellum as Determined by Microarray Analysis of Chemostat Cultures on Cellulose or Cellobiose journal December 2010
Studies of the Extracellular Glycocalyx of the Anaerobic Cellulolytic Bacterium Ruminococcus albus 7 journal October 2006
Targeted A-to-G base editing of chloroplast DNA in plants journal December 2022
Cellulosomes: Highly Efficient Nanomachines Designed to Deconstruct Plant Cell Wall Complex Carbohydrates journal June 2010
Bioconductor : open software development for computational biology and bioinformatics text January 2004
Sequence of egV and Properties of EgV, a Ruminococcus albus Endoglucanase Containing a Dockerin Domain journal January 2000
Subcellular distribution of glycanases and related components in Ruminococcus albus SY3 and their role in cell adhesion to cellulose journal October 2001
Expression of 17 Genes in Clostridium thermocellum ATCC 27405 during Fermentation of Cellulose or Cellobiose in Continuous Culture journal August 2005
Effect of Phenotypic Residual Feed Intake and Dietary Forage Content on the Rumen Microbial Community of Beef Cattle journal May 2012
Microbial Cellulose Utilization: Fundamentals and Biotechnology journal September 2002
Unconventional Mode of Attachment of the Ruminococcus flavefaciens Cellulosome to the Cell Surface journal November 2005
Adhesion to cellulose by Ruminococcus albus : a combination of cellulosomes and Pil-proteins? journal April 2000
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding journal May 1976
Dominance of Prevotella and low abundance of classical ruminal bacterial species in the bovine rumen revealed by relative quantification real-time PCR journal January 2007
Effect of 3-Phenylpropanoic Acid on Capsule and Cellulases of Ruminococcus albus 8 journal July 1984
Bioconductor: open software development for computational biology and bioinformatics journal September 2004
A novel family of carbohydrate-binding modules identified with Ruminococcus albus proteins journal April 2004
The Carbohydrate-Active EnZymes database (CAZy): an expert resource for Glycogenomics journal January 2009
InterPro: the integrative protein signature database journal January 2009
Proteome‐wide systems analysis of a cellulosic biofuel‐producing microbe journal January 2011
The Ruminococcus albus pilA1-pilA2 locus: expression and putative role of two adjacent pil genes in pilus formation and bacterial adhesion to cellulose journal April 2005
A segmented gas/liquid delivery system for continuous culture of microorganisms on insoluble substrates and its use for growth of Ruminococcus flavefaciens on cellulose journal November 1991
Competition among three predominant ruminal cellulolytic bacteria in the absence or presence of non-cellulolytic bacteria journal January 2001
Measurement of carboxymethylcellulase activity journal September 1960

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Response of Gut Microbiota to Dietary Fiber and Metabolic Interaction With SCFAs in Piglets journal September 2018
Regulatory Properties of the ADP-Glucose Pyrophosphorylase from the Clostridial Firmicutes Member Ruminococcus albus journal June 2018
The Ruminococci: key symbionts of the gut ecosystem journal February 2018
Comparing the Microbial Community in Four Stomach of Dairy Cattle, Yellow Cattle and Three Yak Herds in Qinghai-Tibetan Plateau journal July 2019
Bacterial colonisation of reeds and cottonseed hulls in the rumen of Tarim red deer (Cervus elaphus yarkandensis) journal April 2019
Regulation of CD4+CD8−CD25+ and CD4+CD8+CD25+ T cells by gut microbiota in chicken journal June 2018
Zinc AA supplementation alters yearling ram rumen bacterial communities but zinc sulfate supplementation does not1 journal December 2018
Intestinal permeability in the pathogenesis of liver damage: From non-alcoholic fatty liver disease to liver transplantation journal September 2019
Taxonomic and functional assessment using metatranscriptomics reveals the effect of Angus cattle on rumen microbial signatures journal October 2019
Enhancing the Resolution of Rumen Microbial Classification from Metatranscriptomic Data Using Kraken and Mothur journal December 2017
Progressive Colonization of Bacteria and Degradation of Rice Straw in the Rumen by Illumina Sequencing journal November 2017
Sequence-based analysis of the genus Ruminococcus resolves its phylogeny and reveals strong host association journal December 2016
Redundancy, resilience, and host specificity of the ruminal microbiota: implications for engineering improved ruminal fermentations journal April 2015
The severity of nonalcoholic fatty liver disease is associated with gut dysbiosis and shift in the metabolic function of the gut microbiota: Boursier et al. journal January 2016
The Planktonic Core Microbiome and Core Functions in the Cattle Rumen by Next Generation Sequencing journal September 2018