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Comparative Analysis of Extremely Thermophilic Caldicellulosiruptor Species Reveals Common and Unique Cellular Strategies for Plant Biomass Utilization

Journal Article · · Applied and Environmental Microbiology
DOI:https://doi.org/10.1128/AEM.01622-15· OSTI ID:1335326
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  1. North Carolina State Univ., Raleigh, NC (United States)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  3. Univ. of Georgia, Athens, GA (United States)

Microbiological, genomic and transcriptomic analyses were used to examine three species from the bacterial genus Caldicellulosiruptor with respect to their capacity to convert the carbohydrate content of lignocellulosic biomass at 70 degrees C to simple sugars, acetate, lactate, CO2, and H-2. Caldicellulosiruptor bescii, C. kronotskyensis, and C. saccharolyticus solubilized 38%, 36%, and 29% (by weight) of unpretreated switchgrass (Panicum virgatum) (5 g/liter), respectively, which was about half of the amount of crystalline cellulose (Avicel; 5 g/liter) that was solubilized under the same conditions. The lower yields with C. saccharolyticus, not appreciably greater than the thermal control for switchgrass, were unexpected, given that its genome encodes the same glycoside hydrolase 9 (GH9)-GH48 multidomain cellulase (CelA) found in the other two species. However, the genome of C. saccharolyticus lacks two other cellulases with GH48 domains, which could be responsible for its lower levels of solubilization. Transcriptomes for growth of each species comparing cellulose to switchgrass showed that many carbohydrate ABC transporters and multidomain extracellular glycoside hydrolases were differentially regulated, reflecting the heterogeneity of lignocellulose. However, significant differences in transcription levels for conserved genes among the three species were noted, indicating unexpectedly diverse regulatory strategies for deconstruction for these closely related bacteria. Genes encoding the Che-type chemotaxis system and flagellum biosynthesis were upregulated in C. kronotskyensis and C. bescii during growth on cellulose, implicating motility in substrate utilization. The results here show that capacity for plant biomass deconstruction varies across Caldicellulosiruptor species and depends in a complex way on GH genome inventory, substrate composition, and gene regulation.

Research Organization:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
Sponsoring Organization:
USDOE
DOE Contract Number:
AC05-00OR22725
OSTI ID:
1335326
Journal Information:
Applied and Environmental Microbiology, Journal Name: Applied and Environmental Microbiology Journal Issue: 20 Vol. 81; ISSN 0099-2240
Publisher:
American Society for Microbiology
Country of Publication:
United States
Language:
English

References (55)

Compositional Analysis of Water-Soluble Materials in Switchgrass journal March 2010
Complete Genome Sequences for the Anaerobic, Extremely Thermophilic Plant Biomass-Degrading Bacteria Caldicellulosiruptor hydrothermalis, Caldicellulosiruptor kristjanssonii, Caldicellulosiruptor kronotskyensis, Caldicellulosiruptor owensensis, and Caldicellulosiruptor lactoaceticus journal January 2011
Description of Caldicellulosiruptor saccharolyticus gen. nov., sp. nov: An obligately anaerobic, extremely thermophilic, cellulolytic bacterium journal July 1994
Deletion of Caldicellulosiruptor besciiCelA reveals its crucial role in the deconstruction of lignocellulosic biomass journal October 2014
Glycolytic pathway and hydrogen yield studies of the extreme thermophile Caldicellulosiruptor saccharolyticus journal January 2007
The c-di-GMP Binding Protein YcgR Controls Flagellar Motor Direction and Speed to Affect Chemotaxis by a “Backstop Brake” Mechanism journal April 2010
S-Layer Homology Domain Proteins Csac_0678 and Csac_2722 Are Implicated in Plant Polysaccharide Deconstruction by the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus journal December 2011
Pectin structure and biosynthesis journal June 2008
Caldicellulosiruptor kronotskyensis sp. nov. and Caldicellulosiruptor hydrothermalis sp. nov., two extremely thermophilic, cellulolytic, anaerobic bacteria from Kamchatka thermal springs journal June 2008
Evidence for Cyclic Di-GMP-Mediated Signaling in Bacillus subtilis journal July 2012
Complete Genome Sequence of the Cellulolytic Thermophile Caldicellulosiruptor obsidiansis OB47T journal September 2010
Glycoside hydrolase inventory drives plant polysaccharide deconstruction by the extremely thermophilic bacterium Caldicellulosiruptor saccharolyticus journal March 2011
Structural basis of activity and allosteric control of diguanylate cyclase journal November 2004
Genome Sequence of the Anaerobic, Thermophilic, and Cellulolytic Bacterium "Anaerocellum thermophilum" DSM 6725 journal April 2009
Diversity in Chemotaxis Mechanisms among the Bacteria and Archaea journal June 2004
Revealing Nature's Cellulase Diversity The Digestion Mechanism of Caldicellulosiruptor bescii CelA journal December 2013
Label-free Quantitative Proteomics for the Extremely Thermophilic Bacterium Caldicellulosiruptor obsidiansis Reveal Distinct Abundance Patterns upon Growth on Cellobiose, Crystalline Cellulose, and Switchgrass journal December 2011
Caldicellulosiruptor owensensis sp. nov., an anaerobic, extremely thermophilic, xylanolytic bacterium journal January 1998
Phylogenetic, Microbiological, and Glycoside Hydrolase Diversities within the Extremely Thermophilic, Plant Biomass-Degrading Genus Caldicellulosiruptor journal October 2010
Evaluation of assimilatory sulphur metabolism in Caldicellulosiruptor saccharolyticus journal October 2014
Microbial carbohydrate esterases deacetylating plant polysaccharides journal November 2012
Isolation and characterization of Caldicellulosiruptor lactoaceticus sp. nov., an extremely thermophilic, cellulolytic, anaerobic bacterium journal March 1995
Search and clustering orders of magnitude faster than BLAST journal August 2010
The carbohydrate-active enzymes database (CAZy) in 2013 journal November 2013
Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal journal July 2010
Sugar transport in (hyper)thermophilic archaea journal March 2002
Caldicellulosiruptor Core and Pangenomes Reveal Determinants for Noncellulosomal Thermophilic Deconstruction of Plant Biomass journal May 2012
Carbohydrate Utilization Patterns for the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus Reveal Broad Growth Substrate Preferences journal October 2009
Bacterial Chemotaxis and the Molecular Logic of Intracellular Signal Transduction Networks journal June 1991
Degradation of high loads of crystalline cellulose and of unpretreated plant biomass by the thermophilic bacterium Caldicellulosiruptor bescii journal January 2014
Influence of Extractives on the Analysis of Herbaceous Biomass journal February 1997
Activation of the Diguanylate Cyclase PleD by Phosphorylation-mediated Dimerization journal July 2007
Caldicellulosiruptor obsidiansis sp. nov., an Anaerobic, Extremely Thermophilic, Cellulolytic Bacterium Isolated from Obsidian Pool, Yellowstone National Park journal December 2009
The role of FeS clusters for molybdenum cofactor biosynthesis and molybdoenzymes in bacteria journal June 2015
Use of Label-Free Quantitative Proteomics To Distinguish the Secreted Cellulolytic Systems of Caldicellulosiruptor bescii and Caldicellulosiruptor obsidiansis journal April 2011
fSpatial and temporal dynamics of cellulose degradation and biofilm formation by Caldicellulosiruptor obsidiansis and Clostridium thermocellum journal January 2011
Mathematical modeling of hydrolysate diffusion and utilization in cellulolytic biofilms of the extreme thermophile Caldicellulosiruptor obsidiansis journal February 2011
Substrate and product inhibition of hydrogen production by the extreme thermophile,Caldicellulosiruptor saccharolyticus journal December 2002
The PilZ Domain Is a Receptor for the Second Messenger c-di-GMP journal August 2006
Classification of 'Anaerocellum thermophilum' strain DSM 6725 as Caldicellulosiruptor bescii sp. nov. journal October 2009
Thermophilic lignocellulose deconstruction journal May 2014
Cyclic Di-GMP Riboswitch-Regulated Type IV Pili Contribute to Aggregation of Clostridium difficile journal December 2014
Colorimetric Method for Determination of Sugars and Related Substances journal March 1956
Deletion of a gene cluster encoding pectin degrading enzymes in Caldicellulosiruptor bescii reveals an important role for pectin in plant biomass recalcitrance journal October 2014
Uronic polysaccharide degrading enzymes journal October 2014
Direct conversion of plant biomass to ethanol by engineered Caldicellulosiruptor bescii journal June 2014
Regulation of flagellar motility during biofilm formation journal November 2013
Discrete and Structurally Unique Proteins (Tāpirins) Mediate Attachment of Extremely Thermophilic Caldicellulosiruptor Species to Cellulose journal February 2015
Biofilm formation by designed co-cultures of Caldicellulosiruptor species as a means to improve hydrogen productivity journal January 2015
Heat Shock Response by the Hyperthermophilic Archaeon Pyrococcus furiosus journal April 2003
Hydrogenomics of the Extremely Thermophilic Bacterium Caldicellulosiruptor saccharolyticus journal September 2008
Carbohydrate and lignin are simultaneously solubilized from unpretreated switchgrass by microbial action at high temperature journal January 2013
Principles of c-di-GMP signalling in bacteria journal April 2009
Novel domains of the prokaryotic two-component signal transduction systems journal September 2001
A chemosensory system that regulates biofilm formation through modulation of cyclic diguanylate levels journal September 2005

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