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Title: Dramatic performance of Clostridium thermocellum explained by its wide range of cellulase modalities

Journal Article · · Science Advances
 [1];  [2];  [1];  [3];  [1];  [1];  [4];  [4];  [5];  [1];  [4];  [4];  [5];  [6];  [1];  [1]
  1. National Renewable Energy Lab. (NREL), Golden, CO (United States); BioEnergy Science Center, Oak Ridge, TN (United States)
  2. BioEnergy Science Center, Oak Ridge, TN (United States); National Renewable Energy Lab. (NREL), Golden, CO (United States)
  3. National Renewable Energy Lab. (NREL), Golden, CO (United States)
  4. BioEnergy Science Center, Oak Ridge, TN (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States)
  5. BioEnergy Science Center, Oak Ridge, TN (United States); Dartmouth College, Hanover, NH (United States)
  6. The Weizmann Institute of Science, Rehovot (Israel)

Clostridium thermocellum is the most efficient microorganism for solubilizing lignocellulosic biomass known to date. Its high cellulose digestion capability is attributed to efficient cellulases consisting of both a free-enzyme system and a tethered cellulosomal system wherein carbohydrate active enzymes (CAZymes) are organized by primary and secondary scaffoldin proteins to generate large protein complexes attached to the bacterial cell wall. This study demonstrates that C. thermocellum also uses a type of cellulosomal system not bound to the bacterial cell wall, called the “cell-free” cellulosomal system. The cell-free cellulosome complex can be seen as a “long range cellulosome” because it can diffuse away from the cell and degrade polysaccharide substrates remotely from the bacterial cell. The contribution of these two types of cellulosomal systems in C. thermocellum was elucidated by characterization of mutants with different combinations of scaffoldin gene deletions. The primary scaffoldin, CipA, was found to play the most important role in cellulose degradation by C. thermocellum, whereas the secondary scaffoldins have less important roles. Additionally, the distinct and efficient mode of action of the C. thermocellum exoproteome, wherein the cellulosomes splay or divide biomass particles, changes when either the primary or secondary scaffolds are removed, showing that the intact wild-type cellulosomal system is necessary for this essential mode of action. This new transcriptional and proteomic evidence shows that a functional primary scaffoldin plays a more important role compared to secondary scaffoldins in the proper regulation of CAZyme genes, cellodextrin transport, and other cellular functions.

Research Organization:
National Renewable Energy Laboratory (NREL), Golden, CO (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Sponsoring Organization:
USDOE Office of Science (SC); USDOE Bioenergy Science Center (BESC)
Grant/Contract Number:
AC36-08GO28308; AC05-00OR22725
OSTI ID:
1244830
Alternate ID(s):
OSTI ID: 1286890
Report Number(s):
NREL/JA-2700-65384
Journal Information:
Science Advances, Vol. 2, Issue 2; ISSN 2375-2548
Publisher:
AAASCopyright Statement
Country of Publication:
United States
Language:
English
Citation Metrics:
Cited by: 74 works
Citation information provided by
Web of Science

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Genomics-informed isolation and characterization of a symbiotic Nanoarchaeota system from a terrestrial geothermal environment journal July 2016
Cellulosomes: bacterial nanomachines for dismantling plant polysaccharides journal December 2016
Structural basis of cell wall anchoring by SLH domains in Paenibacillus alvei journal August 2018
Identification of endoxylanase XynE from Clostridium thermocellum as the first xylanase of glycoside hydrolase family GH141 journal September 2017
Regulation of biomass degradation by alternative σ factors in cellulolytic clostridia journal July 2018
Specialized activities and expression differences for Clostridium thermocellum biofilm and planktonic cells journal February 2017
Cellulosomes localise on the surface of membrane vesicles from the cellulolytic bacterium Clostridium thermocellum journal June 2019
Inducing effects of cellulosic hydrolysate components of lignocellulose on cellulosome synthesis in Clostridium thermocellum journal June 2018
Unique genetic cassettes in a Thermoanaerobacterium contribute to simultaneous conversion of cellulose and monosugars into butanol journal March 2018
The effects of micronutrient deficiencies on bacterial species from the human gut microbiota journal May 2017
Temporal proteome dynamics of Clostridium cellulovorans cultured with major plant cell wall polysaccharides journal June 2019
Integrated omics analyses reveal the details of metabolic adaptation of Clostridium thermocellum to lignocellulose-derived growth inhibitors released during the deconstruction of switchgrass journal January 2017
Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring journal March 2017
The LacI family protein GlyR3 co-regulates the celC operon and manB in Clostridium thermocellum journal June 2017
Unique organization and unprecedented diversity of the Bacteroides (Pseudobacteroides) cellulosolvens cellulosome system journal September 2017
How does cellulosome composition influence deconstruction of lignocellulosic substrates in Clostridium (Ruminiclostridium) thermocellum DSM 1313? journal September 2017
Adding tetrahydrofuran to dilute acid pretreatment provides new insights into substrate changes that greatly enhance biomass deconstruction by Clostridium thermocellum and fungal enzymes journal November 2017
Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics journal April 2018
An iterative computational design approach to increase the thermal endurance of a mesophilic enzyme journal July 2018
Optimizing the composition of a synthetic cellulosome complex for the hydrolysis of softwood pulp: identification of the enzymatic core functions and biochemical complex characterization journal August 2018
Multiple levers for overcoming the recalcitrance of lignocellulosic biomass journal January 2019
Unraveling essential cellulosomal components of the (Pseudo)Bacteroides cellulosolvens reveals an extensive reservoir of novel catalytic enzymes journal May 2019
Characterization of a leukocidin identified in Staphylococcus pseudintermedius journal September 2018
Substrate-Related Factors Affecting Cellulosome-Induced Hydrolysis for Lignocellulose Valorization journal July 2019
Simultaneous achievement of high ethanol yield and titer in Clostridium thermocellum journal June 2016
Efficient whole-cell-catalyzing cellulose saccharification using engineered Clostridium thermocellum journal May 2017
The Cellulosome Paradigm in An Extreme Alkaline Environment journal September 2019