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Title: The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading

Abstract

Background: Clostridium thermocellum is a model thermophilic organism for the production of biofuels from lignocellulosic substrates. The majority of publications studying the physiology of this organism use substrate concentrations of ≤10 g/L. However, industrially relevant concentrations of substrate start at 100 g/L carbohydrate, which corresponds to approximately 150 g/L solids. To gain insight into the physiology of fermentation of high substrate concentrations, we studied the growth on, and utilization of high concentrations of crystalline cellulose varying from 50 to 100 g/L by C. thermocellum. Results: Using a defined medium, batch cultures of C. thermocellum achieved 93% conversion of cellulose (Avicel) initially present at 100 g/L. The maximum rate of substrate utilization increased with increasing substrate loading. During fermentation of 100 g/L cellulose, growth ceased when about half of the substrate had been solubilized. However, fermentation continued in an uncoupled mode until substrate utilization was almost complete. In addition to commonly reported fermentation products, amino acids - predominantly L-valine and L-alanine - were secreted at concentrations up to 7.5 g/L. Uncoupled metabolism was also accompanied by products not documented previously for C. thermocellum, including isobutanol, meso- and RR/SS-2,3-butanediol and trace amounts of 3-methyl-1-butanol, 2-methyl-1-butanol and 1-propanol. We hypothesize that C. thermocellummore » uses overflow metabolism to balance its metabolism around the pyruvate node in glycolysis. In conclusion: C. thermocellum is able to utilize industrially relevant concentrations of cellulose, up to 93 g/L. We report here one of the highest degrees of crystalline cellulose utilization observed thus far for a pure culture of C. thermocellum, the highest maximum substrate utilization rate and the highest amount of isobutanol produced by a wild-type organism.« less

Authors:
 [1];  [2];  [1];  [3];  [4];  [4];  [5];  [6]
  1. Dartmouth College, Hanover, NH (United States). Thayer School of Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  2. Mascoma Corp., Lebanon, NH (United States)
  3. Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
  4. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
  5. Delft Univ. of Technology (Netherlands)
  6. Dartmouth College, Hanover, NH (United States). Thayer School of Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Mascoma Corp., Lebanon, NH (United States)
Publication Date:
Research Org.:
Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
Sponsoring Org.:
USDOE Office of Science (SC)
OSTI Identifier:
1163586
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Biotechnology for Biofuels
Additional Journal Information:
Journal Volume: 7; Journal Issue: 1; Journal ID: ISSN 1754-6834
Publisher:
BioMed Central
Country of Publication:
United States
Language:
English
Subject:
09 BIOMASS FUELS; Clostridium thermocellum; Cellulose fermentation; Isobutanol; 2,3-butanediol; Amino acids; High solids; Fusel alcohols

Citation Formats

Holwerda, Evert K., Thorne, Philip G., Olson, Daniel G., Amador-Noguez, Daniel, Engle, Nancy L., Tschaplinski, Timothy J., van Dijken, Johannes P., and Lynd, Lee R. The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading. United States: N. p., 2014. Web. doi:10.1186/s13068-014-0155-1.
Holwerda, Evert K., Thorne, Philip G., Olson, Daniel G., Amador-Noguez, Daniel, Engle, Nancy L., Tschaplinski, Timothy J., van Dijken, Johannes P., & Lynd, Lee R. The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading. United States. https://doi.org/10.1186/s13068-014-0155-1
Holwerda, Evert K., Thorne, Philip G., Olson, Daniel G., Amador-Noguez, Daniel, Engle, Nancy L., Tschaplinski, Timothy J., van Dijken, Johannes P., and Lynd, Lee R. Tue . "The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading". United States. https://doi.org/10.1186/s13068-014-0155-1. https://www.osti.gov/servlets/purl/1163586.
@article{osti_1163586,
title = {The exometabolome of Clostridium thermocellum reveals overflow metabolism at high cellulose loading},
author = {Holwerda, Evert K. and Thorne, Philip G. and Olson, Daniel G. and Amador-Noguez, Daniel and Engle, Nancy L. and Tschaplinski, Timothy J. and van Dijken, Johannes P. and Lynd, Lee R.},
abstractNote = {Background: Clostridium thermocellum is a model thermophilic organism for the production of biofuels from lignocellulosic substrates. The majority of publications studying the physiology of this organism use substrate concentrations of ≤10 g/L. However, industrially relevant concentrations of substrate start at 100 g/L carbohydrate, which corresponds to approximately 150 g/L solids. To gain insight into the physiology of fermentation of high substrate concentrations, we studied the growth on, and utilization of high concentrations of crystalline cellulose varying from 50 to 100 g/L by C. thermocellum. Results: Using a defined medium, batch cultures of C. thermocellum achieved 93% conversion of cellulose (Avicel) initially present at 100 g/L. The maximum rate of substrate utilization increased with increasing substrate loading. During fermentation of 100 g/L cellulose, growth ceased when about half of the substrate had been solubilized. However, fermentation continued in an uncoupled mode until substrate utilization was almost complete. In addition to commonly reported fermentation products, amino acids - predominantly L-valine and L-alanine - were secreted at concentrations up to 7.5 g/L. Uncoupled metabolism was also accompanied by products not documented previously for C. thermocellum, including isobutanol, meso- and RR/SS-2,3-butanediol and trace amounts of 3-methyl-1-butanol, 2-methyl-1-butanol and 1-propanol. We hypothesize that C. thermocellum uses overflow metabolism to balance its metabolism around the pyruvate node in glycolysis. In conclusion: C. thermocellum is able to utilize industrially relevant concentrations of cellulose, up to 93 g/L. We report here one of the highest degrees of crystalline cellulose utilization observed thus far for a pure culture of C. thermocellum, the highest maximum substrate utilization rate and the highest amount of isobutanol produced by a wild-type organism.},
doi = {10.1186/s13068-014-0155-1},
journal = {Biotechnology for Biofuels},
number = 1,
volume = 7,
place = {United States},
year = {Tue Oct 21 00:00:00 EDT 2014},
month = {Tue Oct 21 00:00:00 EDT 2014}
}

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Mechanisms of enhanced cellulosic bioethanol fermentation by co-cultivation of Clostridium and Thermoanaerobacter spp.
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Closing the carbon balance for fermentation by Clostridium thermocellum (ATCC 27405)
journal, January 2012


Biotechnological production of 2,3-butanediol—Current state and prospects
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Consolidated bioprocessing of cellulosic biomass: an update
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The Clostridium Thermocellum-Clostridium Thermosaccharolyticum Ethanol Production Process: Nutritional Studies and Scale-Down
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Ethanol from Cellulosic Biomass [and Discussion]
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Influence of Environment on the Content and Composition of Microbial Free Amino Acid Pools
journal, December 1970

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  • Journal of General Microbiology, Vol. 64, Issue 2
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Stability of Glutamine and Pyroglutamic Acid under Model System Conditions: Influence of Physical and Technological Factors
journal, November 1987


Stability of N-Acetylglutamine and Glutamine in Aqueous Solution and in a Liquid Nutritional Product by an Improved HPLC Method
journal, January 2002


Uptake and excretion of amino acids by saccharolytic clostridia
journal, March 1989


Isoprenoid quinone, cellular fatty acid composition and diaminopimelic acid isomers of newly classified thermophilic anaerobic Gram-positive bacteria
journal, April 1998


Development of pyrF-Based Genetic System for Targeted Gene Deletion in Clostridium thermocellum and Creation of a pta Mutant
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Fermentation of cellulose and cellobiose by Clostridium thermocellum in the absence of Methanobacterium thermoautotrophicum.
journal, January 1977


Chemically Defined Minimal Medium for Growth of the Anaerobic Cellulolytic Thermophile Clostridium thermocellum
journal, January 1981


Characterization of Clostridium thermocellum JW20
journal, January 1988

  • Freier, Doris; Mothershed, Cheryle P.; Wiegel, Juergen
  • Applied and Environmental Microbiology, Vol. 54, Issue 1
  • DOI: 10.1128/aem.54.1.204-211.1988

Enhanced Cellulose Fermentation by an Asporogenous and Ethanol-Tolerant Mutant of Clostridium thermocellum
journal, January 1989


Fermentation of Cellulosic Substrates in Batch and Continuous Culture by Clostridium thermocellum
journal, January 1989


Effect of Yeast Extract and Vitamin B12 on Ethanol Production from Cellulose by Clostridium thermocellum I-1-B
journal, January 1992


Clostridium thermocellum JW20 (ATCC 31549) is a coculture with Thermoanaerobacter ethanolicus.
journal, January 1997


Improvement of Cellulolytic Properties of Clostridium cellulolyticum by Metabolic Engineering
journal, January 2002


Role of the CipA Scaffoldin Protein in Cellulose Solubilization, as Determined by Targeted Gene Deletion and Complementation in Clostridium thermocellum
journal, November 2012

  • Olson, D. G.; Giannone, R. J.; Hettich, R. L.
  • Journal of Bacteriology, Vol. 195, Issue 4
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Adherence of Clostridium thermocellum to cellulose.
journal, January 1983


Formate synthesis by Clostridium thermocellum during anaerobic fermentation
journal, July 2006

  • Sparling, Richard; Islam, Rumana; Cicek, Nazim
  • Canadian Journal of Microbiology, Vol. 52, Issue 7
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The Cellulosomes: Multienzyme Machines for Degradation of Plant Cell Wall Polysaccharides
journal, October 2004


Works referencing / citing this record:

CO 2 -fixing one-carbon metabolism in a cellulose-degrading bacterium Clostridium thermocellum
journal, October 2016

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Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics
journal, April 2018

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  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1095-y

Specialized activities and expression differences for Clostridium thermocellum biofilm and planktonic cells
journal, February 2017

  • Dumitrache, Alexandru; Klingeman, Dawn M.; Natzke, Jace
  • Scientific Reports, Vol. 7, Issue 1
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Enhanced ethanol formation by Clostridium thermocellum via pyruvate decarboxylase
journal, October 2017


Metabolome analysis reveals a role for glyceraldehyde 3-phosphate dehydrogenase in the inhibition of C. thermocellum by ethanol
journal, November 2017

  • Tian, Liang; Perot, Skyler J.; Stevenson, David
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0961-3

Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring
journal, March 2017

  • Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
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Enhanced depolymerization and utilization of raw lignocellulosic material by co-cultures of Ruminiclostridium thermocellum with hemicellulose-utilizing partners
journal, April 2019

  • Froese, Alan; Schellenberg, John; Sparling, Richard
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Isotope-Assisted Metabolite Analysis Sheds Light on Central Carbon Metabolism of a Model Cellulolytic Bacterium Clostridium thermocellum
journal, August 2018


Biomass augmentation through thermochemical pretreatments greatly enhances digestion of switchgrass by Clostridium thermocellum
journal, August 2018

  • Kothari, Ninad; Holwerda, Evert K.; Cai, Charles M.
  • Biotechnology for Biofuels, Vol. 11, Issue 1
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Rex in Caldicellulosiruptor bescii : Novel regulon members and its effect on the production of ethanol and overflow metabolites
journal, April 2018

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Challenges and Advances for Genetic Engineering of Non-model Bacteria and Uses in Consolidated Bioprocessing
journal, October 2017


Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation
journal, December 2015

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  • Biotechnology for Biofuels, Vol. 8, Issue 1
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Metabolic and evolutionary responses of Clostridium thermocellum to genetic interventions aimed at improving ethanol production
journal, March 2020

  • Holwerda, Evert K.; Olson, Daniel G.; Ruppertsberger, Natalie M.
  • Biotechnology for Biofuels, Vol. 13, Issue 1
  • DOI: 10.1186/s13068-020-01680-5

Elimination of formate production in Clostridium thermocellum
journal, July 2015

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  • Journal of Industrial Microbiology & Biotechnology, Vol. 42, Issue 9
  • DOI: 10.1007/s10295-015-1644-3

Improved growth rate in Clostridium thermocellum hydrogenase mutant via perturbed sulfur metabolism
journal, January 2017

  • Biswas, Ranjita; Wilson, Charlotte M.; Giannone, Richard J.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-016-0684-x

Expressing the Thermoanaerobacterium saccharolyticum pforA in engineered Clostridium thermocellum improves ethanol production
journal, September 2018

  • Hon, Shuen; Holwerda, Evert K.; Worthen, Robert S.
  • Biotechnology for Biofuels, Vol. 11, Issue 1
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Simultaneous achievement of high ethanol yield and titer in Clostridium thermocellum
journal, June 2016


A metabolic and genomic assessment of sugar fermentation profiles of the thermophilic Thermotogales, Fervidobacterium pennivorans
journal, September 2018


Cellulose hydrolysis by Clostridium thermocellum is agnostic to substrate structural properties in contrast to fungal cellulases
journal, January 2019

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  • Green Chemistry, Vol. 21, Issue 10
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Development of a core Clostridium thermocellum kinetic metabolic model consistent with multiple genetic perturbations
journal, May 2017


Elimination of formate production in Clostridium thermocellum
journal, July 2015

  • Rydzak, Thomas; Lynd, Lee R.; Guss, Adam M.
  • Journal of Industrial Microbiology & Biotechnology, Vol. 42, Issue 9
  • DOI: 10.1007/s10295-015-1644-3

Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum
journal, February 2017

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  • Scientific Reports, Vol. 7, Issue 1
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Specialized activities and expression differences for Clostridium thermocellum biofilm and planktonic cells
journal, February 2017

  • Dumitrache, Alexandru; Klingeman, Dawn M.; Natzke, Jace
  • Scientific Reports, Vol. 7, Issue 1
  • DOI: 10.1038/srep43583

Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation
journal, December 2015

  • Sander, Kyle; Wilson, Charlotte M.; Rodriguez, Miguel
  • Biotechnology for Biofuels, Vol. 8, Issue 1
  • DOI: 10.1186/s13068-015-0394-9

Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring
journal, March 2017

  • Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0756-6

Development of a core Clostridium thermocellum kinetic metabolic model consistent with multiple genetic perturbations
journal, May 2017


The effect of switchgrass loadings on feedstock solubilization and biofuel production by Clostridium thermocellum
journal, November 2017

  • Verbeke, Tobin J.; Garcia, Gabriela M.; Elkins, James G.
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0917-7

Metabolome analysis reveals a role for glyceraldehyde 3-phosphate dehydrogenase in the inhibition of C. thermocellum by ethanol
journal, November 2017

  • Tian, Liang; Perot, Skyler J.; Stevenson, David
  • Biotechnology for Biofuels, Vol. 10, Issue 1
  • DOI: 10.1186/s13068-017-0961-3

Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics
journal, April 2018

  • Whitham, Jason M.; Moon, Ji-Won; Rodriguez, Miguel
  • Biotechnology for Biofuels, Vol. 11, Issue 1
  • DOI: 10.1186/s13068-018-1095-y

Metabolic and evolutionary responses of Clostridium thermocellum to genetic interventions aimed at improving ethanol production
journal, March 2020

  • Holwerda, Evert K.; Olson, Daniel G.; Ruppertsberger, Natalie M.
  • Biotechnology for Biofuels, Vol. 13, Issue 1
  • DOI: 10.1186/s13068-020-01680-5

Challenges and Advances for Genetic Engineering of Non-model Bacteria and Uses in Consolidated Bioprocessing
journal, October 2017


Isotope-Assisted Metabolite Analysis Sheds Light on Central Carbon Metabolism of a Model Cellulolytic Bacterium Clostridium thermocellum
journal, August 2018