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

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.

doi:10.1186/s13068-014-0155-1

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

Journal Article · Tue Oct 21 00:00:00 EDT 2014 · Biotechnology for Biofuels

DOI:https://doi.org/10.1186/s13068-014-0155-1· OSTI ID:1163586

Holwerda, Evert K. ^[1]; Thorne, Philip G. ^[2]; Olson, Daniel G. ^[1]; Amador-Noguez, Daniel ^[3]; Engle, Nancy L. ^[4]; Tschaplinski, Timothy J. ^[4]; van Dijken, Johannes P. ^[5]; Lynd, Lee R. ^[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)
Univ. of Wisconsin, Madison, WI (United States). Dept. of Bacteriology
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
Delft Univ. of Technology (Netherlands)
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)

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.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)

Sponsoring Organization:: USDOE Office of Science (SC)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1163586

Journal Information:: Biotechnology for Biofuels, Vol. 7, Issue 1; ISSN 1754-6834

Publisher:: BioMed CentralCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 74 works

Citation information provided by
Web of Science

References (79)

The Cellulosomes: Multienzyme Machines for Degradation of Plant Cell Wall Polysaccharides Bayer, Edward A.; Belaich, Jean-Pierre; Shoham, Yuval Annual Review of Microbiology, Vol. 58, Issue 1 https://doi.org/10.1146/annurev.micro.57.030502.091022	journal	October 2004
Cellulose Catabolism by Clostridium cellulolyticum Growing in Batch Culture on Defined Medium Desvaux, M.; Guedon, E.; Petitdemange, H. Applied and Environmental Microbiology, Vol. 66, Issue 6 https://doi.org/10.1128/AEM.66.6.2461-2470.2000	journal	June 2000
Biotechnological production of 2,3-butanediol—Current state and prospects Celińska, E.; Grajek, W. Biotechnology Advances, Vol. 27, Issue 6 https://doi.org/10.1016/j.biotechadv.2009.05.002	journal	November 2009
The production of extracellular amino acids by rumen bacteria Stevenson, I. L. Canadian Journal of Microbiology, Vol. 24, Issue 10 https://doi.org/10.1139/m78-198	journal	October 1978
Formation of l-alanine as a reduced end product in carbohydrate fermentation by the hyperthermophilic archaeon Pyrococcus furiosus Kengen, Serv� W. M.; Stams, Alfons J. M. Archives of Microbiology, Vol. 161, Issue 2 https://doi.org/10.1007/s002030050038	journal	February 1994
Ethanol Production by Thermophilic Bacteria: Relationship Between Fermentation Product Yields of and Catabolic Enzyme Activities in Clostridium thermocellum and Thermoanaerobium brockii Lamed, R.; Zeikus, J. G. Journal of Bacteriology, Vol. 144, Issue 2 https://doi.org/10.1128/JB.144.2.569-578.1980	journal	January 1980
KEGG: Kyoto Encyclopedia of Genes and Genomes Kanehisa, Minoru; Goto, Susumu Nucleic Acids Research, Vol. 28, Issue 1, p. 27-30 https://doi.org/10.1093/nar/28.1.27	journal	January 2000
Xylitol production from corn fiber and sugarcane bagasse hydrolysates by Candida tropicalis Rao, R. Sreenivas; Jyothi, Ch. Pavana; Prakasham, R. S. Bioresource Technology, Vol. 97, Issue 15 https://doi.org/10.1016/j.biortech.2005.08.015	journal	October 2006
Characterization of Clostridium thermocellum strains with disrupted fermentation end-product pathways van der Veen, Douwe; Lo, Jonathan; Brown, Steven D. Journal of Industrial Microbiology & Biotechnology, Vol. 40, Issue 7 https://doi.org/10.1007/s10295-013-1275-5	journal	May 2013
Consolidated bioprocessing of cellulosic biomass: an update Lynd, Lee R.; van Zyl, Willem H.; McBride, John E. Current Opinion in Biotechnology, Vol. 16, Issue 5, p. 577-583 https://doi.org/10.1016/j.copbio.2005.08.009	journal	October 2005
An agr Quorum Sensing System That Regulates Granulose Formation and Sporulation in Clostridium acetobutylicum Steiner, Elisabeth; Scott, Jamie; Minton, Nigel P. Applied and Environmental Microbiology, Vol. 78, Issue 4 https://doi.org/10.1128/AEM.06376-11	journal	December 2011
Metabolic Engineering of Clostridium cellulolyticum for Production of Isobutanol from Cellulose Higashide, Wendy; Li, Yongchao; Yang, Yunfeng Applied and Environmental Microbiology, Vol. 77, Issue 8 https://doi.org/10.1128/AEM.02454-10	journal	March 2011
Evaluation of ethanol productivity from cellulose by clostridium thermocellum Kurose, Naotaka; Yagyu, Junji; Miyazaki, Takayuki Journal of Fermentation Technology, Vol. 64, Issue 5 https://doi.org/10.1016/0385-6380(86)90033-6	journal	October 1986
Uptake and excretion of amino acids by saccharolytic clostridia Szech, Ulrike; Braun, Manfred; Kleiner, Diethelm FEMS Microbiology Letters, Vol. 58, Issue 1 https://doi.org/10.1111/j.1574-6968.1989.tb03009.x	journal	March 1989
Enzyme-microbe synergy during cellulose hydrolysis by Clostridium thermocellum Lu, Y.; Zhang, Y. -H. P.; Lynd, L. R. Proceedings of the National Academy of Sciences, Vol. 103, Issue 44 https://doi.org/10.1073/pnas.0605381103	journal	October 2006
Investigation of the ethanol tolerance of Clostridium thermosaccharolyticum in continuous culture Baskaran, Sunitha; Ahn, Hyung-Jun; Lynd, Lee R. Biotechnology Progress, Vol. 11, Issue 3 https://doi.org/10.1021/bp00033a006	journal	May 1995
Carbohydrate utilization by Clostridium thermocellum: Importance of internal pH in regulating growth Nochur, Saraswathy V.; Demain, Arnold L.; Roberts, Mary F. Enzyme and Microbial Technology, Vol. 14, Issue 5 https://doi.org/10.1016/0141-0229(92)90001-5	journal	May 1992
Salt Accumulation Resulting from Base Added for pH Control, and Not Ethanol, Limits Growth of Thermoanaerobacterium thermosaccharolyticum HG-8 at Elevated Feed Xylose Concentrations in Continuous Culture Lynd, L. R.; Baskaran, S.; Casten, S. Biotechnology Progress, Vol. 17, Issue 1 https://doi.org/10.1021/bp000158n	journal	February 2001
The Characteristics of Clostridium Thermocellum1 McBee, R. H. Journal of Bacteriology, Vol. 67, Issue 4 https://doi.org/10.1128/JB.67.4.505-506.1954	journal	January 1954
Studies on cellulase production by Clostridium thermocellum Garcia-Martinez, D. V.; Shinmyo, A.; Madia, A. European Journal of Applied Microbiology and Biotechnology, Vol. 9, Issue 3 https://doi.org/10.1007/BF00504485	journal	January 1980
Stability of N-Acetylglutamine and Glutamine in Aqueous Solution and in a Liquid Nutritional Product by an Improved HPLC Method Snowden, M. K.; Baxter, J. H.; Mamula Bergana, M. Journal of Food Science, Vol. 67, Issue 1 https://doi.org/10.1111/j.1365-2621.2002.tb11415.x	journal	January 2002
Direct glucose production from lignocellulose using Clostridium thermocellum cultures supplemented with a thermostable β-glucosidase Prawitwong, Panida; Waeonukul, Rattiya; Tachaapaikoon, Chakrit Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-184	journal	January 2013
Optimization of Clostridium thermocellum growth on cellulose and pretreated wood substrates Saddler, J. N.; Chan, M. K. -H. European Journal of Applied Microbiology and Biotechnology, Vol. 16, Issue 2-3 https://doi.org/10.1007/BF00500734	journal	January 1982
Direct hydrogen production from cellulosic waste materials with a single-step dark fermentation process Magnusson, L.; Islam, R.; Sparling, R. International Journal of Hydrogen Energy, Vol. 33, Issue 20 https://doi.org/10.1016/j.ijhydene.2008.06.018	journal	October 2008
Isoprenoid quinone, cellular fatty acid composition and diaminopimelic acid isomers of newly classified thermophilic anaerobic Gram-positive bacteria Yamamoto, Kazunori; Murakami, Ritsuko; Takamura, Yoshichika FEMS Microbiology Letters, Vol. 161, Issue 2 https://doi.org/10.1111/j.1574-6968.1998.tb12968.x	journal	April 1998
Expanding metabolism for biosynthesis of nonnatural alcohols Zhang, K.; Sawaya, M. R.; Eisenberg, D. S. Proceedings of the National Academy of Sciences, Vol. 105, Issue 52 https://doi.org/10.1073/pnas.0807157106	journal	December 2008
The fermentation of cellulose by thermophilic bacteria Viljoen, J. A.; Fred, E. B.; Peterson, W. H. The Journal of Agricultural Science, Vol. 16, Issue 1 https://doi.org/10.1017/S0021859600088249	journal	January 1926
Metabolic selectivity and growth of Clostridium thermocellum in continuous culture under elevated hydrostatic pressure Bothun, G. D.; Knutson, B. L.; Berberich, J. A. Applied Microbiology and Biotechnology, Vol. 65, Issue 2 https://doi.org/10.1007/s00253-004-1554-1	journal	January 2004
Development and evaluation of methods to infer biosynthesis and substrate consumption in cultures of cellulolytic microorganisms Holwerda, Evert K.; Ellis, Lucas D.; Lynd, Lee R. Biotechnology and Bioengineering, Vol. 110, Issue 9 https://doi.org/10.1002/bit.24915	journal	April 2013
Cellulase, Clostridia, and Ethanol Demain, A. L.; Newcomb, M.; Wu, J. H. D. Microbiology and Molecular Biology Reviews, Vol. 69, Issue 1, p. 124-154 https://doi.org/10.1128/MMBR.69.1.124-154.2005	journal	March 2005
The Anaerobic Thermophilic Cellulolytic Bacteria 1 McBee, R. H. Bacteriological Reviews, Vol. 14, Issue 1 https://doi.org/10.1128/MMBR.14.1.51-63.1950	journal	January 1950
Combined inactivation of the Clostridium cellulolyticum lactate and malate dehydrogenase genes substantially increases ethanol yield from cellulose and switchgrass fermentations Li, Yongchao; Tschaplinski, Timothy J.; Engle, Nancy L. Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-2	journal	January 2012
Thermophilic fermentation of acetoin and 2,3-butanediol by a novel Geobacillus strain Xiao, Zijun; Wang, Xiangming; Huang, Yunling Biotechnology for Biofuels, Vol. 5, Issue 1 https://doi.org/10.1186/1754-6834-5-88	journal	January 2012
Conversion of pretreated lignocellulosic substrates to ethanol by Clostridium thermocellum in mono- and co-culture with Clostridium thermosaccharolyticum and Clostridium thermohydrosulphuricum Saddler, J. N.; Chan, M. K. -H. Canadian Journal of Microbiology, Vol. 30, Issue 2 https://doi.org/10.1139/m84-032	journal	February 1984
Free and totalpara-aminobenzoic acid analysis in plants with high-performance liquid chromatography/tandem mass spectrometry Zhang, Guo-Fang; Mortier, Kjell A.; Storozhenko, Sergei Rapid Communications in Mass Spectrometry, Vol. 19, Issue 8 https://doi.org/10.1002/rcm.1878	journal	January 2005
High Ethanol Titers from Cellulose by Using Metabolically Engineered Thermophilic, Anaerobic Microbes Argyros, D. Aaron; Tripathi, Shital A.; Barrett, Trisha F. Applied and Environmental Microbiology, Vol. 77, Issue 23, p. 8288-8294 https://doi.org/10.1128/AEM.00646-11	journal	September 2011
Ethanol from Cellulosic Biomass [and Discussion] Wang, D. I. C.; Avgerinos, G. C.; Biocic, I. Philosophical Transactions of the Royal Society B: Biological Sciences, Vol. 300, Issue 1100 https://doi.org/10.1098/rstb.1983.0008	journal	January 1983
Effect of substrate loading on hydrogen production during anaerobic fermentation by Clostridium thermocellum 27405 Islam, Rumana; Cicek, Nazim; Sparling, Richard Applied Microbiology and Biotechnology, Vol. 72, Issue 3 https://doi.org/10.1007/s00253-006-0316-7	journal	May 2006
Economic impact of total solids loading on enzymatic hydrolysis of dilute acid pretreated corn stover Humbird, David; Mohagheghi, Ali; Dowe, Nancy Biotechnology Progress, Vol. 26, Issue 5 https://doi.org/10.1002/btpr.441	journal	April 2010
The Clostridium Thermocellum-Clostridium Thermosaccharolyticum Ethanol Production Process: Nutritional Studies and Scale-Down Venkateswaran, Saraswathy; Demain, Arnold L. Chemical Engineering Communications, Vol. 45, Issue 1-6 https://doi.org/10.1080/00986448608911371	journal	July 1986
Nutritional interdependence betweenThermoanaerobacter thermohydrosulfuricus andClostridium thermocellum Mori, Yutaka Archives of Microbiology, Vol. 164, Issue 2 https://doi.org/10.1007/BF02525321	journal	August 1995
Growth of the thermophilic bacterium Clostridium thermocellum in continuous culture Strobel, Herbert J. Current Microbiology, Vol. 31, Issue 4 https://doi.org/10.1007/BF00298375	journal	October 1995
Closing the carbon balance for fermentation by Clostridium thermocellum (ATCC 27405) Ellis, Lucas D.; Holwerda, Evert K.; Hogsett, David Bioresource Technology, Vol. 103, Issue 1 https://doi.org/10.1016/j.biortech.2011.09.128	journal	January 2012
Influence of Environment on the Content and Composition of Microbial Free Amino Acid Pools Tempest, D. W.; Meers, J. L.; Brown, C. M. Journal of General Microbiology, Vol. 64, Issue 2 https://doi.org/10.1099/00221287-64-2-171	journal	December 1970
Functional heterologous expression of an engineered full length CipA from Clostridium thermocellum in Thermoanaerobacterium saccharolyticum Currie, Devin H.; Herring, Christopher D.; Guss, Adam M. Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-32	journal	January 2013
The detection of environmental autoinducing peptide quorum-sensing genes from an uncultured Clostridium sp. in landfill leachate reactor biomass Burrell, P. C. Letters in Applied Microbiology, Vol. 43, Issue 4 https://doi.org/10.1111/j.1472-765X.2006.01968.x	journal	October 2006
Impact of Pretreated Switchgrass and Biomass Carbohydrates on Clostridium thermocellum ATCC 27405 Cellulosome Composition: A Quantitative Proteomic Analysis Raman, Babu; Pan, Chongle; Hurst, Gregory B. PLoS ONE, Vol. 4, Issue 4, Article No. e5271 https://doi.org/10.1371/journal.pone.0005271	journal	April 2009
Mechanisms of enhanced cellulosic bioethanol fermentation by co-cultivation of Clostridium and Thermoanaerobacter spp. He, Qiang; Hemme, Christopher L.; Jiang, Helong Bioresource Technology, Vol. 102, Issue 20 https://doi.org/10.1016/j.biortech.2011.07.098	journal	October 2011
Cellulolytic and physiological properties of Clostridium thermocellum Ng, T. K.; Weimer, P. J.; Zeikus, J. G. Archives of Microbiology, Vol. 114, Issue 1 https://doi.org/10.1007/BF00429622	journal	January 1977
Formate synthesis by Clostridium thermocellum during anaerobic fermentation Sparling, Richard; Islam, Rumana; Cicek, Nazim Canadian Journal of Microbiology, Vol. 52, Issue 7 https://doi.org/10.1139/w06-021	journal	July 2006
Global transcriptome analysis of Clostridium thermocellum ATCC 27405 during growth on dilute acid pretreated Populus and switchgrass Wilson, Charlotte M.; Rodriguez, Miguel; Johnson, Courtney M. Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-179	journal	January 2013
A Targetron System for Gene Targeting in Thermophiles and Its Application in Clostridium thermocellum Mohr, Georg; Hong, Wei; Zhang, Jie PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0069032	journal	July 2013
A defined growth medium with very low background carbon for culturing Clostridium thermocellum Holwerda, Evert K.; Hirst, Kyle D.; Lynd, Lee R. Journal of Industrial Microbiology & Biotechnology, Vol. 39, Issue 6 https://doi.org/10.1007/s10295-012-1091-3	journal	February 2012
Ethanol Production by Thermophilic Bacteria: Fermentation of Cellulosic Substrates by Cocultures of Clostridium thermocellum and Clostridium thermohydrosulfuricum Ng, Thomas K.; Ben-Bassat, Arie; Zeikus, J. G. Applied and Environmental Microbiology, Vol. 41, Issue 6 https://doi.org/10.1128/AEM.41.6.1337-1343.1981	journal	January 1981
Stability of Glutamine and Pyroglutamic Acid under Model System Conditions: Influence of Physical and Technological Factors Airaudo, Charles B.; Gayte-Sorbier, AndrÉ; Armand, Paul Journal of Food Science, Vol. 52, Issue 6 https://doi.org/10.1111/j.1365-2621.1987.tb05926.x	journal	November 1987
Metabolic Engineering of Clostridium cellulolyticum for Production of Isobutanol from Cellulose Higashide, Wendy; Li, Yongchao; Yang, Yunfeng Applied and Environmental Microbiology, Vol. 78, Issue 19 https://doi.org/10.1128/aem.02335-12	journal	September 2012
The Anaerobic Thermophilic Cellulolytic Bacteria McBee, R. H. Bacteriological Reviews, Vol. 14, Issue 1 https://doi.org/10.1128/br.14.1.51-63.1950	journal	March 1950
Fermentation of cellulose and cellobiose by Clostridium thermocellum in the absence of Methanobacterium thermoautotrophicum. Weimer, P. J.; Zeikus, J. G. Applied and Environmental Microbiology, Vol. 33, Issue 2 https://doi.org/10.1128/aem.33.2.289-297.1977	journal	January 1977
Chemically Defined Minimal Medium for Growth of the Anaerobic Cellulolytic Thermophile Clostridium thermocellum Johnson, Eric A.; Madia, Ashwin; Demain, Arnold L. Applied and Environmental Microbiology, Vol. 41, Issue 4 https://doi.org/10.1128/aem.41.4.1060-1062.1981	journal	January 1981
Adherence of Clostridium thermocellum to cellulose. Bayer, E. A.; Kenig, R.; Lamed, R. Journal of Bacteriology, Vol. 156, Issue 2 https://doi.org/10.1128/jb.156.2.818-827.1983	journal	January 1983
Fermentation of Cellulosic Substrates in Batch and Continuous Culture by Clostridium thermocellum Lynd, Lee Rybeck; Grethlein, Hans E.; Wolkin, Richard H. Applied and Environmental Microbiology, Vol. 55, Issue 12 https://doi.org/10.1128/aem.55.12.3131-3139.1989	journal	January 1989
Enhanced Cellulose Fermentation by an Asporogenous and Ethanol-Tolerant Mutant of Clostridium thermocellum Tailliez, P.; Girard, H.; Millet, J. Applied and Environmental Microbiology, Vol. 55, Issue 1 https://doi.org/10.1128/aem.55.1.207-211.1989	journal	January 1989
Characterization of Clostridium thermocellum JW20 Freier, Doris; Mothershed, Cheryle P.; Wiegel, Juergen Applied and Environmental Microbiology, Vol. 54, Issue 1 https://doi.org/10.1128/aem.54.1.204-211.1988	journal	January 1988
Clostridium thermocellum JW20 (ATCC 31549) is a coculture with Thermoanaerobacter ethanolicus. Erbeznik, M.; Jones, C. R.; Dawson, K. A. Applied and environmental microbiology, Vol. 63, Issue 7 https://doi.org/10.1128/aem.63.7.2949-2951.1997	journal	January 1997
Effect of Yeast Extract and Vitamin B12 on Ethanol Production from Cellulose by Clostridium thermocellum I-1-B Sato, Kanji; Goto, Shingo; Yonemura, Sotaro Applied and Environmental Microbiology, Vol. 58, Issue 2 https://doi.org/10.1128/aem.58.2.734-736.1992	journal	January 1992
Butanediol production from lignocellulosic substrates by Klebsiella pneumoniae grown in sequential co-culture with Clostridium thermocellum Yu, ErnestK. C.; Chan, MariaK. -H.; Saddler, JohnN. Applied Microbiology and Biotechnology, Vol. 22, Issue 6 https://doi.org/10.1007/BF00252780	journal	October 1985
Relationships between cellobiose catabolism, enzyme levels, and metabolic intermediates inClostridium cellulolyticum grown in a synthetic medium Guedon, E.; Payot, S.; Desvaux, M. Biotechnology and Bioengineering, Vol. 67, Issue 3 https://doi.org/10.1002/(sici)1097-0290(20000205)67:3<327::aid-bit9>3.0.co;2-u	journal	February 2000
Formation of l-alanine as a reduced end product in carbohydrate fermentation by the hyperthermophilic archaeon Pyrococcus furiosus Kengen, Serv� W. M.; Stams, Alfons J. M. Archives of Microbiology, Vol. 161, Issue 2 https://doi.org/10.1007/bf00276479	journal	January 1994
Analysis of amino acid requirements ofClostridium thermocellum Vuillet, S.; Spinnler, H. E.; Blachere, H. Applied Microbiology and Biotechnology, Vol. 23, Issue 6 https://doi.org/10.1007/bf02346067	journal	March 1986
Determination of protein concentration by total organic carbon analysis Rouwenhorst, Robert J.; Frank Jzn, Johannes; Scheffers, W. Alexander Journal of Biochemical and Biophysical Methods, Vol. 22, Issue 2 https://doi.org/10.1016/0165-022x(91)90024-q	journal	February 1991
Inhibitory effect of l-pyroglutamate on extremophiles: correlation with growth temperature and pH Park, Chan Beum; Ryu, Dewey D. Y.; Lee, Sun Bok FEMS Microbiology Letters, Vol. 221, Issue 2 https://doi.org/10.1016/s0378-1097(03)00213-1	journal	April 2003
Effect of pressurized solvents on ethanol production by the thermophilic bacterium Clostridium thermocellum Knutson, B. L.; Strobel, H. J.; Nokes, S. E. The Journal of Supercritical Fluids, Vol. 16, Issue 2 https://doi.org/10.1016/s0896-8446(99)00026-1	journal	November 1999
Production of ethanol and xylitol from corn cobs by yeasts Latif, Farooq; Rajoka, Mohammad Ibrahim Bioresource Technology, Vol. 77, Issue 1, p. 57-63 https://doi.org/10.1016/s0960-8524(00)00134-6	journal	March 2001
Red versus green leaves: transcriptomic comparison of foliar senescence between two Prunus cerasifera genotypes Vangelisti, Alberto; Guidi, Lucia; Cavallini, Andrea Scientific Reports, Vol. 10, Issue 1 https://doi.org/10.1038/s41598-020-58878-8	journal	February 2020
Development of pyrF-Based Genetic System for Targeted Gene Deletion in Clostridium thermocellum and Creation of a pta Mutant Tripathi, S. A.; Olson, D. G.; Argyros, D. A. Applied and Environmental Microbiology, Vol. 76, Issue 19, p. 6591-6599 https://doi.org/10.1128/aem.01484-10	journal	August 2010
d-2,3-Butanediol Production Due to Heterologous Expression of an Acetoin Reductase in Clostridium acetobutylicum Siemerink, Marco A. J.; Kuit, Wouter; López Contreras, Ana M. Applied and Environmental Microbiology, Vol. 77, Issue 8 https://doi.org/10.1128/aem.01616-10	journal	February 2011
Atypical Glycolysis in Clostridium thermocellum Zhou, Jilai; Olson, Daniel G.; Argyros, D. Aaron Applied and Environmental Microbiology, Vol. 79, Issue 9, p. 3000-3008 https://doi.org/10.1128/aem.04037-12	journal	February 2013
Improvement of Cellulolytic Properties of Clostridium cellulolyticum by Metabolic Engineering Guedon, E.; Desvaux, M.; Petitdemange, H. Applied and Environmental Microbiology, Vol. 68, Issue 1 https://doi.org/10.1128/aem.68.1.53-58.2002	journal	January 2002
Role of the CipA Scaffoldin Protein in Cellulose Solubilization, as Determined by Targeted Gene Deletion and Complementation in Clostridium thermocellum Olson, D. G.; Giannone, R. J.; Hettich, R. L. Journal of Bacteriology, Vol. 195, Issue 4 https://doi.org/10.1128/jb.02014-12	journal	November 2012

Cited By (27)

CO ₂ -fixing one-carbon metabolism in a cellulose-degrading bacterium Clostridium thermocellum Xiong, Wei; Lin, Paul P.; Magnusson, Lauren Proceedings of the National Academy of Sciences, Vol. 113, Issue 46 https://doi.org/10.1073/pnas.1605482113	journal	October 2016
Clostridium thermocellum LL1210 pH homeostasis mechanisms informed by transcriptomics and metabolomics Whitham, Jason M.; Moon, Ji-Won; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1095-y	journal	April 2018
Specialized activities and expression differences for Clostridium thermocellum biofilm and planktonic cells Dumitrache, Alexandru; Klingeman, Dawn M.; Natzke, Jace Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43583	journal	February 2017
Integrated omics analyses reveal the details of metabolic adaptation of Clostridium thermocellum to lignocellulose-derived growth inhibitors released during the deconstruction of switchgrass Poudel, Suresh; Giannone, Richard J.; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-016-0697-5	journal	January 2017
Single mutation at a highly conserved region of chloramphenicol acetyltransferase enables isobutyl acetate production directly from cellulose by Clostridium thermocellum at elevated temperatures Seo, Hyeongmin; Lee, Jong-Won; Garcia, Sergio Biotechnology for Biofuels, Vol. 12, Issue 1 https://doi.org/10.1186/s13068-019-1583-8	journal	October 2019
Enhanced ethanol formation by Clostridium thermocellum via pyruvate decarboxylase Tian, Liang; Perot, Skyler J.; Hon, Shuen Microbial Cell Factories, Vol. 16, Issue 1 https://doi.org/10.1186/s12934-017-0783-9	journal	October 2017
Metabolome analysis reveals a role for glyceraldehyde 3-phosphate dehydrogenase in the inhibition of C. thermocellum by ethanol Tian, Liang; Perot, Skyler J.; Stevenson, David Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0961-3	journal	November 2017
Cellulosic ethanol production via consolidated bioprocessing by a novel thermophilic anaerobic bacterium isolated from a Himalayan hot spring Singh, Nisha; Mathur, Anshu S.; Tuli, Deepak K. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0756-6	journal	March 2017
Enhanced depolymerization and utilization of raw lignocellulosic material by co-cultures of Ruminiclostridium thermocellum with hemicellulose-utilizing partners Froese, Alan; Schellenberg, John; Sparling, Richard Canadian Journal of Microbiology, Vol. 65, Issue 4 https://doi.org/10.1139/cjm-2018-0535	journal	April 2019
Isotope-Assisted Metabolite Analysis Sheds Light on Central Carbon Metabolism of a Model Cellulolytic Bacterium Clostridium thermocellum Xiong, Wei; Lo, Jonathan; Chou, Katherine J. Frontiers in Microbiology, Vol. 9 https://doi.org/10.3389/fmicb.2018.01947	journal	August 2018
Overflow metabolism and growth cessation in Clostridium thermocellum DSM1313 during high cellulose loading fermentations : Overflow Metabolism and Growth Cessation in Thompson, R. Adam; Trinh, Cong T. Biotechnology and Bioengineering, Vol. 114, Issue 11 https://doi.org/10.1002/bit.26374	journal	August 2017
Biomass augmentation through thermochemical pretreatments greatly enhances digestion of switchgrass by Clostridium thermocellum Kothari, Ninad; Holwerda, Evert K.; Cai, Charles M. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1216-7	journal	August 2018
Exploring complex cellular phenotypes and model-guided strain design with a novel genome-scale metabolic model of Clostridium thermocellum DSM 1313 implementing an adjustable cellulosome Thompson, R. Adam; Dahal, Sanjeev; Garcia, Sergio Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0607-x	journal	September 2016
Rex in Caldicellulosiruptor bescii : Novel regulon members and its effect on the production of ethanol and overflow metabolites Sander, Kyle; Chung, Daehwan; Hyatt, Doug MicrobiologyOpen, Vol. 8, Issue 2 https://doi.org/10.1002/mbo3.639	journal	April 2018
Challenges and Advances for Genetic Engineering of Non-model Bacteria and Uses in Consolidated Bioprocessing Yan, Qiang; Fong, Stephen S. Frontiers in Microbiology, Vol. 8 https://doi.org/10.3389/fmicb.2017.02060	journal	October 2017
A mutation in the AdhE alcohol dehydrogenase of Clostridium thermocellum increases tolerance to several primary alcohols, including isobutanol, n-butanol and ethanol Tian, Liang; Cervenka, Nicholas D.; Low, Aidan M. Scientific Reports, Vol. 9, Issue 1 https://doi.org/10.1038/s41598-018-37979-5	journal	February 2019
Clostridium thermocellum DSM 1313 transcriptional responses to redox perturbation Sander, Kyle; Wilson, Charlotte M.; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0394-9	journal	December 2015
Metabolic and evolutionary responses of Clostridium thermocellum to genetic interventions aimed at improving ethanol production Holwerda, Evert K.; Olson, Daniel G.; Ruppertsberger, Natalie M. Biotechnology for Biofuels, Vol. 13, Issue 1 https://doi.org/10.1186/s13068-020-01680-5	journal	March 2020
Elimination of formate production in Clostridium thermocellum Rydzak, Thomas; Lynd, Lee R.; Guss, Adam M. Journal of Industrial Microbiology & Biotechnology, Vol. 42, Issue 9 https://doi.org/10.1007/s10295-015-1644-3	journal	July 2015
Improved growth rate in Clostridium thermocellum hydrogenase mutant via perturbed sulfur metabolism Biswas, Ranjita; Wilson, Charlotte M.; Giannone, Richard J. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-016-0684-x	journal	January 2017
Expressing the Thermoanaerobacterium saccharolyticum pforA in engineered Clostridium thermocellum improves ethanol production Hon, Shuen; Holwerda, Evert K.; Worthen, Robert S. Biotechnology for Biofuels, Vol. 11, Issue 1 https://doi.org/10.1186/s13068-018-1245-2	journal	September 2018
Simultaneous achievement of high ethanol yield and titer in Clostridium thermocellum Tian, Liang; Papanek, Beth; Olson, Daniel G. Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0528-8	journal	June 2016
A metabolic and genomic assessment of sugar fermentation profiles of the thermophilic Thermotogales, Fervidobacterium pennivorans Wushke, Scott; Fristensky, Brian; Zhang, Xiang Li Extremophiles, Vol. 22, Issue 6 https://doi.org/10.1007/s00792-018-1053-4	journal	September 2018
Cellulose hydrolysis by Clostridium thermocellum is agnostic to substrate structural properties in contrast to fungal cellulases Kothari, Ninad; Bhagia, Samarthya; Zaher, Maher Green Chemistry, Vol. 21, Issue 10 https://doi.org/10.1039/c9gc00262f	journal	January 2019
Development of a core Clostridium thermocellum kinetic metabolic model consistent with multiple genetic perturbations Dash, Satyakam; Khodayari, Ali; Zhou, Jilai Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0792-2	journal	May 2017
Pentose sugars inhibit metabolism and increase expression of an AgrD-type cyclic pentapeptide in Clostridium thermocellum Verbeke, Tobin J.; Giannone, Richard J.; Klingeman, Dawn M. Scientific Reports, Vol. 7, Issue 1 https://doi.org/10.1038/srep43355	journal	February 2017
The effect of switchgrass loadings on feedstock solubilization and biofuel production by Clostridium thermocellum Verbeke, Tobin J.; Garcia, Gabriela M.; Elkins, James G. Biotechnology for Biofuels, Vol. 10, Issue 1 https://doi.org/10.1186/s13068-017-0917-7	journal	November 2017

Similar Records

Expressing the Thermoanaerobacterium saccharolyticum pforA in engineered Clostridium thermocellum improves ethanol production

Journal Article · Thu Sep 06 00:00:00 EDT 2018 · Biotechnology for Biofuels · OSTI ID:1163586

Hon, Shuen; Holwerda, Evert K.; Worthen, Robert S.; +6 more

Coculture with hemicellulose-fermenting microbes reverses inhibition of corn fiber solubilization by Clostridium thermocellum at elevated solids loadings

Journal Article · Mon Jan 18 00:00:00 EST 2021 · Biotechnology for Biofuels · OSTI ID:1163586

Beri, Dhananjay; Herring, Christopher D.; Blahova, Sofie; +4 more

Elimination of metabolic pathways to all traditional fermentation products increases ethanol yields in Clostridium thermocellum

Journal Article · Sat Sep 12 00:00:00 EDT 2015 · Metabolic Engineering · OSTI ID:1163586

Papanek, Beth A.; Biswas, Ranjita; Rydzak, Thomas; +1 more

Related Subjects

09 BIOMASS FUELS
Clostridium thermocellum
Cellulose fermentation
Isobutanol
2
3-butanediol
Amino acids
High solids
Fusel alcohols

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

Citation Formats

References (79)

Cited By (27)

Similar Records

Related Subjects