Metabolically engineered Caldicellulosiruptor bescii as a platform for producing acetone and hydrogen from lignocellulose

Straub, Christopher T.; Bing, Ryan G.; Otten, Jonathan K.; Keller, Lisa M.; Zeldes, Benjamin M.; Adams, Michael W. W.; Kelly, Robert M.

doi:10.1002/bit.27529

Metabolically engineered Caldicellulosiruptor bescii as a platform for producing acetone and hydrogen from lignocellulose

Journal Article · Mon Aug 24 00:00:00 EDT 2020 · Biotechnology and Bioengineering

DOI:https://doi.org/10.1002/bit.27529· OSTI ID:1786038

Straub, Christopher T. ^[1]; Bing, Ryan G. ^[1]; Otten, Jonathan K. ^[1]; Keller, Lisa M. ^[1]; Zeldes, Benjamin M. ^[1]; ^[2]; ^[1]

Department of Chemical and Biomolecular Engineering North Carolina State University Raleigh North Carolina
Department of Biochemistry and Molecular Biology University of Georgia Athens Georgia

Abstract

The production of volatile industrial chemicals utilizing metabolically engineered extreme thermophiles offers the potential for processes with simultaneous fermentation and product separation. An excellent target chemical for such a process is acetone ( T _b = 56°C), ideally produced from lignocellulosic biomass. Caldicellulosiruptor bescii ( T _opt 78°C), an extremely thermophilic fermentative bacterium naturally capable of deconstructing and fermenting lignocellulose, was metabolically engineered to produce acetone. When the acetone pathway construct was integrated into a parent strain containing the bifunctional alcohol dehydrogenase from Clostridium thermocellum , acetone was produced at 9.1 mM (0.53 g/L), in addition to minimal ethanol 3.3 mM (0.15 g/L), along with net acetate consumption. This demonstrates that C. bescii can be engineered with balanced pathways in which renewable carbohydrate sources are converted to useful metabolites, primarily acetone and H ₂ , without net production of its native fermentation products, acetate and lactate.

View Accepted Manuscript (Publisher)

Sponsoring Organization:: USDOE

Grant/Contract Number:: SC0019391

OSTI ID:: 1786038

Alternate ID(s):: OSTI ID: 1853180

Journal Information:: Biotechnology and Bioengineering, Journal Name: Biotechnology and Bioengineering Journal Issue: 12 Vol. 117; ISSN 0006-3592

Publisher:: Wiley Blackwell (John Wiley & Sons)Copyright Statement

Country of Publication:: United States

Language:: English

References (37)

Beyond Petrochemicals: The Renewable Chemicals Industry Vennestrøm, P. N. R.; Osmundsen, C. M.; Christensen, C. H. Angewandte Chemie International Edition, Vol. 50, Issue 45 https://doi.org/10.1002/anie.201102117	journal	October 2011
Substrate and product inhibition of hydrogen production by the extreme thermophile,Caldicellulosiruptor saccharolyticus van Niel, Ed W. J.; Claassen, Pieternel A. M.; Stams, Alfons J. M. Biotechnology and Bioengineering, Vol. 81, Issue 3 https://doi.org/10.1002/bit.10463	journal	December 2002
A synthetic enzymatic pathway for extremely thermophilic acetone production based on the unexpectedly thermostable acetoacetate decarboxylase from Clostridium acetobutylicum: ZELDES et al. Zeldes, Benjamin M.; Straub, Christopher T.; Otten, Jonathan K. Biotechnology and Bioengineering, Vol. 115, Issue 12 https://doi.org/10.1002/bit.26829	journal	October 2018
Initiation of solvent production, clostridial stage and endospore formation in Clostridium acetobutylicum P262 Long, Susan; Jones, DavidT.; Woods, DavidR. Applied Microbiology and Biotechnology, Vol. 20, Issue 4 https://doi.org/10.1007/BF00250635	journal	October 1984
Effect of pH and butyrate concentration on the production of acetone and butanol by Clostridium acetobutylicum grown in continuous culture Bahl, Hubert; Andersch, Wolfram; Braun, Konstantin European Journal of Applied Microbiology and Biotechnology, Vol. 14, Issue 1 https://doi.org/10.1007/BF00507998	journal	January 1982
Achievements and perspectives to overcome the poor solvent resistance in acetone and butanol-producing microorganisms Ezeji, Thaddeus; Milne, Caroline; Price, Nathan D. Applied Microbiology and Biotechnology, Vol. 85, Issue 6 https://doi.org/10.1007/s00253-009-2390-0	journal	December 2009
Conversion of glutaconate CoA-transferase from Acidaminococcus fermentans into an acyl-CoA hydrolase by site-directed mutagenesis Mack, Matthias; Buckel, Wolfgang FEBS Letters, Vol. 405, Issue 2 https://doi.org/10.1016/S0014-5793(97)00187-7	journal	March 1997
The Thermal Inactivation of Acetoacetate Decarboxylase Autor, Anne P.; Fridovich, I. Journal of Biological Chemistry, Vol. 245, Issue 20 https://doi.org/10.1016/S0021-9258(18)62744-9	journal	October 1970
A review on reduction of acetone to isopropanol with Ni nano superactive, heterogeneous catalysts as an environmentally benevolent approach Rahman, Ateeq; S-Al-Deyab, Salem Applied Catalysis A: General, Vol. 469 https://doi.org/10.1016/j.apcata.2013.10.015	journal	January 2014
Degradation of high loads of crystalline cellulose and of unpretreated plant biomass by the thermophilic bacterium Caldicellulosiruptor bescii Basen, Mirko; Rhaesa, Amanda M.; Kataeva, Irina Bioresource Technology, Vol. 152 https://doi.org/10.1016/j.biortech.2013.11.024	journal	January 2014
Effect of acetone accumulation on structure and dynamics of lipid membranes studied by molecular dynamics simulations Posokhov, Yevgen O.; Kyrychenko, Alexander Computational Biology and Chemistry, Vol. 46 https://doi.org/10.1016/j.compbiolchem.2013.04.005	journal	October 2013
Engineering redox-balanced ethanol production in the cellulolytic and extremely thermophilic bacterium, Caldicellulosiruptor bescii Williams-Rhaesa, Amanda M.; Rubinstein, Gabriel M.; Scott, Israel M. Metabolic Engineering Communications, Vol. 7 https://doi.org/10.1016/j.mec.2018.e00073	journal	December 2018
Hydrogenesis in hyperthermophilic microorganisms: Implications for biofuels Chou, Chung-Jung; Jenney, Francis E.; Adams, Michael W.W. Metabolic Engineering, Vol. 10, Issue 6, p. 394-404 https://doi.org/10.1016/j.ymben.2008.06.007	journal	November 2008
A modified pathway for the production of acetone in Escherichia coli May, Antje; Fischer, Ralf-Jörg; Maria Thum, Simone Metabolic Engineering, Vol. 15 https://doi.org/10.1016/j.ymben.2012.08.001	journal	January 2013
A hybrid synthetic pathway for butanol production by a hyperthermophilic microbe Keller, Matthew W.; Lipscomb, Gina L.; Loder, Andrew J. Metabolic Engineering, Vol. 27 https://doi.org/10.1016/j.ymben.2014.11.004	journal	January 2015
Mechanism of the Reaction Catalyzed by Acetoacetate Decarboxylase. Importance of Lysine 116 in Determining the p K _a of Active-Site Lysine 115 ^† Highbarger, Lane A.; Gerlt, John A.; Kenyon, George L. Biochemistry, Vol. 35, Issue 1 https://doi.org/10.1021/bi9518306	journal	January 1996
Correlation of Vapor-Liquid Equilibrium Data for Acetone-Water System. Eduljee, H.; Kumarkrishnaroo, V.; Rao, M. Industrial & Engineering Chemistry Chemical & Engineering Data Series, Vol. 3, Issue 1 https://doi.org/10.1021/i460003a010	journal	April 1958
The origin of the electrostatic perturbation in acetoacetate decarboxylase Ho, Meng-Chiao; Ménétret, Jean-François; Tsuruta, Hiro Nature, Vol. 459, Issue 7245 https://doi.org/10.1038/nature07938	journal	May 2009
CO2 fixation by anaerobic non-photosynthetic mixotrophy for improved carbon conversion Jones, Shawn W.; Fast, Alan G.; Carlson, Ellinor D. Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms12800	journal	September 2016
Quantitative fermentation of unpretreated transgenic poplar by Caldicellulosiruptor bescii Straub, Christopher T.; Khatibi, Piyum A.; Wang, Jack P. Nature Communications, Vol. 10, Issue 1 https://doi.org/10.1038/s41467-019-11376-6	journal	August 2019
Lignocellulosic biomass: a sustainable platform for the production of bio-based chemicals and polymers Isikgor, Furkan H.; Becer, C. Remzi Polymer Chemistry, Vol. 6, Issue 25 https://doi.org/10.1039/C5PY00263J	journal	January 2015
Synthesis of aviation fuel from bio-derived isophorone Ryan, Courtney Ford; Moore, Cameron M.; Leal, Juan H. Sustainable Energy & Fuels, Vol. 4, Issue 3 https://doi.org/10.1039/C9SE01014A	journal	January 2020
Studies on the acetone-butanol fermentation Davies, R. Biochemical Journal, Vol. 37, Issue 2 https://doi.org/10.1042/bj0370230	journal	July 1943
Metabolic engineering of a thermophilic bacterium to produce ethanol at high yield Shaw, A. J.; Podkaminer, K. K.; Desai, S. G. Proceedings of the National Academy of Sciences, Vol. 105, Issue 37, p. 13769-13774 https://doi.org/10.1073/pnas.0801266105	journal	September 2008
ATP drives direct photosynthetic production of 1-butanol in cyanobacteria Lan, E. I.; Liao, J. C. Proceedings of the National Academy of Sciences, Vol. 109, Issue 16 https://doi.org/10.1073/pnas.1200074109	journal	April 2012
Oxygen Exchange between Acetate and the Catalytic Glutamate Residue in Glutaconate CoA-transferase from Acidaminococcus fermentans Selmer, Thorsten; Buckel, Wolfgang Journal of Biological Chemistry, Vol. 274, Issue 30 https://doi.org/10.1074/jbc.274.30.20772	journal	July 1999
The thermophilic biomass-degrading bacterium Caldicellulosiruptor bescii utilizes two enzymes to oxidize glyceraldehyde 3-phosphate during glycolysis Scott, Israel M.; Rubinstein, Gabriel M.; Poole, Farris L. Journal of Biological Chemistry, Vol. 294, Issue 25 https://doi.org/10.1074/jbc.RA118.007120	journal	May 2019
Hydrogen production by hyperthermophilic and extremely thermophilic bacteria and archaea: mechanisms for reductant disposal Verhaart, Marcel R. A.; Bielen, Abraham A. M.; Oost, John van der Environmental Technology, Vol. 31, Issue 8-9 https://doi.org/10.1080/09593331003710244	journal	July 2010
Bio-Ethanol Based Ethylene Morschbacker, Antonio Polymer Reviews, Vol. 49, Issue 2 https://doi.org/10.1080/15583720902834791	journal	May 2009
Recent progress in biobutanol tolerance in microbial systems with an emphasis on Clostridium Peabody, George L.; Kao, Katy C. FEMS Microbiology Letters, Vol. 363, Issue 5 https://doi.org/10.1093/femsle/fnw017	journal	January 2016
Classification of 'Anaerocellum thermophilum' strain DSM 6725 as Caldicellulosiruptor bescii sp. nov. Yang, S. -J.; Kataeva, I.; Wiegel, J. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 60, Issue 9 https://doi.org/10.1099/ijs.0.017731-0	journal	October 2009
Isolation from oil reservoirs of novel thermophilic anaerobes phylogenetically related to Thermoanaerobacter subterraneus: reassignment of T. subterraneus, Thermoanaerobacter yonseiensis, Thermoanaerobacter tengcongensis and Carboxydibrachium pacificum to Caldanaerobacter subterraneus gen. nov., sp. nov., comb. nov. as four novel subspecies Fardeau, M. -L. INTERNATIONAL JOURNAL OF SYSTEMATIC AND EVOLUTIONARY MICROBIOLOGY, Vol. 54, Issue 2 https://doi.org/10.1099/ijs.0.02711-0	journal	March 2004
Bioavailability of Carbohydrate Content in Natural and Transgenic Switchgrasses for the Extreme Thermophile Caldicellulosiruptor bescii Zurawski, Jeffrey V.; Khatibi, Piyum A.; Akinosho, Hannah O. Applied and Environmental Microbiology, Vol. 83, Issue 17 https://doi.org/10.1128/AEM.00969-17	journal	June 2017
Energy conservation in chemotrophic anaerobic bacteria. Thauer, R. K.; Jungermann, K.; Decker, K. Bacteriological Reviews, Vol. 41, Issue 1 https://doi.org/10.1128/br.41.1.100-180.1977	journal	January 1977
In Vivo Thermodynamic Analysis of Glycolysis in Clostridium thermocellum and Thermoanaerobacterium saccharolyticum Using ¹³ C and ² H Tracers Jacobson, Tyler B.; Korosh, Travis K.; Stevenson, David M. mSystems, Vol. 5, Issue 2 https://doi.org/10.1128/mSystems.00736-19	journal	March 2020
Anaerobic detoxification of acetic acid in a thermophilic ethanologen Shaw, A. Joe; Miller, Bethany B.; Rogers, Stephen R. Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0257-4	journal	May 2015
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

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