Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants
Abstract
Because cellulosic ethanol production remains cost-prohibitive„ advances in consolidated bioprocessing (CBP) have been directed towards lifting this restriction. CBP reduces the need for added enzymes and can potentially slash ethanol production costs through process integration. Clostridium thermocellum, a CBP microorganism, organizes its enzymes in a multi-enzyme complex - a stark contrast to fungal enzymes. Nonetheless, recalcitrance may limit the extent of biomass deconstruction. Here in this study, six Populus were treated with C. thermocellum (ATCC 27405) and characterized to determine structural changes that resulted from CBP. The 2D HSQC NMR spectra of lignin-enriched residues revealed that higher S/G ratio (2.6) and fewer carbon-carbon interunit linkages (generally 2–5%) were present in the top performing poplar. Furthermore, cellulose degree of polymerization data suggests that C. thermocellum likely circumvents long chain cellulose, while cellulose crystallinity and hemicellulose molecular weight data do not provide a direct indication of features connected to recalcitrance. Hence, C. thermocellum is similarly impacted by the proposed lignin properties that negatively impact biomass deconstruction using fungal enzymes.
- Authors:
-
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division; Georgia Inst. of Technology, Atlanta, GA (United States). Dept. of Chemistry and Biochemistry
- Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Univ. of Tennessee, Knoxville, TN (United States). Center for Renewable Carbon at Wildlife, and Fisheries, Dept. of Chemical and Biomolecular Engineering & Department of Forestry; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Univ. of Tennessee, Knoxville, TN (United States). Center for Renewable Carbon at Wildlife, and Fisheries, Dept. of Chemical and Biomolecular Engineering & Department of Forestry; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Biosciences Division
- Publication Date:
- Research Org.:
- Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)
- Sponsoring Org.:
- USDOE Office of Science (SC), Biological and Environmental Research (BER)
- OSTI Identifier:
- 1410909
- Alternate Identifier(s):
- OSTI ID: 1410886
- Grant/Contract Number:
- AC05-00OR22725
- Resource Type:
- Accepted Manuscript
- Journal Name:
- Chemistry Select
- Additional Journal Information:
- Journal Volume: 2; Journal Issue: 33; Journal ID: ISSN 2365-6549
- Publisher:
- Wiley
- Country of Publication:
- United States
- Language:
- English
- Subject:
- 59 BASIC BIOLOGICAL SCIENCES; cellulosic ethanol; Clostridium thermocellum; lignin; Populus trichocarpa; recalcitrance
Citation Formats
Akinosho, Hannah, Yee, Kelsey, Rodriguez, Miguel, Muchero, Wellington, Yoo, Chang Geun, Li, Mi, Thompson, Olivia, Pu, Yunqiao Joseph, Brown, Steven D., Mielenz, Johnathan R., and Ragauskas, Arthur J. Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants. United States: N. p., 2017.
Web. doi:10.1002/slct.201701572.
Akinosho, Hannah, Yee, Kelsey, Rodriguez, Miguel, Muchero, Wellington, Yoo, Chang Geun, Li, Mi, Thompson, Olivia, Pu, Yunqiao Joseph, Brown, Steven D., Mielenz, Johnathan R., & Ragauskas, Arthur J. Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants. United States. https://doi.org/10.1002/slct.201701572
Akinosho, Hannah, Yee, Kelsey, Rodriguez, Miguel, Muchero, Wellington, Yoo, Chang Geun, Li, Mi, Thompson, Olivia, Pu, Yunqiao Joseph, Brown, Steven D., Mielenz, Johnathan R., and Ragauskas, Arthur J. Wed .
"Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants". United States. https://doi.org/10.1002/slct.201701572. https://www.osti.gov/servlets/purl/1410909.
@article{osti_1410909,
title = {Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants},
author = {Akinosho, Hannah and Yee, Kelsey and Rodriguez, Miguel and Muchero, Wellington and Yoo, Chang Geun and Li, Mi and Thompson, Olivia and Pu, Yunqiao Joseph and Brown, Steven D. and Mielenz, Johnathan R. and Ragauskas, Arthur J.},
abstractNote = {Because cellulosic ethanol production remains cost-prohibitive„ advances in consolidated bioprocessing (CBP) have been directed towards lifting this restriction. CBP reduces the need for added enzymes and can potentially slash ethanol production costs through process integration. Clostridium thermocellum, a CBP microorganism, organizes its enzymes in a multi-enzyme complex - a stark contrast to fungal enzymes. Nonetheless, recalcitrance may limit the extent of biomass deconstruction. Here in this study, six Populus were treated with C. thermocellum (ATCC 27405) and characterized to determine structural changes that resulted from CBP. The 2D HSQC NMR spectra of lignin-enriched residues revealed that higher S/G ratio (2.6) and fewer carbon-carbon interunit linkages (generally 2–5%) were present in the top performing poplar. Furthermore, cellulose degree of polymerization data suggests that C. thermocellum likely circumvents long chain cellulose, while cellulose crystallinity and hemicellulose molecular weight data do not provide a direct indication of features connected to recalcitrance. Hence, C. thermocellum is similarly impacted by the proposed lignin properties that negatively impact biomass deconstruction using fungal enzymes.},
doi = {10.1002/slct.201701572},
journal = {Chemistry Select},
number = 33,
volume = 2,
place = {United States},
year = {Wed Nov 22 00:00:00 EST 2017},
month = {Wed Nov 22 00:00:00 EST 2017}
}
Web of Science
Works referenced in this record:
Increase in Ethanol Yield via Elimination of Lactate Production in an Ethanol-Tolerant Mutant of Clostridium thermocellum
journal, February 2014
- Biswas, Ranjita; Prabhu, Sandeep; Lynd, Lee R.
- PLoS ONE, Vol. 9, Issue 2
Enzymatic hydrolysis of lignocellulose: SEC-MALLS analysis and reaction mechanism
journal, January 2013
- Du, Ruoyu; Huang, Renliang; Su, Rongxin
- RSC Adv., Vol. 3, Issue 6
Fungal cellulases and complexed cellulosomal enzymes exhibit synergistic mechanisms in cellulose deconstruction
journal, January 2013
- Resch, Michael G.; Donohoe, Bryon S.; Baker, John O.
- Energy & Environmental Science, Vol. 6, Issue 6
Two-year field analysis of reduced recalcitrance transgenic switchgrass
journal, April 2014
- Baxter, Holly L.; Mazarei, Mitra; Labbe, Nicole
- Plant Biotechnology Journal, Vol. 12, Issue 7
Assessing the molecular structure basis for biomass recalcitrance during dilute acid and hydrothermal pretreatments
journal, January 2013
- Pu, Yunqiao; Hu, Fan; Huang, Fang
- Biotechnology for Biofuels, Vol. 6, Issue 1
The degradation pattern of cellulose by extracellular cellulases of aerobic and anaerobic microorganisms
journal, January 1991
- Puls, J.; Wood, T. M.
- Bioresource Technology, Vol. 36, Issue 1
Adsorption of Clostridium thermocellum cellulases onto pretreated mixed hardwood, avicel, and lignin
journal, September 1993
- Bernardez, Timothy D.; Lyford, Kimberly; Hogsett, David A.
- Biotechnology and Bioengineering, Vol. 42, Issue 7, p. 899-907
Xylooligomers are strong inhibitors of cellulose hydrolysis by enzymes
journal, December 2010
- Qing, Qing; Yang, Bin; Wyman, Charles E.
- Bioresource Technology, Vol. 101, Issue 24, p. 9624-9630
End-product induced metabolic shifts in Clostridium thermocellum ATCC 27405
journal, August 2011
- Rydzak, Thomas; Levin, David B.; Cicek, Nazim
- Applied Microbiology and Biotechnology, Vol. 92, Issue 1
Lignin content in natural Populus variants affects sugar release
journal, March 2011
- Studer, M. H.; DeMartini, J. D.; Davis, M. F.
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305
Mutations in the Scaffoldin Gene, cipA, of Clostridium thermocellum with Impaired Cellulosome Formation and Cellulose Hydrolysis: Insertions of a New Transposable Element, IS1447, and Implications for Cellulase Synergism on Crystalline Cellulose
journal, April 2008
- Zverlov, V. V.; Klupp, M.; Krauss, J.
- Journal of Bacteriology, Vol. 190, Issue 12
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass
journal, February 2011
- Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong
- Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808
Two-Dimensional NMR Evidence for Cleavage of Lignin and Xylan Substituents in Wheat Straw Through Hydrothermal Pretreatment and Enzymatic Hydrolysis
journal, September 2012
- Yelle, Daniel J.; Kaparaju, Prasad; Hunt, Christopher G.
- BioEnergy Research, Vol. 6, Issue 1
Mitigation of cellulose recalcitrance to enzymatic hydrolysis by ionic liquid pretreatment
journal, April 2007
- Dadi, Anantharam P.; Schall, Constance A.; Varanasi, Sasidhar
- Applied Biochemistry and Biotechnology, Vol. 137-140, Issue 1-12, p. 407-421
Enzymatic Hydrolysis of Cellulose with Different Crystallinities Studied by Means of SEC-MALLS
journal, October 2011
- Zhang, Mingjia; Su, Rongxin; Qi, Wei
- Chinese Journal of Chemical Engineering, Vol. 19, Issue 5
Ethanol Production by Thermophilic Bacteria: Relationship Between Fermentation Product Yields of and Catabolic Enzyme Activities in Clostridium thermocellum and Thermoanaerobium brockii
journal, January 1980
- Lamed, R.; Zeikus, J. G.
- Journal of Bacteriology, Vol. 144, Issue 2
Elimination of metabolic pathways to all traditional fermentation products increases ethanol yields in Clostridium thermocellum
journal, November 2015
- Papanek, Beth; Biswas, Ranjita; Rydzak, Thomas
- Metabolic Engineering, Vol. 32
The emergence of Clostridium thermocellum as a high utility candidate for consolidated bioprocessing applications
journal, August 2014
- Akinosho, Hannah; Yee, Kelsey; Close, Dan
- Frontiers in Chemistry, Vol. 2
Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum
journal, January 2015
- Biswas, Ranjita; Zheng, Tianyong; Olson, Daniel G.
- Biotechnology for Biofuels, Vol. 8, Issue 1
Decrement of cellulose recalcitrance by treatment with ionic liquid (1-ethyl-3-methylimidazolium acetate) as a strategy to enhance enzymatic hydrolysis
journal, January 2012
- Xiros, Charilaos; Vafiadi, Christina; Topakas, Evangelos
- Journal of Chemical Technology & Biotechnology, Vol. 87, Issue 5
Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase
journal, June 2016
- Cai, Yuanheng; Zhang, Kewei; Kim, Hoon
- Nature Communications, Vol. 7, Issue 1
Effect of cellulose structure on enzymatic hydrolysis
journal, June 2011
- Ioelovich, Michael; Morag, Ely
- BioResources, Vol. 6, Issue 3
Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification: Reduction in lignin DP enhances saccharification
journal, March 2012
- Eudes, Aymerick; George, Anthe; Mukerjee, Purba
- Plant Biotechnology Journal, Vol. 10, Issue 5
Determination of the Number-Average Degree of Polymerization of Cellodextrins and Cellulose with Application to Enzymatic Hydrolysis
journal, May 2005
- Zhang, Y. -H. Percival; Lynd, Lee R.
- Biomacromolecules, Vol. 6, Issue 3
Effects of Cellulose Crystallinity, Hemicellulose, and Lignin on the Enzymatic Hydrolysis of Miscanthus sinensis to Monosaccharides
journal, March 2008
- Yoshida, Makoto; Liu, Yuan; Uchida, Satoshi
- Bioscience, Biotechnology, and Biochemistry, Vol. 72, Issue 3
Conversion for Avicel and AFEX pretreated corn stover by Clostridium thermocellum and simultaneous saccharification and fermentation: Insights into microbial conversion of pretreated cellulosic biomass
journal, September 2011
- Shao, Xiongjun; Jin, Mingjie; Guseva, Anna
- Bioresource Technology, Vol. 102, Issue 17
Digestion of crystalline cellulose substrates by the Clostridium thermocellum cellulosome: structural and morphological aspects
journal, June 1999
- Boisset, Claire; Chanzy, Henri; Henrissat, Bernard
- Biochemical Journal, Vol. 340, Issue 3
Cellulose solvent-based biomass pretreatment breaks highly ordered hydrogen bonds in cellulose fibers of switchgrass
journal, November 2010
- Sathitsuksanoh, Noppadon; Zhu, Zhiguang; Wi, Sungsool
- Biotechnology and Bioengineering, Vol. 108, Issue 3
Recent progress in consolidated bioprocessing
journal, June 2012
- Olson, Daniel G.; McBride, John E.; Joe Shaw, A.
- Current Opinion in Biotechnology, Vol. 23, Issue 3, p. 396-405
Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure
journal, February 2016
- Dumitrache, Alexandru; Akinosho, Hannah; Rodriguez, Miguel
- Biotechnology for Biofuels, Vol. 9, Issue 1
Cellulose and lignin colocalization at the plant cell wall surface limits microbial hydrolysis of Populus biomass
journal, January 2017
- Dumitrache, Alexandru; Tolbert, Allison; Natzke, Jace
- Green Chemistry, Vol. 19, Issue 9
Enzymatic diversity of the Clostridium thermocellum cellulosome is crucial for the degradation of crystalline cellulose and plant biomass
journal, October 2016
- Hirano, Katsuaki; Kurosaki, Masahiro; Nihei, Satoshi
- Scientific Reports, Vol. 6, Issue 1
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
- Poudel, Suresh; Giannone, Richard J.; Rodriguez, Miguel
- Biotechnology for Biofuels, Vol. 10, Issue 1
Consolidated bioprocessing of transgenic switchgrass by an engineered and evolved Clostridium thermocellum strain
journal, January 2014
- Yee, Kelsey L.; Rodriguez Jr, Miguel; Thompson, Olivia A.
- Biotechnology for Biofuels, Vol. 7, Issue 1
Works referencing / citing this record:
Bridging the gap between feedstock growers and users: the study of a coppice poplar-based biorefinery
journal, March 2018
- Dou, Chang; Gustafson, Rick; Bura, Renata
- Biotechnology for Biofuels, Vol. 11, Issue 1
Bridging the gap between feedstock growers and users: the study of a coppice poplar-based biorefinery
journal, March 2018
- Dou, Chang; Gustafson, Rick; Bura, Renata
- Biotechnology for Biofuels, Vol. 11, Issue 1