Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants

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.

doi:10.1002/slct.201701572

Title: Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants

Journal Article · Tue Nov 21 23:00:00 EST 2017 · Chemistry Select

DOI: https://doi.org/10.1002/slct.201701572 · OSTI ID:1410909

Akinosho, Hannah ^[1]; Yee, Kelsey ^[2];

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^[3];

^[3]; Thompson, Olivia ^[2];

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^[2]; Mielenz, Johnathan R. ^[2];

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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

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.

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Research Organization:: Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States)

Sponsoring Organization:: USDOE Office of Science (SC), Biological and Environmental Research (BER)

Grant/Contract Number:: AC05-00OR22725

OSTI ID:: 1410909

Journal Information:: Chemistry Select, Journal Name: Chemistry Select Journal Issue: 33 Vol. 2; ISSN 2365-6549

Publisher:: WileyCopyright Statement

Country of Publication:: United States

Language:: English

References (35)

Cellulose solvent-based biomass pretreatment breaks highly ordered hydrogen bonds in cellulose fibers of switchgrass Sathitsuksanoh, Noppadon; Zhu, Zhiguang; Wi, Sungsool Biotechnology and Bioengineering, Vol. 108, Issue 3 https://doi.org/10.1002/bit.22964	journal	November 2010
Adsorption of Clostridium thermocellum cellulases onto pretreated mixed hardwood, avicel, and lignin Bernardez, Timothy D.; Lyford, Kimberly; Hogsett, David A. Biotechnology and Bioengineering, Vol. 42, Issue 7, p. 899-907 https://doi.org/10.1002/bit.260420715	journal	September 1993
Decrement of cellulose recalcitrance by treatment with ionic liquid (1-ethyl-3-methylimidazolium acetate) as a strategy to enhance enzymatic hydrolysis Xiros, Charilaos; Vafiadi, Christina; Topakas, Evangelos Journal of Chemical Technology & Biotechnology, Vol. 87, Issue 5 https://doi.org/10.1002/jctb.2756	journal	January 2012
End-product induced metabolic shifts in Clostridium thermocellum ATCC 27405 Rydzak, Thomas; Levin, David B.; Cicek, Nazim Applied Microbiology and Biotechnology, Vol. 92, Issue 1 https://doi.org/10.1007/s00253-011-3511-0	journal	August 2011
Mitigation of cellulose recalcitrance to enzymatic hydrolysis by ionic liquid pretreatment Dadi, Anantharam P.; Schall, Constance A.; Varanasi, Sasidhar Applied Biochemistry and Biotechnology, Vol. 137-140, Issue 1-12, p. 407-421 https://doi.org/10.1007/s12010-007-9068-9	journal	April 2007
Two-Dimensional NMR Evidence for Cleavage of Lignin and Xylan Substituents in Wheat Straw Through Hydrothermal Pretreatment and Enzymatic Hydrolysis Yelle, Daniel J.; Kaparaju, Prasad; Hunt, Christopher G. BioEnergy Research, Vol. 6, Issue 1 https://doi.org/10.1007/s12155-012-9247-6	journal	September 2012
The degradation pattern of cellulose by extracellular cellulases of aerobic and anaerobic microorganisms Puls, J.; Wood, T. M. Bioresource Technology, Vol. 36, Issue 1 https://doi.org/10.1016/0960-8524(91)90096-3	journal	January 1991
Enzymatic Hydrolysis of Cellulose with Different Crystallinities Studied by Means of SEC-MALLS Zhang, Mingjia; Su, Rongxin; Qi, Wei Chinese Journal of Chemical Engineering, Vol. 19, Issue 5 https://doi.org/10.1016/S1004-9541(11)60055-4	journal	October 2011
Xylooligomers are strong inhibitors of cellulose hydrolysis by enzymes Qing, Qing; Yang, Bin; Wyman, Charles E. Bioresource Technology, Vol. 101, Issue 24, p. 9624-9630 https://doi.org/10.1016/j.biortech.2010.06.137	journal	December 2010
Conversion for Avicel and AFEX pretreated corn stover by Clostridium thermocellum and simultaneous saccharification and fermentation: Insights into microbial conversion of pretreated cellulosic biomass Shao, Xiongjun; Jin, Mingjie; Guseva, Anna Bioresource Technology, Vol. 102, Issue 17 https://doi.org/10.1016/j.biortech.2011.05.021	journal	September 2011
Recent progress in consolidated bioprocessing Olson, Daniel G.; McBride, John E.; Joe Shaw, A. Current Opinion in Biotechnology, Vol. 23, Issue 3, p. 396-405 https://doi.org/10.1016/j.copbio.2011.11.026	journal	June 2012
Elimination of metabolic pathways to all traditional fermentation products increases ethanol yields in Clostridium thermocellum Papanek, Beth; Biswas, Ranjita; Rydzak, Thomas Metabolic Engineering, Vol. 32 https://doi.org/10.1016/j.ymben.2015.09.002	journal	November 2015
Determination of the Number-Average Degree of Polymerization of Cellodextrins and Cellulose with Application to Enzymatic Hydrolysis Zhang, Y. -H. Percival; Lynd, Lee R. Biomacromolecules, Vol. 6, Issue 3 https://doi.org/10.1021/bm049235j	journal	May 2005
Enhancing digestibility and ethanol yield of Populus wood via expression of an engineered monolignol 4-O-methyltransferase Cai, Yuanheng; Zhang, Kewei; Kim, Hoon Nature Communications, Vol. 7, Issue 1 https://doi.org/10.1038/ncomms11989	journal	June 2016
Enzymatic diversity of the Clostridium thermocellum cellulosome is crucial for the degradation of crystalline cellulose and plant biomass Hirano, Katsuaki; Kurosaki, Masahiro; Nihei, Satoshi Scientific Reports, Vol. 6, Issue 1 https://doi.org/10.1038/srep35709	journal	October 2016
Enzymatic hydrolysis of lignocellulose: SEC-MALLS analysis and reaction mechanism Du, Ruoyu; Huang, Renliang; Su, Rongxin RSC Adv., Vol. 3, Issue 6 https://doi.org/10.1039/C2RA21781C	journal	January 2013
Cellulose and lignin colocalization at the plant cell wall surface limits microbial hydrolysis of Populus biomass Dumitrache, Alexandru; Tolbert, Allison; Natzke, Jace Green Chemistry, Vol. 19, Issue 9 https://doi.org/10.1039/C7GC00346C	journal	January 2017
Fungal cellulases and complexed cellulosomal enzymes exhibit synergistic mechanisms in cellulose deconstruction Resch, Michael G.; Donohoe, Bryon S.; Baker, John O. Energy & Environmental Science, Vol. 6, Issue 6 https://doi.org/10.1039/c3ee00019b	journal	January 2013
Digestion of crystalline cellulose substrates by the Clostridium thermocellum cellulosome: structural and morphological aspects Boisset, Claire; Chanzy, Henri; Henrissat, Bernard Biochemical Journal, Vol. 340, Issue 3 https://doi.org/10.1042/bj3400829	journal	June 1999
Lignin content in natural Populus variants affects sugar release Studer, M. H.; DeMartini, J. D.; Davis, M. F. Proceedings of the National Academy of Sciences, Vol. 108, Issue 15, p. 6300-6305 https://doi.org/10.1073/pnas.1009252108	journal	March 2011
Genetic manipulation of lignin reduces recalcitrance and improves ethanol production from switchgrass Fu, Chunxiang; Mielenz, Jonathan R.; Xiao, Xirong Proceedings of the National Academy of Sciences, Vol. 108, Issue 9, p. 3803-3808 https://doi.org/10.1073/pnas.1100310108	journal	February 2011
Biosynthesis and incorporation of side-chain-truncated lignin monomers to reduce lignin polymerization and enhance saccharification: Reduction in lignin DP enhances saccharification Eudes, Aymerick; George, Anthe; Mukerjee, Purba Plant Biotechnology Journal, Vol. 10, Issue 5 https://doi.org/10.1111/j.1467-7652.2012.00692.x	journal	March 2012
Two-year field analysis of reduced recalcitrance transgenic switchgrass Baxter, Holly L.; Mazarei, Mitra; Labbe, Nicole Plant Biotechnology Journal, Vol. 12, Issue 7 https://doi.org/10.1111/pbi.12195	journal	April 2014
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 Zverlov, V. V.; Klupp, M.; Krauss, J. Journal of Bacteriology, Vol. 190, Issue 12 https://doi.org/10.1128/JB.00097-08	journal	April 2008
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
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
Assessing the molecular structure basis for biomass recalcitrance during dilute acid and hydrothermal pretreatments Pu, Yunqiao; Hu, Fan; Huang, Fang Biotechnology for Biofuels, Vol. 6, Issue 1 https://doi.org/10.1186/1754-6834-6-15	journal	January 2013
Consolidated bioprocessing of transgenic switchgrass by an engineered and evolved Clostridium thermocellum strain Yee, Kelsey L.; Rodriguez Jr, Miguel; Thompson, Olivia A. Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-75	journal	January 2014
Elimination of hydrogenase active site assembly blocks H2 production and increases ethanol yield in Clostridium thermocellum Biswas, Ranjita; Zheng, Tianyong; Olson, Daniel G. Biotechnology for Biofuels, Vol. 8, Issue 1 https://doi.org/10.1186/s13068-015-0204-4	journal	January 2015
Consolidated bioprocessing of Populus using Clostridium (Ruminiclostridium) thermocellum: a case study on the impact of lignin composition and structure Dumitrache, Alexandru; Akinosho, Hannah; Rodriguez, Miguel Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-016-0445-x	journal	February 2016
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
Effects of Cellulose Crystallinity, Hemicellulose, and Lignin on the Enzymatic Hydrolysis of Miscanthus sinensis to Monosaccharides Yoshida, Makoto; Liu, Yuan; Uchida, Satoshi Bioscience, Biotechnology, and Biochemistry, Vol. 72, Issue 3 https://doi.org/10.1271/bbb.70689	journal	March 2008
Increase in Ethanol Yield via Elimination of Lactate Production in an Ethanol-Tolerant Mutant of Clostridium thermocellum Biswas, Ranjita; Prabhu, Sandeep; Lynd, Lee R. PLoS ONE, Vol. 9, Issue 2 https://doi.org/10.1371/journal.pone.0086389	journal	February 2014
Effect of cellulose structure on enzymatic hydrolysis Ioelovich, Michael; Morag, Ely BioResources, Vol. 6, Issue 3 https://doi.org/10.15376/biores.6.3.2818-2835	journal	June 2011
The emergence of Clostridium thermocellum as a high utility candidate for consolidated bioprocessing applications Akinosho, Hannah; Yee, Kelsey; Close, Dan Frontiers in Chemistry, Vol. 2 https://doi.org/10.3389/fchem.2014.00066	journal	August 2014

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59 BASIC BIOLOGICAL SCIENCES
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Populus trichocarpa
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Title: Lignin Exhibits Recalcitrance-Associated Features Following the Consolidated Bioprocessing of Populus trichocarpa Natural Variants

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