An In-Depth Understanding of Biomass Recalcitrance Using Natural Poplar Variants as the Feedstock

Meng, Xianzhi; Pu, Yunqiao; Yoo, Chang Geun; Li, Mi; Bali, Garima; Park, Doh-Yeon; Gjersing, Erica; Davis, Mark F.; Muchero, Wellington; Tuskan, Gerald A.; Tschaplinski, Timothy J.; Ragauskas, Arthur J.

doi:10.1002/cssc.201601303

Title: An In-Depth Understanding of Biomass Recalcitrance Using Natural Poplar Variants as the Feedstock

Journal Article · Wed Nov 23 00:00:00 EST 2016 · ChemSusChem

DOI:https://doi.org/10.1002/cssc.201601303· OSTI ID:1343083

Meng, Xianzhi ^[1]; Pu, Yunqiao ^[2]; Yoo, Chang Geun ^[2]; Li, Mi ^[2]; Bali, Garima ^[3]; Park, Doh-Yeon ^[3]; Gjersing, Erica ^[4]; Davis, Mark F. ^[4]; Muchero, Wellington ^[2]; Tuskan, Gerald A. ^[2]; Tschaplinski, Timothy J. ^[2]; Ragauskas, Arthur J. ^[5]

Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center and Biosciences Division
Georgia Inst. of Technology, Atlanta, GA (United States). Renewable Bioproducts Inst.
Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center and Biosciences Division; National Renewable Energy Lab. (NREL), Golden, CO (United States)
Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering and Biosciences Division and Inst. of Agriculture

Here, in an effort to better understand the biomass recalcitrance, six natural poplar variants were selected as feedstocks based on previous sugar release analysis. Compositional analysis and physicochemical characterizations of these poplars were performed and the correlations between these physicochemical properties and enzymatic hydrolysis yield were investigated. Gel permeation chromatography (GPC) and ¹³C solid state NMR were used to determine the degree of polymerization (DP) and crystallinity index (CrI) of cellulose, and the results along with the sugar release study indicated that cellulose DP likely played a more important role in enzymatic hydrolysis. Simons’ stain revealed that the accessible surface area of substrate significantly varied among these variants from 17.3 to 33.2 mg g$$–1\atop{biomass}$$ as reflected by dye adsorption, and cellulose accessibility was shown as one of the major factors governing substrates digestibility. HSQC and ³¹P NMR analysis detailed the structural features of poplar lignin variants. Overall, cellulose relevant factors appeared to have a stronger correlation with glucose release, if any, than lignin structural features. Lignin structural features, such as a phenolic hydroxyl group and the ratio of syringyl and guaiacyl (S/G), were found to have a more convincing impact on xylose release. Low lignin content, low cellulose DP, and high cellulose accessibility generally favor enzymatic hydrolysis; however, recalcitrance cannot be simply judged on any single substrate factor.

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Research Organization:: National Renewable Energy Laboratory (NREL), Golden, CO (United States); Oak Ridge National Laboratory (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)

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

Grant/Contract Number:: AC36-08GO28308; AC05-00OR22725

OSTI ID:: 1343083

Alternate ID(s):: OSTI ID: 1337507

Report Number(s):: NREL/JA-5100-67897

Journal Information:: ChemSusChem, Vol. 10, Issue 1; ISSN 1864-5631

Publisher:: ChemPubSoc EuropeCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 75 works

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References (45)

Substrate and Enzyme Characteristics that Limit Cellulose Hydrolysis Mansfield, S. D.; Mooney, C.; Saddler, J. N. Biotechnology Progress, Vol. 15, Issue 5 https://doi.org/10.1021/bp9900864	journal	October 1999
Sodium hydroxide pretreatment and enzymatic hydrolysis of coastal Bermuda grass Wang, Ziyu; Keshwani, Deepak R.; Redding, Arthur P. Bioresource Technology, Vol. 101, Issue 10 https://doi.org/10.1016/j.biortech.2009.12.097	journal	May 2010
The characterization of pretreated lignocellulosic substrates prior to enzymatic hydrolysis, part 1: A modified Simons' staining technique Chandra, Richard; Ewanick, Shannon; Hsieh, Carmen Biotechnology Progress, Vol. 24, Issue 5 https://doi.org/10.1002/btpr.33	journal	September 2008
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
Characterization and analysis of the molecular weight of lignin for biorefining studies Tolbert, Allison; Akinosho, Hannah; Khunsupat, Ratayakorn Biofuels, Bioproducts and Biorefining, Vol. 8, Issue 6 https://doi.org/10.1002/bbb.1500	journal	June 2014
Application of quantitative 31P NMR in biomass lignin and biofuel precursors characterization Pu, Yunqiao; Cao, Shilin; Ragauskas, Arthur J. Energy & Environmental Science, Vol. 4, Issue 9 https://doi.org/10.1039/c1ee01201k	journal	January 2011
Physicochemical Structural Changes of Poplar and Switchgrass during Biomass Pretreatment and Enzymatic Hydrolysis Meng, Xianzhi; Sun, Qining; Kosa, Matyas ACS Sustainable Chemistry & Engineering, Vol. 4, Issue 9 https://doi.org/10.1021/acssuschemeng.6b00603	journal	July 2016
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
Pretreatment and Lignocellulosic Chemistry Hu, Fan; Ragauskas, Art BioEnergy Research, Vol. 5, Issue 4 https://doi.org/10.1007/s12155-012-9208-0	journal	May 2012
Structural Characterization of Lignin in Wild-Type versus COMT Down-Regulated Switchgrass Samuel, Reichel; Pu, Yunqiao; Jiang, Nan Frontiers in Energy Research, Vol. 1 https://doi.org/10.3389/fenrg.2013.00014	journal	January 2014
Microbial Cellulose Utilization: Fundamentals and Biotechnology Lynd, L. R.; Weimer, P. J.; van Zyl, W. H. Microbiology and Molecular Biology Reviews, Vol. 66, Issue 3, p. 506-577 https://doi.org/10.1128/MMBR.66.3.506-577.2002	journal	September 2002
Effects of drying-induced fiber hornification on enzymatic saccharification of lignocelluloses Luo, Xiaolin; Zhu, J. Y. Enzyme and Microbial Technology, Vol. 48, Issue 1 https://doi.org/10.1016/j.enzmictec.2010.09.014	journal	January 2011
Effect of Lignin Chemistry on the Enzymatic Hydrolysis of Woody Biomass Yu, Zhiying; Gwak, Ki-Seob; Treasure, Trevor ChemSusChem, Vol. 7, Issue 7 https://doi.org/10.1002/cssc.201400042	journal	June 2014
Analyzing cellulose degree of polymerization and its relevancy to cellulosic ethanol Hallac, Bassem B.; Ragauskas, Arthur J. Biofuels, Bioproducts and Biorefining, Vol. 5, Issue 2 https://doi.org/10.1002/bbb.269	journal	January 2011
Effects of wet-pressing-induced fiber hornification on enzymatic saccharification of lignocelluloses Luo, X. L.; Zhu, J. Y.; Gleisner, R. Cellulose, Vol. 18, Issue 4 https://doi.org/10.1007/s10570-011-9541-z	journal	April 2011
Antisense Down-Regulation of 4CL Expression Alters Lignification, Tree Growth, and Saccharification Potential of Field-Grown Poplar Voelker, Steven L.; Lachenbruch, Barbara; Meinzer, Frederick C. Plant Physiology, Vol. 154, Issue 2 https://doi.org/10.1104/pp.110.159269	journal	August 2010
Theory, practice and prospects of X-ray and neutron scattering for lignocellulosic biomass characterization: towards understanding biomass pretreatment Cheng, Gang; Zhang, Xin; Simmons, Blake Energy & Environmental Science, Vol. 8, Issue 2 https://doi.org/10.1039/C4EE03147D	journal	January 2015
Genomics of cellulosic biofuels Rubin, Edward M. Nature, Vol. 454, Issue 7206 https://doi.org/10.1038/nature07190	journal	August 2008
Biomass Characterization: Recent Progress in Understanding Biomass Recalcitrance Foston, Marcus; Ragauskas, Arthur J. Industrial Biotechnology, Vol. 8, Issue 4 https://doi.org/10.1089/ind.2012.0015	journal	August 2012
Helically agitated mixing in dry dilute acid pretreatment enhances the bioconversion of corn stover into ethanol He, Yanqing; Zhang, Longping; Zhang, Jian Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-1	journal	January 2014
Structural Transformation of Isolated Poplar and Switchgrass Lignins during Dilute Acid Treatment Sun, Qining; Pu, Yunqiao; Meng, Xianzhi ACS Sustainable Chemistry & Engineering, Vol. 3, Issue 9 https://doi.org/10.1021/acssuschemeng.5b00426	journal	August 2015
Biomass Recalcitrance: Engineering Plants and Enzymes for Biofuels Production Himmel, M. E.; Ding, S.-Y.; Johnson, D. K. Science, Vol. 315, Issue 5813, p. 804-807 https://doi.org/10.1126/science.1137016	journal	February 2007
Recent advances in understanding the role of cellulose accessibility in enzymatic hydrolysis of lignocellulosic substrates Meng, Xianzhi; Ragauskas, Arthur Jonas Current Opinion in Biotechnology, Vol. 27 https://doi.org/10.1016/j.copbio.2014.01.014	journal	June 2014
Unconventional Relationships for Hemicellulose Hydrolysis and Subsequent Cellulose Digestion Yang, Bin; Gray, Matthew C.; Liu, Chaogang ACS Symposium Series https://doi.org/10.1021/bk-2004-0889.ch006	book	July 2004
Cellulose crystallinity - a key predictor of the enzymatic hydrolysis rate: Cellulose crystallinity Hall, Mélanie; Bansal, Prabuddha; Lee, Jay H. FEBS Journal, Vol. 277, Issue 6 https://doi.org/10.1111/j.1742-4658.2010.07585.x	journal	February 2010
Porosity and Its Effect on the Digestibility of Dilute Sulfuric Acid Pretreated Corn Stover Ishizawa, Claudia I.; Davis, Mark F.; Schell, Daniel F. Journal of Agricultural and Food Chemistry, Vol. 55, Issue 7 https://doi.org/10.1021/jf062131a	journal	April 2007
Inhibition of cellulase, xylanase and β-glucosidase activities by softwood lignin preparations Berlin, Alex; Balakshin, Mikhail; Gilkes, Neil Journal of Biotechnology, Vol. 125, Issue 2, p. 198-209 https://doi.org/10.1016/j.jbiotec.2006.02.021	journal	September 2006
The Path Forward for Biofuels and Biomaterials Ragauskas, Arthur J.; Williams, Charlotte K.; Davison, Brian H. Science, Vol. 311, Issue 5760, p. 484-489 https://doi.org/10.1126/science.1114736	journal	January 2006
The effect of initial pore volume and lignin content on the enzymatic hydrolysis of softwoods Mooney, Caitriona A.; Mansfield, Shawn D.; Touhy, Maria G. Bioresource Technology, Vol. 64, Issue 2, p. 113-119 https://doi.org/10.1016/S0960-8524(97)00181-8	journal	May 1998
Substrate-Related Factors Affecting Enzymatic Saccharification of Lignocelluloses: Our Recent Understanding Leu, Shao-Yuan; Zhu, J. Y. BioEnergy Research, Vol. 6, Issue 2 https://doi.org/10.1007/s12155-012-9276-1	journal	November 2012
High-resolution genetic mapping of allelic variants associated with cell wall chemistry in Populus Muchero, Wellington; Guo, Jianjun; DiFazio, Stephen P. BMC Genomics, Vol. 16, Issue 1 https://doi.org/10.1186/s12864-015-1215-z	journal	January 2015
Increase in 4-Coumaryl Alcohol Units during Lignification in Alfalfa ( Medicago sativa ) Alters the Extractability and Molecular Weight of Lignin Ziebell, Angela; Gracom, Kristen; Katahira, Rui Journal of Biological Chemistry, Vol. 285, Issue 50 https://doi.org/10.1074/jbc.M110.137315	journal	October 2010
Changes in lignocellulosic supramolecular and ultrastructure during dilute acid pretreatment of Populus and switchgrass Foston, Marcus; Ragauskas, Art J. Biomass and Bioenergy, Vol. 34, Issue 12 https://doi.org/10.1016/j.biombioe.2010.07.023	journal	December 2010
Comparison Study on the Biomass Recalcitrance of Different Tissue Fractions of Sugarcane Culm Brienzo, Michel; Ferreira, Solange; Vicentim, Marcos P. BioEnergy Research, Vol. 7, Issue 4 https://doi.org/10.1007/s12155-014-9487-8	journal	June 2014
Investigating plant cell wall components that affect biomass recalcitrance in poplar and switchgrass DeMartini, Jaclyn D.; Pattathil, Sivakumar; Miller, Jeffrey S. Energy & Environmental Science, Vol. 6, Issue 3 https://doi.org/10.1039/c3ee23801f	journal	January 2013
Techno-economic evaluation of integrated first- and second-generation ethanol production from grain and straw Joelsson, Elisabeth; Erdei, Borbála; Galbe, Mats Biotechnology for Biofuels, Vol. 9, Issue 1 https://doi.org/10.1186/s13068-015-0423-8	journal	January 2016
Effect of structural and physico-chemical features of cellulosic substrates on the efficiency of enzymatic hydrolysis Sinitsyn, A. P.; Gusakov, A. V.; Vlasenko, E. Yu. Applied Biochemistry and Biotechnology, Vol. 30, Issue 1 https://doi.org/10.1007/BF02922023	journal	July 1991
Cellulose Isolation Methodology for NMR Analysis of Cellulose Ultrastructure Foston, Marcus B.; Hubbell, Chistopher A.; Ragauskas, Art J. Materials, Vol. 4, Issue 11 https://doi.org/10.3390/ma4111985	journal	November 2011
Insights into the effect of dilute acid, hot water or alkaline pretreatment on the cellulose accessible surface area and the overall porosity of Populus Meng, Xianzhi; Wells, Tyrone; Sun, Qining Green Chemistry, Vol. 17, Issue 8 https://doi.org/10.1039/C5GC00689A	journal	January 2015
Role of Functional Groups in Lignin Inhibition of Enzymatic Hydrolysis of Cellulose to Glucose Pan, Xuejun Journal of Biobased Materials and Bioenergy, Vol. 2, Issue 1 https://doi.org/10.1166/jbmb.2008.005	journal	March 2008
Toward an aggregated understanding of enzymatic hydrolysis of cellulose: Noncomplexed cellulase systems Zhang, Yi-Heng Percival; Lynd, Lee R. Biotechnology and Bioengineering, Vol. 88, Issue 7, p. 797-824 https://doi.org/10.1002/bit.20282	journal	November 2004
Variation of S/G Ratio and Lignin Content in a <i>Populus</i> Family Influences the Release of Xylose by Dilute Acid Hydrolysis Davison, Brian H.; Drescher, Sadie R.; Tuskan, Gerald A. Applied Biochemistry and Biotechnology, Vol. 130, Issue 1-3 https://doi.org/10.1385/ABAB:130:1:427	journal	January 2006
Determination of porosity of lignocellulosic biomass before and after pretreatment by using Simons’ stain and NMR techniques Meng, Xianzhi; Foston, Marcus; Leisen, Johannes Bioresource Technology, Vol. 144 https://doi.org/10.1016/j.biortech.2013.06.091	journal	September 2013
Enhancing the enzymatic hydrolysis of lignocellulosic biomass by increasing the carboxylic acid content of the associated lignin Nakagame, Seiji; Chandra, Richard P.; Kadla, John F. Biotechnology and Bioengineering, Vol. 108, Issue 3 https://doi.org/10.1002/bit.22981	journal	November 2010
Lignin content in natural Populus variants affects sugar release Studer, Michael Hans-Peter; DeMartini, J. D.; Davis, M. F. National Academy of Sciences https://doi.org/10.24451/arbor.10127	text	January 2011

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