Progressive structural changes of Avicel, bleached softwood, and bacterial cellulose during enzymatic hydrolysis

Kafle, Kabindra; Shin, Heenae; Lee, Christopher M.; Park, Sunkyu; Kim, Seong H.

doi:10.1038/srep15102

Title: Progressive structural changes of Avicel, bleached softwood, and bacterial cellulose during enzymatic hydrolysis

Journal Article · Wed Oct 14 00:00:00 EDT 2015 · Scientific Reports

DOI:https://doi.org/10.1038/srep15102· OSTI ID:1239291

Kafle, Kabindra ^[1]; Shin, Heenae ^[2]; Lee, Christopher M. ^[1]; Park, Sunkyu ^[2]; Kim, Seong H. ^[1]

Pennsylvania State Univ., University Park, PA (United States)
North Carolina State Univ., Raleigh, NC (United States)

A comprehensive picture of structural changes of cellulosic biomass during enzymatic hydrolysis is essential for a better understanding of enzymatic actions and development of more efficient enzymes. In this study, a suite of analytical techniques including sum frequency generation (SFG) spectroscopy, infrared (IR) spectroscopy, x-ray diffraction (XRD), and x-ray photoelectron spectroscopy (XPS) were employed for lignin-free model biomass samples—Avicel, bleached softwood, and bacterial cellulose—to find correlations between the decrease in hydrolysis rate over time and the structural or chemical changes of biomass during the hydrolysis reaction. The results showed that the decrease in hydrolysis rate over time appears to correlate with the irreversible deposition of non-cellulosic species (either reaction side products or denatured enzymes, or both) on the cellulosic substrate surface. The crystallinity, degree of polymerization, and meso-scale packing of cellulose do not seem to positively correlate with the decrease in hydrolysis rate observed for all three substrates tested in this study. Moreover, it was also found that the cellulose Iα component of the bacterial cellulose is preferentially hydrolyzed by the enzyme than the cellulose Iβ component.

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Research Organization:: Pennsylvania State Univ., University Park, PA (United States); Energy Frontier Research Centers (EFRC) (United States). Center for Lignocellulose Structure and Formation (CLSF)

Sponsoring Organization:: USDOE Office of Science (SC), Basic Energy Sciences (BES)

Grant/Contract Number:: SC0001090

OSTI ID:: 1239291

Journal Information:: Scientific Reports, Vol. 5; ISSN 2045-2322

Publisher:: Nature Publishing GroupCopyright Statement

Country of Publication:: United States

Language:: English

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Cited by: 53 works

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References (60)

Fuel Ethanol from Cellulosic Biomass Lynd, L. R.; Cushman, J. H.; Nichols, R. J. Science, Vol. 251, Issue 4999 https://doi.org/10.1126/science.251.4999.1318	journal	March 1991
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
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
Correlation between X-ray diffraction measurements of cellulose crystalline structure and the susceptibility to microbial cellulase Sasaki, Takashi; Tanaka, Takashi; Nanbu, Noriko Biotechnology and Bioengineering, Vol. 21, Issue 6 https://doi.org/10.1002/bit.260210608	journal	June 1979
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
Effect of enzymatic hydrolysis on the morphology and fine structure of pretreated cellulosic residues Ramos, L. P.; Nazhad, M. M.; Saddler, J. N. Enzyme and Microbial Technology, Vol. 15, Issue 10 https://doi.org/10.1016/0141-0229(93)90093-H	journal	October 1993
Effect of crystallinity and degree of polymerization of cellulose on enzymatic saccharification Puri, Vinod P. Biotechnology and Bioengineering, Vol. 26, Issue 10 https://doi.org/10.1002/bit.260261010	journal	October 1984
Comparison of pretreatment methods on the basis of available surface area Thompson, David N.; Chen, Hsin-Chih; Grethlein, Hans E. Bioresource Technology, Vol. 39, Issue 2, p. 155-163 https://doi.org/10.1016/0960-8524(92)90135-K	journal	January 1992
Pretreatment for enhanced hydrolysis of cellulosic biomass Grethlein, Hans E. Biotechnology Advances, Vol. 2, Issue 1, p. 43-62 https://doi.org/10.1016/0734-9750(84)90240-4	journal	January 1984
Common processes drive the thermochemical pretreatment of lignocellulosic biomass Langan, Paul; Petridis, Loukas; O'Neill, Hugh M. Green Chem., Vol. 16, Issue 1 https://doi.org/10.1039/C3GC41962B	journal	January 2014
Effects of Delignification on Crystalline Cellulose in Lignocellulose Biomass Characterized by Vibrational Sum Frequency Generation Spectroscopy and X-ray Diffraction Kafle, Kabindra; Lee, Christopher M.; Shin, Heenae BioEnergy Research, Vol. 8, Issue 4 https://doi.org/10.1007/s12155-015-9627-9	journal	May 2015
Structural coarsening of aspen wood by hydrothermal pretreatment monitored by small- and wide-angle scattering of X-rays and neutrons on oriented specimens Nishiyama, Yoshiharu; Langan, Paul; O’Neill, Hugh Cellulose, Vol. 21, Issue 2 https://doi.org/10.1007/s10570-013-0069-2	journal	October 2013
Cellulase digestibility of pretreated biomass is limited by cellulose accessibility Jeoh, Tina; Ishizawa, Claudia I.; Davis, Mark F. Biotechnology and Bioengineering, Vol. 98, Issue 1, p. 112-122 https://doi.org/10.1002/bit.21408	journal	January 2007
Effects of hemicellulose removal on cellulose fiber structure and recycling characteristics of eucalyptus pulp Wan, JinQuan; Wang, Yan; Xiao, Qing Bioresource Technology, Vol. 101, Issue 12 https://doi.org/10.1016/j.biortech.2010.01.026	journal	June 2010
Characterization of crystalline cellulose in biomass: Basic principles, applications, and limitations of XRD, NMR, IR, Raman, and SFG Kim, Seong H.; Lee, Christopher M.; Kafle, Kabindra Korean Journal of Chemical Engineering, Vol. 30, Issue 12 https://doi.org/10.1007/s11814-013-0162-0	journal	October 2013
Cellulose crystallinity index: measurement techniques and their impact on interpreting cellulase performance Park, Sunkyu; Baker, John O.; Himmel, Michael E. Biotechnology for Biofuels, Vol. 3, Issue 1 https://doi.org/10.1186/1754-6834-3-10	journal	January 2010
Quantification of crystalline cellulose in lignocellulosic biomass using sum frequency generation (SFG) vibration spectroscopy and comparison with other analytical methods Barnette, Anna L.; Lee, Christopher; Bradley, Laura C. Carbohydrate Polymers, Vol. 89, Issue 3 https://doi.org/10.1016/j.carbpol.2012.04.014	journal	July 2012
Cellulose polymorphy, crystallite size, and the Segal Crystallinity Index French, Alfred D.; Santiago Cintrón, Michael Cellulose, Vol. 20, Issue 1 https://doi.org/10.1007/s10570-012-9833-y	journal	February 2013
Cellulose polymorphism study with sum-frequency-generation (SFG) vibration spectroscopy: identification of exocyclic CH2OH conformation and chain orientation Lee, Christopher M.; Mittal, Ashutosh; Barnette, Anna L. Cellulose, Vol. 20, Issue 3 https://doi.org/10.1007/s10570-013-9917-3	journal	April 2013
Nanodomains of I _α and I _β Cellulose in Algal Microfibrils Imai, Tomoya; Sugiyama, Junji Macromolecules, Vol. 31, Issue 18 https://doi.org/10.1021/ma980664h	journal	September 1998
Enzymatic Hydrolysis of Cellulose (II): X-Ray Photoelectron Spectroscopy Studies on Cellulase Adsorption. Effect of the Surfactant Tween 85 Gama, F. M.; Mota, M. Biocatalysis and Biotransformation, Vol. 15, Issue 3 https://doi.org/10.3109/10242429709103512	journal	January 1997
Probing crystal structure and mesoscale assembly of cellulose microfibrils in plant cell walls, tunicate tests, and bacterial films using vibrational Sum Frequency Generation (SFG) spectroscopy Lee, Christopher M.; Kafle, Kabindra; Park, Yong Bum Physical Chemistry Chemical Physics, Vol. 16, Issue 22 https://doi.org/10.1039/c4cp00515e	journal	January 2014
Monitoring Meso-Scale Ordering of Cellulose in Intact Plant Cell Walls Using Sum Frequency Generation Spectroscopy Park, Y. B.; Lee, C. M.; Koo, B. -W. PLANT PHYSIOLOGY, Vol. 163, Issue 2 https://doi.org/10.1104/pp.113.225235	journal	August 2013
Selective Detection of Crystalline Cellulose in Plant Cell Walls with Sum-Frequency-Generation (SFG) Vibration Spectroscopy Barnette, Anna L.; Bradley, Laura C.; Veres, Brandon D. Biomacromolecules, Vol. 12, Issue 7 https://doi.org/10.1021/bm200518n	journal	July 2011
Cellulose microfibril orientation in onion (Allium cepa L.) epidermis studied by atomic force microscopy (AFM) and vibrational sum frequency generation (SFG) spectroscopy Kafle, Kabindra; Xi, Xiaoning; Lee, Christopher M. Cellulose, Vol. 21, Issue 2 https://doi.org/10.1007/s10570-013-0121-2	journal	December 2013
Cellulose polymorphs and physical properties of cotton fabrics processed with commercial textile mills for mercerization and liquid ammonia treatments Kafle, Kabindra; Greeson, Kenneth; Lee, Christopher Textile Research Journal, Vol. 84, Issue 16 https://doi.org/10.1177/0040517514527379	journal	March 2014
Vibrational sum-frequency-generation (SFG) spectroscopy study of the structural assembly of cellulose microfibrils in reaction woods Kafle, Kabindra; Shi, Rui; Lee, Christopher M. Cellulose, Vol. 21, Issue 4 https://doi.org/10.1007/s10570-014-0322-3	journal	June 2014
Cellulose produced by Gluconacetobacter xylinus strains ATCC 53524 and ATCC 23768: Pellicle formation, post-synthesis aggregation and fiber density Lee, Christopher M.; Gu, Jin; Kafle, Kabindra Carbohydrate Polymers, Vol. 133 https://doi.org/10.1016/j.carbpol.2015.06.091	journal	November 2015
Effect of mechanical disruption on the effectiveness of three reactors used for dilute acid pretreatment of corn stover Part 1: chemical and physical substrate analysis Wang, Wei; Chen, Xiaowen; Donohoe, Bryon S. Biotechnology for Biofuels, Vol. 7, Issue 1 https://doi.org/10.1186/1754-6834-7-57	journal	January 2014
An Empirical Method for Estimating the Degree of Crystallinity of Native Cellulose Using the X-Ray Diffractometer Segal, L.; Creely, J. J.; Martin, A. E. Textile Research Journal, Vol. 29, Issue 10 https://doi.org/10.1177/004051755902901003	journal	October 1959
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
Evaluation of several microcrystalline celluloses obtained from agricultural by-products Rojas, John; Lopez, Alvin; Guisao, Santiago Journal of Advanced Pharmaceutical Technology & Research, Vol. 2, Issue 3 https://doi.org/10.4103/2231-4040.85527	journal	January 2011
Effects of Plant Cell Wall Matrix Polysaccharides on Bacterial Cellulose Structure Studied with Vibrational Sum Frequency Generation Spectroscopy and X-ray Diffraction Park, Yong Bum; Lee, Christopher M.; Kafle, Kabindra Biomacromolecules, Vol. 15, Issue 7 https://doi.org/10.1021/bm500567v	journal	May 2014
Study on crystal structures of enzyme-hydrolyzed cellulosic materials by X-ray diffraction Cao, Yu; Tan, Huimin Enzyme and Microbial Technology, Vol. 36, Issue 2-3 https://doi.org/10.1016/j.enzmictec.2004.09.002	journal	February 2005
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
Correlations of Apparent Cellulose Crystallinity Determined by XRD, NMR, IR, Raman, and SFG Methods Lee, Christopher; Dazen, Kevin; Kafle, Kabindra Advances in Polymer Science https://doi.org/10.1007/12_2015_320	book	January 2015
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
Changes in Submicrometer Structure of Enzymatically Hydrolyzed Microcrystalline Cellulose Penttilä, Paavo A.; Várnai, Anikó; Leppänen, Kirsi Biomacromolecules, Vol. 11, Issue 4 https://doi.org/10.1021/bm1001119	journal	April 2010
Molecular-Scale Investigations of Cellulose Microstructure during Enzymatic Hydrolysis Santa-Maria, Monica; Jeoh, Tina Biomacromolecules, Vol. 11, Issue 8 https://doi.org/10.1021/bm100366h	journal	August 2010
Visualizing cellulase activity Bubner, Patricia; Plank, Harald; Nidetzky, Bernd Biotechnology and Bioengineering, Vol. 110, Issue 6 https://doi.org/10.1002/bit.24884	journal	March 2013
Changes in pore size distribution during the drying of cellulose fibers as measured by differential scanning calorimetry Park, S.; Venditti, R.; Jameel, H. Carbohydrate Polymers, Vol. 66, Issue 1 https://doi.org/10.1016/j.carbpol.2006.02.026	journal	October 2006
Effect of pore size in substrate and diffusion of enzyme on hydrolysis of cellulosic materials with cellulases Tanaka, Mitsuo; Ikesaka, Makoto; Matsuno, Ryuichi Biotechnology and Bioengineering, Vol. 32, Issue 5 https://doi.org/10.1002/bit.260320515	journal	August 1988
Sum-Frequency-Generation Vibration Spectroscopy and Density Functional Theory Calculations with Dispersion Corrections (DFT-D2) for Cellulose Iα and Iβ Lee, Christopher M.; Mohamed, Naseer M. A.; Watts, Heath D. The Journal of Physical Chemistry B, Vol. 117, Issue 22 https://doi.org/10.1021/jp402998s	journal	May 2013
Nanostructure of cellulose microfibrils in spruce wood Fernandes, A. N.; Thomas, L. H.; Altaner, C. M. Proceedings of the National Academy of Sciences, Vol. 108, Issue 47 https://doi.org/10.1073/pnas.1108942108	journal	November 2011
Reproducible XPS on biopolymers: cellulose studies Johansson, Leena-Sisko; Campbell, J. M. Surface and Interface Analysis, Vol. 36, Issue 8 https://doi.org/10.1002/sia.1827	journal	August 2004
XPS characterization of naturally aged wood Popescu, Carmen-Mihaela; Tibirna, Carmen-Mihaela; Vasile, Cornelia Applied Surface Science, Vol. 256, Issue 5 https://doi.org/10.1016/j.apsusc.2009.08.087	journal	December 2009
Changes in the enzymatic hydrolysis rate of Avicel cellulose with conversion Yang, Bin; Willies, Deidre M.; Wyman, Charles E. Biotechnology and Bioengineering, Vol. 94, Issue 6 https://doi.org/10.1002/bit.20942	journal	January 2006
Evaluation of the factors affecting avicel reactivity using multi-stage enzymatic hydrolysis Yu, Zhiying; Jameel, Hasan; Chang, Hou-min Biotechnology and Bioengineering, Vol. 109, Issue 5 https://doi.org/10.1002/bit.24386	journal	December 2011
Mineral components of plant cell walls Jones, L. H. P. The American Journal of Clinical Nutrition, Vol. 31, Issue 10 https://doi.org/10.1093/ajcn/31.10.S94	journal	October 1978
Structural Features and Properties of Bacterial Cellulose Produced in Agitated Culture Watanabe, Kunihiko; Tabuchi, Mari; Morinaga, Yasushi Cellulose, Vol. 5, Issue 3, p. 187-200 https://doi.org/10.1023/A:1009272904582	journal	September 1998
Effects of alkaline or liquid-ammonia treatment on crystalline cellulose: changes in crystalline structure and effects on enzymatic digestibility Mittal, Ashutosh; Katahira, Rui; Himmel, Michael E. Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-41	journal	January 2011
Molecular-Level Origins of Biomass Recalcitrance: Decrystallization Free Energies for Four Common Cellulose Polymorphs Beckham, Gregg T.; Matthews, James F.; Peters, Baron The Journal of Physical Chemistry B, Vol. 115, Issue 14 https://doi.org/10.1021/jp1106394	journal	April 2011
The enzymatic susceptibility of cellulose microfibrils of the algal-bacterial type and the cotton-ramie type Hayashi, Noriko; Sugiyama, Junji; Okano, Takeshi Carbohydrate Research, Vol. 305, Issue 2 https://doi.org/10.1016/S0008-6215(97)10032-5	journal	December 1997
Enzymatic hydrolysis of different allomorphic forms of microcrystalline cellulose Ciolacu, Diana; Gorgieva, Selestina; Tampu, Daniel Cellulose, Vol. 18, Issue 6 https://doi.org/10.1007/s10570-011-9601-4	journal	October 2011
Allomorphs of native crystalline cellulose I evaluated by two equatoriald-spacings Wada, Masahisa; Okano, Takeshi; Sugiyama, Junji Journal of Wood Science, Vol. 47, Issue 2 https://doi.org/10.1007/BF00780560	journal	April 2001
Idealized powder diffraction patterns for cellulose polymorphs French, Alfred D. Cellulose, Vol. 21, Issue 2 https://doi.org/10.1007/s10570-013-0030-4	journal	August 2013
In situ crystallization of bacterial cellulose II. Influences of different polymeric additives on the formation of celluloses Iα and Iβ at the early stage of incubation Yamamoto, Hiroyuki; Horii, Fumitaka; Hirai, Asako Cellulose, Vol. 3, Issue 1 https://doi.org/10.1007/BF02228804	journal	December 1996
Varietal difference in cellulose microfibril dimensions observed by infrared spectroscopy Horikawa, Yoshiki; Clair, Bruno; Sugiyama, Junji Cellulose, Vol. 16, Issue 1 https://doi.org/10.1007/s10570-008-9252-2	journal	September 2008
Evaluation of ammonia fibre expansion (AFEX) pretreatment for enzymatic hydrolysis of switchgrass harvested in different seasons and locations Bals, Bryan; Rogers, Chad; Jin, Mingjie Biotechnology for Biofuels, Vol. 3, Issue 1 https://doi.org/10.1186/1754-6834-3-1	journal	January 2010
In planta expression of A. cellulolyticus Cel5A endocellulase reduces cell wall recalcitrance in tobacco and maize Brunecky, Roman; Selig, Michael J.; Vinzant, Todd B. Biotechnology for Biofuels, Vol. 4, Issue 1 https://doi.org/10.1186/1754-6834-4-1	journal	January 2011

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