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Title: A Multifunctional Cosolvent Pair Reveals Molecular Principles of Biomass Deconstruction

Abstract

The complex structure of plant cell walls resists chemical or biological degradation, challenging the breakdown of lignocellulosic biomass into renewable chemical precursors that could form the basis of future production of green chemicals and transportation fuels. In this report, experimental and computational results reveal that the effect of the tetrahydrofuran (THF)–water cosolvents on the structure of lignin and on its interactions with cellulose in the cell wall drives multiple synergistic mechanisms leading to the efficient breakdown and fractionation of biomass into valuable chemical precursors. Molecular simulations reflect that THF–water is an excellent “theta” solvent, such that lignin dissociates from itself and from cellulose and expands to form a random coil. The expansion of the lignin molecules exposes interunit linkages, rendering them more susceptible to depolymerization by acid-catalyzed cleavage of aryl-ether bonds. Nanoscale infrared sensors confirm cosolvent-mediated molecular rearrangement of lignin in the cell wall of micrometer-thick hardwood slices and track the disappearance of lignin. At bulk scale, adding dilute acid to the cosolvent mixture liberates the majority of the hemicellulose and lignin from biomass, allowing unfettered access of cellulolytic enzymes to the remaining cellulose-rich material, allowing them to sustain high rates of hydrolysis to glucose without enzyme deactivation. Through thismore » multiscale analysis, synergistic mechanisms for biomass deconstruction are confirmed, portending a paradigm shift toward first-principles design and evaluation of other cosolvent methods to realize low cost fuels and bioproducts.« less

Authors:
 [1]; ORCiD logo [2]; ORCiD logo [3];  [4];  [4]; ORCiD logo [5];  [6]; ORCiD logo [7];  [6];  [4]; ORCiD logo [8]; ORCiD logo [5]; ORCiD logo [5]; ORCiD logo [6]
+ Show Author Affiliations
  1. Univ. of California, Riverside, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC)
  2. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). UT/ORNL Center for Molecular Biophysics; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Biological Sciences
  3. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Biological Sciences
  4. Univ. of Central Florida, Orlando, FL (United States). NanoScience Technology Center
  5. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). UT/ORNL Center for Molecular Biophysics; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Biochemistry
  6. Univ. of California, Riverside, CA (United States); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
  7. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). UT/ORNL Center for Molecular Biophysics; The Ohio State Univ., Columbus, OH (United States). College of Pharmacy
  8. Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). BioEnergy Science Center (BESC); Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Joint Inst. for Biological Sciences; Univ. of Tennessee, Knoxville, TN (United States). Dept. of Chemical and Biomolecular Engineering; Oak Ridge National Lab. (ORNL), Oak Ridge, TN (United States). Center for Bioenergy Innovation (CBI)
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:
1558519
Grant/Contract Number:  
AC05-00OR22725
Resource Type:
Accepted Manuscript
Journal Name:
Journal of the American Chemical Society
Additional Journal Information:
Journal Volume: 141; Journal Issue: 32; Journal ID: ISSN 0002-7863
Publisher:
American Chemical Society (ACS)
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY

Citation Formats

Patri, Abhishek S., Mostofian, Barmak, Pu, Yunqiao, Ciaffone, Nicholas, Soliman, Mikhael, Smith, Micholas Dean, Kumar, Rajeev, Cheng, Xiaolin, Wyman, Charles E., Tetard, Laurene, Ragauskas, Arthur J., Smith, Jeremy C., Petridis, Loukas, and Cai, Charles M. A Multifunctional Cosolvent Pair Reveals Molecular Principles of Biomass Deconstruction. United States: N. p., 2019. Web. doi:10.1021/jacs.8b10242.
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Patri, Abhishek S., Mostofian, Barmak, Pu, Yunqiao, Ciaffone, Nicholas, Soliman, Mikhael, Smith, Micholas Dean, Kumar, Rajeev, Cheng, Xiaolin, Wyman, Charles E., Tetard, Laurene, Ragauskas, Arthur J., Smith, Jeremy C., Petridis, Loukas, & Cai, Charles M. A Multifunctional Cosolvent Pair Reveals Molecular Principles of Biomass Deconstruction. United States. https://doi.org/10.1021/jacs.8b10242
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Patri, Abhishek S., Mostofian, Barmak, Pu, Yunqiao, Ciaffone, Nicholas, Soliman, Mikhael, Smith, Micholas Dean, Kumar, Rajeev, Cheng, Xiaolin, Wyman, Charles E., Tetard, Laurene, Ragauskas, Arthur J., Smith, Jeremy C., Petridis, Loukas, and Cai, Charles M. Mon . "A Multifunctional Cosolvent Pair Reveals Molecular Principles of Biomass Deconstruction". United States. https://doi.org/10.1021/jacs.8b10242. https://www.osti.gov/servlets/purl/1558519.
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@article{osti_1558519,
title = {A Multifunctional Cosolvent Pair Reveals Molecular Principles of Biomass Deconstruction},
author = {Patri, Abhishek S. and Mostofian, Barmak and Pu, Yunqiao and Ciaffone, Nicholas and Soliman, Mikhael and Smith, Micholas Dean and Kumar, Rajeev and Cheng, Xiaolin and Wyman, Charles E. and Tetard, Laurene and Ragauskas, Arthur J. and Smith, Jeremy C. and Petridis, Loukas and Cai, Charles M.},
abstractNote = {The complex structure of plant cell walls resists chemical or biological degradation, challenging the breakdown of lignocellulosic biomass into renewable chemical precursors that could form the basis of future production of green chemicals and transportation fuels. In this report, experimental and computational results reveal that the effect of the tetrahydrofuran (THF)–water cosolvents on the structure of lignin and on its interactions with cellulose in the cell wall drives multiple synergistic mechanisms leading to the efficient breakdown and fractionation of biomass into valuable chemical precursors. Molecular simulations reflect that THF–water is an excellent “theta” solvent, such that lignin dissociates from itself and from cellulose and expands to form a random coil. The expansion of the lignin molecules exposes interunit linkages, rendering them more susceptible to depolymerization by acid-catalyzed cleavage of aryl-ether bonds. Nanoscale infrared sensors confirm cosolvent-mediated molecular rearrangement of lignin in the cell wall of micrometer-thick hardwood slices and track the disappearance of lignin. At bulk scale, adding dilute acid to the cosolvent mixture liberates the majority of the hemicellulose and lignin from biomass, allowing unfettered access of cellulolytic enzymes to the remaining cellulose-rich material, allowing them to sustain high rates of hydrolysis to glucose without enzyme deactivation. Through this multiscale analysis, synergistic mechanisms for biomass deconstruction are confirmed, portending a paradigm shift toward first-principles design and evaluation of other cosolvent methods to realize low cost fuels and bioproducts.},
doi = {10.1021/jacs.8b10242},
journal = {Journal of the American Chemical Society},
number = 32,
volume = 141,
place = {United States},
year = {Mon Jul 15 00:00:00 EDT 2019},
month = {Mon Jul 15 00:00:00 EDT 2019}
}
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https://doi.org/10.1021/jacs.8b10242
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Cited by: 47 works
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Figures / Tables:

Figure-1 Figure-1: (A) MD simulation of lignocellulose in aqueous solution (left) and co-solvent mixture (right) after ~50 ns. The cellulose fiber is shown in green and the lignin molecules in brown. In the co-solvent environment, almost all lignin molecules have dissociated from the cellulose fiber and from each other, changing theirmore » structure from compact (globular) to extended (coil) states. 15 (B) Average lignin-cellulose, (C) lignin-lignin contact numbers, (D) lignin radius of gyration, and (E) solvent accessible surface area of all ß-O-4 lignin linkage atoms in the aqueous (blue) and in the co-solvent mixture (orange). The time-dependence of the number of contacts is shown in Figure S1B. (F) (Left) Starting structure of lignin simulation in water with different lignin decamers shown in different colors (average end-to-end distance de = 6.2 nm). (Middle) Within ~100 ns, all lignin polymers have collapsed to a spherical aggregate binding non-covalently to each other non-covalently (de = 2.2 nm). (Right) Upon addition of the co-solvent, the aggregate dissolves to individual lignin molecules (de = 3.4 nm) in less than 50 ns.« less
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    Performance of three delignifying pretreatments on hardwoods: hydrolysis yields, comprehensive mass balances, and lignin properties
    journal, September 2019

    Pretreatment for biorefineries: a review of common methods for efficient utilisation of lignocellulosic materials
    journal, December 2019

    Performance of three delignifying pretreatments on hardwoods: hydrolysis yields, comprehensive mass balances, and lignin properties
    journal, September 2019

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