Abstract
Abstract
A novel process for the separation of crystalline cellulose in water into single polysaccharide strands is proposed that does not require high temperatures or other chemical reactants. We have modeled the behavior of a 36-strand cellulose \(\hbox {I}\beta\) crystalline bundle when subjected to picosecond mid-infrared laser pulses using all-atom non-equilibrium molecular dynamics simulations. We show that mid-infrared laser pulses that induce resonance deformations in the C–O–H angles of the hydroxyl groups that are involved in the hydrogen bonding network of cellulose, rapidly cause the cellulose bundles to dissociate into single strands solvated by the water. The laser pulses selectively disrupt intra- and inter-chain hydrogen bonds that maintain the polysaccharide strands in sheets and bundles, causing cellulose to dissolve into single strands whose end-to-end lengths remain similar to those in the original cellulose crystalline bundle. This proof-of-concept work provides guidance for experiments that may provide insight into the mechanism of cellulase enzymes whose improvement could lead to increased production of ethanol from cellulose, and possibly spur the development of new nanomaterial engineering techniques.
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References
Aden A, Foust T (2009) Technoeconomic analysis of the dilute sulfuric acid and enzymatic hydrolysis process for the conversion of corn stover to ethanol. Cellulose 16(4):535. https://doi.org/10.1007/s10570-009-9327-8
Agarwal V, Huber GW, Conner WC, Auerbach SM (2011) Simulating infrared spectra and hydrogen bonding in cellulose i\(\beta\) at elevated temperatures. J Chem Phys 135(13):134506. https://doi.org/10.1063/1.3646306
Backus EHG, Nguyen PH, Botan V, Pfister R, Moretto A, Crisma M, Toniolo C, Stock G, Hamm P (2008) Energy transport in peptide helices: a comparison between high- and low-energy excitations. J Phys Chem B 112:9091
Berendsen HJC, Postma JPM, van Gunsteren WF, Hermans J (1981) Intermolecular forces. Reidel, Dordrecht
Berendsen HJC, Postma JPM, van Gunsteren WF, Dinola A, Haak JR (1984) Molecular-dynamics with coupling to an external bath. J Chem Phys 81:3684
Bergenstrahle M, Berglund L, Mazeau K (2007) Thermal response in crystalline i cellulose: a molecular dynamics study. J Phys Chem B 111:9138
Botan VV, Backus EHG, Pfister R, Moretto A, Crisma M, Toniolo C, Nguyen PH, Stock G, Hamm P (2007) Energy transport in peptide helices. Proc Natl Acad Sci U S A 104:12749
Chen P, Nishiyama Y, Putaux JL, Mazeau K (2014) Diversity of potential hydrogen bonds in cellulose i revealed by molecular dynamics simulation. Cellulose 21:897
Cho HM, Gross AS, Chu J (2011) Dissecting force interactions in cellulose deconstruction reveals the required solvent versatility for overcoming biomass recalcitrance. J Am Chem Soc 133:14033
Chundawat SPS, Bellesia G, Uppugundla N, da Costa Sousa L, Gao D, Cheh AM, Agarwal UP, Bianchetti CM, Phillips GN, Langan P, Balan V, Gnanakaran S, Dale BE (2011) Restructuring the crystalline cellulose hydrogen bond network enhances its depolymerization rate. J Am Chem Soc 133(29):11163. https://doi.org/10.1021/ja2011115 PMID: 21661764
Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22:122. https://doi.org/10.1016/j.pbi.2014.11.001, http://www.sciencedirect.com/science/article/pii/S1369526614001538. SI: Cell biology
Darden T, York D, Pedersen L (1993) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J Chem Phys 98:10089
Ding SY, Himmel ME (2006) The maize primary cell wall microfibril: a new model derived from direct visualization. J Agric Food Chem 54:597
Glass DC, Moritsugu K, Cheng X, Smith JC (2012) Reach coarse-grained simulation of a cellulose fiber. Biomacromolecules 13:2634
Gomes TC, Skaf MS (2012) Cellulose-builder: a toolkit for building crystalline structures of cellulose. J Comput Chem 33:1338
Gross AS, Chu JW (2010) On the molecular origins of biomass recalcitrance: the interaction network and solvation structures of cellulose microfibrils. J Phys Chem B 114:1333
Gross AS, Bell AT, Chu JW (2011) Thermodynamics of cellulose solvation in water and the ionic liquid 1-butyl-3-methylimidazolim chloride. J Phys Chem B 115(46):13433. https://doi.org/10.1021/jp202415v PMID: 21950594
Gupta KM, Jiang J (2015) Cellulose dissolution and regeneration in ionic liquids: a computational perspective. Chem Eng Sci 121:180. https://doi.org/10.1016/j.ces.2014.07.025.2013 Danckwerts special issue on molecular modelling in chemical engineering
Guvench O, Greene SN, Kamath G, Brady JW, Venable RM, Pastor RW, Mackerell ADJ (2008) Additive empirical force field for hexopyranose monosaccharides. J Comput Chem 29:2543
Guvench O, Hatcher ER, Venable RM, Pastor RW, Mackerell AJ (2009) Charmm additive all-atom force field for glycosidic linkages between hexopyranoses. J Chem Theory Comput 5:2353
Higgins H, Stewart C, Harrington K (1961) Infrared spectra of cellulose and related polysaccharides. J Polym Sci 51(155):59. https://doi.org/10.1002/pol.1961.1205115505, https://onlinelibrary.wiley.com/doi/abs/10.1002/pol.1961.1205115505
Himmel ME, Ding SY, Johnson DK, Adney WS, Nimlos MR, Brady JW, Foust TD (2007) Biomass recalcitrance: engineering plants and enzymes for biofuels production. Science 315(5813):804. https://doi.org/10.1126/science.1137016. http://science.sciencemag.org/content/315/5813/804
Hishikawa Y, Togawa E, Kondo T (2017) Characterization of individual hydrogen bonds in crystalline regenerated cellulose using resolved polarized ftir spectra. ACS Omega 2(4):1469. https://doi.org/10.1021/acsomega.6b00364
Jisuke H, Akinori S, Junji O, Sadayoshi W (1975) The confirmation of existences of cellulose iiii, iiiii, ivi, and ivii by the x-ray method. J Polym Sci Polym Lett Edit 13(1):23. https://doi.org/10.1002/pol.1975.130130104, https://onlinelibrary.wiley.com/doi/abs/10.1002/pol.1975.130130104
Jorgensen WL, Chandrasekhar J, Madura JD, Impey RW, Klein ML (1983) Comparison of simple potential functions for simulating liquid water. J Chem Phys 79:926
Kawasaki T, Fujioka J, Imai T, Tsukiyama K (2012) Effect of mid-infrared free-electron laser irradiation on refolding of amyloid-like fibrils of lysozyme into native form. Protein J 31(8):710 http://view.ncbi.nlm.nih.gov/pubmed/23054332
Kawasaki T, Fujioka J, Imai T, Torigoe K, Tsukiyama K (2014a) Mid-infrared free-electron laser tuned to the amide I band for converting insoluble amyloid-like protein fibrils into the soluble monomeric form. Lasers Med Sci 29(5):1701. https://doi.org/10.1007/s10103-014-1577-5
Kawasaki T, Imai T, Tsukiyama K (2014b) Use of a mid-infrared free-electron laser (MIR-FEL) for dissociation of the amyloid fibril aggregates of a peptide. J Anal Sci Methods Instrum 04(01):9. https://doi.org/10.4236/jasmi.2014.41002
Kawasaki T, Yaji T, Imai T, Ohta T, Tsukiyama K (2014c) Synchrotron-infrared microscopy analysis of amyloid fibrils irradiated by mid-infrared free-electron laser. Am J Anal Chem 05(06):384. https://doi.org/10.4236/ajac.2014.56047
Kawasaki T, Yaji T, Ohta T, Tsukiyama K (2016) IUCr, application of mid-infrared free-electron laser tuned to amide bands for dissociation of aggregate structure of protein. J Synchrotron Radiat 23(1):152. https://doi.org/10.1107/yi5014
Kondo T (1997) The assignment of ir absorption bands due to free hydroxyl groups in cellulose. Cellulose 4(4):281. https://doi.org/10.1023/A:1018448109214
Langan P, Nishiyama Y, Chanzy H (1999) A revised structure and hydrogen-bonding system in cellulose ii from a neutron fiber diffraction analysis. J Am Chem Soc 121(43):9940. https://doi.org/10.1021/ja9916254
Langan P, Nishiyama Y, Chanzy H (2001) X-ray structure of mercerized cellulose ii at 1 resolution. Biomacromolecules 2(2):410. https://doi.org/10.1021/bm005612q PMID: 11749200
Levine SE, Fox JM, Blanch HW, Clark DS (2010) A mechanistic model of the enzymatic hydrolysis of cellulose. Biotechnol Bioeng 107(1):37. https://doi.org/10.1002/bit.22789
Lindahl E, Hess B, van der Spoel D (2001) Gromacs 3.0: a package for molecular simulation and trajectory analysis. J Mol Mod 7:306
Lindman B, Karlstrom G, Stigsson L (2010) On the mechanism of dissolution of cellulose. J Mol Liq 156:76
Luo J, Fang Z, Smith RL Jr (2013) Ultrasound-enhanced conversion of biomass to biofuels. Progress Energy Combust Sci 41:56
Man VH, Pan F, Sagui C, Roland C (2016a) Comparative melting and healing of B-DNA and Z-DNA by an infrared laser pulse. J Chem Phys 144(14):145101+. https://doi.org/10.1063/1.4945340
Man VH, Van-Oanh NT, Derreumaux P, Li MS, Roland C, Sagui C, Nguyen PH (2016b) Picosecond infrared laser-induced all-atom nonequilibrium molecular dynamics simulation of dissociation of viruses. Phys Chem Chem Phys. https://doi.org/10.1039/c5cp07711g
Marchessault R, Liang C (1960) Infrared spectra of crystalline polysaccharides. III. Mercerized cellulose. J Polym Sci 43(141):71. https://doi.org/10.1002/pol.1960.1204314107, https://onlinelibrary.wiley.com/doi/abs/10.1002/pol.1960.1204314107
Marechal Y (2011) The molecular structure of liquid water delivered by absorption spectroscopy in the whole ir region completed with thermodynamics data. J Mol Struct 1004(1):146. https://doi.org/10.1016/j.molstruc.2011.07.054, http://www.sciencedirect.com/science/article/pii/S0022286011006247
Marechal Y, Chanzy H (2000) The hydrogen bond network in i\(\beta\) cellulose as observed by infrared spectrometry. J Mol Phys 523:183
Matthews JF, Skopec CE, Mason P, Zuccato P, Torget R, Sugiyama J, Himmel M, Brady J (2006a) Computer simulation studies of microcrystalline cellulose i\(\beta\). Carbohydr Res 341:138
Matthews JF, Skopec CE, Mason PE, Zuccato P, Torget RW, Sugiyama J, Himmel ME, Brady JW (2006b) Computer simulation studies of microcrystalline cellulose i. Carbohydr Res 341(1):138. https://doi.org/10.1016/j.carres.2005.09.028
Matthews JF, Bergenstrahle M, Beckham GT, Himmel ME, Nimlos MR, Brady JW, Crowley MF (2011a) High-temperature behavior of cellulose i. J Phys Chem B 115:2155
Matthews JF, Himmel ME, Crowley MF (2011b) Conversion of cellulose i\(\alpha\) to i\(\beta\) via a high temperature intermediate (i-ht) and other cellulose phase transformations. Cellulose 19:297
Matthews JF, Beckham GT, Bergenstrahle-Wohlert M, Brady JW, Himmel ME, Crowley MF (2012) Comparison of cellulose i\(\beta\) simulations with three carbohydrate force fields. J Chem Theory Comput 8:735
Max J, Chapados C (2009) Isotope effects in liquid water by infrared spectroscopy. III. h2o and d2o spectra from 6000to0cm ’1. J Chem Phys 131(18):184505. https://doi.org/10.1063/1.3258646
Mazeau K (2005) Structural micro-heterogeneities of crystalline i\(\beta\)-cellulose. Cellulose 12:339
Medronho B, Lindman B (2014) Competing forces during cellulose dissolution: from solvents to mechanisms. Curr Opin Colloid Interface Sci 19(1):32. https://doi.org/10.1016/j.cocis.2013.12.001, http://www.sciencedirect.com/science/article/pii/S1359029413001350
Mikkola JP, Kirilin A, Tuuf JC, Pranovich A, Holmbom B, Kustov LM, Murzin DY, Salmi T (2007) Ultrasound enhancement of cellulose processing in ionic liquids: from dissolution towards functionalization. Green Chem 9:1229
Mittal A, Katahira R, Himmel ME, Johnson DK (2011) Effects of alkaline or liquid-ammonia treatment on crystalline cellulose: changes in crystalline structure and effects on enzymatic digestibility. Biotechnol Biofuels 4(1):41. https://doi.org/10.1186/1754-6834-4-41
Nelson M, O’Connor RT (1964a) Relation of certain infrared bands to cellulose crystallinity and crystal latticed type. part i. spectra of lattice types i, ii, iii and of amorphous cellulose. J Appl Polym Sci 8(3):1311. https://doi.org/10.1002/app.1964.070080322. https://onlinelibrary.wiley.com/doi/abs/10.1002/app.1964.070080322
Nelson M, O’Connor RT (1964b) Relation of certain infrared bands to cellulose crystallinity and crystal latticed type. part ii. a new infrared ratio for estimation of crystallinity in celluloses i and ii. J Appl Polym Sci 8(3):1325. https://doi.org/10.1002/app.1964.070080323. https://onlinelibrary.wiley.com/doi/abs/10.1002/app.1964.070080323
Nguyen P, Stock G (2006) Nonequilibrium molecular dynamics simulation of a photoswitchable peptide. Chem Phys 323:36
Nguyen P, Gorbunov RD, Stock G (2006) Photoinduced conformational dynamics of a photoswitchable peptide: a nonequilibrium molecular dynamics simulation study. Biophys J 91:1224
Nguyen PH, Park SY, Stock G (2010) Nonequilibrium molecular dynamics simulation of the energy transport through a peptide helix. J Chem Phys 132:025102
Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen bonding system in cellulose i(beta) from synchrotron x-ray and neutron fiber diffraction. J Am Chem Soc 124:9074
Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose i(alpha) from synchrotron x-ray and neutron fiber diffraction. J Am Chem Soc 125:14300
Oehme DP, Downton MT, Doblin MS, Wagner J, Gidley MJ, Bacic A (2015) Unique aspects of the structure and dynamics of elementary i\(\beta\) cellulose microfibrils revealed by computational simulations. Plant Physiol 168:3
Park SY, Nguyen PH, Stock G (2009) Molecular dynamics simulation of cooling: Heat transfer from a photoexcited peptide to the solvent. J Chem Phys 131:184503
Payne CM, Knott BC, Mayes HB, Hansson H, Himmel ME, Sandgren M, Ståhlberg J, Beckham GT (2015) Fungal cellulases. Chem Rev 115(3):1308. https://doi.org/10.1021/cr500351c
Pinkert A, Marsh KN, Pang S, Staiger MP (2009) Ionic liquids and their interaction with cellulose. Chem Rev 109:6712
Poma AB, Chwastyk M, Cieplak M (2016) Coarse-grained model of the native cellulose i\(\alpha\)i and the transformation pathways to the i\(\beta\) allomorph. Cellulose 23:1573
Rabideau BD, Agarwal A, Ismail AE (2013) Observed mechanism for the breakup of small bundles of cellulose i\(\alpha\) and i\(\beta\) in ionic liquids from molecular dynamics simulations. J Phys Chem B 117:3469
Ryckaert JP, Cicotti G, Berendsen HJC (1977) Numerical integration of the cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys 23:327
Srinivas G, Cheng X, Smith JC (2014) Coarse-grain model for natural cellulose fibrils in explicit water. J Phys Chem B 118:3026
Swatloski RP, Spear SK, Holbrey JD, Rogers RD (2002) Dissolution of cellose with ionic liquids. J Am Chem Soc 124(18):4974. https://doi.org/10.1021/ja025790m
Tsuboi M (1957) Infrared spectrum and crystal structure of cellulose. J Polym Sci 25(109):159. https://doi.org/10.1002/pol.1957.1202510904, https://onlinelibrary.wiley.com/doi/abs/10.1002/pol.1957.1202510904
Van-Oanh NT, Falvo C, Calvo F, Lauvergnat D, Basire M, Gaigeot MP, Parneix P (2012) Improving anharmonic infrared spectra using semiclassically prepared molecular dynamics simulations. Phys Chem Chem Phys 14(7):2381. https://doi.org/10.1039/c2cp23101h
Viet MH, Derreumaux P, Li MS, Roland C, Sagui C, Nguyen PH (2015a) Picosecond dissociation of amyloid fibrils with infrared laser: a nonequilibrium simulation study. J Chem Phys 143:155101
Viet MH, Truong PM, Derreumaux P, Li MS, Roland C, Sagui C, Nguyen PH (2015b) Picosecond melting of peptide nanotubes using an infrared laser: a nonequilibrium simulation study. Phys Chem Chem Phys 17:27275
Wang H, Gurau G, Rogers RD (2012) Ionic liquid processing of cellulose. Chem Soc Rev 41:1519. https://doi.org/10.1039/C2CS15311D
Warden AC, Little BA, Haritos VS (2011) A cellular automaton model of crystalline cellulose hydrolysis by cellulases. Biotechnol Biofuels 4(1):1. https://doi.org/10.1186/1754-6834-4-39
Wohlert J, Berglund LA (2011) A coarse-grained model for molecular dynamics simulations of native cellulose. J Chem Theory Comput 7:753
Zhang YHP, Cui J, Lynd LR, Kuang LR (2006) A transition from cellulose swelling to cellulose dissolution by o-phosphoric acid: evidence from enzymatic hydrolysis and supramolecular structure. Biomacromolecules 7(2):644. https://doi.org/10.1021/bm050799c PMID: 16471942
Zhang Q, Bulone V, Agren H, Tu Y (2011) A molecular dynamics study of the thermal response of crystalline cellulose i\(\beta\). Cellulose 18:207
Zhong L, Matthews JF, Hansen PI, Crowley MF, Cleary JM, Walker RC, Nimlos MR, Brooks C III, Adney WS, Himmel ME, Brady JW (2009) Computational simulations of the trchoderma reesei cellobiohydrolase i acting on microcrystalline cellulose i\(\beta\): The enzyme-substrate complex. Carbohydr Res 344:1984
Acknowledgments
This work has been supported by CNRS, the Grant ANR-11-LABEX-0011-01, the National Science Foundation (NSF) USA via Grants SI2-1148144 and 154941, the National Institutes of Health (NIH) USA via Grants R01-GM079383 and R21- GM097617, and the IDRIS, CINES, TGCC centers for providing computer facilities (Grants x2015077198, A0020710174 and A0030707721).
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Domin, D., Man, V.H., Van-Oanh, NT. et al. Breaking down cellulose fibrils with a mid-infrared laser. Cellulose 25, 5553–5568 (2018). https://doi.org/10.1007/s10570-018-1973-2
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DOI: https://doi.org/10.1007/s10570-018-1973-2