An evaluation of the structures of cellulose generated by the CHARMM force field: comparisons to in planta cellulose
Molecular dynamics simulations of cellulose regularly sample a conformational space different to the crystal structures they were initiated from, with changes to the tilt of chains, expansion of the unit cell and variation in exocyclic group conformations. Given the differences in the structures sampled the question presents itself as to whether these simulations are sampling structures that resemble cellulose in planta. To investigate this question, we have performed MD simulations on different size and shaped Iα and Iβ cellulose microfibrils with the structures generated characterized with regards to changes in expansion, chain shift along the polymerization axis, tilt, exocyclic conformation and H-bonding. Structures were then input into a quantum mechanical NMR chemical shift calculation protocol with the resulting 13C chemical shifts compared to experimental data. Chemical shifts were shown to be strongly dependent on the exocyclic group conformation with the structures of Iα simulations more closely replicating experimental data than the Iβ simulations, especially at the C4 and C6 positions which suggests that the conformational space was not being accurately represented for the Iβ microfibrils. Despite this, peak sizes based on the sampling occupancy of exocyclic conformations from unrestrained simulations were found to replicate experimental peak sizes better than simulations where exocyclic groups of interior chains were restrained to the tg conformation, suggesting that exocyclic groups have greater freedom to sample different conformations than suggested by their crystal structures.
KeywordsCellulose Microfibril Molecular dynamics NMR Quantum mechanics Exocyclic group
This work was partly funded by a grant from the Australia Research Council (ARC) to the ARC Centre of Excellence in Plant Cell Walls (DPO) [CE110001007]; the Victorian Life Sciences Computation Initiative (VLSCI) grant number “VR0319” on its Peak Computing Facility at the University of Melbourne, an initiative of the Victorian State Government; and the Center for Lignocellulose Structure and Formation, an Energy Frontier Research Center funded by the U.S. Department of Energy, Office of Science, Basic Energy Sciences under Award # DE- SC0001090. Parts of this work were completed while DPO was at IBM Research—Australia. Portions of this research were conducted with Advanced Cyber Infrastructure computational resources provided by the Institute for Cyber Science at The Pennsylvania State University (http://ics.psu.edu). We also thank Prof. Mei Hong for the experimental triple mutant intact Arabidopsis spectra.
- Bühl M, Kaupp M, Malkina OL, Malkin VG (1999) The DFT route to NMR chemical shifts. J Comput Chem 20:91–105. https://doi.org/10.1002/(sici)1096-987x(19990115)20:1<91::aid-jcc10>3.0.co;2-cGoogle Scholar
- Busse-Wicher M, Gomes TCF, Tryfona T et al (2014) The pattern of xylan acetylation suggests xylan may interact with cellulose microfibrils as a two-fold helical screw in the secondary plant cell wall of Arabidopsis thaliana. Plant J 79:492–506. https://doi.org/10.1111/tpj.12575 CrossRefPubMedPubMedCentralGoogle Scholar
- Funahashi R, Okita Y, Hondo H, et al (2017) Different conformations of surface cellulose molecules in native cellulose microfibrils revealed by layer-by-layer peeling. 0–3. https://doi.org/10.1021/acs.biomac.7b01173
- Hansen HS, Hünenberger PH (2011) A reoptimized GROMOS force field for hexopyranose-based carbohydrates accounting for the relative free energies of ring conformers, anomers, epimers, hydroxymethyl rotamers, and glycosidic linkage conformers. J Comput Chem 32:998–1032. https://doi.org/10.1002/jcc CrossRefPubMedGoogle Scholar
- Kubicki JD, Watts HD, Zhao Z, Zhong L (2014) Quantum mechanical calculations on cellulose–water interactions: structures, energetics, vibrational frequencies and NMR chemical shifts for surfaces of Iα and Iβ cellulose. Cellulose 21:909–926. https://doi.org/10.1007/s10570-013-0029-x CrossRefGoogle Scholar
- Lee CM, Kafle K, Park YB, Kim SH (2014) 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. Phys Chem Chem Phys 16:10844–10853. https://doi.org/10.1039/c4cp00515e CrossRefPubMedGoogle Scholar
- Lee CM, Kubicki JD, Fan B, et al (2015) Hydrogen-bonding network and OH stretch vibration of cellulose: comparison of computational modeling with polarized IR and SFG spectra. J Phys Chem B. https://doi.org/10.1021/acs.jpcb.5b08015
- Thibaudeau C, Stenutz R, Hertz B et al (2004) Correlated C–C and C–O bond conformations in saccharide hydroxymethyl groups: parametrization and application of redundant 1 H–1 H, 13 C–1 H, and 13 C–13 C NMR J-couplings. J Am Chem Soc 126:15668–15685. https://doi.org/10.1021/ja0306718 CrossRefPubMedGoogle Scholar
- Wang T, Yang H, Kubicki JD, Hong M (2016) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules. https://doi.org/10.1021/acs.biomac.6b00441