Abstract
The insufficient resolution of conventional methods has long limited the structural elucidation of cellulose and its derivatives, especially for those with relatively low crystallinities or in native cell walls. Recent 2D/3D solid-state NMR studies of 13C uniformly labeled plant biomaterials have initiated a re-investigation of our existing knowledge in cellulose structure and its interactions with matrix polymers but for unlabeled materials, this spectroscopic method becomes impractical due to limitations in sensitivity. Here, we investigate the molecular structure of unlabeled cotton cellulose by combining natural abundance 13C–13C 2D correlation solid-state NMR spectroscopy, as enabled by the sensitivity-enhancing technique of dynamic nuclear polarization, with statistical analysis of the observed and literature-reported chemical shifts. The atomic resolution allows us to monitor the loss of Iα and Iβ allomorphs and the generation of a novel structure during ball-milling, which reveals the importance of large crystallite size for maintaining the Iα and Iβ model structures. Partial order has been identified in the “disordered” domains, as evidenced by a discrete distribution of well-resolved peaks. This study not only provides heretofore unavailable high-resolution insights into cotton cellulose but also presents a widely applicable strategy for analyzing the structure of cellulose-rich materials without isotope-labeling. This work was part of a multi-technique study of ball-milled cotton described in the previous article in the same issue.
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Atalla RH, Vanderhart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285. https://doi.org/10.1126/science.223.4633.283
Atalla RH, Vanderhart DL (1999) The role of solid state 13C NMR spectroscopy in studies of the nature of native celluloses. Solid State Nucl Magn Reson 15:1–19
Cosgrove DJ (2014) Re-constructing our models of cellulose and primary cell wall assembly. Curr Opin Plant Biol 22C:122–131. https://doi.org/10.1016/j.pbi.2014.11.001
Cosgrove DJ, Jarvis MC (2012) Comparative structure and biomechanics of plant primary and secondary cell walls. Front Plant Sci. https://doi.org/10.3389/fpls.2012.00204
Dubroca T et al (2018) A quasi-optical and corrugated waveguide microwave transmission system for simultaneous dynamic nuclear polarization NMR on two separate 14.1 T spectrometers. J Magn Reson 289:35–44. https://doi.org/10.1016/j.jmr.2018.01.015
Fernandes AN et al (2011) Nanostructure of cellulose microfibrils in spruce wood. Proc Natl Acad Sci USA 108:E1195–E1203. https://doi.org/10.1073/pnas.1108942108
Forziati FH, Stone WK, Rowen JW, Appel WD (1950) Cotton powder for infrared transmission measurements. J Res Nat Bur Stand 45:109–113. https://doi.org/10.6028/jres.045.009
Hill JL, Hammudi MB, Tien M (2014) The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell 26:4834–4842. https://doi.org/10.1105/tpc.114.131193
Hohwy M, Rienstra CM, Jaroniec CP, Griffin RG (1999) Fivefold symmetric homonuclear dipolar recoupling in rotating solids: application to double quantum spectroscopy. J Chem Phys 110:7983–7992. https://doi.org/10.1063/1.478702
Jarvis M (2003) Chemistry: cellulose stacks up. Nature 426:611–612. https://doi.org/10.1038/426611a
Kang X et al (2018) Molecular architecture of fungal cell walls revealed by solid-state NMR. Nat Commun 9:2747. https://doi.org/10.1038/S41467-018-05199-0
Koers EJ et al (2014) NMR-based structural biology enhanced by dynamic nuclear polarization at high magnetic field. J Biomol NMR 60:157–168. https://doi.org/10.1007/s10858-014-9865-8
Kono H, Numata Y (2006) Structural investigation of cellulose Ia and Ib by 2D RFDR NMR spectroscopy: determination of sequence of magnetically inequivalent d-glucose units along cellulose chain. Cellulose 13:317–326
Kono H, Erata T, Takai M (2003a) Complete assignment of the CP/MAS 13C NMR spectrum of cellulose IIII. Macromolecules 36:3589–3592. https://doi.org/10.1021/Ma021015f
Kono H, Erata T, Takai M (2003b) Determination of the through-bond carbon–carbon and carbon–proton connectivities of the native celluloses in the solid state. Macromolecules 36:5131–5138. https://doi.org/10.1021/Ma021769u
Kono H, Numata Y, Erata T, Takai M (2004) 13C and 1H resonance assignment of mercerized cellulose II by two-dimensional MAS NMR spectroscopies. Macromolecules 37:5310–5316. https://doi.org/10.1021/Ma030465k
Kubicki JD, Mohamed MNA, Watts HD (2013) Quantum mechanical modeling of the structures, energetics and spectral properties of I alpha and I beta cellulose. Cellulose 20:9–23. https://doi.org/10.1007/s10570-012-9838-6
Kubicki JD, Watts HD, Zhao Z, Zhong LH (2014) Quantum mechanical calculations on cellulose-water interactions: structures, energetics, vibrational frequencies and NMR chemical shifts for surfaces of I alpha and I beta cellulose. Cellulose 21:909–926. https://doi.org/10.1007/s10570-013-0029-x
Larsson PT, Westlund PO (2005) Line shapes in CP/MAS 13C NMR spectra of cellulose I. Spectrochim Acta A 62:539–546. https://doi.org/10.1016/j.saa.2005.01.021
Larsson PT, Hult EL, Wickholm K, Pettersson E, Iversen T (1999) CP/MAS 13C NMR spectroscopy applied to structure and interaction studies on cellulose I. Solid State Nucl Magn Reson 15:31–40. https://doi.org/10.1016/S0926-2040(99)00044-2
Lee D, Hediger S, De Paepe G (2015) Is solid-state NMR enhanced by dynamic nuclear polarization? Solid State Nucl Magn Reson 66–67:6–20. https://doi.org/10.1016/j.ssnmr.2015.01.003
Lesage A, Auger C, Caldarelli S, Emsley L (1997) Determination of through-bond carbon–carbon connectivities in solid-state NMR using the INADEQUATE experiment. J Am Chem Soc 119:7867–7868. https://doi.org/10.1021/Ja971089k
Ling Z, Wang T, Makarem M, Cheng HN, Bacher M, Potthast A, Rosenau T, King H, Delhom CD, Nam S, Edwards JV, Kim SH, Xu F, French AD (2019) Effects of ball milling on the structure of cotton cellulose. Cellulose 26:XXXX–XXYY (Submitted)
Mentink-Vigier F et al (2017) Efficient cross-effect dynamic nuclear polarization without depolarization in high-resolution MAS NMR. Chem Sci 8:8150–8163. https://doi.org/10.1039/c7sc02199b
Newman RH (1998) Evidence for assignment of 13C NMR signals to cellulose crystallite surfaces in wood, pulp and isolated celluloses. Holzforschung 52:157–159
Newman RH, Hill SJ, Harris PJ (2013) Wide-angle x-ray scattering and solid-state nuclear magnetic resonance data combined to test models for cellulose microfibrils in mung bean cell walls. Plant Physiol 163:1558–1567. https://doi.org/10.1104/pp.113.228262
Ni QZ et al (2013) High frequency dynamic nuclear polarization. Acc Chem Res 46:1933–1941
Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Ib from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082. https://doi.org/10.1021/Ja0257319
Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Ia, from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125:14300–14306. https://doi.org/10.1021/Ja037055w
Perras FA, Luo H, Zhang X, Mosier NS, Pruski M, Abu-Omar MM (2017) Atomic-level structure characterization of biomass pre- and post-lignin treatment by dynamic nuclear polarization-enhanced solid-state NMR. J Phys Chem A 121:623–630. https://doi.org/10.1021/acs.jpca.6b11121
Phyo P, Wang T, Yang Y, O’Neill H, Hong M (2018) Direct determination of hydroxymethyl conformations of plant cell wall cellulose using 1H polarization transfer solid-state NMR. Biomacromolecules 19:1485–1497. https://doi.org/10.1021/acs.biomac.8b00039
Rossini AJ et al (2012) Dynamic nuclear polarization NMR spectroscopy of microcrystalline solids. J Am Chem Soc 134:16899–16908. https://doi.org/10.1021/ja308135r
Rossini AJ, Zagdoun A, Lelli M, Lesage A, Coperet C, Emsley L (2013) Dynamic nuclear polarization surface enhanced NMR spectroscopy. Acc Chem Res 46:1942–1951. https://doi.org/10.1021/ar300322x
Saliba EP et al (2017) Electron decoupling with dynamic nuclear polarization in rotating solids. J Am Chem Soc 139:6310–6313. https://doi.org/10.1021/jacs.7b02714
Sauvee C, Rosay M, Casano G, Aussenac F, Weber RT, Ouari O, Tordo P (2013) Highly efficient, water-soluble polarizing agents for dynamic nuclear polarization at high frequency. Angew Chem Int Ed 52:10858–10861. https://doi.org/10.1002/anie.201304657
Sethaphong L, Haigler CH, Kubicki JD, Zimmer J, Bonetta D, DeBolt S, Yingling YG (2013) Tertiary model of a plant cellulose synthase. Proc Natl Acad Sci USA 110:7512–7517. https://doi.org/10.1073/pnas.1301027110
Simmons TJ et al (2016) Folding of xylan onto cellulose fibrils in plant cell walls revealed by solid-state NMR. Nat Commun 7:13902. https://doi.org/10.1038/ncomms13902
Takahashi H, Lee D, Dubois L, Bardet M, Hediger S, De Paepe G (2012) Rapid natural-abundance 2D 13C-13C correlation spectroscopy using dynamic nuclear polarization enhanced solid-state NMR and matrix-free sample preparation. Angew Chem Int Ed 51:11766–11769. https://doi.org/10.1002/anie.201206102
Takahashi H, Ayala I, Bardet M, De Paepe G, Simorre JP, Hediger S (2013a) Solid-state NMR on bacterial cells: selective cell wall signal enhancement and resolution improvement using dynamic nuclear polarization. J Am Chem Soc 135:5105–5110. https://doi.org/10.1021/ja312501d
Takahashi H, Hediger S, De Paepe G (2013b) Matrix-free dynamic nuclear polarization enables solid-state NMR C-13-C-13 correlation spectroscopy of proteins at natural isotopic abundance. Chem Commun 49:9479–9481. https://doi.org/10.1039/c3cc45195j
Vandavasi VG et al (2016) A structural study of CESA1 catalytic domain of arabidopsis cellulose synthesis complex: evidence for CESA trimers. Plant Physiol 170:123–135. https://doi.org/10.1104/pp.15.01356
Verlhac C, Dedier J, Chanzy H (1990) Availability of surface hydroxyl groups in valonia and bacterial cellulose. Polym Sci Part A 28:1171–1177
Wang T, Hong M (2016) Solid-state NMR investigations of cellulose structure and interactions with matrix polysaccharides in plant primary cell walls. J Exp Bot 67:503–514. https://doi.org/10.1093/jxb/erv416
Wang T, Zabotina O, Hong M (2012) Pectin-cellulose interactions in the Arabidopsis primary cell wall from two-dimensional magic-angle-spinning solid-state nuclear magnetic resonance. Biochemistry 51:9846–9856. https://doi.org/10.1021/Bi3015532
Wang T, Park YB, Caporini MA, Rosay M, Zhong LH, Cosgrove DJ, Hong M (2013) Sensitivity-enhanced solid-state NMR detection of expansin’s target in plant cell walls. Proc Natl Acad Sci USA 110:16444–16449. https://doi.org/10.1073/pnas.1316290110
Wang T, Salazar A, Zabotina O, Hong M (2014) Structure and dynamics of Brachypodium primary cell walls polysaccharides from two-dimensional 13C solid-state NMR spectroscopy. Biochemistry 53:2840–2854. https://doi.org/10.1021/bi500231b
Wang T, Park YB, Cosgrove DJ, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis thaliana primary cell walls: evidence from solid-state NMR. Plant Physiol 168:871–884. https://doi.org/10.1104/pp.15.00665
Wang T, Phyo P, Hong M (2016a) Multidimensional solid-state NMR spectroscopy of plant cell walls. Solid State Nucl Magn Reson 78:56–63. https://doi.org/10.1016/j.ssnmr.2016.08.001
Wang T, Yang H, Kubicki JD, Hong M (2016b) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17:2210–2222. https://doi.org/10.1021/acs.biomac.6b00441
Yang H, Wang T, Oehme D, Petridis L, Hong M, Kubicki JD (2018) Structural factors affecting 13C NMR chemical shifts of cellulose: a computational study. Cellulose 25:23–36. https://doi.org/10.1007/s10570-017-1549-6
Acknowledgments
This work is supported by the National Science Foundation through NSF OIA-1833040. The National High Magnetic Field Laboratory is supported by the National Science Foundation through NSF/DMR-1644779 and the State of Florida. The MAS-DNP system at NHMFL is funded in part by NIH S10 OD018519 and NSF CHE-1229170.
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Kirui, A., Ling, Z., Kang, X. et al. Atomic resolution of cotton cellulose structure enabled by dynamic nuclear polarization solid-state NMR. Cellulose 26, 329–339 (2019). https://doi.org/10.1007/s10570-018-2095-6
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DOI: https://doi.org/10.1007/s10570-018-2095-6