Journal of Biomolecular NMR

, Volume 68, Issue 4, pp 257–270 | Cite as

2H–13C correlation solid-state NMR for investigating dynamics and water accessibilities of proteins and carbohydrates

  • Martin D. Gelenter
  • Tuo Wang
  • Shu-Yu Liao
  • Hugh O’Neill
  • Mei Hong
Article

Abstract

Site-specific determination of molecular motion and water accessibility by indirect detection of 2H NMR spectra has advantages over dipolar-coupling based techniques due to the large quadrupolar couplings and the ensuing high angular resolution. Recently, a Rotor Echo Short Pulse IRrAdiaTION mediated cross polarization (RESPIRATIONCP) technique was developed, which allowed efficient transfer of 2H magnetization to 13C at moderate 2H radiofrequency field strengths available on most commercial MAS probes. In this work, we investigate the 2H–13C magnetization transfer characteristics of one-bond perdeuterated CDn spin systems and two-bond H/D exchanged C–(O)–D and C–(N)–D spin systems in carbohydrates and proteins. Our results show that multi-bond, broadband 2H–13C polarization transfer can be achieved using 2H radiofrequency fields of ~50 kHz, relatively short contact times of 1.3–1.7 ms, and with sufficiently high sensitivity to enable 2D 2H–13C correlation experiments with undistorted 2H spectra in the indirect dimension. To demonstrate the utility of this 2H–13C technique for studying molecular motion, we show 2H–13C correlation spectra of perdeuterated bacterial cellulose, whose surface glucan chains exhibit a motionally averaged C6 2H quadrupolar coupling that indicates fast trans-gauche isomerization about the C5–C6 bond. In comparison, the interior chains in the microfibril core are fully immobilized. Application of the 2H–13C correlation experiment to H/D exchanged Arabidopsis primary cell walls show that the O–D quadrupolar spectra of the highest polysaccharide peaks can be fit to a two-component model, in which 74% of the spectral intensity, assigned to cellulose, has a near-rigid-limit coupling, while 26% of the intensity, assigned to matrix polysaccharides, has a weakened coupling of 50 kHz. The latter O–D quadrupolar order parameter of 0.22 is significantly smaller than previously reported C–D dipolar order parameters of 0.46–0.55 for pectins, suggesting that additional motions exist at the C–O bonds in the wall polysaccharides. 2H–13C polarization transfer profiles are also compared between statistically deuterated and H/D exchanged GB1.

Keywords

Molecular motion RESPIRATIONCP Cellulose Plant primary cell walls Trans-gauche isomerization 

References

  1. Akbey Ü et al (2014) Quadruple-resonance magic-angle spinning nmr spectroscopy of deuterated solid proteins. Angew Chem Int Edit 53:2438–2442CrossRefGoogle Scholar
  2. Andreas LB, Le Marchand T, Jaudzems K, Pintacuda G (2015) High-resolution proton-detected NMR of proteins at very fast MAS. J Magn Reson 253:36–49ADSCrossRefGoogle Scholar
  3. Atalla RH, VanderHart DL (1984) Native cellulose: a composite of two distinct crystalline forms. Science 223:283–285ADSCrossRefGoogle Scholar
  4. Bali G, Foston MB, O’Neill HM, Evans BR, He J, Ragauskas AJ (2013) The effect of deuteration on the structure of bacterial cellulose. Carbohyd Res 374:82–88CrossRefGoogle Scholar
  5. Bennett AE, Rienstra CM, Auger M, Lakshmi KV, Griffin RG (1995) Heteronuclear decoupling in rotating solids. J Chem Phys 103:6951–6958ADSCrossRefGoogle Scholar
  6. Burnett L, Muller B (1971) Deuteron quadrupole coupling constants in three solid deuterated paraffin hydrocarbons: C2D6, C4D10, C6D14. J Chem Phys 55:5829–5831ADSCrossRefGoogle Scholar
  7. Clymer JW, Ragle JL (1982) Deuterium quadrupole coupling in methanol, salicyclic acid, catechol, resorcinol, and hydroquinone. J Chem Phys 77:4366–4373ADSCrossRefGoogle Scholar
  8. Cobo MF, Achilles A, Reichert D, Deazevedo ER, Saalwächter K (2012) Recoupled separated-local-field experiments and applications to study intermediate-regime molecular motions. J Magn Reson 221:85–96ADSCrossRefGoogle Scholar
  9. Dick-Perez M, Wang T, Salazar A, Zabotina OA, Hong M (2012) Multidimensional solid-state NMR studies of the structure and dynamics of pectic polysaccharides in uniformly 13C-labeled Arabidopsis primary cell walls. Magn Reson Chem 50:539–550CrossRefGoogle Scholar
  10. Dick-Pérez M, Zhang Y, Hayes J, Salazar A, Zabotina OA, Hong M (2011) Structure and Interactions of plant cell-wall polysaccharides by two- and three-dimensional magic-angle-spinning solid-state NMR. Biochem-US 50:989–1000CrossRefGoogle Scholar
  11. Earl WL, VanderHart DL (1981) Observations by high-resolution carbon-13 nuclear magnetic resonance of cellulose I related to morphology and crystal structure. Macromolecules 14:570–574ADSCrossRefGoogle Scholar
  12. Franks WT et al (2005) Magic-angle spinning solid-state NMR spectroscopy of the β1 immunoglobulin binding domain of protein G (GB1): 15N and 13C chemical shift assignments and conformational analysis. J Am Chem Soc 127:12291–12305CrossRefGoogle Scholar
  13. Frey MH, Opella SJ (1984) 13C spin exchange in amino acids and peptides. J Am Chem Soc 106:4942–4945CrossRefGoogle Scholar
  14. Gallagher T, Alexander P, Bryan P, Gilliland GL (1994) Two crystal structures of the B1 immunoglobulin-binding domain of streptococcal protein G and comparison with NMR. BioChemistry 33:4721–4729CrossRefGoogle Scholar
  15. Gronenborn AM, Filpula DR, Essig NZ, Achari A, Whitlow M, Wingfield PT, Clore GM (1991) A novel, highly stable fold of the immunoglobulin binding domain of streptococcal protein G. Science 253:657–661ADSCrossRefGoogle Scholar
  16. He J et al (2014) Controlled incorporation of deuterium into bacterial cellulose. Cellulose 21:927–936CrossRefGoogle Scholar
  17. Hologne M, Faelber K, Diehl A, Reif B (2005) Characterization of dynamics of perdeuterated proteins by MAS solid-state NMR. J Am Chem Soc 127:11208–11209CrossRefGoogle Scholar
  18. Hong M, Gross JD, Rienstra CM, Griffin RG, Kumashiro KK, Schmidt-Rohr K (1997) Coupling amplification in 2D MAS NMR and its application to torsion angle determination in peptides. J Magn Reson 129:85–92ADSCrossRefGoogle Scholar
  19. Hou G, Byeon IJ, Ahn J, Gronenborn AM, Polenova T (2011) 1 H-13C/1 H-15N heteronuclear dipolar recoupling by R-symmetry sequences under fast magic angle spinning for dynamics analysis of biological and organic solids. J Am Chem Soc 133:18646–18655CrossRefGoogle Scholar
  20. Hoyland JR (1968) Ab initio bond-orbital calculations. I. Application to methane, ethane, propane, and propylene. J Am Chem Soc 90:2227–2232CrossRefGoogle Scholar
  21. Hunt MJ, MaCkay AL (1974) Deuterium and nitrogen pure quadrupole resonance in deuterated amino acids. J Magn Reson 15:402–414ADSGoogle Scholar
  22. Jain S, Bjerring M, Nielsen NC (2012) Efficient and robust heteronuclear cross-polarization for high-speed-spinning biological solid-state NMR spectroscopy. J Phys Chem Lett 3:703–708CrossRefGoogle Scholar
  23. Jain SK et al (2014) Low-power polarization transfer between deuterons and spin-1/2 nuclei using adiabatic RESPIRATIONCP in solid-state NMR. Phys Chem Chem Phys 16:2827–2830CrossRefGoogle Scholar
  24. Kačuráková M, Smith AC, Gidley MJ, Wilson RH (2002) Molecular interactions in bacterial cellulose composites studied by 1D FT-IR and dynamic 2D FT-IR spectroscopy. Carbohyd Res 337:1145–1153CrossRefGoogle Scholar
  25. Komatsu T, Kikuchi J (2013) Selective signal detection in solid-state NMR using rotor-synchronized dipolar dephasing for the analysis of hemicellulose in lignocellulosic biomass. J Phys Chem Lett 4:2279–2283CrossRefGoogle Scholar
  26. 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 13:317–326CrossRefGoogle Scholar
  27. Kono H, Yunoki S, Shikano T, Fujiwara M, Erata T, Takai M (2002) CP/MAS 13C NMR study of cellulose and cellulose derivatives. 1. Complete assignment of the CP/MAS 13C NMR spectrum of the native cellulose. J Am Chem Soc 124:7506–7511CrossRefGoogle Scholar
  28. Lesage A, Steuernagel S, Emsley L (1998) Carbon-13 spectral editing in solid-state NMR using heteronuclear scalar couplings. J Am Chem Soc 120:7095–7100CrossRefGoogle Scholar
  29. Liepinsh E, Otting G (1996) Proton exchange rates from amino acid side chains—implications for image contrast. Magn Reson Med 35:30–42CrossRefGoogle Scholar
  30. Lu X, Zhang H, Lu M, Vega AJ, Hou G, Polenova T (2016) Improving dipolar recoupling for site-specific structural and dynamics studies in biosolids NMR: windowed RN-symmetry sequences. Phys Chem Chem Phys 18:4035–4044CrossRefGoogle Scholar
  31. Mao JD, Schmidt-Rohr K (2004) Separation of aromatic-carbon C-13 NMR signals from di-oxygenated alkyl bands by a chemical-shift-anisotropy filter. Solid State Nucl Magn 26:36–45CrossRefGoogle Scholar
  32. Mao J-D, Schmidt-Rohr K (2005) Methylene spectral editing in solid-state 13C NMR by three-spin coherence selection. J Magn Reson 176:1–6ADSCrossRefGoogle Scholar
  33. Massiot D et al. (2002) Modelling one- and two-dimensional solid-state NMR spectra. Mag Reson Chem 40:70–76CrossRefGoogle Scholar
  34. Masuda K, Adachi M, Hirai A, Yamamoto H, Kaji H, Horii F (2003) Solid-state 13C and 1H spin diffusion NMR analyses of the microfibril structure for bacterial cellulose. Solid State Nucl Mag Reson 23:198–212CrossRefGoogle Scholar
  35. Metz G, Wu XL, Smith SO (1994) Ramped-amplitude cross polarization in magic-angle-spinning NMR. J Magn Reson Series A 110:219–227ADSCrossRefGoogle Scholar
  36. Morcombe CR, Zilm KW (2003) Chemical shift referencing in MAS solid state NMR. J Magn Reson 162:479–486ADSCrossRefGoogle Scholar
  37. Munowitz M, Griffin R, Bodenhausen G, Huang T (1981) Two-dimensional rotational spin-echo nuclear magnetic resonance in solids: correlation of chemical shift and dipolar interactions. J Am Chem Soc 103:2529–2533CrossRefGoogle Scholar
  38. Nadaud PS, Helmus JJ, Höfer N, Jaroniec CP (2007) Long-range structural restraints in spin-labeled proteins probed by solid-state nuclear magnetic resonance spectroscopy. J Am Chem Soc 129:7502–7503CrossRefGoogle Scholar
  39. Nand D, Cukkemane A, Becker S, Baldus M (2012) Fractional deuteration applied to biomolecular solid-state NMR spectroscopy. J Biomol NMR 52:91–101CrossRefGoogle Scholar
  40. Nielsen NC, Bildso/e H, Jakobsen HJ, Levitt MH (1994) Double-quantum homonuclear rotary resonance: efficient dipolar recovery in magic-angle spinning nuclear magnetic resonance. J Chem Phys 101:1805–1812ADSCrossRefGoogle Scholar
  41. Nishiyama Y, Langan P, Chanzy H (2002) Crystal structure and hydrogen-bonding system in cellulose Iβ from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 124:9074–9082CrossRefGoogle Scholar
  42. Nishiyama Y, Sugiyama J, Chanzy H, Langan P (2003) Crystal structure and hydrogen bonding system in cellulose Iα from synchrotron X-ray and neutron fiber diffraction. J Am Chem Soc 125:14300–14306CrossRefGoogle Scholar
  43. O’Neill H et al (2015) Chapter six - production of bacterial cellulose with controlled deuterium–hydrogen substitution for neutron scattering studies. In: Zvi K (ed) Method Enzymol, vol 565. Academic Press, San Diego, pp 123–146Google Scholar
  44. Palmer AG, Williams J, McDermott A (1996) Nuclear magnetic resonance studies of biopolymer dynamics. J Phys Chem 100:13293–13310CrossRefGoogle Scholar
  45. Pines A, Gibby MG, Waugh JS (1972) Proton-Enhanced nuclear induction spectroscopy. A method for high resolution NMR of dilute spins in solids. J Chem Phys 56:1776–1777ADSCrossRefGoogle Scholar
  46. Reif B (2012) Deuterated peptides and proteins: structure and dynamics studies by MAS solid-state NMR. Methods Mol Biol 831:279–301CrossRefGoogle Scholar
  47. Sanchis MJ, Carsí M, Gómez CM, Culebras M, Gonzales KN, Torres FG (2017) Monitoring molecular dynamics of bacterial cellulose composites reinforced with graphene oxide by carboxymethyl cellulose addition. Carbohyd Polym 157:353–360CrossRefGoogle Scholar
  48. Schmidt HL, Sperling LJ, Gao YG, Wylie BJ, Boettcher JM, Wilson SR, Rienstra CM (2007) Crystal polymorphism of protein GB1 examined by solid-state NMR spectroscopy and X-ray diffraction. J Phys Chem B 111:14362–14369CrossRefGoogle Scholar
  49. Schmidt-Rohr K, Mao JD (2002) Efficient CH-group selection and identification in C-13 solid-state NMR by dipolar DEPT and H-1 chemical-shift filtering. J Am Chem Soc 124:13938–13948CrossRefGoogle Scholar
  50. Schmidt-Rohr K, Spiess HW (1994) Multidimensional Solid-State NMR and Polymers. Series vol., 1st edn. Academic Press, San DiegoGoogle Scholar
  51. Schmidt-Rohr K, Fritzsching KJ, Liao SY, Hong M (2012) Spectral editing of two-dimensional magic-angle-spinning solid-state NMR spectra for protein resonance assignment and structure determination. J Biomol NMR 54:343–353CrossRefGoogle Scholar
  52. Shi X, Rienstra CM (2016) Site-specific internal motions in GB1 protein microcrystals revealed by 3D 2H–13C–13C solid-state NMR spectroscopy. J Am Chem Soc 138:4105–4119CrossRefGoogle Scholar
  53. 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 67:503–514CrossRefGoogle Scholar
  54. Wang T, Zabotina OA, Miller RC, Hong M (2012) Pectin-cellulose interactions in arabidopsis primary cell wall from two-dimensional magic-angle-spinning solid-state NMR. BioChemistry 51:9846–9856CrossRefGoogle Scholar
  55. Wang T, Salazar A, Zabotina OA, Hong M (2014) Structure and dynamics of brachypodium primary cell wall polysaccharides from two-dimensional 13C solid-state nuclear magnetic resonance spectroscopy. Biochem-US 53:2840–2854CrossRefGoogle Scholar
  56. Wang T, Park YB, Cosgrove DJ, Hong M (2015) Cellulose-pectin spatial contacts are inherent to never-dried Arabidopsis primary cell walls: evidence from solid-state nuclear magnetic resonance. Plant Physiol 168:871–884CrossRefGoogle Scholar
  57. Wang T, Chen Y, Tabuchi A, Cosgrove DJ, Hong M (2016a) The target of β-expansin EXPB1 in maize cell walls from binding and solid-state NMR studies. Plant Physiol 172:2107–2119CrossRefGoogle Scholar
  58. Wang T, Phyo P, Hong M (2016b) Multidimensional solid-state NMR spectroscopy of plant cell walls. Solid State Nucl Mag 78:56–63CrossRefGoogle Scholar
  59. Wang T, Yang H, Kubicki JD, Hong M (2016c) Cellulose structural polymorphism in plant primary cell walls investigated by high-field 2D solid-state NMR spectroscopy and density functional theory calculations. Biomacromolecules 17:2210–2222CrossRefGoogle Scholar
  60. Wei D, Akbey Ü, Paaske B, Oschkinat H, Reif B, Bjerring M, Nielsen NC (2011) Optimal 2H rf Pulses and 2H–13C cross-polarization methods for solid-state 2H MAS NMR of perdeuterated proteins. J Phys Chem Lett 2:1289–1294CrossRefGoogle Scholar
  61. White PB, Wang T, Park YB, Cosgrove DJ, Hong M (2014) Water–polysaccharide interactions in the primary cell wall of Arabidopsis thaliana from polarization transfer solid-state NMR. J Am Chem Soc 136:10399–10409CrossRefGoogle Scholar
  62. Williams JK, Schmidt-Rohr K, Hong M (2015) Aromatic spectral editing techniques for magic-angle-spinning solid-state NMR spectroscopy of uniformly 13C-labeled proteins. Solid State Nucl Mag 72:118–126CrossRefGoogle Scholar
  63. Wu XL, Burns ST, Zilm KW (1994) Spectral editing in CPMAS NMR. Generating subspectra based on proton multiplicities. J Magn Reson Series A 111:29–36ADSCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media B.V. 2017

Authors and Affiliations

  • Martin D. Gelenter
    • 1
  • Tuo Wang
    • 1
  • Shu-Yu Liao
    • 1
  • Hugh O’Neill
    • 2
  • Mei Hong
    • 1
  1. 1.Department of ChemistryMassachusetts Institute of TechnologyCambridgeUSA
  2. 2.Center for Structural Molecular BiologyOak Ridge National LaboratoryOak RidgeUSA

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