Molecular Details of Amorphous Silica Surfaces Determine Binding

Mar 11, 2014 - Molecular Details of Amorphous Silica Surfaces Determine Binding Specificity to Small Amino Acids. Ira Ben Shir, Shifi Kababya, and Ash...
5 downloads 6 Views 362KB Size
Download PDF
Article pubs.acs.org/JPCC

Molecular Details of Amorphous Silica Surfaces Determine Binding Specificity to Small Amino Acids Ira Ben Shir, Shifi Kababya, and Asher Schmidt* Schulich Faculty of Chemistry and Russell Berrie Nanotechnology Institute, Technion−Israel Institute of Technology, Technion City, Haifa 32000, Israel ABSTRACT: Molecular details of glycine adsorbed on mesoporous MCM-41 silica surfaces were determined, and their comparison to binding onto SBA-15 surfaces provided a correlation between surface structure and reactivity. Employing solid-state NMR techniques, the interfacial interactions and structural and dynamic states of surface-bound glycine and L-alanine were revealed as a function of hydration and temperature. These small amino acids with nonpolar side-chains show a general pattern of interactions with silica surfaces via their −NH3+ group with pendent carboxylate. While SBA-15 uses specific surface binding sites consisting of closely spaced 3−4 silanols, MCM-41 exhibits weaker and therefore less specific binding employing fewer surface silanols and/or longer Si···N distances, as is also manifested by enhanced temperature-dependent dynamics. A single population of likely bound amino acids exists when the surfaces are dehydrated. Upon minute hydration and/or temperature increase, new populations form in which the pendent carboxylates reorient, and their motional amplitude increases as the water cluster at the binding site grows larger. Onset of dissolution manifested by rapid isotropic reorientation is reached when only one or two water molecules are present at the binding site. This study demonstrates the unique sensitivity of solid-state NMR to probe surface binding strength, structure, and dynamics.

■

INTRODUCTION In the past decade, the interactions between bioorganic molecules and inorganic surfaces have drawn considerable interest due to their significant role in a wide range of multidisciplinary topics,1 including catalysis,2 biomineralization,3−5 biosensors,6 implants,7 and prebiotic chemistry.8,9 Being the most abundant mineral on Earth and one of the most abundant biominerals, silica was studied extensively and used for a wide range of applications.10 All silicas are threedimensional networks composed of the common SiO 4 tetrahedral building blocks, where the flexibility of the Si− O−Si bond angle is responsible for the diverse properties of the materials formed. Mesoporous silica is a class of synthetic materials having a high surface area composed of amorphous silica, however, with a tunable structure that is periodic on the mesoscopic length scale.11 The silica surfaces in these materials are composed of siloxanes and silanols. Silanols may exist as either isolated with a single hydroxyl group attached to the silicon (denoted Q3) or geminal with two hydroxyl groups bonded to the silicon (denoted Q2). The average density of silicon atoms at amorphous silica surfaces was found to be a universal value of 4.6 Si-atoms/nm2 (identified by TGA analysis);12 yet the relative Q2:Q3:Q4 abundance may vary depending on the synthetic conditions. Mesoporous silica materials have many applications in heterogeneous catalysis, separation techniques, and slow drug release. Such applications depend on inner surface characteristics such as surface area, surface density , and surface distribution of silanol groups and the relative abundance of different silicon species. The © 2014 American Chemical Society

characterization of the structure of the pore walls and the state of guest molecules at the atomic level is of fundamental and applied importance. Two well-known examples of mesoporous silica, MCM-4113 (Mobil Crystalline Materials) and SBA-1514 (Santa Barbara Amorphous), consist of an ordered, two-dimensional array of parallel channels of uniform size separated by thin walls (hexagonal, space group P6mm. These materials have pore diameters in the range of 2−4 and 5−30 nm, respectively, and typical wall thicknesses of 25−50% of the pore diameter. In SBA-15, the presence of some surface roughness caused by small SiO2 islands15,16 and the larger wall thickness result in higher hydrothermal stability up to 850 °C.17 While the void channels of MCM-41 are not connected, those of SBA-15 are interconnected via micropores. The respective concentration of silanol groups at the surface of the pore walls is about 2.9/nm2 and 3.7/nm2.15,18,19 The structure of mesoporous silicas has been studied extensively by X-ray20−22 and neutron diffraction,21 EPR,23,24 transmission and scanning electron microscopy,2 and solid-state nuclear magnetic resonance (NMR),15,16 making these materials relatively welldefined and thus excellent model surfaces. Amino acids, the simplest biomolecular building blocks, are used widely for the functionalization of solid surfaces and so tune protein−surface interactions.1 Moreover, upon binding, their altered reactivity may result in peptide bond formation.25 Received: September 10, 2013 Revised: February 5, 2014 Published: March 11, 2014 7901

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

the hydrated state; extended pumping for seven days yielded the dry state. The hydration level was raised by sample exposure to ambient atmosphere for a limited time period (several hours), which yielded the intermediate state. We note that many hydration−dehydration cycles were made in order to reach the intermediate state. Three hydration states of the sample, denoted dry, intermediate, and hydrated, all representing minute water content, are considered. The water content of the three hydration states was evaluated by 1H magic angle spinning (MAS) NMR.2,32 We emphasize that the different hydration states and temperatures represent reversible states. The short notation Gly/MCM-41 will be used throughout to denote the [1-13C,15N]glycine loaded on MCM-41. Solid-State NMR. NMR spectroscopy measurements were carried out on a Chemagnetics/Varian 300 MHz CMX-infinity solid-state NMR spectrometer equipped with three radio frequency channels and a 5 mm triple-resonance APEX Chemagnetics probe using 5 mm Zirconia rotors. Samples were spun at 10000 ± 2 for 1H and Hz 5000 ± 2 Hz for 15N and 29Si experiments. Cross-polarization (CP) MAS echo experiments (indirect excitation) were carried out with a 5.0 μs π/2, 10.0 μs π pulse widths, and echo interval τ, 200 μs, identical to the rotor period TR, a 1H decoupling level of 100 kHz; Hartmann−Hahn rf levels were matched at 50 kHz, with a contact time of 1 ms for 15N and 1.5 ms for 29Si and relaxation delays of 1.5 and 2 s, respectively. Direct 1H, 15N and 29Si excitation echo experiments, DE, were carried out with 5.0 μs π/2, 10.0 μs π pulse widths, an echo interval τ equal to the rotor period TR (200 μs), a 1H decoupling level of 100 kHz, and relaxation delays of 2 and 300 s, respectively. 15N{29Si}, 29Si{15N}, and 15N{13C} REDOR experiments were conducted using a REDOR pulse sequence, with refocusing π pulses on each rotor period (TR) on the observed channel and dephasing π pulses in the middle of each rotor period on the nonobserved nuclei, followed by an additional two rotor periods with a chemical shift echo π pulse in the middle. REDOR π pulses employed xy8 phase cycling for the refocusing and recoupling pulses.30,33 Data acquisition employed an alternating block scheme, collecting a single S0 transient with recoupling pulses turned off, followed by SR transient collection with recoupling pulses turned on. REDOR difference data obtained via S0 − SR subtraction, ΔS, yield spectra that exclusively exhibit peaks of dipolar-coupled chemical species. All REDOR data presented in the figures were collected using the CP excitation scheme. The number of transients collected was set to yield adequate signal-to-noise ratio; the typical number of transients is 2048 and 10 240 for experiments detecting 15N and 29Si, respectively. The chemical shifts of 15N, 29Si and 1H are reported relative to ( 15 NH4 ) 2 SO4 (solid) and tetramethylsilane (TMS), respectively. Simulations and fitting of REDOR data were performed using SpinEvolution.34 Peak areas were calculated by deconvolution using DMFIT.35 The SLF solid-state NMR technique was modified to include the phase modulated Lee−Goldberg (wPMLG5)36−40 homonuclear decoupling. Specifically, the odd dipolar−rotational spin−echo (ODRSE) experimental scheme of Bork et al. was used.41 The experimental parameters of the optimized PMLG5 cycle employed on-resonance 1H irradiation with a 1.9 μs pulse width, 90 kHz rf level, 0.1 μs delay for phase setting, and an overall cycle time of 20 μs. For the simulations, 11.4 kHz N−H dipolar coupling (1.01 Å N−H distance) was used, reduced to

Despite the wide applicability and vast interest in surface− adduct systems, molecular level characterization of their interactions is scant and often contradicting.26,27 A detailed description of the interactions of amino acids with inorganic surfaces and the elucidation of general binding patterns, as well as binding sites requirements, would promote the rational design of functional surfaces and contribute to the basic understanding of bioorganic−surface interfaces. In earlier studies28,29 using primarily solid-state NMR, we investigated the binding of the smallest amino acids, glycine and L-alanine, onto SBA-15 surfaces. The molecular details that describe the interacting functional groups, binding site specificity, and robustness, as well as the effect of water molecules on the adsorbent dynamics and dissolution were elucidated. The current study is extended to examine binding to MCM-41 surfaces and to reveal how the subtle alteration of surface molecular characteristics affects binding strength, dynamics, and dissolution modes. Applying molecule−surface dipolar recoupling NMR experiments, intermolecular 15N{29Si} and 29Si{15N} REDOR30 to the [1-13C,15N]glycine-loaded mesoporous silica, MCM-41, we identify the interacting functional groups and determine binding geometry and stoichiometry. Resorting to intramolecular dipolar recoupling techniques, 15N{13C} REDOR NMR and 15N{1H} separated local field (SLF),31 we determine the bound amino acid dynamics and its dependence on hydration and temperature elevation through the onset of dissolution. This study, in comparing the binding details between two surfaces, enables a further understanding of how functionality is exercised on inorganic surfaces. We show that, much like the enzyme’s catalytic site, functionality is achieved through the use of particular chemical moieties, the surface silanols, and their assembly in a proper geometric arrangement. Hence, high sensitivity of the solid-state NMR technique to binding strength, stoichiometry, and dynamics is demonstrated.

■

EXPERIMENTAL SECTION Materials. Specifically labeled compounds with stable isotope enrichment levels of 98% were used as received. [1-13C,15N]Glycine was purchased from CIL (USA) and L[u-15N,13C]lysine·2HCl was purchased from D-Chem (Israel). MCM-41 (natural abundance 29Si) was the kind gift of Prof. M. Landau, Ben Gurion University of the Negev. The MCM-41 was characterized by N2 adsorption/desorption isotherm measurements with a NOVA-2000 (Quantachrome, version 7.01) apparatus. Surface area of 1458 g/m2, pore volume 1.4 g/ cm3, and pore diameter of 38 Å were determined from the isotherms using BET and BJH methods. Sample Preparation. Loading of 0.2 [1-13C,15N]glycine molecules/nm2 on MCM-41 was performed as previously reported by Vega and co-workers.32 Fifty milligrams of calcined MCM-41, which was initially heated to 180 °C for 3 h to remove residual water, was added to a 1.0 mL aqueous solution of 23 mg of [1-13C,15N]glycine (0.26 M). Glycine concentration is reduced relative to that used in the SBA-15/Gly study28 and therefore suppresses surface-induced crystallization.9 The suspension was stirred for 3 h at room temperature. The mixture was then filtered (Nanosep 300k omega), and the remaining powder was allowed to dry in air. The remaining powder was then packed inside 5 mm Zirconia rotors with Teflon plugs and Vespel drive tips. The hydration level was reduced by evacuating the sample (while inside the rotor with cap removed): pumping (10−3 Torr) for a few hours yielded 7902

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

3.88 kHz to account for the internal fast C3 rotation, and additionally multiplied by the PMLG5 scaling factor of 0.47.

■

RESULTS Spectral Characterization of MCM-41 Adsorbed Glycine. MCM-41 mesoporous silica was loaded with [1-13C,15N]Gly from aqueous solution. Three distinct hydration states denoted dry, intermediate, and hydrated were studied. Their respective 1H MAS NMR spectra (Figure 1a,c,e) allow

Figure 2. 15N and 13C CPMAS NMR spectra of [1-13C,15N]Gly/ MCM-41 (a,b) and [1-13C,15N]Gly/SBA-15 (c,d) in the dry hydration state.

Interacting Surface Sites. The peaks of the different chemical species of the amorphous silica, Q 2 (Si*(OSi)3(OH)2), Q3 (Si*(OSi)3OH), and Q4 (Si*(OSi)4),19,43 are shown by the representative 29Si DE and CP MAS spectra (Figure 3a,b) of Gly/MCM-41 in the intermediate hydration

Figure 1. 1H (left) and 15N CP (right) MAS NMR spectra of [1-13C,15N]Gly/MCM-41 in the three hydration states: dry, p ≤ 1 Hatom/nm2 (a,b); intermediate, p ≈ 2−3 atom/nm2 (c,d); and hydrated, p > 10 H-atom/nm2 (e,f). The 1H spectra clearly show the presence of mainly hydroxyl hydrogens in the dry state (1.7 ppm), to which hydrogen clusters (3.0 ppm) are added in the intermediate state; in the hydrated state, water clusters (5.0 ppm) dominate the spectrum in accordance with ref 32.

estimating the increasing average hydrogen density,32 p, from 10 H-atom/nm2, and clearly show that larger sized H-clusters are formed and become more abundant upon hydration. We emphasize that all these hydration levels represent minute water content. The 15N and 13C CPMAS spectra of [1-13C,15N]Gly/MCM41 exhibit broad ammonium and carboxylate peaks representing surface adsorbed Gly (Figure 2a,b; dry hydration state). The respective spectra of [1-13C,15N]Gly/SBA-1528 (Figure 2c,d; dry hydration state) similarly show the broad peaks of the surface-adsorbed species, however, in addition, resolve the narrow peaks of the surface-induced crystalline polymorphs;28 the occurrence of the latter was also reported for Gly on MCM4127 and Aerosil 380 silica.42 The absence of surface-induced crystalline peaks for Gly on MCM-41 is attributed to the lower concentration of the loading glycine solution (0.26 vs 0.36 M with SBA-15). Similar to Gly/SBA-15,28,42 both 15N ammonium and 13C carboxylate chemical shifts of Gly/MCM-41 are shifted to lower ppm values relative to the crystalline chemical shifts. We note that both 15N ammonium (Figure 1b,d,f) and 13 C carboxylate peak widths (not shown) of Gly/MCM-41 narrow upon increased hydration. The chemical shift variations between Gly adsorbed on MCM-41 vs SBA-15 (Figure 2) may reflect binding differences, as will be shown below.

Figure 3. 29Si MAS spectra of [1-13C,15N]Gly/MCM-41 in the intermediate state: (a) DE MAS 300 s relaxation delay; peak areas approximate the relative abundances of the Q2, Q3, and Q4 silica species; (b) CP MAS ct 5 s, spectrum emphasizes silica species based on their proximity to hydrogenated, primarily surface; species: silanols and surface-bound glycine and water.

state. The 1H → 29Si CP MAS spectrum enhances peaks of 29Si species proximate to 1H nuclei, hence emphasizing surface sites populated by water and glycine molecules in addition to the intrinsic hydroxyls. The relative contribution of the amino acid to cross-polarization is largest in the lowest hydration state (dry), where its hydrogen atoms constitute the major fraction of the proton density. The 29Si{15N} CP-REDOR technique,30,44 by reintroducing the intermolecular, surface−glycine, dipolar interactions sensitive for 29Si···15N proximities below 5 Å, is used to identify interacting Si species. The CP (as above) ensures enhancement of the surface species. The resulting REDOR spectra of Gly/ MCM-41 in the dry state (Figure 4a) show that all peaks of the Q2, Q3, and Q4 species are affected. Their respective extent of 7903

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

Figure 4. 29Si{15N} 128TR (25.6 ms) CP-REDOR spectra of [1-13C,15N]Gly adsorbed on (a) MCM-41 in the dry hydration state at 4 °C, (b) in the intermediate state at −20 °C, and (c) SBA-15 in the dry state at 4 °C. Reference spectra (S0) are black, REDOR spectra (SR) are red, and the difference spectra (ΔS) with 4-fold vertical magnification are drawn above in blue.

attenuation with respect to reference peak intensity (deconvoluted peak area), ΔS/S0, amount to ∼20, 11, and 6 ± 3%, for recoupling time of 25.6 ms (128TR). When the recoupling time is halved (64TR), the respective attenuation is 13, 6, and 4% (not shown). Accounting for the relative abundances 1− 3:100:400 of the Q2/Q3/Q4 species15,19 and for the higher efficiency of CP to Q2, the main species of MCM-41 silica that interact with glycine amine are identified as Q3 and Q4. For comparison, the analogous REDOR spectra of the Gly/SBA-15 in the dry state (Figure 4c) show a similar, yet much more pronounced ΔS. Such a difference may originate from a smaller fraction of surface species interacting with Gly and/or from weaker interactions of glycine with MCM-41. In the following, the second implication will be substantiated. Glycine Ammonium Interaction with the Silica Surface: Geometry and Stoichiometry. Switching the REDOR experiment to observe the amine nitrogen and probe for its interaction with surface Si species, we further refine the evidence regarding the local geometry of the binding site interactions.29 The 32−128TR 15N{29Si} CP-REDOR spectra of the [1-13C,15N]Gly/MCM-41 in the dry state result in a pronounced, monotonously decreasing REDOR signal (SR/S0) of the surface adsorbed glycine peak (Figure 5, black squares; SR/S0 vs NTR). This further confirms our identification of molecular proximity interactions between glycine-charged ammonium moiety (vide infra) and the surface species of MCM-41 (primarily Q3). Although describing interactions similar to alanine and glycine with SBA-15,29 there are marked differences, as pointed out below. The observed ∼6.6% maximal attenuation of the REDOR peak (128TR, 25.6 ms), exceeding the 4.7% natural abundance of 29Si, suggests that the ammonium group must reside in proximity to two or more Si atoms. This maximal 15N{29Si} REDOR attenuation is much lower than the ∼11% found for glycine and alanine bound to SBA-15 (Figure 5), which implied a minimum of three contacts with surface Si species. This pronounced difference indicates that the binding mode and binding site of MCM-41 are different from those of SBA-15. For a quantitative geometric assessment of glycine interactions with the MCM-41 surface, the model in which the ammonium group is centered above 2, 3, or 4 surface Si atoms, such that the 15N nucleus is equidistant to each of the Si

Figure 5. Experimental 15N{29Si} REDOR dipolar evolution data, SR/ S0 vs NTR, of [1-13C,15N]Gly/MCM-41 in the dry state at 4 °C (left, black squares), and intermediate state at −20 °C, blue squares (right). Simulated REDOR curves for different N···Si distances that span the width of the experimental spread are normalized to maximum relative attenuations of (a, d) 9.4% (two Si), (b, e) 14.1% (three Si), and (c, f) 18.8% (four Si). Experimental 15N{29Si} REDOR dipolar evolution data, SR/S0 vs NTR, of [1-13C,15N]Gly/SBA-15 in the dry state at 4 °C (left, hollow circles) is presented for comparison (adopted with permission from ref 28).

atoms, was employed. In such geometric arrangements, the maximum possible REDOR attenuation is 9.4% (2 × 4.7), 14.1% (3 × 4.7), and 18.8% (4 × 4.7), respectively, similar to those considered for the SBA-15 surface.29 Using these geometric models, the N···Si internuclear distance for isolated 15 N···29Si pairs is determined by fitting the experimental data with simulated REDOR evolution curves.34 For each of the geometric models, the best fits yield the respective 15N···29Si dipolar coupling strengths of 33, 28, and 23 Hz corresponding to r[N···Si] of 4.0 ± 0.2, 4.4 ± 0.2, and 4.7 ± 0.3 Å (Figure 5a− c). The estimated contribution to ΔS/S0 from 15N···29Si pairs at distances exceeding 5 Å is ∼2% at 128TR (25.6 ms), which is well within the span (∼4%) of the simulated curves (Figure 5). For this estimate we have considered a simplified model in which the 15N atom is 2.5 Å above a silica plane (surface), and weighted REDOR contributions from cap volumes confined between incrementally growing radii were summed; the weights were computed using characteristic amorphous silica density of 2.2 g/cm3. We note that if a single silanol binder is considered, it would impose N···Si distance ≤ 3.5 Å (full dephasing at 128TR and accounting for remote Si dephasers). However, guided by the characteristics of the interactions on SBA-15 such a tight single binder mode is not plausible. The N···Si distances of the binding models of the amino acids that employ three or four silanols are ∼0.4 Å longer for MCM-41 compared to SBA-15, indicative of a weaker binding potential for MCM-41. The third geometric realization of two Si neighbors gives rise to a 4.0 ± 0.2 Å distance for MCM-41. 7904

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

For SBA-15, this geometric−stoichiometric binding possibility is excluded (11.3% REDOR attenuation). We emphasize that on MCM-41 the maximal REDOR dephasing is too low to narrow down the geometric and/or stoichiometric determination, and the models that were considered represent only a partial set of binders’ configurations that may be consistent with the experimental data. Nevertheless, these models qualitatively indicate the occurrence of longer distances and/or lower stoichiometry and so attest to structural differences between the binding sites/modes of the two surfaces. In concert with the increased sensitivity to temperature and hydration (vide infra), the unequivocal conclusion is that glycine binding to MCM-41 is of reduced strength and therefore of reduced specificity relative to SBA-15. Protonation State of Amino Group. To identify the protonation state of the bound amine group, we measured its N−H dipolar interaction using the 15N{1H} SLF NMR experiment. For the dry state, the resulting N−H dipolar evolution (Figure 6a, squares) overlaps the characteristic29

Figure 7. Experimental 15N{13C} SR/S0 REDOR evolution of [1-13C,15N]Gly/MCM-41 (squares) for the two hydration states, (a) dry and (b) “intermediate, at different temperatures (squares; blue −20 °C, black 4 °C, and red 20 °C). The calculated gray curve represents 189 Hz dipolar 15N···13C coupling of a static glycine as in the molecular crystal.46 The other curves represent REDOR simulations that best fit the experimental data (with emphasis on the initial decay). The curves that fit the REDOR data of adsorbed glycine in the dry state at temperatures of −20 and 20 °C were generated by single REDOR evolutions with 168 and 147 Hz dipolar couplings with DC offset of 4%, and further apodized with an exponential, T2-like, decay of 30 ms (10.67 Hz line broadening) and 50 ms (6.3 Hz line broadening), respectively. Each curve that fits the experimental data of the intermediate hydration state at each of the three temperatures (−20, 4, and 20 °C) was obtained by a weighted summation of three calculated REDOR evolutions with distinct dipolar coupling strengths, as listed in Table 1. Experimental 15N{13C} SR/S0 REDOR evolution of [1-13C,15N]Gly/SBA-15 in the dry state (hollow circles) presented for comparison (adapted with permission from ref 28).

Since the surface-bound glycine molecules are anchored via their ammonium group, the only possible reorientation of the N···C1 vector is such that the carboxylate (C1) is pendent and exerts the motion. The reorientation spans solid angles of 23° and 33° as derived from the respective 12 and 20% averaging of dipolar coupling.47 The increase of motional amplitude with temperature is slightly more pronounced for Gly/MCM-41 than that for Gly/ SBA-15. This observation further substantiates the weaker binding to MCM-41 and demonstrates binding dependence on the molecular details of the surfaces. In summary, the physical picture in the lowest hydration state (dry) is of a single population of all likely bound glycine molecules; glycine is anchored to the silica surface via its positively charged ammonium moiety, while the carboxylate end is pendent, undergoing fast, small amplitude motion. Qualitatively, this description remains similar to the one obtained for amino acids bound on SBA-15. Increased Hydration: Multiple Glycine Populations and Onset of Dissolution. Upon hydration of Gly/MCM-41 to the intermediate state, the 15N{13C} REDOR evolution of the adsorbed glycine changes dramatically and shows a strong temperature dependence (Figure 7b). These increasingly slower REDOR evolutions can no longer be fit by a single dipolar coupling, and as in our earlier study of Gly/SBA-15 and Ala/SBA-15, we fit the data with three distinct populations.29 In each one, glycine undergoes different dynamics that leads to a differently averaged dipolar interaction. We also assume that all dynamic processes are at the fast limit relative to the inverse dipolar coupling strength (5 ms). The three populations and the respective dipolar coupling strengths at each temperature are listed in Table 1, and the resulting fits are shown in Figure 7b. The 147 Hz population is identical to that seen in the dry state at 20 °C; the 44 Hz population, with farther averaged

Figure 6. Experimental 15N{1H} SLF[PMLG5] dipolar evolution monitoring the 15N peak intensity for [1-13C,15N]Gly/MCM-41 at different temperatures (squares; blue −20 °C, black −4 °C, and red 20 °C) as a function of homonuclear decoupling time t, (a) in the dry hydration state and (b) in the intermediate state. Simulations (curves) were calculated using N−H dipolar coupling of 11.4 kHz (1.01 Å for −NH3+), which is reduced by the C3 rotation of −NH3+ and homonuclear dipolar decoupling scaling factor of 0.47. The adsorbed glycine peak gives rise to evolution, which closely overlaps that of the simulated curve of −NH3+ for the dry state and for the intermediate state at −20 °C. The 4 °C curve was obtained by considering 40% isotropic population with 0 Hz coupling.

(calculated and model compounds) −NH3+ dipolar evolution curve (Figure 6 a, curves). This indicates that the amine moiety of surface-bound glycine is the protonated, charged ammonium group, −NH3+, as observed for the SBA-15 surfaces.29 Dynamic Behavior of Adsorbed Glycine. Dry State: Single-Bound Population. To identify the dynamics that glycine undergoes while surface-bound we have monitored its intramolecular 15N···13C1 dipolar interaction using 15N{13C} CP-REDOR (Figure 7). Accounting for small amplitude librations, the fixed internuclear 15N···13C1 distance45 of 2.49 Å translates to a measurable 189 Hz dipolar coupling strength (reflecting an effective longer distance of 2.54 Å)46 and calculated SR/S0 REDOR evolution, as exhibited by the continuous gray curve in Figure 7a. The measured 15N{13C} REDOR data of Gly/MCM-41 in the dry state (Figure 7a) at −20 and 20 °C show slower decays best fit by REDOR curves of 168 and 147 Hz coupling strengths, respectively. This dipolar coupling reduction of 12 and 20% compared to the static (crystalline) value reflects motional averaging of the 15N···13C1 dipolar interaction via fast, small amplitude, anisotropic molecular reorientation of the intramolecular 15N···13C1 vector. 7905

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

state at 4 °C shallows significantly compared to −20 °C, indicating a 40% Gly population with fully averaged N−H3 dipolar coupling. This is in line with the 15N{13C} REDOR observation identifying that 25% of Gly undergo isotropic motion in the intermediate state at 4 °C. Hydrated State: Onset of Complete Dissolution. The hydrated state obtained by further addition of a minute amount of water (p > 10) resulted in almost complete suppression of the cross-polarization to 15N (Figure 1f) where only a residual and substantially narrowed peak is detected. The suppression of the cross-polarization efficiency to 15N indicates that all glycine molecules undergo fast isotropic reorientation. We emphasize this substantial suppression since all the isotropic-motion populations that we discussed so far for both surfaces were CPvisible. The isotropic population of the hydrated Gly/MCM-41 must therefore have reorientation rates of Gly much faster than that exhibited on SBA-15. This much faster motion corroborates the determination that binding affinity of Gly to MCM-41 is weaker. We note that about 10 attempts of hydration−dehydration to reach the measurable (CP-visible) intermediate state resulted in either dry or fully isotropic hydrated states. This sharp transition with respect to surface density of H-atoms is a further manifestation of the structural differences between the MCM-41and SBA-15 surfaces. This observation is consistent with earlier observations32,49 showing that the cluster size distribution of surface water on MCM-41 changed sharply upon hydration, and the transition from sparse to bulk-like waters occurs over a much narrower hydration range than that on SBA-15.

Table 1. 15N···13C1 Dipolar Couplings and Respective Populations Obtained by Best Fitting the 15N{13C} REDOR Data for Gly/MCM-41 in the Intermediate Hydration State at Each Temperature νD

147 Hza θ = 32.5° (%)

44 Hza θ = 67° (%)

0 Hz isotropic (%)

T = −20 °C T = 4 °C T = 20 °C

88 30 15

12 45 40

0 25 45

a

The 2nd and 3rd columns represent bound, ammonium-anchored glycine, with its carboxylate end undergoing rapid anisotropic reorientation spanning a cone whose head angle θ is determined from the extent dipolar coupling strengths (νave/νstatic).47

dipolar interactions, represents glycine molecules undergoing greater amplitude reorientation while anchored via their ammonium moiety. The third population, with average to zero dipolar coupling, consists of dissolved glycine molecules that undergo rapid isotropic reorientation. A schematic representation of the three classes of dynamic states is shown in Figure 8. The cones illustrate the reorientation boundaries of

■

DISCUSSION Our previous studies28,29 identified that binding characteristics of glycine and alanine are similar when loaded to the same SBA-15 silica surfaces. This similarity of interactions and dynamic modes suggested a pattern of interacting moieties and specificity of binding site geometry and stoichiometry for small amino acids with a nonpolar side-chain. In order to examine the sensitivity of this pattern to different silica surfaces, MCM-41 silica was investigated. The adsorbents Gly and L-Ala interact with silica surfaces MCM-41 and SBA-15 predominantly via their amine moiety, while their carboxylate end is pendent; the amino acid binding group is identified as the charged ammonium moiety. This observation suggests that one of the interacting silanols is a negatively charged deprotonated Si−O− species as a counterbalance, which is consistent with the acidic nature of these surfaces. Noteworthy, this experimental observation is opposite to computational studies that propose binding models where the carboxylate facilitates the main anchor of the amino acid (e.g., Gly) to the surface while the ammonium is pendent.25,27,50 While focusing on the chemical identity and geometric arrangement of the functional groups on the two different surfaces, the amino acids become a sensitive probe to detect surface details and expose the similarities and differences between MCM-41 and SBA-15. Both surface binding sites consist of several closely spaced silanols, primarily Q3s. Despite this apparent similarity, MCM-41 surfaces offer weaker binding than SBA-15. The SBA-15 surface binding site was shown to be a specific one consisting of a close and nonabundant arrangement of 3−4 Si atoms. These form the binding potential for the ammonium moiety with the nitrogen closely

Figure 8. Schematic representation of the three classes of dynamic states of Gly on MCM-41.

the anchored glycine and the circle illustrates the isotropic motion;47 the cone angles that correspond to the Gly populations on MCM-41 are listed in Table 1. Similar to SBA-15, these three dynamic populations are interpreted in terms of glycine bound at surface sites accommodating water clusters of growing sizes.32,48 The larger the cluster, the weaker the binding potential and the wider the reorientation amplitude spanned by the pendent carboxylate. Temperature increase acts to shift the distribution toward the more mobile populations (Table 1). Further examining the characteristics of the intermediate hydration state at −20 °C, we note that the 15N{29Si} REDOR evolution (Figure 5) and the N−H dipolar evolution (15N{1H} SLF[PMLG5]; Figure 6b, blue squares) are indistinguishable from their dry state, 4 °C counterparts, which further substantiates our assignment of glycine populations with 44 Hz 15N−13C dipolar coupling as ammonium anchored. As an apparent exception to the above-noted similarities, the 128TR 29 Si{15N} REDOR spectra (Figure 4b) of Gly/MCM-41 in the intermediate hydration state at −20 °C exhibits smaller REDOR attenuation (ΔS, blue trace), primarily by the Q3 silanols, compared to the dry state. While confirming the persistence of interactions with glycine ammonium, the reduced REDOR effect merely reflects increased cross-polarization efficiency of surface species at the higher hydration level and hence a higher Q3 peak (S0) of which the fraction of interacting silanols becomes smaller. Finally, the N−H dipolar evolution (15N{1H} SLF[PMLG5]; Figure 6b, black squares) of Gly/MCM-41 in the intermediate 7906

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

equidistant, 4.1 ± 0.5 Å, to each Si. This tight geometry on SBA-15 identifies the interaction as direct, namely, not mediated by water molecule(s). For MCM-41 the REDOR effect of 6.6% is too low to narrow down the geometric and/or stoichiometric determination. Two representative classes of equally valid binding site structures are shown. In the first, the geometric arrangements of the sites are similar to those on SBA-15, however, with ∼0.4 Å longer Si···N distances (4.5 ± 0.5 Å). In the second valid structure, the site is made of only two adjacent Si atoms, keeping ∼4.0 Å Si···N distances as on SBA-15. The weaker binding on MCM-41 compared to SBA-15 is alluded to by both binding classes. Our observations are consistent and well rationalized considering the known differences between the two mesoporous silica surfaces. Aside from the smaller pore diameter and wall thickness, MCM-41 has altered surface characteristics that are critical for our discussion. MCM-41 has a lower density of Q2 and Q3 species than SBA-15, with (average) densities of silanol groups at the pore walls of ∼2.9 and ∼3.7/nm2, respectively.15,18,19 On the atomic length scale, the inner pore surfaces of high-quality MCM-4118,20 are smooth and relatively ordered, yet rough and with higher disorder for SBA-15.15,19 This fact was also demonstrated32 by observing the buildup of water clusters on the two surfaces (1H and 2H MAS NMR), showing a much narrower transition to the hydrated state (primarily large hydrogen clusters with more than 2 water molecules) on MCM-41. The weaker interaction of MCM-41 with Gly, together with its higher atomic smoothness and sparser average occurrence of surface silanols, lead to the conclusion that the binding sites (as found on SBA-15) are not only less abundant but are also structured differently, hence exposing a looser binding potential, which is also with reduced specificity. Minutely and gradually hydrating the amino acid loaded surfaces (intermediate and hydrated states) suffices to enable isotropic motion of the adsorbents, as shown for both SBA-15 and MCM-41. This isotropic motion indicates that the adsorbent is no longer surface anchored and serves as a criterion for onset of dissolution. The isotropic reorientation of the amino acids mimic a solute in aqueous solution, yet with far slower dynamic rates (≤106 vs ∼1012 s−1 in bulk water).29 The onset of dissolution is understood as a local phenomenon, where the binding site is occupied simultaneously by the amino acid and water, forming a hydrogen cluster from silanol hydroxyls, water, and the charged ammonium. When the average water density increases to 1−3 water molecules/nm2, onset of dissolution is observed throughout. In fact, at lower hydration levels as in the intermediate state, different populations of adsorbent Gly or Ala are identified to coexist depending on the hydrogen cluster size at the binding site. At a site where the cluster is small, e.g., one water molecule added at the binding site, only increased motional amplitude occurs while the ammonium is steel anchored. Isotropic motion sets in with additional 1−2 water molecules at the binding site. In one case, Gly/SBA-15 in the hydrated state, for a population with surface-anchored Gly, the fast hydrogen exchange within the cluster could be detected as part of the approach to dissolution. This H-cluster description is fully consistent with earlier detailed reports of water cluster formation and growth upon hydration of the very same surfaces.32,51 The coexisting different populations of amino acids with different dynamics reflect the (small) hydrogen cluster size distribution as dictated by the hydration level.

Comparing the behavior of the two surfaces, Gly reaches complete onset of dissolution on MCM-41 at a much lower hydration level than on SBA-15. This observation is consistent with earlier studies (1H/2H MAS NMR) of water, amino acids, and short peptides on the two surfaces showing the narrow transition to the hydrated state.32,51 Notwithstanding, additional direct confirmation for the lower affinity of MCM-41 to Gly (compared to SBA-15) is manifested by the much faster reorientation rates that Gly experiences upon onset of dissolution from MCM-41 than from SBA-15 (demonstrated by the much lower cross-polarization efficiency of Gly on MCM-41). The above evidence is consistent with the MCM-41 surface being more hydrophobic than SBA-15. Our results indicate that while the general pattern of amino acid−silica surface interactions reflects involvement of the same functional groups, charged amine vs silanols, significant alteration of binding occurs depending on the detailed structure of the surface. This directly inflicts on its own reactivity and may also therefore affect the adsorbent reactivity.

■

CONCLUSIONS The comprehensive molecular level, solid-state NMR characterization of the binding of small amino acids with a nonpolar side chain (Gly and L-Ala) to different amorphous silica surfaces (MCM-41 and SBA-15) exposes the common and distinctive binding motifs. In particular, the latter are correlated directly with changes in surface structure as they lead to alteration of binding strength. These are manifested by different compositions and geometries of surface sites, which are the main factors that determine surface reactivity. When dehydrated, the adsorption of the amino acids onto the amorphous silica surfaces is via direct interaction of their charged amine end with 3 or 4 silanols on SBA-15 yet 2−4 on MCM-41. The binding strength exerted by the specific SBA-15 site is stronger than that of MCM-41. For the latter, surface−amino acid distances (Si···N) are longer and/or the binding stoichiometry is lower. As a consequence, onset of dissolution (desorption) is reached at lower hydration levels. In the least hydrated state, the single population of bound amino acids exhibits higher temperature dependence on MCM, indicating a lower reorientation barrier. The above observations clearly indicate that the different geometric surface structures found on SBA-15 vs MCM-41 result in different surface reactivity. Their occurrence on one surface and absence on the other correlates with the known different surface characteristics resulting from the two synthetic pathways: higher atomic smoothness and sparser average occurrence of surface silanols on MCM-41. In this study, we demonstrate an experimental and methodological NMR framework that relies largely on dipolar recoupling techniques. These are capable of spectral editing that reveals interacting moieties (surface and adsorbents) and are also capable of directly measuring binding geometry, stoichiometry, and dynamics as a function of hydration and temperature. To date, these binding modes have not been identified and were often implied by controversial, indirect evidence (computational and experimental). The three case studies of the binding of Gly and Ala to SBA-15 and MCM-41 surfaces provide, for the first time, direct evidence of the binding modes of amino acids to mesoporous silica surfaces, exposing the nature of the surface binding sites, and show the relationship by which structural variations of the surfaces determine its reactivity. Such findings are of fundamental 7907

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

(18) Edler, K. J.; Reynolds, P. A.; White, J. W. Small-Angle Neutron Scattering Studies on the Mesoporous Molecular Sieve MCM-41. J. Phys. Chem. B 1998, 102, 3676−3683. (19) Shenderovich, I. G.; Mauder, D.; Akcakayiran, D.; Buntkowsky, G.; Limbach, H. H.; Findenegg, G. H. NMR Provides Checklist of Generic Properties for Atomic-Scale Models of Periodic Mesoporous Silicas. J. Phys. Chem. B 2007, 111, 12088−12096. (20) Edler, K. J.; Reynolds, P. A.; White, J. W.; Cookson, D. Diffuse Wall Structure and Narrow Mesopores in Highly Crystalline MCM-41 Materials Studied by X-ray Diffraction. J. Chem. Soc., Faraday Trans. 1997, 93, 199−202. (21) Solovyov, L. A.; Kirik, S. D.; Shmakov, A. N.; Romannikov, V. N. X-ray Structural Modeling of Silicate Mesoporous Mesophase Material. Microporous Mesoporous Mater. 2001, 44, 17−23. (22) Sauer, J.; Marlow, F.; Schuth, F. Simulation of Powder Diffraction Patterns of Modified Ordered Mesoporous Materials. Phys. Chem. Chem. Phys. 2001, 3, 5579−5584. (23) Zhang, J. Y.; Luz, Z.; Goldfarb, D. EPR Studies of the Formation Mechanism of the Mesoporous Materials MCM-41 and MCM-50. J. Phys. Chem. B 1997, 101, 7087−7094. (24) Ruthstein, S.; Schmidt, J.; Kesselman, E.; Talmon, Y.; Goldfarb, D. Resolving Intermediate Solution Structures during the Formation of Mesoporous SBA-15. J. Am. Chem. Soc. 2006, 128, 3366−3374. (25) Stievano, L.; Piao, L. Y.; Lopes, I.; Meng, M.; Costa, D.; Lambert, J. Glycine and Lysine Adsorption and Reactivity on the Surface of Amorphous Silica. Eur. J. Mineral. 2007, 19, 321−331. (26) Zhao, Y. L.; Koippen, S.; Frauenheim, T. An SCC-DFTB/MD Study of the Adsorption of Zwitterionic Glycine on a Geminal Hydroxylated Silica Surface in an Explicit Water Environment. J. Phys. Chem. C 2011, 115, 9615−9621. (27) Folliet, N.; Gervais, C.; Costa, D.; Laurent, G.; Babonneau, F.; Stievano, L.; Lambert, J.; Tielens, F. A Molecular Picture of the Adsorption of Glycine in Mesoporous Silica through NMR Experiments Combined with DFT-D Calculations. J. Phys. Chem. C 2013, 117, 4104−4114. (28) Ben Shir, I.; Kababya, S.; Schmidt, A. Binding Specificity of Amino Acids to Amorphous Silica Surfaces: Solid-State NMR of Glycine on SBA-15. J. Phys. Chem. C 2012, 116, 9691−9702. (29) Ben Shir, I.; Kababya, S.; Amitay-Rosen, T.; Balazs, Y. S.; Schmidt, A. Molecular Level Characterization of the Inorganic− Bioorganic Interface by Solid-State NMR: Alanine on a Silica Surface, a Case Study. J. Phys. Chem. B 2010, 114, 5989−5996. (30) Gullion, T.; Schaefer, J. Rotational-Echo Double-Resonance NMR. J. Magn. Reson. 1989, 81, 196−200. (31) Hester, R. K.; Ackerman, J. L.; Neff, B. L.; Waugh, J. S. Separated Local Field Spectra in NMR: Determination of Structure of Solids. Phys. Rev. Lett. 1976, 36, 1081−1083. (32) Amitay-Rosen, T.; Kababya, S.; Vega, S. A Dynamic Magic Angle Spinning NMR Study of the Local Mobility of Alanine in an Aqueous Environment at the Inner Surface of Mesoporous Materials. J. Phys. Chem. B 2009, 113, 6267−6282. (33) Gullion, T.; Schaefer, J. Detection of Weak Heteronuclear Dipolar Coupling by Rotational Echo Double Resonance Nuclear Magnetic Resonance. Adv. Magn. Opt. Reson. 1989, 13, 57. (34) Veshtort, M.; Griffin, R. G. Spinevolution: A Powerful Tool for the Simulation of Solid and Liquid State NMR Experiments. J. Magn. Reson. 2006, 178, 248−282. (35) Massiot, D.; Fayon, F.; Capron, M.; King, I.; Calvé, S. L.; Alonso, B.; Durand, J.; Bujoli, B.; Gan, Z.; Hoatson, G. Modelling One- and Two-Dimensional Solid-State NMR Spectra. Magn. Reson. Chem. 2002, 40, 70−76. (36) Vinogradov, E.; Madhu, P. K.; Vega, S. High-Resolution Proton Solid-State NMR Spectroscopy by Phase-Modulated Lee−Goldburg Experiment. Chem. Phys. Lett. 1999, 314, 443−450. (37) Vinogradov, E.; Madhu, P. K.; Vega, S. Phase Modulated Lee− Goldburg Magic Angle Spinning Proton Nuclear Magnetic Resonance Experiments in the Solid State: A Bimodal Floquet Theoretical Treatment. J. Chem. Phys. 2001, 115, 8983−9000.

importance and their implications also extend to a wide variety of technological aspects.

■

AUTHOR INFORMATION

Corresponding Author

*(A.S.) Phone: +972-4-8292583. E-mail: [email protected]. ac.il. Notes

The authors declare no competing financial interest.

■ ■

ACKNOWLEDGMENTS This research was supported by the German−Israel Foundation grant 76-2009. REFERENCES

(1) Nakanishi, K.; Sakiyama, T.; Imamura, K. On the adsorption of proteins on solid surfaces, a common but very complicated phenomenon. J. Biosci. Bioeng. 2001, 91, 233−244. (2) Taguchi, A.; Schuth, F. Ordered mesoporous materials in catalysis. Microporous Mesoporous Mater. 2005, 77, 1−45. (3) Mann, S. Biomineralizatiom Principles an Concepts in Bioinorganic Materials Chemistry; Oxford University Press: Oxford, U.K., 2001. (4) Jahren, A. H.; Skinner, H. C. W. Biomineralization; Elsevier Science: Oxford, U.K., 2007; Vol. 8, Chapter 4, Biogeochemistry, pp 1−69. (5) Lowenstam, H. A.; Weiner, S. On Biomineralization; Oxford University Press: New York, 1989; p 324. (6) Besteman, K.; Lee, J.; Wiertz, F. G. M.; Heering, H. A.; Dekker, C. Enzyme-Coated Carbon Nanotubes as Single-Molecule Biosensors. Nano Lett. 2003, 3, 727−730. (7) Hersel, U.; Dahmen, C.; Kessler, H. RGD Modified Polymers: Biomaterials for Stimulated Cell Adhesion and Beyond. Biomaterials 2003, 24, 4385−4415. (8) Rimola, A.; Tosoni, S.; Sodupe, M.; Ugliengo, P. Does Silica Surface Catalyse Peptide Bond Formation? New Insights from FirstPrinciples Calculations. ChemPhysChem 2006, 7, 157−163. (9) Lambert, J. Adsorption and Polymerization of Amino Acids on Mineral Surfaces: A Review. Origins Life Evol. Biospheres 2008, 38, 211−242. (10) Giraldo, L. F.; López, B. L.; Pérez, L.; Urrego, S.; Sierra, L.; Mesa, M. Mesoporous Silica Applications. Macromol. Symp. 2007, 258, 129−141. (11) Linssen, T.; Cassiers, K.; Cool, P.; Vansant, E. F. Mesoporous Templated Silicates: An Overview of Their Synthesis, Catalytic Activation and Evaluation of the Stability. Adv. Colloid Interface Sci. 2003, 103, 121−147. (12) Zhuravlev, L. T. The Surface Chemistry of Amorphous Silica. Zhuravlev Model. Colloids Surf., A 2000, 173, 1−38. (13) Kresge, C. T.; Leonowicz, M. E.; Roth, W. J.; Vartuli, J. C.; Beck, J. S. Ordered Mesoporous Molecular-Sieves Synthesized by a LiquidCrystal Template Mechanism. Nature 1992, 359, 710−712. (14) Zhao, D. Y.; Feng, J. L.; Huo, Q. S.; Melosh, N.; Fredrickson, G. H.; Chmelka, B. F.; Stucky, G. D. Triblock Copolymer Syntheses of Mesoporous Silica with Periodic 50 to 300 Angstrom Pores. Science 1998, 279, 548−552. (15) Shenderovich, I. G.; Buntkowsky, G.; Schreiber, A.; Gedat, E.; Sharif, S.; Albrecht, J.; Golubev, N. S.; Findenegg, G. H.; Limbach, H. H. Pyridine-N-15: A Mobile NMR Sensor for Surface Acidity and Surface Defects of Mesoporous Silica. J. Phys. Chem. B 2003, 107, 11924−11939. (16) Baccile, N.; Laurent, G.; Bonhomme, C.; Innocenzi, P.; Babonneau, F. Solid-State NMR Characterization of the SurfactantSilica Interface in Templated Silicas: Acidic versus Basic Conditions. Chem. Mater. 2007, 19, 1343−1354. (17) Shi, L.; Zou, Y.; He, H. 1H NMR Study of Hydroxy Groups in Mesoporous Molecular Sieve SBA-15. Chem. Lett. 2001, 30, 1164− 1165. 7908

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909

The Journal of Physical Chemistry C

Article

(38) Vinogradov, E.; Madhu, P. K.; Vega, S. Proton Spectroscopy in Solid State Nuclear Magnetic Resonance with Windowed Phase Modulated Lee−Goldburg Decoupling Sequences. Chem. Phys. Lett. 2002, 354, 193−202. (39) Leskes, M.; Madhu, P. K.; Vega, S. A Broad-Banded z-Rotation Windowed Phase-Modulated Lee−Goldburg Pulse Sequence for H-1 Spectroscopy in Solid-State NMR. Chem. Phys. Lett. 2007, 447, 370− 374. (40) Leskes, M.; Madhu, P. K.; Vega, S. Proton Line Narrowing in Solid-State Nuclear Magnetic Resonance: New Insights from Windowed Phase-Modulated Lee−Goldburg Sequence. J. Chem. Phys. 2006, 125, 124506. (41) deAzevedo, E. R.; Saalwachter, K.; Pascui, O.; de Souza, A. A.; Bonagamba, T. J.; Reichert, D. Intermediate Motions As Studied by Solid-State Separated Local Field NMR Experiments. J. Chem. Phys. 2008, 128, 104505. (42) Stievano, L.; Tielens, F.; Lopes, I.; Folliet, N.; Gervais, C.; Costa, D.; Lambert, J. Density Functional Theory Modeling and Calculation of NMR Parameters: An ab Initio Study of the Polymorphs of Bulk Glycine. Cryst. Growth Des. 2010, 10, 3657−3667. (43) Chuang, I. S.; Maciel, G. E. A Detailed Model of Local Structure and Silanol Hydrogen Banding of Silica Gel Surfaces. J. Phys. Chem. B 1997, 101, 3052−3064. (44) Gullion, T. Introduction to Rotational-Echo, Double-Resonance NMR. Concepts Magn. Reson. 1998, 10, 277−289. (45) Legros, J.-P.; Kvick, A. Deformation Electron Density of alphaGlycine at 120 K. Acta Crystallogr., Sect. B: Struct. Sci. 1980, 36, 3052− 3059. (46) Goetz, J. M.; Schaefer, J. REDOR Dephasing by Multiple Spins in the Presence of Molecular Motion. J. Magn. Reson. 1997, 127, 147− 154. (47) Jayanthi, S.; Frydman, V.; Vega, S. Dynamic Deuterium Magic Angle Spinning NMR of a Molecule Grafted at the Inner Surface of a Mesoporous Material. J. Phys. Chem. B 2012, 116, 10398−10405. (48) Grunberg, B.; Emmler, T.; Gedat, E.; Shenderovich, J.; Findenegg, G. H.; Limbach, H. H.; Buntkowsky, G. Hydrogen Bonding of Water Confined in Mesoporous Silica MCM-41 and SBA15 Studied by H-1 Solid-State NMR. Chem.Eur. J. 2004, 10, 5689− 5696. (49) Pizzanelli, S.; Kababya, S.; Frydman, V.; Landau, M.; Vega, S. NMR Study of the Adsorption-Desorption Kinetics of Dissolved Tetraalanine in MCM-41 Mesoporous Material. J. Phys. Chem. B 2005, 109, 8029−8039. (50) Costa, D.; Tougerti, A.; Tielens, F.; Gervais, C.; Stievano, L.; Lambert, J. F. DFT Study of the Adsorption of Microsolvated Glycine on a Hydrophilic Amorphous Silica Surface. Phys. Chem. Chem. Phys. 2008, 10, 6360−6368. (51) Amitay-Rosen, T.; Vega, S. A Deuterium MAS NMR Study of the Local Mobility of Dissolved Methionine and Di-Alanine at the Inner Surface of SBA-15. Phys. Chem. Chem. Phys. 2010, 12, 6763− 6773.

7909

dx.doi.org/10.1021/jp409030w | J. Phys. Chem. C 2014, 118, 7901−7909