Chirality-Induced Electron Spin Polarization and Enantiospecific

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Chirality-Induced Electron Spin Polarization and Enantiospecific Response in Solid State Cross-Polarization Nuclear Magnetic Resonance José Ignacio Santos, Iván Rivilla, Fernando P. Cossio, Jon M. Matxain, Marek Grzelczak, Shobeir K. S. Mazinani, Jesus M. Ugalde, and Vladimiro Mujica ACS Nano, Just Accepted Manuscript • DOI: 10.1021/acsnano.8b06467 • Publication Date (Web): 08 Nov 2018 Downloaded from http://pubs.acs.org on November 9, 2018

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Chirality-Induced Electron Spin Polarization and Enantiospecific Response in Solid State CrossPolarization Nuclear Magnetic Resonance Jose I. Santos†, Iván Rivilla‡,§ *, Fernando P. Cossío‡, § , Jon M. Matxain∥, §, Marek Grzelczak§,⊥ , Shobeir K. S. Mazinani∇, Jesus M. Ugalde∥, §,*, and Vladimiro Mujica∇,* †

SGIker-UPV/EHU; Centro "Joxe Mari Korta"; Tolosa Hiribidea, 72; E-20018, Donostia - San

Sebastián, Spain ‡

Department of Organic Chemistry I, Universidad del País Vasco/Euskal Herriko

Unibertsitatea (UPV/EHU), Centro de Innovación en Química Avanzada (ORFEO−CINQA), Paseo de Manuel Lardizabal 3, 20018, Donostia - San Sebastián, Spain §

Donostia International Physics Center, Paseo de Manuel Lardizabal 4, 20018, Donostia -

San Sebastián, Spain ∥

Kimika Fakultatea, Euskal Herriko Unibertsitatea (UPV/EHU) Paseo de Manuel Lardizabal

3, 20018, Donostia - San Sebastián, Spain ⊥

Ikerbasque, Basque Foundation for Science, 48013, Bilbao, Spain

∇

Arizona State University, School of Molecular Sciences, Tempe, AZ 85287, U.S.A.

ACS Paragon Plus Environment

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KEYWORDS: CISS, CP-MAS, Solid State -NMR, Chiral, Spin, Aminoacids, enantiomers

ABSTRACT NMR-based techniques are supposed to be incapable of distinguishing pure crystalline chemical enantiomers. However, through systematic studies of cross-polarization magic angle spinning (CP-MAS) NMR in a series of aminoacids, we have found a rather unexpected behavior in the intensity pattern of optical isomers in hydrogen/nitrogen nuclear polarization transfer that would allow the use of CP NMR as a non-destructive enantioselective detection technique. In all molecules considered, the D isomer yields higher intensity than the L form, while the chemical shift for all nuclei involved remains unchanged. We attribute this striking result to the onset of electron spin polarization, accompanying bond charge polarization through a chiral center, a secondary mechanism for polarization transfer that is triggered only in the CP experimental setup. Electron spin polarization is due to the chiralinduced spin selectivity effect (CISS), which creates an enantioselective response, analogous to the one involved in molecular recognition and enantiospecific separation with achiral magnetic substrates. This polarization influences the molecular magnetic environment, modifying the longitudinal relaxation time T1 of 1H, ultimately provoking the observed asymmetry in the enantiomeric response.

In the last years, Solid-State NMR spectroscopy has been introduced as a real alternative for the analysis and determination of compounds with isotopic natural abundance. Additionally, since this


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technique provides key structural information1, to the point of becoming an alternative to X-ray diffraction to characterize crystal solids2, the use of this technique for the structural elucidation of proteins,3 organic4 and inorganic5 materials has become ubiquitous.

However, Solid-State NMR spectroscopy has two important limitations, the one related to its poor sensitivity for nuclei with low natural abundance such as 15N or 13C, and the other connected to the long relaxation times for these nuclei, which create experimental difficulties. One of the most important techniques to overcome these shortcomings, known as “cross polarization” is based in the transfer of nuclear spin polarization from abundant, usually 1H, to less abundant nuclei. This methodology not only enhances the signal strength of the rare nuclear spins, but also allows the experiment to be repeated at larger rates because it is governed by the relatively short longitudinal relaxation time T1 of 1H.

In addition to other limitations mentioned above, Solid State NMR is incapable of distinguishing pure samples of enantiomers. Some authors have proposed the use of CP-MAS (Cross Polarization Magic Angle Spinning) NMR, in the presence of chiral solvating agents,6 for determining the enantiomeric excess (ee) of chiral mixtures. In a related direction, specific 2D pulse sequences have been developed and modified, aiming to differentiate an enantiomer from its partner. In this context, the use of a specific pulse sequence ODESSA7-9 allows obtaining intermolecular distances in crystalline solids and polymorphs, thus becoming a powerful tool towards ee determination.10 It is worth to emphasize that in the absence of a chiral environment the expectation was that CPMAS would not be capable of generating an enantioselective signal. It is precisely this expectation that needs to be revised in light of the results of our work.


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As mentioned above, CP-MAS NMR takes advantage of the pulse-induced nuclear-spin polarization transfer between abundant nuclei, such as 1H, and dilute nuclei, e.g.,

15N.

The

dominant mechanism for this CP transfer is via the nuclear magnetic dipolar interaction, upon fulfillment of the Hartmann-Hahn (H-H) condition, which is essential for the polarization transfer to be effective.11 This direct dipolar nuclear coupling does not involve bond polarization, however, a secondary mechanism, known as indirect coupling, is mediated by electrons associated to the chemical bonds linking the nuclei involved in the transfer of nuclear magnetic polarization. The bond polarization produced by the pulse needed to enforce the H-H condition generates an electronic polarization through a chiral center, which is essential for the enantiospecific response we observe in the experiment. In a recent article appeared in Science, Paltiel and co-workers12 have demonstrated that bond polarization in chiral molecules, exactly the same mechanism we are considering in CP transfer, is responsible for the enantiospecific interaction of enantiomers with achiral magnetic substrates. This revolutionary technique, is the basis for a non-chemical separation of enantiomers, and has far-reaching technological implications. In our case, bond polarization involved in CP, makes our technique depending on both the molecular geometry, as determined by a specific chemical bonding pattern, and on the specific dynamics of the electronic charge polarization through chemical bonds, which is coupled to electron spin polarization via the CISS effect.13-23 It is remarkable that most instances of the CISS effect in the literature are reported in diamagnetic systems with no unpaired electrons, and this provides a clear opportunity to separate the subtle electron spin polarization effects from the much stronger effects observed in paramagnetic systems, via EPR or ENDOR, which occur in an entirely different frequency domain of the electromagnetic pulse.


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We have designed several experiments aimed at exploring the use of CP-MAS NMR as a tool to determine values of ee. To this end, we tested 15N CP-MAS NMR with pure crystalline samples of a series of essential aminoacids. Recall that all aminoacids, except glycine, are found in two optical isomeric forms, L and D. Eight enantiopure L and D essential aminoacids were selected for this investigation (Figure 1).

O H 2N

OH

H 2N

O

O

O OH O

H 2N

OH

H 2N

OH

OH Phenylglycine

Aspartic acid

OH

H 2N

Tyrosine

O OH

SH Valine

Phenylalanine

O

O H 2N

OH

Cysteine

H 2N

O OH

OH Serine

H 2N

OH

HO Threonine

Figure 1. Selected aminoacids for this study.

During these tests, we encountered a rather unexpected systematic asymmetry in the spectra of the two optical isomeric forms for each aminoacid; namely that the intensity for the D form was consistently higher than that of the L form. For example, the intensity ratio I(D)/I(L) for the Aspartic Acid is 2.20, a striking result that to the best of our knowledge differs from all conventional NMR studies of crystalline enantiomeric mixtures. This unexpected finding, which


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cannot be attributed to differences in molecular structures, together with developing a theoretical model for its interpretation, is our core result in the investigation reported here. As discussed earlier in the introduction CP-MAS NMR strongly depends on the time T1, which describes the longitudinal lattice relaxation of 1H, in accordance with the double-exponential kinetics described in reference (24) for a simple model of CP. To illustrate this behavior, we have determined the optimal repetition time TR, which must be of the same order of magnitude as T1 for efficient signal acquisition. This way we can ascertain that the I(D)>I(L) condition does not result from the selection of non-optimal TR for the L isomer. Figure 2 shows the results for the commercially available 15N-labeled L-isomer of Aspartic acid. To optimize the TR, measurements at different contact times, CT, (spin lock times), and TR between pulses were carried out. In the conventional experimental setup, the approximate value of TR is taken from the literature and once signal is detected for one of the enantiomers, it remains fixed.25But in our case a thorough optimization process is essential for the understanding of our results, because it reveals the role of T1 as the crucial physical parameter to explain the difference in intensity of the D and L enantiomers. The optimal value of TR is selected as the minimum value yielding a stable maximum in the intensity, i.e., that further increases in TR do not lead to increasing the intensity. For the case shown in figure 2a the optimal RT corresponds to 20 s, for a value of CT of 2 ms. Panel b in figure 2, shows that the chemical shift for the L-isomer is constant for various repetition times. Panels (c) and (d) display the spectra for the two isomers for optimal and non-optimal TR, respectively, confirming the strong dependence of the signal on this experimental parameter. These two figures, are especially relevant because they evidence that the chemical shifts of the two isomers are essentially unaltered (Figure 2c and 2d), indicating that whatever variation in the local magnetic environment


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of the nuclei, due to the CISS effect, that may be involved in CP is a transient effect in the time scale of the experiment, because otherwise it would translate into a change in the chemical shift.

Figure 2. (a) 15N{1H} CP-MAS intensity curves of labeled 15N L-Aspartic acid recorded with CP experiments at different CT (range 0.5-8 ms) and TR (range 1-20s) (b) 15N{1H} CP-MAS spectra at the same CT=2 ms and optimized TR c) 15N{1H} CP-MAS spectra by L & D Asp-Acid at CT = 2ms and TR = 20 s. d) 15N{1H} CP-MAS spectra by L & D Asp-Acid at CT = 2ms and TR = 1 s.

Since experiments are usually run with unlabeled nuclei, we have performed a limited version of the measurements reported on Figure 2, to determine optimal TR of L-Serine and D-Serine to be 38 s and 20 s, using unlabeled samples. Figure 3a and 3b display the intensity curves and the


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spectra for the two optical isomers using the optimized value of TR = 20 s obtained for the Disomer. The intensities for the two enantiomers are clearly measurable and different, and there is no displacement of the chemical shift. Figure 3c displays the spectra of the D and L enantiomers for variable TR for L-Serine while keeping TR for D-Serine constant (equal to its optimal value). The spectra show that not even for a threefold increase in the TR for L-Serine the intensity becomes equal to the D-Serine case. Finally, Figure 3d displays the comparison between the D- and LSerine for optimal values of TR for each enantiomer. All these results are clearly consistent with those obtained using the labeled samples and verify the robustness of our findings under the actual conditions of the CP experiment.

This optimization procedure has also been followed for the remaining molecules, and the obtained TR for each species are shown in Table 1. As emphasized above, the determination of these times is a critical issue, since depending on the experimental conditions one can get a vanishing (below the detection level) response for one of the two isomers. A particularly striking example of this behavior is the Asp case of where the L isomer yields an essentially vanishing response as compared to the D form, at TR equal to 20s (see Figure 2d). However, Figure 2c shows that both optical isomers yield measurable intensities, when properly optimized CT and TR are chosen, as opposed to the data shown in Figure 2d for non-optimal conditions. All required fine chemicals were employed directly without purification unless otherwise stated (Sigma-Aldrich).


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Figure 3. (a) 15N{1H} CP-MAS intensity curves for 15N L & D-Serine at different CT (range 0.5-8 ms) and TR (range 1-20s) (b)

15N{1H}

CP-MAS spectra for L & D-Serine at CT = 2ms and

constant TR equal to 20 s. (c) 15N{1H} CP-MAS spectra for L & D-Serine at CT = 2ms and variable TR for the L enantiomer. (range 20-70 s) (d) 15N{1H} CP-MAS spectra for L & D-Serine at CT = 2ms and the optimal values of TR for the L(38s), and D(20s) enantiomers. The L curve for TR = 20s is included for comparison. Solid-state NMR spectra were recorded on a Bruker AVANCE III, 9.4 T (Larmor frecuency 400.17 MHz for 1H) equipped with MASDVT BL4 X/Y/H probe head at a spinning rate 10KHz. 100 mg amino acid samples were used to record the spectra. 15N chemical shift were calibrated indirectly with NH4Cl at 0 ppm. The 15N {1H} CP-MAS spectra were recorded and a 1H 90º pulse of 2.5 μs was used. TR's ranging from 1s to 40 s and CT's from 0.5 ms to 8 ms, in accordance with


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the above discussion, were scanned. Table 1 summarizes our results for the whole series of aminoacids. As stated above, the most conspicuous finding is that in all cases the ratio of intensities for the D and L isomers is larger than 1, The table also includes other relevant information, the signal to noise ratio, and the signal area, to ascertain the quality of the experimental results.

Table 1. Chemical shifts () in ppm, optimal repetition time (TR) in s for the L isomer, contact time (CT) in ms, relative D/L intensities (I(D)/I(L)) and relative D/L signal area (Area) for the studied systems. aSignal to Noise Ratio, SNR was calculated using the Bruker command of ‘‘sino real’’ to limit deviations due to baseline correction applied to only the real part of the spectrum, and 50 ppm wide noise region was used Aminoacid D Aspartic acid L Aspartic acid D Cysteine

 (ppm)

TR (s)

CT (ms)

0.14

20

2

8.92

5

D Serine L Serine D-Valine L-Valine

13 6.35 12.68

2

L Cysteine D Phenylalanine L Phenylalanine D Phenylglycine L Phenylglycine D Threonine L Threonine D Tyrosine L Tyrosine

SNRa

Intensity (D)/(L)

Area (D/L)

1.95

2.20

1.88

1.82

8.25 3.1

40

0.5

10.1; 1.7

5

1.5

-0.64

5

2

0.80

30

1.5

-3.01

20

2.0

-1.81

1

6.66 5.16 5.37 5.24 88.38 72.63 5.57 5.03 23.96 22.45 12.77

0.5

1.30

1.20

1.03; 1.07

1.14; 1.01

1.09

1.12

1.14

1.10

1.05

1.13

1.22

1.08

12.32


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One possible explanation for this unexpected NMR asymmetries in chiral molecules is the possibility of polymorphic crystalline forms, which is a rather common phenomenon associated with the environmental influence of the crystal structure of the compound under study. Since solidstate NMR is capable of distinguishing between the different polymorphs we can investigate further this contingency. In order to discard the polymorphism explanation of the experimentally observed I(D) > I(L) effect, we recrystallized our pure L and D phenylglicine samples in a mixture of solvents (EtOH: H2O: Toluene, 1:0.2:0.7; v:v) and heated them up to 100 ºC to promote the solubility and the subsequent recrystallization of the aminoacids. When the CP-MAS NMR experiments are carried out with these recrystallized samples, the presence of polymorphs is evidenced by the appearance of more than one peak in the spectrum. It is clear from Figure 4 that we have the capability of detecting polymorphs whenever they are present in the sample. However, in all our 15N spectra only one peak was observed, which rules out polymorphism as the source of the observed signal intensity asymmetry. We conducted similar experiments in

13C-CP-MAS

NMR, and, opposed to the 15N-CP-MAS NMR samples, we found the existence of polymorphs in this case (see supporting information). In both L and D cases, similar polymorphs were observed, with signals at the same chemical displacements. As in the case of 15N-CP-MAS NMR, the signal intensities were different for all polymorphs (Figure 4)


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Figure 4 15N CP-MAS Phenylglicine spectra (a) D and L, (b) D and L Phenylglicine recrystallized recorded with CP experiment at CT 1.5ms and TR 5s. We have also considered some other alternative explanations, like the effects of paramagnetic molecular oxygen adsorbed at the crystal surface, but this leads to a different peak structure for the CPMAS-NMR signal.26 Having ruled out these alternative explanations, we return to the analysis of the CP-MAS NMR experimental data collected in Table 1. As mentioned above, our working hypothesis is that the CISS effect is responsible for a change in the longitudinal relaxation time of 1H due to changes in the local electron spin density accompanying the bond polarization involved in CP. To simplify the discussion, we concentrate on a simple model for the two relevant nuclei involved in the nuclear spin polarization transfer process. The dominant factor in determining the polarization transfer is the hetero-nuclear dipole-dipole interaction between nuclear magnetic moments II (1H) and IS (15N), and a smaller effect referred to as indirect or Jcoupling that involves the electronic polarization of the chemical bonds. These interactions are represented in a simplified way by the following terms in the total magnetic Hamiltonian27

(1)

𝐻 = 𝐼𝐼 ⋅ 𝐷 ⋅ 𝐼𝑆 + 𝐼𝐼 ⋅ 𝐽 ⋅ 𝐼𝑆


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where D and J are the nuclear-spin dipolar and electronic coupling tensors, respectively. The first term in the Hamiltonian is mostly responsible for the nuclear spin polarization transfer. The second term accounts for the effect of the chiral environment on the nuclear spin cross polarization transfer (vide infra). This term was rightly not considered in the seminal paper by Garbacz and Buckingham28 because the type of physics considered in that work requires free molecular rotation, which restricts the Garbacz-Buckingham model to the case of liquid samples. We have also included in this context a number of important references about previous work related to the development of physical and chemical models for the recognition of enantiomers of chiral molecules.29-32 This positions our work into the right historical perspective, which would also provide greater understanding of its importance. In the case of crystalline samples, as the ones considered in this work, we claim that chirality operates through the subtler, CISS, effect33-45 that we now describe.

A way to understand spin polarization in the presence of any process involving electronic charge transfer, charge polarization or bond polarization involving a chiral molecule, stems from a basic result obtained by solving Schrödinger equation for an electron in a helix including spin-orbit interaction, which is characterized by the Hamiltonian:

ℏ2∂2𝜙

𝐻 = ― 2𝑚(𝑎2 + 𝑏2) +𝛼𝐸𝜌(𝑝 × 𝜎)

(2)

written in the cylindrical coordinates(𝑧, 𝜌,𝜙). 𝜙 is the angular variable, 𝑎 and 𝑏 are the geometrical parameters of the helix, its pitch and radius respectively, 𝛼is the spin-orbit coupling


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constant and 𝐸𝜌 is the radial electric field. The momemtum operator 𝑝 and the Pauli matrices, 𝜎, are also written in cylindrical coordinates For our present discussion, the most important result is that the average values of the velocities of the two spin components involved in the charge polarization process, namely: ℏ2𝑎

𝛼𝑎2

⟨𝛹↑,↓│𝑣𝜙│𝛹↑,↓⟩ = 𝑚(𝑎2 + 𝑏2) ± 𝑎2 + 𝑏2

(3)

differ by a quantity directly proportional to the spin-orbit coupling constant, ,

2𝛼𝑎2

⟨ ⟩ ― ⟨ ⟩ = ― 𝑎 2 + 𝑏2 𝑣↑𝜙

𝑣↓𝜙

(4)

This effect is reflected in the recently measured transmittance of the electron density through a chiral helix.46 As discussed by Mujica et al.46 and others, 47,48 the transmission coefficient, 𝜏 , for each spin component depends explicitly on the chirality of the molecule through which the electron moves, and the helicity of the travelling electron. The latter is specified by the helicity index, i.e: the normalized scalar product µ=s·k/(|s|×|k|)=±1, which gives the projection of the travelling electron's spin vector, s, on the direction of propagation, k. This information is codified by adding a set of three sub-indices (M,k,µ) to the transmission coefficient. The molecular index M can take the values L and D, k indicates the propagation direction, and µ = ±1 is the abovementioned helicity index. Assuming that the D isomer filters out the negative helicity state, we have shown46 that the transmission coefficient obeys important symmetry constraints,


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𝜏𝐷,𝑘, + . = 𝜏𝐷, ― 𝑘, + . (5) (6)

𝜏𝐿,𝑘, ― = 𝜏𝐿, ― 𝑘, ― and

(7)

𝜏𝐷,𝑘, ― = 𝜏𝐿,𝑘, + . ≪ 1

These symmetry conditions imply that electrons with spins aligned in the direction of propagation, have the same transmittance as electrons travelling in the opposite direction with spin aligned in that direction, in both the D and L isomers. However, the transmittance of the D isomer is not equal to the transmittance of the L isomer for the same spin helicity. The symmetry constraints in equations 5-6, also imply that the enantioselective response will only be obtained under the conditions of the CP experiment that is involving polarization transfer between different nuclei, a result that is confirmed by the direct pulse experiments for 1H. The effective longitudinal spin polarization along the z-axis of the helix axis, Pz which is a measure of the difference in density for the two spin components at a distance z from the origin of the polarization event, can be obtained directly as the expectation value of the Pauli matrix σz and is given by18

𝑃𝑧 =

𝐶2 ( 2 𝜏𝐷,𝑘, +

― 𝜏𝐷,𝑘, ― ) = 𝜌𝐷, + ― 𝜌𝐷, ― = Δ𝜌𝐷

(8)

where C is a constant, whose value can be determined from the connection between the scattering amplitude and the t-matrix in the Lippmann-Schwinger equation and 𝜌𝐷, + , 𝜌𝐷, ― , are the spin densities corresponding to each helicity, respectively.47 The derivation of equation (8) assumes that transport is purely coherent tunneling; the description of hopping transport requires additional


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considerations. The case of a perfect filter corresponds to 𝜏𝐷, 𝑘,

―

= 𝜏𝐿, 𝑘,

+.

= 0 in equation (7),

which leads to maximum polarization in equation (8). An equation similar to (8) holds for the L isomer. It is worth noticing that the aminoacid molecules do not have the “extended” chirality of a helix, however in both cases the symmetry properties and the onset of electron-spin polarization, which is the key element in distinguish L and D isomers are present. It seems to be accepted in the NMR literature that the bond chiral path for all molecules in Figure 1 includes both the alpha and beta carbons relative to the 15N. Further exploration of the comparison between the continuous helical model and real molecules with non-extended chirality will be needed.

The interaction of the radiofrequency pulse with the electrons of the 1HCᵦ-CαH–15N chiral path will trigger the building up of uncompensated electron-spin densities of different sign, according to (8), but equal magnitude, at the 1H and the

15N

atomic basins, respectively. An additional

asymmetry is introduced by the presence of the magnetic field in the CP NMR experiment which stabilizes, due to the Zeeman effect, the spin polarization pattern determined by the molecular filter that allows the preferential passage of the spin component preferentially aligned with the field. As emphasized in reference (47), the presence of an external bias breaks time reversal symmetry, forcing a specific direction, either +k or –k, to prevail so that the chiral molecule acts as a spin filter in the direction of propagation, i.e., each optical isomer selects an electron spin polarization (determined by helicity). This leads in turn to spin accumulation around atomic centers located in the chiral path. It is precisely the pulse needed to establish the H-H condition in the CP experiment, which triggers the bond polarizationrough the chiral center, that makes the CP technique enantioselective, while direct pulse Solid State NMR, not involving CP, is not.


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Our physical model is that changes in electron spin density translate into changes in the longitudinal relaxation time T1. This transient phenomenon occurs in a fast time scale without modifying the average magnetic environment of the nuclei, consequently the two isomers should exhibit the same chemical shift, as they do.49 To get a better understanding of the deep connection between the polarization effect described by equation (8) in the local electron spin densities, and the longitudinal relaxation time of nuclear spins, we resort to a very recent publication where the longitudinal relaxation time for a magnetic ad-atom in a lattice has been determined using TimeDependent Density Functional Theory. Although the system considered in this reference differs from ours, the physical formalism is applicable to our case with minor variations. For our purposes, the main result is that the longitudinal relaxation time is directly proportional to the total electronic spin density at the position of the atom,44 which in our case translates into

(10)

𝑇1,𝐷 ∝ 𝜌𝐷 + + 𝜌𝐷 ―

where 𝜌𝐷 + + 𝜌𝐷 ― is the total accumulated spin density at the position of the atom, assuming transport occurs preferentially along the D isomer, and 𝑇1, 𝐷, is the relaxation time when the nuclei involved in CP are connected through the D isomer. Notice, however, that the magnitude of the local electron-spin density in equation (10) for the D and L isomers will not be the same, according to equation (10) this explains why 𝑇1𝐷 ≠ 𝑇1𝐿. The CP pulse interact with the bonding electrons which move through the chiral carbon center, C*, located between the H and N nuclei. The chirality of C* filters the moving electrons by their spin in accordance with its D or L chiral


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character establishing in this way a distinction between the two chiral forms, which is further enhance by the presence of the magnetic field.

We are now able to summarize our argument: We attribute the experimental observation that I(D)>I(L) to the fact that local electron-spin polarization, due to the CISS mediated electron-spin filtering, induces a transient (relative to the duration of the RF pulse) change in the longitudinal relaxation time of

1H.

This effect does not modify the chemical shift, and the Hartmann-Hahn

condition, which is essential for the transfer of nuclear polarization, is still satisfied. The change in T1 translates into a change in the relevant physical time scale for signal acquisition, which is determined by the experimental parameter TR. This ultimately yields a large intensity signal for the D isomer with respect to its L counterpart. We have been unable to measure directly the relaxation parameters for the two enantiomers due to the difficulty and cost of obtaining labeled 15N samples for the two optical isomers. However, we could perform the experiment (see supporting information) for the case of 1H/13C CP and determine the relaxation parameters for the two enantiomers of the aspartic acid, which are supposed to be identical. In fact, they differ substantially and this result renders additional support to our model. Of course, the detailed interpretation of these experiments is more involved due to the fact that are several carbon nuclei to which the polarization can be transferred from the more abundant hydrogens, but the physical conclusions are very robust. In summary, we have observed unexpected experimentally measurable differences in the CPMAS NMR signal intensities of the two optical isomers of a series of aminoacids. This conspicuous behavior cannot be attributed neither to differences in the local chiral environment, as it would be the case in techniques using either a chiral solid matrix or a chiral solvent, nor to


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polymorphism because we have made sure that the samples used are pure crystals. Lacking a more detailed theoretical analysis, that is currently under way, we conjecture that the same physics of CISS15 is also at play here. This model naturally leads to the prediction that reversing the direction of the magnetic field in the NMR equipment, something we are currently unable to do, would lead to an inversion of the here reported CP-MAS NMR intensity pattern. In this context, the importance of our finding is directly connected to the fact that charge and spin polarization can be jointly detected in an NMR experiment.

Besides providing a striking example of the importance of CISS in understanding the effect of electron spin polarization in a rather unexpected domain, CP MAS NMR, which differs from the results for liquid-state NMR,50 our finding might provide opportunities to develop other tools, along with better-adapted pulses and sequences, to unequivocally identify and quantify the ratio of diastereoisomers and enantiomers present in samples of biochemical relevance. The breakthrough in non-chemical enantioselective separation reported by Paltiel et al.12 clearly indicates the relevance of the bond polarization mechanism for different materials, including the very important case of nanomaterials and bio-nano interfaces. In fact, within the limitations imposed by the synthetic process of nanomaterials and the amount of sample needed for the CP MAS NMR experiment, we have successfully recorded the CP MAS Solid State NMR spectra of Carbon-Based Dots modified with L & D Cysteine. We are much encouraged by the fact that we do observe a measurable difference in intensity between CQD@L-Cys and CQD@D-Cys. See SI. Our use of CP MAS can actually become the ideal complement of the enantioselective separation developed by Paltiel et al., providing a non-destructive enantioselective detection technique, potentially of great importance for the pharmacological industry.12


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In a different and important direction, we are currently planning experiments to measure directly T1. One of the possibilities would be using a saturation recovery pulse sequence. There are important obstacles to carry out this experiment in our systems, but it could eventually prove very valuable in providing an independent verification of our model.

ASSOCIATED CONTENT Supporting Information 15N

and 13C {1H}-NMR spectra and graphics

AUTHOR INFORMATION Corresponding Author *Email: [email protected], [email protected], [email protected]

Author Contributions These authors contributed equally.

ACKNOWLEDGMENT Financial support was provided by the Ministerio de Economia y Competitividad (MINECO) of Spain and FEDER (Project CTQ2013-45415-P, CTQ2015-67660-P), the UPV/EHU (UFI11/22 QOSYC), and the Basque Government (GV/EJ, grant IT-324-07) and (project IT58813). The authors thank the NMR facility and SGI/IZO-SGIker UPV/EHU and the DIPC for generous allocation of computational and analytical resources. VM acknowledges the support of the Donostia International Physics Center (DIPC) during his Sabbatical Year from Arizona State University.


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48 Aragonès, A. C.; Aravena, D; Cerda, J. I.; Acís-Castillo, Z.; Li, H.; Real, J. A.; Sanz, F.; Hihath, J.; Ruiz, E.; Díez-Pérez, I. Large Conductance Switching in a Single-Molecule Device through Room Temperature Spin-Dependent Transport. Nano Lett. 2016, 16, 218-226. 49 Ibañez-Azpiroz, J.; dos Santos Dias, M.; Blügel, S.; Lounis, Samir L. Longitudinal and Transverse Spin Relaxation Times of Magnetic Single Adatoms: An ab initio Analysis. Phys. Rev. B. 2017, 96, 144410-10.


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Table of Contents/Abstract Graphic TOC 82x44mm (300 x 300 DPI)


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Chirality-Induced Electron Spin Polarization and Enantiospecific

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