ACTA PHYSICO-CHIMICA SINICA Volume 24, Issue 12, December 2008 Online English edition of the Chinese language journal Cite this article as: Acta Phys. -Chim. Sin., 2008, 24(12): 2153−2158. Received: July 7, 2008; Revised: September 30, 2008. *Corresponding author. Email: wangwqchem@pku.edu.cn; Tel: +8610-62752457. The project was supported by the Special Program for Key Basic Research of the Ministry of Science and Technology of China (2004-973-36) and the National Natural Science Foundation of China (20452002). Copyright © 2008, Chinese Chemical Society and College of Chemistry and Molecular Engineering, Peking University. Published by Elsevier BV. All rights reserved. Chinese edition available online at www.whxb.pku.edu.cn ARTICLE Dynamical Spin Chirality and Magnetoelectric Effect of α -Glycine Xinchun Shen 1 , Wenqing Wang 1, *, Yan Gong 2 , Yan Zhang 3 1 Beijing National Laboratory for Molecular Sciences, Department of Applied Chemistry, College of Chemistry and Molecular Engineering, Peking University, Beijing 100871, P. R. China; 2 School of Medicine, Tsinghua University, Beijing 100084, P. R. China; 3 School of Physics, Peking University, Beijing 100871, P. R. China Abstract: Dynamical spin chirality of α -glycine crystal at 301−302 K was investigated by DC (direct current)-magnetic susceptibility measurement at temperatures ranging from 2 to 315 K under the external magnetic fields (H=±1 T) parallel to the b axis. The α -glycine crystallizes in space group P2 1 /n with four molecules in a cell, which has centrosymmetric charge distribution. The bifurcated hydrogen bonds N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) are stacked along the b axis with different bond intensities and angles, which form anti-parallel double layers. Atomic force spectroscopy result at 303 K indicated that the surface molecular structures of α -glycine formed a regular flexuous framework in the b axis direction. The strong temperature dependence is related to the reorientation of NH 3 + group and the electron spin flip-flop of (N + H) mode. Under the opposite external magnetic field of 1 T and −1 T, the electron spins of N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) flip-flop at 301−302 K. These results suggested a mechanism of the magnetoelectric effect based on the dynamical spin chirality of (N + H), which induced the electric polarization to produce the onset of pyroelectricity of α -glycine around 304 K. Key Words: α -Glycine; Dynamical spin chirality; Magnetoelectric effect; Pyroelectricity; DC-magnetic susceptibility; Atomic force spectroscopy Most natural proteins are comprised of 19 L-amino acids and glycine, which is achiral. Up to date, it remains a puzzle in the origin of biochirality. Crystalline glycine exists in three modifications, viz. α with point group C 2h , β with point group C 2 , and γ with C 3 symmetry. α -Glycine crystals are centro- symmetric and do not exhibit piezoeffect, whereas β - and γ - glycine have polar symmetry groups, i.e., pyroelectrics and ferroelectrics [1−5] . In 1999, Chilcott et al. [6] discovered the onset of pyroelec- tricity in α -glycine around 304 K. This unusual electric be- havior was not explained readily by the conduction mecha- nism. Pyroelectricity arises only in non-symmetric materials. The onset of pyroelectricity was speculated to accompany with a change from the centrosymmetric space group P2 1 /n to a non-centrosymmetric space group. Langan et al. [7] speculated on the anomalous electrical be- havior as the possible correlation with structural phase transi- tion. Neutron diffraction measurement did not show any evi- dence of change in the space group symmetry with tempera- ture. However, the thermal expansion was found to be very anisotropic in the unit-cell parameters. The most striking fea- ture is the large increase in b axis with increasing temperature. The relative change in b is far greater than the changes in the other lattice parameters a and c. The significant structural change is the bifurcated hydrogen bonds N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) that link molecular layers stacked in the b axis direction. The glycine molecule itself possesses a relatively large dipole moment lying approximately to the c axis. The anomalous electronic properties of α -glycine most likely arise from libration-driven changes in stacking interac- Xinchun Shen et al. / Acta Physico-Chimica Sinica, 2008, 24(12): 2153 − 2158 tions between anti-ferroelectric molecular dipole layers, which can have large effects on the dielectric properties of crystals. Dawson et al. [8] studied the effect of high pressure on the crystal structure of α -glycine and also found that the variation of b-axis length reflected the increase of the stacking distance between the layers. Murli et al. [9,10] performed Raman scattering study on α-glycine crystal in the temperature range of 83−360 K and high-pressure behavior from 0.76 GPa up to 23 GPa. They found that the N + H stretch frequency (3145 cm −1 ) corre- sponding to the interlayer hydrogen bond N + (3)−H(8)···O(1) shows rather large pressure induced blue shift, 3.8 cm −1 ·GPa −1 . However, as this hydrogen bond is a bent bifurcated hydrogen bond, with N + (3)−H(8)···O(1) angle being 154°, the correla- tion of pressure induced changes in N−H···O distance is not straightforward [11] . They speculated that the shift of N + (3)− H(8)···O(1) may be owing to the dipole nature of molecule [12] . Alternatively, the intralayer hydrogen bonds N(3)−H(6)···O(1) and N(3)−H(7)···O(2) were found to stiffen at pressures above 3 GPa. To account for the above studies, the conduction mecha- nism remains unclear yet. For a crystal to be ferroelectric, it is necessary for the centers of gravity of the positive and nega- tive electric charges to be distinct and the crystal has no center of symmetry. In α-glycine, the distribution of the electric charges and the magnitude of the individual electric dipoles (NH 3 + -CO 2 − ) are sensitive to a change of temperature. On heat- ing, the individual dipoles (NH 3 + ) are oriented in one direction. The permanent electrical polarization can appear during varia- tion of the temperature to produce ferroelectricity and the crystal has undergone an anti-ferroelectric/ferroelectric transi- tion. The interplay between the magnetism and ferroelectricity is a phenomena of magnetoelectric (ME) effect in which the magnetization is induced by the electric field or the electric polarization is induced by the magnetic field [13] . Li et al. [14] found that the energy barriers for internal rotation of the NH 3 + and CO 2 − groups in glycine were 14.4 and 255 kJ·mol −1 , re- spectively. The internal rotation barriers indicate that the CO 2 − group is no rotation in agreement with the solid structure of double layers of molecule held together by hydrogen bonds. The dynamics of NH 3 + group provides most of the contribu- tion [15] . In this article, we study the ME effect and spin flip-flop transition of N + (3)−H(8) mode in NH 3 + group of α-glycine by DC-magnetic susceptibility measurement from 2 to 315 K under the external magnetic field strength of ±1 T parallel to the b axis. 1 1 Experimental 1.1 Sample recrystallization and characterization α-Glycine (Sigma Corporation, minimum 99% TLC) was recrystallized from thrice distilled water by slow evaporation at 277 K. Optically clear seed crystals were obtained after a period of 7 days [16,17] . The obtained crystals were thoroughly dried under vacuum and stored under moisture-free condition. Powder XRD pattern of α-glycine was performed using X-ray diffractometer (Rigaku D/Max-3B, Japan) with Cu K α radia- tion of λ=0.15406 nm. The sample was scanned in the 2 θ val- ues ranging from 10° to 50° at a rate of 4 (°)·min −1 . The XRD result was shown to be the monoclinic α-polymorph only, without characteristic peak of the γ-glycine [18,19] , Fig.1. 1.2 N−H ··· O bond length, angle, and direction The unit cell parameters of α -glycine were measured by X-ray diffraction as follows: a=0.5107(2) nm, b=1.2040(2) nm, c=0.5460(2) nm, β =111.82(2)° [20] . α -Glycine is the most stable modification at ambient conditions, existing as zwit- terionic form (NH 3 + CH 2 CO 2 − ) in monoclinic structure (space group symmetry P2 1 /n). The unit cell contains four symmetri- cally related molecules, which are hydrogen bonded pairwise, A−B and C−D, around the centers of symmetry [21] . The mo- lecular pairs are linked together by means of a two-dimen- sional network of the hydrogen bonds forming an anti-parallel double layer of molecules perpendicular to the monoclinic b axis, with the intra-layer linkage of two relatively short hy- drogen bonds N(3)−H(6)···O(1) (length of 0.2771 nm) with H(6)···O(1) (length of 0.1729 nm) and N(3)−H(7)···O(2) (length of 0.2847 nm) with H(7)···O(2) (length of 0.1820 nm). In sub-layer, the molecules are related by simple translation. A two-fold screw axis perpendicular to the layer (i.e., parallel to the b axis) transforms one (A−B) of the two molecular pairs in a unit cell to the other one (C−D) belonging to the adjacent double layer. These layers are connected by interlayer longer bifurcated hydrogen bonds N + (3)−H(8)···O(1) (length of 0.2950 nm) with H(8)···O(1) (length of 0.2362 nm) and bond angle of 154.26° and N + (3)−H(8)···O(2) (length of 0.3065 nm) with H(8)···O(2) (length of 0.2101 nm) and bond angle 114.91° to form anti-parallel double layers. The different dou- ble layers are joined by weak C(5)−H(9)···O bonds with H(9)···O(1) (length of 0.2446 nm) and H(9)···O(2) (length of 0.2378 nm) hydrogen bonds. Neutron diffraction has shown the structure of α-glycine with atomic numbering (Fig.2(a)). The direction of N(3)−H(6)···O, N(3)−H(7)···O, and N + (3)− Fig.1 Powde r XRD pattern of α -glycine at room tempe r ature Xinchun Shen et al. / Acta Physico-Chimica Sinica, 2008, 24(12): 2153 − 2158 H(8)···O bonds was viewed down the c axis (Fig.2(b)). The interlayer hydrogen bonds N + (3)−H(8)···O(1) and N + (3)− H(8)···O(2) formed anti-parallel double layers as shown in Fig.2(c) [7,22,23] The DC-magnetic susceptibility was measured on α-glycine using SQUID magnetometer ranging from 2 to 315 K [24] . A transparent small crystal of α-glycine was selected as seed under triple recrystallization for obtaining a large crystal. The crystal face and b-axis were ascertained by XRD diffraction. The quantum design SQUID XL-5 magnetometer was used to measure the DC-magnetic susceptibility of the α-glycine crys- tals (0.08357 g) from 2 to 315 K. The external magnetic field was implied to provide a certain preferred atomic direction of electron spin in the molecule. Measurements were taken by the applied magnetic field strength (H=100 Oe, ±10 kOe) par- allel to the b axis. The magnetic moments (M) were measured by scanning three times and the mass susceptibility values were calculated from χ ρ =M/(H×m), where, M is the magnetic moment, H is the magnetic field strength, and m is the sample mass. 2 2 Results and discussion 2.1 DC-magnetic susceptibility of α-glycine α -Glycine molecules in crystals exist as parallel chains of hydrogen bonded zwitterions (NH 3 + −CO 2 − ) that form magnetic dipoles. The quasi-metallic hydrogen N + (3)−H(8) has a mag- netic moment μ B ( μ B =1 Bohr magneton=0.927×10 −23 A·m 2 ), which runs along the b axis. The orientational potential energy is − μ B B when the dipole is parallel to the field, and it is + μ B B when the dipole is anti-parallel to the field. So the energy that must be supplied to turn the dipole is 2 μ B B. B=1 T=1 J·A −1 ·m −2 2 μ B B=2×0.927×10 −23 ×1≈1.85×10 −23 J=1.16×10 −4 eV Although this energy is small, the dipole moment cannot turn unless the energy is supplied. At low magnetic field Fig.2 (a) Structure of α -glycine with the atomic numbering (bond length in nm); (b) hydrogen bonded double layers of α -glycine (NH 3 + CH 2 CO 2 − ) viewed down the c axis, N + (3)−H(8) along the b axis, N(3)−H(6) along the c axis, N(3)−H(7) approximately along the a axis, α = γ =90°, β =111.697°; (c) hydrogen bonded double layers of α -glycine (NH 3 + CH 2 CO 2 − ) viewed down the a axis, the interlayer hy- drogen bonds N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) formed anti-parallel double layers Xinchun Shen et al. / Acta Physico-Chimica Sinica, 2008, 24(12): 2153 − 2158 strength of 100 Oe with H//b axis, there is no peak appearing in Fig.3. An external magnetic field strength was applied with mag- nitude H=1 T=10 kOe=1 J·A −1 ·m −2 . The potential energy of the field is required to turn the magnetic dipole anti-parallel to the field. In the case of H=±10 kOe, the spin-flop peaks of α -glycine appeared at 301−302 K (Figs.4a, 5a). When T=302 K, kT=2.6×10 −2 eV μ B B/kT=5.8×10 −5 eV/2.6×10 −2 eV≈2.2×10 −3 The assumption μ B B<<kT is valid at ordinary temperature and fields, μ B B being about 0.2% of kT. We have seen that μ B B≈10 −4 eV at H=10 kOe, which is a very small energy shift compared to the Fermi energy, ε F ≈1 eV, hence, the number of electrons with parallel moments is only slightly larger than those with anti-parallel moments. Because the randomizing thermal effect dominated over μ B B, the mass susceptibility should have a small value. Conversely, if the dipole is origi- nally aligned anti-parallel to the field, it cannot turn to align itself parallel to the field unless it can release the same amount of energy [25] . Since N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) are bifur- cated hydrogen bonds connected the interlayer of α -glycine. The corresponding H(8)···O(1) distance of 0.2362 nm is longer than H(8)···O(2) of 0.2101 nm. The dipole of N + (3)− H(8)···O(1) is parallel to the field. A spin-flop peak of N + (3)−H(8)···O(1) was observed at 301−302 K under H=10 kOe (Fig.4a). The N + (3)−H(8)···O(2) was anti-parallel to the field, therefore, the spin-flop peak of N + (3)−H(8)···O(2) was observed at H=−10 kOe (Fig.5a). The spin flip-flop peaks in the plot of d χ ρ /dT versus T at 301−302 K (Figs.4b, 5b) indi- cate the dynamical spin chirality and spin anisotropy along the b axis. It can be concluded that the dynamical spin chirality of N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) of α -glycine is a property of the ensemble rather than a molecular characteris- tic [26] . 2 2.2 Surface structure of α -glycine crystal by atomic force microscopy Nanoscope IIIa produced by Digital Instruments Company was used for direct observation of the surface structure of α -glycine crystal at 303 K. The image was obtained by re- cording the Z coordinate of the tip as it scans the surface in contact mode with deflection set point from −2 to −3 V, scan rate 20.35 Hz, and scan size 4.22 nm [27] . The surface molecu- Fig.3 Temperature-dependent susceptibility χ ρ of α -glycine Fig.4 (a) Temperature-dependent susceptibility χ ρ and (b) d χ ρ /dT versus T of α -glycine m=0.08357 g; warming; H=10 kOe, H//b axis Fig.5 (a) Temperature-dependent susceptibility χ ρ and (b) d χ ρ /dT versus T of α -glycine m=0.08357g; warming; H=−10 kOe, H//b axis Xinchun Shen et al. / Acta Physico-Chimica Sinica, 2008, 24(12): 2153 − 2158 lar structures of α -glycine were shown in both the lateral and longitudinal dimensions in Fig.6. In α -glycine, the lateral hy- drogen bonds of N(3)−H(6)···O and N(3)−H(7)···O are stronger than the hydrogen bonds of N + (3)−H(8)···O. These chains are packed together by the lateral hydrogen bonds, forming a three-dimensional network of the hydrogen bonds, which provides the evidence of the ferroelectricity in α -glycine crystal. The dominating surface feature of the intermolecular pack- ing is bifurcated hydrogen bonds N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2), which link the molecules into right- and left-handed helices around the threefold screw axes. It helps to solve the puzzle of how glycine can play an important role in the critical folding of functional protein occurring near room temperature [28] . 3 3 Conclusions Temperature-dependent measurements of DC-magnetic susceptibility of single-crystal α -glycine demonstrate the spin flip-flop transition of N + (3)−H(8)···O(1) and N + (3)−H(8)···O(2) hydrogen bonds. The crystals undergo an anti-ferroelectric/ ferroelectric transition at 301−302 K. Proton seems like a ba- ton and transfers along the intra-layer hydrogen bond chains below 301 K. Drebushchak et al. [29] proposed that NH 3 + tails of zwitterions stick out of the layers uniformly either up (↑) or down (↓) bonding with oxygen in a neighboring layer, which are paired (↑↓↑↓↑↓) in α-glycine and unpaired (↓↓↓↓↓↓) in β -glycine. Katsura et al. [13] proposed the ME effect based on the spin current in terms of a microscopic electronic model for noncol- linear magnets. The spin current is induced between the two spins with generic nonparallel configurations [30] . We propose a mechanism of the ME effect based on the intrinsic dynamical spin chirality, which causes charge separation in glycine and a net spontaneous polarization. Current generated by small changes in temperature below the critical temperature of py- roelectric effect causes a dramatic increase in conductance. 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In α-glycine, the distribution of the electric charges and the magnitude