Achiral Metastable Crystals of Sodium Chlorate Forming Prior to Chiral

Article pubs.acs.org/crystal

Achiral Metastable Crystals of Sodium Chlorate Forming Prior to Chiral Crystals in Solution Growth Hiromasa Niinomi,*,†,§ Tomoya Yamazaki,† Shunta Harada,§ Toru Ujihara,§ Hitoshi Miura,† Yuki Kimura,*,† Takahiro Kuribayashi,† Makio Uwaha,‡ and Katsuo Tsukamoto† †

Department of Earth and Planetary Materials Science, Graduate School of Science, Tohoku University, Aramaki, Aoba, Sendai, 980-8578, Japan ‡ Department of Physics, Graduate School of Science, Nagoya University, Japan, Furo-cho, Chikusa, Nagoya 464-860, Japan § Department of Materials Science and Engineering, Nagoya University, Furo-cho, Chikusa, Nagoya 464-8603, Japan ABSTRACT: Chiral symmetry breaking in NaClO3 crystallization from an aqueous solution with perturbations has been of great interest. To understand the mechanism, several models focusing on the early stage of the crystallization have been proposed. However, they are ambiguous because the early stage has been barely explored directly. Here, we investigate the early stages of the crystallization process driven by droplet evaporation using a combination of direct in situ microscopic observations and cryogenic single-crystal XRD experiments. We demonstrate that an achiral crystal having P21/a symmetry, which is newly discovered for a solution growth, first appears in the droplet and then transforms into the chiral crystals. Additionally, determination of the lattice constants by XRD experiments (a = 8.42 Å, b = 5.26 Å, c = 6.70 Å, β = 109.71°) revealed that the achiral phase should be identical to Phase III (a = 8.78 Å, b = 5.17 Å, c = 6.83 Å, β = 110°), which is a high-temperature phase from a melt growth of NaClO3. We advocate further assessment of the achiral crystal and a new pathway for the formation of chiral crystals via crystalline phase transition from achiral Phase III.

1. INTRODUCTION Chiral asymmetry is ubiquitous in nature; it has been observed across various levels from elementary particle physics to the morphology of winding plants. One example is homochirality where living organisms preferentially select one type from two mirror isomers (enantiomorphs), e.g., L-type amino acids and D-type sugars, as a constituent component. However, the process that produces the asymmetric chiral state is not yet fully understood. Therefore, the transition from the chiral symmetric state, also known as the achiral state, to the chiral state is of general interest. Recently, reports on chiral symmetry breaking in sodium chlorate (NaClO3) crystallization from aqueous solution are arousing great interest,1−7 because these are one of a few examples of the transition achieved by only abiotic physical processes and offer the possibility of an analogical understanding of homochirality. NaClO3 molecules are achiral; they form chiral crystals having cubic symmetry with space group P213 during crystallization.8 Because the two enantiomorphs have equal thermodynamic stability, when NaClO3 is crystallized from a static solution by solvent evaporation, equal proportions of both the enantiomorphs are yielded in each crystallization.9 However, Kondepudi and co-workers found that only one type from the two enantiomorphs crystallizes if the solution is stirred during crystallization.1 It is surprising that the resulting chiral asymmetry contradicts the thermodynamic equality between both the enantiomorphs. Moreover, Viedma showed that a completely asymmetric state can be achieved by grinding a 50:50 racemic mixture of NaClO3 crystals in a saturated solution.7 These two experiments are sometimes © XXXX American Chemical Society

distinguished by their degree of deviation from the equilibrium state.10 Whereas the transition from the achiral state to the chiral state in Kondepudi’s experiment should occur under supersaturation, that in Viedma’s experiment should occur under near equilibrium because the crystals are already present in the solution in the initial state. Thus, in this study, we differentiate these two processes as chiral symmetry breaking via nucleation and chiral symmetry breaking via recrystallization at equilibrium, respectively. Several crystallization experiments of chiral symmetry breaking via nucleation have been carried out in addition to Kondepudi’s experiment.1−5,11−16 Generally, these crystallizations are interpreted using kinetic theory involving a secondary nucleation process.11−20 The single crystal that initially appeared because of primary nucleation, called the “Eve” crystal, produces many secondary nuclei when it collides with the stir bar or is exposed to shear flow. Because the secondary nuclei possess the same handedness as the “Eve” crystal, the handedness of “Eve” is amplified. In contrast, the opposite handedness is suppressed by the reduction in the solution concentration. Because this secondary nucleation model qualitatively explains chiral crystallization via nucleation events, it builds a certain level of consensus (except for the process of chiral symmetry breaking via recrystallization at equilibrium solution21−23). Received: April 23, 2013 Revised: October 7, 2013

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This model should be inapplicable to some chiral crystallization experiments by homogeneous nucleation from a supersaturated solution.2−4 For instance, Viedma showed that stirring a highly supersaturated solution, where primary nucleation should occur at a high rate (σ ∼ 54%, 60 °C of supercooling), results in a chiral asymmetric state.2 This result contradicts the secondary nucleation model, because the model assumes the existence of a single “Eve” crystal, and yet such a high rate of primary nucleation should significantly decrease the possibility that the primary nucleation functions as an “Eve” crystal. Thus, chiral crystallization from a highly supersaturated solution is often interpreted by deracemization during the primary nucleation event,2 or even before it, in a period of a precritical cluster.3,4 Here, we believe that an in situ investigation of chiral crystallization from a highly supersaturated solution will explain chiral symmetry breaking via nucleation, in contrast to most of the previous studies that relied on measurements of the resulting crystals. To confirm the early stage crystallization process involving nucleation, we carried out an in situ direct microscopic observation of crystallization driven by droplet evaporation and demonstrate a new pathway to chiral crystal formation. Figure 1. Micrographs of NaClO3 crystals captured by in situ observation using polarized-light microscopy. (a−c) Time-lapse micrographs of NaClO3 crystallization process driven by evaporation of solvent, under the crossed Nicol prism. (d) Crystallization process observed under the noncrossed Nicol prism. (e) Micrograph showing the perfect parallelogram shape of noncubic crystal. (f) Micrograph showing the perfect square shape of cubic crystal. Micrographs (e) and (f) were taken from separate observations.

2. CRYSTALLIZATION AND OBSERVATION All experiments were performed starting with a saturated solution prepared using the following procedure. An aqueous solution of NaClO3 was prepared by dissolving 110 g of NaClO3 (Analytical grade, Wako Pure Chemical Industries, Ltd., Osaka, Japan) in distilled water (100 mL) at room temperature (22 °C). The resulting solution was heated to 30 °C under stirring with a magnetic hot plate stirrer and then left for a week at room temperature to precipitate the excess solute and thus to equilibrate the solution. The crystallization experiments were performed by pipetting a drop (6 μL) of the supernatant saturated solution on a glass slide. The glass slide was placed on a Peltier stage with the temperature set at 22 °C. Then, the solution was allowed to crystallize (forming NaClO3 crystals) by evaporation. After approximately 10 min, crystals appeared in the droplet because of nucleation from a supersaturated solution. We observed in situ the process of this crystallization with a polarized-light microscope [BX51-P (custom-made); Olympus Corp., Tokyo, Japan] equipped with a video recording system.

crystal appearing first is noncubic. In addition, the dark crystal formed after the noncubic crystal is a cubic chiral crystal. Figure 1e shows a noncubic crystal observed in a similar experiment, with the perfect shape of a parallelogram (Figure 1e) unlike that of the chiral cubic crystal (Figure 1f). This observation demonstrated that a noncubic crystal nucleates prior to the formation of chiral cubic crystals; it transforms into the cubic crystal, indicating that the noncubic crystal is less stable than the chiral cubic crystal. Thus, the noncubic crystal should be a metastable phase. This observation raises a question: whether this transformation is a transition from an achiral state to a chiral state. To answer this question, it is necessary to determine whether the crystal is chiral. Therefore, we performed an X-ray structural analysis on the metastable crystal.

3. RESULTS OF IN SITU OBSERVATION Figure 1a−d shows time-lapse images of the in situ polarizedlight microscopic observation. Figure 1a shows an image taken just after the nucleation of NaClO3. Nucleation started from the droplet fringe 5−10 min after pipetting the droplet on the glass slide. The crystal that first appeared in the droplet exhibited a bright color under the crossed Nicol prism (when two polarizers are orthogonally oriented). The needle-shaped bright crystal grew toward the center of the droplet. After a few seconds of growth, the bright color started to become extinct from the fringe (Figure 1b). Then, the extinct region gradually spread (Figure 1c) along with the bright crystal. Eventually, the entire bright region became extinct within a few minutes. Noncrossed Nicol observation showed that the extinct regions comprised the crystal (Figure 1d). Because all crystals except for the cubic ones exhibit bright color under crossed Nicol owing to birefringence, the bright

4. CRYOGENIC SINGLE-CRYSTAL X-RAY STRUCTURAL ANALYSIS It was difficult to conduct a typical X-ray diffraction experiment because the metastable crystals are extremely unstable. To overcome this problem, we preserved the metastable crystal inside the droplet by flash-freezing with liquid nitrogen at −195.8 °C. We constructed a cryogenic single-crystal X-ray structure-analysis system for the frozen droplet. A similar technique has been used in the analysis of protein crystals.24 Figure 2 shows a schematic overview of the experimental setup that consists of three systems: (1) the low-temperature instrument; (2) the X-ray diffraction system; and (3) the polarized-light microscopy system. A metastable single crystal was produced upon a glass sheet mounted on a sample holder of the X-ray diffraction system by B

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systematic absence rules were observed in the analytic data set of the X-ray diffraction intensities: h = 2n + 1 in the h0l series, k = 2n + 1 in the 0k0 series, and h = 2n + 1in the h00 series. These results indicate that the space group of the monoclinic phase is P21/a. Figure 3 shows a photograph of the X-ray

Figure 2. Schematic experimental setup for cryogenic single-crystal Xray diffraction: (1) Cryostat system using Cryostream (Oxford Cryosystems Inc.), indicated by dotted−dashed blue arrow; (2) Xray diffraction system, indicated by solid red arrow; and (3) polarizedlight microscopy system, indicated by dotted green arrow.

means of the droplet-evaporation method described above. When the single crystal had grown to 100−300 μm, the solution surrounding the crystal was removed using a wipe, and the crystal was covered with glycerin that acts as a cryoprotectant. The glycerin droplet containing the crystal was instantaneously frozen using liquid nitrogen. The frozen sample was then installed into the cryogenic single-crystal X-ray structure-analysis system. A full X-ray diffraction analysis requires the specimen to be kept as-is throughout the measurement, which means that the droplet should be kept frozen for several hours. This requirement was achieved by the continuous blowing of lowtemperature nitrogen gas generated by a Cryostream system (Oxford Cryosystems, Oxford, U.K.). The temperature surrounding the droplet was maintained at −27(±1) °C, which was measured using a K-type thermocouple, throughout the measurement. Diffraction data were collected from the sample with an approximately 100 × 80 × 10 μm size by the oscillation method using R-AXIS IV++ (Rigaku Corp., Tokyo, Japan) with an imaging plate. All the oscillation images were processed using the CrystalClear software (Rigaku) to determine the crystallographic parameters. The experimental conditions for the X-ray diffraction measurements are listed in Table 1.

Figure 3. X-ray diffraction image at an oscillation range of 4°. The halo is caused by frozen glycerin (amorphous), and diffraction spots arise from the metastable phase (crystal). Arrowed spots indicate h0l series. Spots for h = 2n + 1 are absent from the series, indicating a space group of P21/a.

oscillation image with a 4° oscillation range, showing a systematic absence rule of h = 2n + 1 in h0l. One should note that crystals with space group P21/a are achiral because this space group contains an inversion center as the symmetrical element. Therefore, the noncubic metastable crystal is achiral.

6. PHASE DETERMINATION OF NONCUBIC CRYSTAL It has been previously reported that a monoclinic phase named Phase III occurs in the NaClO3 melt growth.25 Phase III appears as a high-temperature phase at 262−237 °C when the melt is cooled down; it transforms into a cubic phase when the temperature falls below 237 °C.26 The structure of Phase III has been previously characterized as follows: space group, P21/a; lattice parameters, a = 8.78(5) Å, b = 5.17(5) Å, c = 6.83(5) Å, and β = 110(1)°.27 These lattice constants are very close to those of the metastable phase that we identified in the current study (Table 2). This implies that the metastable phase should be identical to Phase III. However, the differences in the values of the lattice constants between Phase III and the metastable phase cannot be explained exclusively in terms of statistical

Table 1. Experimental Conditions for X-ray Diffraction Measurements analytical method

oscillation conditions

radiation wavelength (Å) X-ray output (kV, mA) collimator size (μm) crystal-to-imaging plate distance (mm) oscillation range (deg) oscillation step range per image (deg) exposure time (s)

Mo Kα 0.7107 50, 20 300 120 360 2 300

Table 2. Comparison of Lattice Constants of Metastable Crystal Formed by Solution Growth with Those of Phase III, a High-Temperature Phase Formed by Melt Growtha

5. RESULTS OF X-RAY DIFFRACTION EXPERIMENT The cryogenic single-crystal X-ray diffraction experiments successfully provided 4314 reflections. Through an analysis of the distributions of the diffraction spots, the lattice parameters of the metastable crystal were determined to be a = 8.42(2) Å, b = 5.260(7) Å, c = 6.70(1) Å, β = 109.71(1)°, and V = 279.8(8) Å3, where V is the volume of the unit cell. These results indicate a monoclinic symmetry. In addition, three

phase

metastable phase (this study)

metastable phase (calculated values)

crystal system space group a (Å) b (Å) c (Å) β (deg) temp (°C) unit cell volume (Å3)

monoclinic P21/a 8.42(2) 5.260(7) 6.70(1) 109.71(1) −27 279.8(8)

monoclinic P21/a 8.54(2) 5.34(1) 6.80(1)

a

C

250 292.2(8)

Phase III28 monoclinic P21/a 8.78(5) 5.17(5) 6.83(5) 110(1) 237−262 291(4)

Calculated values are values based on α(T) and β(T). dx.doi.org/10.1021/cg401324f | Cryst. Growth Des. XXXX, XXX, XXX−XXX

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equilibrium such as the so-called Viedma deracemization.7,10 The reason why the crystallization from a highly supersaturated solution is uninterpretable is the absence of the “Eve” crystal caused by the high nucleation rate originating from high supersaturation. However, this is the case when the achiral phase was not taken into consideration. Here, we discuss the possible contribution of the achiral metastable phase on the chiral symmetry breaking from a highly supersaturated solution. Generally, the solubility of a metastable phase is higher than that of a stable phase, meaning that the appearance of a metastable phase requires relatively high supersaturation. Therefore, the crystallizations from a highly supersaturated solution mentioned above are suitable for the formation of the achiral metastable phase. The nucleation and growth of the metastable crystals decrease the supersaturation of the mother solution while consuming the solute in the solution. If the rates of the growth and the nucleation of the metastable phase are sufficiently high relative to the induction time for the nucleation of the chiral phase, the supersaturation in which the nucleation of the chiral crystals occurs should become lower than the initial supersaturation because the supersaturation decreases prior to the nucleation of the chiral phase. Consequently, the nucleation rate of chiral crystals becomes lower than that expected from the initial supersaturation. Assuming that formation of the achiral crystals decreases the nucleation rate of chiral crystals such that the secondary nucleation model becomes applicable, the model can explain even the chiral symmetry breaking from a highly supersaturated solution. Additionally, since the metastable phase is achiral, the metastable phase does not have a chiral influence on the nucleation of chiral crystals. In conclusion, the role of the achiral metastable phase is possibly the reduction of the initial supersaturation. In other words, the achiral metastable phase acts as a buffer that suppresses the direct nucleation of chiral phase at extremely high supersaturation, which limits the application of the secondary nucleation model to the chiral symmetry breaking from a highly supersaturated solution. Although the achiral metastable phase may not provide a new insight for the Viedma deracemization, it demands reconsideration of the process of the chiral symmetry breaking via nucleation. To discuss the contribution of the metastable phase on chiral symmetry breaking more precisely, it would be necessary to assess the solubility of the phase and to observe the phase transformation from the achiral crystal to chiral crystal in detail. In the future, we will provide the further assessment of the achiral metastable phase.

error; they might be caused by the difference in temperature. The crystallographic information for the metastable phase was recorded at −27 °C, whereas that for Phase III was obtained at 237−262 °C. By taking thermal expansion into consideration, we can estimate the volume of the unit cell of the metastable phase at 237−262 °C and compare its value to that of Phase III. Here, for simplicity, we estimated the value of the metastable phase at 250 °C (V250°C) from the following equation ⎛ V250°C = V −27°C⎜1 + ⎝

∫−27

250

⎞ β (T ) d T ⎟ ⎠

⎛ = V −27°C⎜1 + ⎝

∫−27

250

⎞ 3α(T ) dT ⎟ ⎠

(1)

where T is the temperature (°C), β(T) is the volume thermal expansion coefficient, α(T) is the linear thermal expansion coefficient, and V−27°C is the volume of the unit cell of the metastable phase at −27 °C. Assuming that (1) the thermal expansion coefficient of the cubic phase is equal to that of the metastable phase and (2) the unit cell expands isotropically, V250°C was calculated to be 292.2(8) Å3 by substituting the value of the linear thermal expansion coefficient of the cubic phase from the previous report.28 These calculated values are equal, within the experimental error, to the volume of the unit cell of Phase III [291(4) Å3].28 Therefore, we concluded that the metastable phase of crystallization from solution is identical to Phase III. Because the noncubic metastable phase is achiral, the crystalline phase transformation observed in the current study is a transition from the achiral state to the chiral state, which means that the chirality of the NaClO3 crystal emerges during the transition (Figure 4).

8. CONCLUSION We examined the initial stages of NaClO3 crystallization from a highly supersaturated aqueous solution in situ using polarizedlight microscopy. We for the first time observed that an unknown crystalline metastable phase appeared prior to the nucleation of chiral crystals with cubic symmetry. The crystal system of the metastable phase determined by cryogenic singlecrystal X-ray diffraction experiments is monoclinic with lattice parameters a = 8.42(2) Å, b = 5.260(7) Å, c = 6.70(1) Å, β = 109.71(1)°, and V = 279.8(8) Å3 at −27 °C. The space group is P21/a, which is chirally symmetric. This crystallographic information suggests that the metastable phase is identical to Phase III, which is known as a high-temperature phase observed during the NaClO 3 melt growth. When the NaClO 3 crystallization process follows a pathway through the metastable

Figure 4. New pathway for the formation of chiral NaClO3 crystals. Chiral cubic crystals are formed after nucleation of achiral Phase III.

7. ROLE OF METASTABLE PHASE IN CHIRAL SYMMETRY BREAKING Most of the chiral symmetry breaking via nucleation can be interpreted by the secondary nucleation model.1,5,13−15 However, some of them cannot be interpreted by this model.2−4 The uninterpretable crystallizations are exclusively from a highly supersaturated solution, as seen in Viedma’s crystallization experiment in 2004, where the initial supersaturation is ∼54% (ref 2). Note that this experiment is different from chiral symmetry breaking via recrystallization at D

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(26) Brooker, M. H.; Shapter, J. G.; Drover, K. J. Phys: Condens. Matter 1990, 2, 2259−2272. (27) Meyer, P.; Gasperin, M. Bull. Soc. Fr. Mineral. Cristallogr. 1973, 96, 18−20. (28) Deshpande, V. T.; Mudholker, V. M. Acta Crystallogr. 1960, 13, 483−486.

phase, the chirality of NaClO3 crystals appears during the phase transition from the achiral metastable phase to the chiral cubic phase. Taking the achiral metastable phase into consideration, the secondary nucleation model might be applicable even to chiral symmetry breaking via nucleation from a highly supersaturated solution, which has not been interpretable by the secondary nucleation model.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected]. Tel & Fax: +81-22-795-6661. *E-mail: [email protected]. Tel & Fax: +81-22-7955903. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS

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REFERENCES

We thank J. M. Garcia-Ruiz from the University of Granada, Spain, for helpful comments. We are grateful for the support by Grant-in-Aid for Challenging Exploratory Research. No. 23656005 from the Scientific Research of the Ministry of Education, Science, and Culture of Japan.

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dx.doi.org/10.1021/cg401324f | Cryst. Growth Des. XXXX, XXX, XXX−XXX