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ISSN: 2052-5206

Effect of pressure on the crystal structure of α-glycylglycine to 4.7 GPa; application of Hirshfeld surfaces to analyse contacts on increasing pressure

aSchool of Chemistry and Centre for Science at Extreme Conditions, The University of Edinburgh, King's Buildings, West Mains Road, Edinburgh EH9 3JJ, Scotland, and bInstitute for Cell and Molecular Biology and Centre for Science at Extreme Conditions, The University of Edinburgh, King's Buildings, West Mains Road, Edinburgh EH9 3JR, Scotland
*Correspondence e-mail: s.moggach@ed.ac.uk

(Received 14 November 2005; accepted 15 December 2005)

The crystal structure of α-glycylglycine (α-GLYGLY) has been determined at room temperature at pressures between 1.4 and 4.7 GPa. The structure can be considered to consist of layers. The arrangement of molecules within each layer resembles the antiparallel β-sheet motif observed in proteins, except that in α-GLYGLY the motif is constructed through NH⋯O hydrogen bonds rather than covalent amide links. Compression of α-GLYGLY proceeds via the reduction in void sizes. Voids close in such a way as to decrease the distances of stabilizing interactions such as hydrogen bonds and dipolar contacts. The largest reductions in interaction distances tend to occur for those contacts which are longest at ambient pressure. These longer interactions are formed between the β-sheet-like layers, and the largest component of the strain tensor lies in the same direction. The N⋯O distance in one NH⋯O hydrogen bond measures 2.624 (9) Å at 4.7 GPa. This is very short for this kind of interaction and the crystal begins to break up above 5.4 GPa, presumably as the result of a phase transition. The changes that occur have been analysed using Hirshfeld surfaces. Changes in the appearance of these surfaces enable rapid assessment of the structural changes that occur on compression.

1. Introduction

Glycylglycine (GLYGLY) is the simplest dipeptide. It is composed of two glycine residues and in the solid state it exists in three different polymorphic forms. These polymorphs were designated α, β and γ by Bernal (1931[Bernal, J. D. (1931). Z. Kristallogr. Kristallgeom. Kristallphys. Kristallchem. 78, 363-369.]). A preliminary investigation made by Bernal (1931[Bernal, J. D. (1931). Z. Kristallogr. Kristallgeom. Kristallphys. Kristallchem. 78, 363-369.]) found that all three polymorphs could be grown simultaneously from the same mother liquor by slow evaporation from concentrated solutions in n-propyl alcohol and water. It was found in this study that the plate-like α form predominates, with numerous recrystallizations required to obtain crystals of the β and γ polymorphs. No report of the γ polymorph has appeared since Bernal's publication in 1931, while no report of the β polymorph has appeared since Hughes & Moore (1949[Hughes, E. W. & Moore, W. J. (1949). J. Am. Chem. Soc. 71, 2618-2623.]). The α-GLYGLY polymorph, however, has been studied more recently by both neutron and X-ray diffraction; the most recent structure was reported by Kvick et al. (1977[Kvick, Å., Karaghouli, A. R. & Koetzle, T. F. (1977). Acta Cryst. B33, 3796-3801.]) in a deformation electron-density study.

Early work on the compressibility of hydrogen-bonded solids was carried out by Katrusiak and co-workers (for example, Katrusiak & Nelmes, 1986[Katrusiak, A. & Nelmes, R. J. (1986). J. Phys. C Solid State Phys. 19, L765-L772.]; Katrusiak, 1990a[Katrusiak, A. (1990a). High Press. Res. 4, 496-498.],b[Katrusiak, A. (1990b). Acta Cryst. B46, 246-256.], 2004[Katrusiak, A. (2004). High-Pressure Crystallography, edited by A. Katrusiak & P. F. McMillan, pp. 513-520. Dordrecht: Kluwer Academic Publishers.]). The responses of the crystal structures of several amino acids to high hydrostatic pressure have been described recently (Dawson et al., 2005[Dawson, A., Allan, D. R., Belmonte, S. A., Clark, S. J., David,W. I. F., McGregor, P. A., Parsons, S., Pulham, C. R. & Sawyer, L. (2005). Cryst. Growth Des. 5, 1415-1427.]; Moggach, Allan, Lozano-Casal & Parsons, 2005[Moggach, S. A., Allan, D. R., Lozano-Casal, P. & Parsons, S. (2005). J. Synchrotron Rad. 12, 590-597.]; Moggach, Allan, Morrison, Parsons & Sawyer, 2005[Moggach, S. A., Allan, D. R., Morrison, C. A., Parsons, S. & Sawyer, L. (2005). Acta Cryst. B61, 58-68.]; Moggach, Allan, Parsons, Sawyer & Warren, 2005[Moggach, S. A., Allan, D. R., Parsons, S., Sawyer, L. & Warren, J. E. (2005). J. Synchrotron Rad. 12, 598-607.]; Boldyreva et al., 2004[Boldyreva, E. V., Ivashevskaya, S. N., Sowa, H., Ahsbahs, H. & Weber, H.-P. (2004). Dokl. Phys. Chem. 396, 111-114.], 2005[Boldyreva, E. V., Kolesnik, E. N., Drebushchak, T. N., Ahsbahs, H., Beukes, J. A. & Weber, H.-P. (2005). Z. Kristallogr. 220, 58-65.]). The behaviour of the distances characterizing intermolecular interactions was rationalized by studying the way in which interstitial voids deform under pressure. It was notable that compression continued until the minimum distance, as observed for a specific interaction (e.g. the N⋯O distance in an N—H⋯O hydrogen bond) under ambient pressure, had been reached (i.e. super-short hydrogen bonds are apparently not formed up to ca 10 GPa) and it was at this point that a phase transition occurred. However, the extent to which our observations have any generality still needs to be established and we now extend this work to the α-polymorph of GLYGLY. Although some studies have appeared recently on the behaviour of proteins under non-ambient pressure conditions, for example on cubic Cowpea mosaic virus crystals (Girard et al., 2005[Girard, E., Kahn, R., Mezouar, M., Dhaussy, A.-C., Lin, T., Johnson, J. E. & Fourme, R. (2005). Biophys. J. 88, 3562-3571.]), this is the first study in which the crystal structure of a dipeptide has been examined at high pressure.1

[Scheme 1]

2. Experimental

2.1. Crystal growth and high-pressure crystallography

Crystals of α-GLYGLY were grown by slow diffusion of ethanol into a concentrated aqueous solution of GLYGLY (99%) obtained from Sigma (catalogue number G, 1002). One block-shaped crystal of dimensions 0.1 × 0.2 × 0.2 mm3 was selected and loaded into a Merrill–Bassett diamond–anvil cell (Merrill & Bassett, 1974[Merrill, L. & Bassett, W. A. (1974). Rev. Sci. Instrum. 45, 290-294.]). The cell had a half-opening angle of 40° and was equipped with 600 µm culets and a tungsten gasket. A 4:1 mixture of methanol and ethanol was used as a hydrostatic medium. A small ruby chip was also loaded into the cell as the pressure calibrant, with the ruby fluorescence method used to measure the pressure (Piermarini et al., 1975[Piermarini, G. J., Block, S., Barnett, J. D. & Forman, R. A. (1975). J. Appl. Phys. 46, 2774-2780.]).

2.2. Data collection, reduction and refinement

A hemisphere of reflections was collected at ambient temperature and pressure in order to provide a comparison with data collected at increasing pressures during the pressure study. All high-pressure data were collected at ambient temperature (see below). Diffraction data were collected (Bruker–Nonius, 2002[Bruker-Nonius (2002). SMART. Bruker-Nonius, Madison, Wisconsin, USA.]) on a Bruker SMART APEX diffractometer with graphite-monochromated Mo Kα radiation (λ = 0.71073 Å). These data were integrated using the program SAINT (Bruker–Nonius, 2004a[Bruker-Nonius (2004a). SAINT, Version V7.12A. Bruker-Nonius, Madison, Wisconsin, USA.]) and an absorption correction was performed with the program SADABS (Sheldrick, 2004[Sheldrick, G. M. (2004). SADABS. University of Göttingen, Germany.]). The α-GLYGLY coordinates of Kvick et al. (1977[Kvick, Å., Karaghouli, A. R. & Koetzle, T. F. (1977). Acta Cryst. B33, 3796-3801.]) were refined against these data to yield a conventional R factor of 0.0488 for 1164 data with I > 2σ(I). A listing of crystal and refinement data is given in Table 1[link]. The molecular structure and numbering scheme used is shown in Fig. 1[link].

Table 1
Crystallographic data for α-GLYGLY at ambient temperature between 0 and 4.7 GPa

Pressure (GPa) 0 1.4 3.0 3.7 4.7
Crystal data
Chemical formula C4H8N2O3 C4H8N2O3 C4H8N2O3 C4H8N2O3 C4H8N2O3
Mr 132.12 132.12 132.12 132.12 132.12
Cell setting, space group Monoclinic, P21/c Monoclinic, P21/c Monoclinic, P21/c Monoclinic, P21/c Monoclinic, P21/c
a, b, c (Å) 8.1233 (18), 9.554 (2), 7.8224 (17) 7.6428 (3), 9.3800 (4), 7.6505 (5) 7.4304 (4), 9.2896 (7), 7.5943 (9) 7.3100 (15), 9.232 (2), 7.550 (3) 7.2437 (8), 9.2083 (13), 7.5328 (17)
β (°) 107.596 (4) 103.882 (4) 102.465 (7) 101.51 (3) 101.214 (14)
V3) 578.7 (2) 532.44 (5) 511.84 (8) 499.3 (3) 492.86 (14)
Z 4 4 4 4 4
Dx (Mg m−3) 1.516 1.648 1.714 1.758 1.780
Radiation type Mo Kα Mo Kα Mo Kα Mo Kα Mo Kα
No. of reflections for cell parameters 1501 1234 1235 1211 1070
θ range (°) 5–56 5–52 6–53 6–53 6–52
μ (mm−1) 0.13 0.14 0.15 0.15 0.15
Temperature (K) 293 293 293 293 293
Crystal form, colour Block, colourless Block, colourless Block, colourless Block, colourless Block, colourless
Crystal size (mm) 0.60 × 0.36 × 0.12 0.20 × 0.20 × 0.10 0.20 × 0.20 × 0.10 0.20 × 0.20 × 0.10 0.20 × 0.20 × 0.10
           
Data collection
Diffractometer Bruker APEX Bruker APEX II Bruker APEX II Bruker APEX II Bruker APEX II
Data collection method ω scans ω scans ω scans ω scans ω scans
Absorption correction Multi-scan (based on symmetry-related measurements) Multi-scan (based on symmetry-related measurements) Multi-scan (based on symmetry-related measurements) Multi-scan (based on symmetry-related measurements) Multi-scan (based on symmetry-related measurements)
Tmin 0.86 0.85 0.86 0.84 0.75
Tmax 0.98 0.99 0.99 0.99 0.98
No. of measured, independent and observed reflections 3696, 1390, 1164 2911, 471, 360 2733, 451, 348 2678, 435, 332 2669, 437, 318
Criterion for observed reflections I > 2.00σ(I) I > 2.00σ(I) I > 2.00σ(I) I > 2.00σ(I) I > 2.00σ(I)
Completeness (%) 99.8 45.4 45.2 45.8 45.8
Rint 0.027 0.052 0.048 0.048 0.052
θmax (°) 28.7 27.2 26.8 26.9 27.2
Range of h, k, l −10 → h → 6 −9 → h → 9 −9 → h → 8 −9 → h → 8 −9 → h → 8
  −11 → k → 12 −11 → k → 11 −10 → k → 10 −10 → k → 10 −10 → k → 10
  −10 → l → 10 −5 → l → 5 −5 → l → 5 −5 → l → 5 −5 → l → 5
           
Refinement
Refinement on F2 F2 F2 F2 F2
R[F2 > 2σ(F2)], wR(F2), S 0.049, 0.140, 1.01 0.076, 0.198, 1.05 0.075, 0.189, 1.03 0.068, 0.163, 1.04 0.072, 0.187, 1.03
No. of reflections 1385 455 434 419 422
No. of parameters 82 37 37 37 37
H-atom treatment Not refined Not refined Not refined Not refined Not refined
Weighting scheme w = 1/[σ2(F2) + (0.08P)2 + 0.11P], where P = [max(Fo2,0) + 2Fc2]/3 w = 1/[σ2(F2) + (0.08P)2 + 2.28P], where P = [max(Fo2,0) + 2Fc2]/3 w = 1/[σ2(F2) + (0.08P)2 + 1.99P], where P = [max(Fo2,0) + 2Fc2]/3 w = 1/[σ2(F2) + (0.05P)2 + 2.18P], where P = [max(Fo2,0) + 2Fc2]/3 w = 1/[σ2(F2) + (0.08P)2 + 2.23P], where P = [max(Fo2,0) + 2Fc2]/3
(Δ/σ)max <0.0001 <0.0001 <0.0001 <0.0001 <0.0001
Δρmax, Δρmin (e Å−3) 0.28, −0.35 0.40, −0.38 0.38, −0.35 0.31, −0.30 0.35, −0.33
[Figure 1]
Figure 1
The molecular structure of GLYGLY at ambient temperature and pressure showing atom labelling. Ellipsoids are drawn at the 30% probability level, H atoms are drawn as spheres of arbitrary radius.

High-pressure diffraction data were collected on a kappa-geometry, Bruker APEX II diffractometer with graphite-monochromated Mo Kα radiation (λ = 0.71073 Å; Bruker–Nonius, 2004b[Bruker-Nonius (2004b). APEX-II, Version V1. Bruker-Nonius, Madison, Wisconsin, USA.]). Data collection procedures followed those of Dawson et al. (2004[Dawson, A., Allan, D. R., Clark, S. J., Parsons, S. & Ruf, M. (2004). J. Appl. Cryst. 37, 410-416.]). Integrations were carried out using the program SAINT, and absorption corrections in a two-stage process with the programs SHADE (Parsons, 2004[Parsons, S. (2004). SHADE. The University of Edinburgh, Scotland.]) and SADABS (Sheldrick, 2004[Sheldrick, G. M. (2004). SADABS. University of Göttingen, Germany.]). Data collections were taken in approximately 1.0 GPa steps from 1.4 GPa up to a final pressure of 5.3 GPa.

Refinements were carried out starting from the coordinates determined at ambient pressure. Minimization was against |F|2 using all data (CRYSTALS; Betteridge et al., 2003[Betteridge, P. W., Carruthers, J. R., Cooper, R. I., Prout, K. & Watkin, D. J. (2003). J. Appl. Cryst. 36, 1487.]). Owing to the low completeness of the data-sets, all 1,2 and 1,3 distances were restrained to values observed in the ambient pressure structure. Specifically, the restraints were as follows: distances (Å): N1—C1 1.473 (5), C1—C2 1.511 (5), C2—O1 1.238 (5), C2—N2 1.330 (5), N2—C3 1.450 (5), C3—C4 1.513 (5), C4—O3 1.240 (5), C4—O2 1.255 (5); angles (°): N1—C1—C2 109 (1), C1—C2—O1 120 (1), O1—C2—N2 123 (1), N2—C2—C1 116 (1), C4—C3—N2 112 (1), C3—C4—O3 115 (1), C3—C4—O2 118 (1), O2—C4—O3 126 (1), C2—N2—C3 121 (1). All non-H atoms were refined with isotropic displacement parameters. Owing to the poor quality of the data set collected at 5.4 GPa, the data collected to 4.7 GPa were used for structural comparison to the ambient temperature and pressure structure. Listings of crystal and refinement data are given in Table 1[link].

Crystal structures were visualized using the programs DIAMOND (Crystal Impact, 2004[Crystal Impact (2004). DIAMOND, Version 3.0. Crystal Impact GbR, Postfach 1251, 53002 Bonn, Germany. http://www.crystalimpact.com/diamond .]) and XP (Sheldrick, 1997[Sheldrick, G. M. (1997). XP. University of Göttingen, Germany.]). Analyses were carried out using PLATON (Spek, 2003[Spek, A. L. (2003). J. Appl. Cryst. 36, 7-13.]), as incorporated in the WIN-GX suite (Farrugia, 1999[Farrugia, L. J. (1999). J. Appl. Cryst. 32, 837-838.]). Searches of the Cambridge Database (Allen, 2002[Allen, F. H. (2002). Acta Cryst. B58, 380-388.]) were performed with the program CONQUEST (Allen & Motherwell, 2002[Allen, F. H. & Motherwell, W. D. S. (2002). Acta Cryst. B58, 407-422.]) and Version 5.26 of the database with updates up to August 2005. Hirshfeld surface analysis was performed using the program CrystalExplorer (Wolff et al., 2005[Wolff, S. K., Grimwood, D. J., McKinnon, J. J., Jayatilaka, D. & Spackman, M. A. (2005). CrystalExplorer, Version 1.5. University of Western Australia. http://www.Theochem.uwa.edu.au/crystal_explorer/ .]).

3. Results

3.1. The structure of α-GLYGLY at ambient temperature and pressure

Hydrogen bonding in amino acids and peptides has been reviewed by Görbitz (1989[Görbitz, C. H. (1989). Acta Cryst. B45, 390-395.]) and by Jeffrey & Maluszynska (1982[Jeffrey, G. A. & Maluszynska, H. (1982). Int. J. Biol. Macromol. 3, 173-185.]). α-GLYGLY crystallizes in its zwitterionic tautomer, with charged carboxyl and ammonium moieties, and the structure of GLYGLY is dominated by the formation of NH⋯O hydrogen bonds, with five such interactions formed under ambient temperature and pressure conditions.

The hydrogen bond N2H6⋯O1 is formed between the N—H and C=O moieties of neighbouring peptide groups and together with N1H3⋯O2 form an R22(10) ring motif (Fig. 2[link]a; Bernstein et al., 1995[Bernstein, J., Davis, R. E., Shimoni, L. & Chang, N.-L. (1995). Angew. Chem. Int. Ed. Engl. 34, 1555-1573.]). Both of these hydrogen bonds are also involved in the formation of a larger R44(18) ring motif created with another of the NH⋯O hydrogen bonds, N1H2⋯O3. The alternating pattern of R22(10) and R44(18) rings builds up layers of GLYGLY molecules which lie parallel to the (10[\overline 1]) plane. The layers are reminiscent of the antiparallel β sheets observed in protein structures (cf. Figs. 2[link]a and b).

[Figure 2]
Figure 2
Ball-and-stick model showing (a) R22(10) and R44(18) ring motifs forming layers within α-GLYGLY. The layers formed within the structure are also reminiscent of those of an antiparallel β sheet motif (b). Hydrogen bonds are drawn as black dotted lines, while weak C=O⋯C=O interactions are shown, only in (a), as pink dotted lines. The second largest component of the strain tensor is drawn as a red arrow in (a). Space-filling plots for (c) α-GLYGLY at ambient pressure and (d) at 4.7 GPa are shown. (a), (c) and (d) are viewed perpendicular to the (10[\overline 1]) plane. Note that voids in R44(18) and R22(10) ring motifs close up on increasing pressure. Colour scheme: N blue, C grey, O red and H white.

A bifurcated interaction, N1H1⋯O2/O3, connects the layers into a three-dimensional hydrogen-bonded array interacting between the layers (Fig. 3[link]a). The shorter of the bifurcated hydrogen bonds, N1H1⋯O2, forms an R44(12) ring motif with N1H2⋯O3 (Fig. 4[link]a), the hydrogen bond involved in the formation of the R44(18) ring motifs. Pairs of centrosymmetrically related N1H1⋯O2 bonds also form R22(16) rings between the layers (Fig. 4[link]a). The longer component of the bifurcated interaction, N1H1⋯O3, is quite long at ambient pressure [3.196 (3) Å], although it decreases in length on compression (Table 2[link]). This bifurcated interaction, together with N1H2⋯O3 and N1H3⋯O2, forms an R23(6) ring motif which, like both the R22(16) and R44(12) ring motifs, acts between the layers (Fig. 3[link]a).

Table 2
Hydrogen-bonding parameters (Å, °) and C=O⋯C=O interactions in α-GLYGLY

The Δ column refers to the 4.7 GPa distance subtracted from the distance at ambient pressure.

Pressure (GPa) 0 1.4 3.0 3.7 4.7 Δ
Hydrogen bonds formed between the β sheet-like layers
N1H1⋯O2i N1⋯O2 2.7541 (18) 2.737 (9) 2.730 (8) 2.723 (8) 2.725 (9) 0.029
N1H1⋯O3ii N1⋯O3 3.202 (2) 3.042 (6) 2.972 (6) 2.928 (6) 2.925 (7) 0.277
             
Hydrogen bonds formed within the β sheet-like layers
N1H2⋯O3iii N1⋯O3 2.7223 (19) 2.674 (9) 2.657 (8) 2.649 (8) 2.624 (9) 0.098
N1H3⋯O2iv N1⋯O2 2.7913 (18) 2.755 (6) 2.731 (6) 2.708 (6) 2.713 (7) 0.078
N2H6⋯O1v N2⋯O1 2.9567 (18) 2.861 (6) 2.814 (5) 2.783 (5) 2.772 (5) 0.185
             
C—H⋯O hydrogen bonds
C1H4⋯O1v C1⋯O1 3.214 (2) 3.160 (7) 3.133 (7) 3.119 (7) 3.125 (7) 0.089
C1H5.⋯O1vi C1⋯O1 3.348 (2) 3.252 (9) 3.207 (8) 3.180 (8) 3.160 (9) 0.188
C3H8⋯O2vii C3⋯O2 3.593 (2) 3.356 (7) 3.265 (6) 3.221 (6) 3.202 (7) 0.391
C3H8⋯O3vi C3⋯O3 3.603 (2) 3.382 (8) 3.308 (7) 3.282 (7) 3.251 (7) 0.352
             
C=O⋯C=O interactions
C2=O1⋯C2=O1iv 3.573 (2) 3.480 (6) 3.435 (6) 3.404 (6) 3.395 (6) 0.178
C4=O2⋯C2=O1i 3.274 (2) 3.105 (7) 3.014 (7) 2.939 (7) 2.909 (7) 0.365
C4=O2⋯C4=O2vii 3.405 (2) 3.127 (7) 3.022 (7) 2.976 (7) 2.952 (7) 0.453
Symmetry codes: (i) 1-x,1-y,-z; (ii) [1+x,{1\over 2}-y,{1\over 2}+z]; (iii) 1+x,y,1+z; (iv) [1-x,-{1\over 2}+y,{1\over 2}-z]; (v) [1-x,{1\over 2}+y,{1\over 2}-z]; (vi) [x,{1\over 2}-y,{1\over 2}+z]; (vii) -x,1-y,-z.
[Figure 3]
Figure 3
Ball-and-stick/wire model showing interactions between layers of GLYGLY molecules as viewed (a) perpendicular to the (10[\overline 1]) plane. Molecules in the upper and lower layers are coloured red and blue, respectively. R23(6) ring motifs between layers of GLYGLY molecules are shown. Black and orange dotted lines represent NH⋯O and CH⋯O hydrogen bonds, respectively, while pink dotted lines represent weak C=O⋯C=O interactions. Space-filling plots of R23(6) ring motifs at (b) ambient pressure and (c) 4.7 GPa are shown, drawn at the same scale and direction with only the ammonium and carboxyl groups involved in the formation of the rings shown. The colour scheme is the same as that in Fig. 2[link].
[Figure 4]
Figure 4
(a) Ball-and-stick model showing the R22(16) and R44(12) ring motifs under ambient pressure conditions between GLYGLY layers. Weak C=O⋯C=O interactions are drawn as pink dotted lines in the far left motif, while NH⋯O hydrogen bonds are drawn as black dotted lines. The largest component of the strain tensor is drawn as a red arrow in (a). Space-filling plots for R22(16) and R44(12) motifs in α-GLYGLY at ambient pressure (b) and (d), and 4.7 GPa (c) and (e) are drawn at the same scale and direction. For clarity, only the ammonium and carboxyl groups are included for comparison in (d) and (e). Note that voids within R22(16) and R44(12) ring motifs close up on increasing pressure. The colour scheme is the same as that in Fig. 2[link].

To summarize, the three-dimensional hydrogen-bonding network within α-GLYGLY can be described by reference to five R-type ring motifs. R22(10) and R44(18) ring motifs form layers, reminiscent of antiparallel β-sheet motifs in protein structures and lie parallel to the (10[\overline 1]) planes, while R44(12), R22(16) and R23(6) ring motifs connect these layers into a three-dimensional hydrogen-bonded network

In amino acid structures the presence of other interactions, particularly weaker CH⋯O interactions, are thought to be important for supporting moderate strength NH⋯O hydrogen bonds (Desiraju & Steiner, 1999[Desiraju, G. R. & Steiner, T. (1999). The Weak Hydrogen Bond in Structural Chemistry and Biology. IUCr Monographs on Crystallography No. 9. Oxford Univerity Press.]; Derewenda et al., 1995[Derewenda, Z. S., Lee, L. & Derewenda, U. (1995). J. Mol. Biol. 252, 248-262.]). We have discussed this recently in high-pressure studies of the crystal structures of polymorphs of glycine (Dawson et al., 2005[Dawson, A., Allan, D. R., Belmonte, S. A., Clark, S. J., David,W. I. F., McGregor, P. A., Parsons, S., Pulham, C. R. & Sawyer, L. (2005). Cryst. Growth Des. 5, 1415-1427.]) and serine (Moggach, Allan, Morrison, Parsons & Sawyer, 2005[Moggach, S. A., Allan, D. R., Morrison, C. A., Parsons, S. & Sawyer, L. (2005). Acta Cryst. B61, 58-68.]). In α-GLYGLY four CH⋯O interactions exist at ambient pressure and temperature. A pair of these, C3H8⋯O2/O3, constitutes a bifurcated hydrogen bond which acts between the layers to the carboxyl O atoms involved in the formation of the R44(18) ring motifs previously described (Fig. 3[link]a). The third CH⋯O interaction, C1H5⋯O1, is hydrogen bonded to the peptide carbonyl oxygen and also acts between the layers. The final CH⋯O hydrogen bond, C1H4⋯O1, like C1H5⋯O1, is also hydrogen bonded to the carbonyl oxygen, however, unlike C1H5⋯O1, this hydrogen bond acts within the layers. The combination of both C1H4⋯O1 and C1H5⋯O1 produces an R24(8) ring motif between the layers (Fig. 5[link]a). C1H4⋯O1 is of particular interest, as it has been shown to have preferred directionality and length in parallel and antiparallel β sheets with typical C⋯O distances of 3.31 and 3.27 Å, respectively (Fabiola et al., 1997[Fabiola, G. F., Krishnaswamy, S., Nagarajan, V. & Pattabhi, V. (1997). Acta Cryst. D53, 316-320.]).

[Figure 5]
Figure 5
(a) Ball-and-stick model showing the formation of R24(8) ring motifs via CH⋯O hydrogen bonds acting between layers of GLYGLY molecules, CH⋯O hydrogen bonds are drawn as orange dotted lines. Space-filling plots of R24(8) ring motifs at (b) ambient pressure and (c) 4.7 GPa are shown, drawn at the same scale and direction. In both (b) and (c), only those atoms involved in the formation of the ring, carbonyl C atoms and ammonium groups are shown for clarity. The colour scheme is the same as that in Fig. 2[link].

C=O⋯C=O interactions have been discussed in detail by Allen et al. (1998[Allen, F. H., Baalham, C. A., Lommerse, J. P. M. & Raithby, P. R. (1998). Acta Cryst. B54, 320-329.]) and are thought to be important in the stabilization of α helices and β sheets (Maccallum et al., 1995[Maccallum, P. H., Poet, R. & Milner-White, J. E. (1995). J. Mol. Biol. 248, 361-373.]). In α-GLYGLY C=O⋯C=O interactions occur within the β sheet-like layers between adjacent carbonyl groups (Fig. 2[link]a). A typical d(O⋯C) distance of ca 3.6 Å is reported for the average of 12 sets of secondary structural features (Maccallum et al., 1995[Maccallum, P. H., Poet, R. & Milner-White, J. E. (1995). J. Mol. Biol. 248, 361-373.]). This value is in agreement with that measured for α-GLYGLY under ambient pressure conditions [3.573 (2) Å]. Carboxyl–carboxyl and carboxyl–carbonyl interactions are formed between the GLYGLY layers. One such interaction occurs between pairs of C4=O2 bonds and is aligned in an antiparallel fashion; another, C4=O2⋯C2=O1, forms a sheared parallel motif (Allen et al., 1998[Allen, F. H., Baalham, C. A., Lommerse, J. P. M. & Raithby, P. R. (1998). Acta Cryst. B54, 320-329.]).

3.2. Effect of pressure on the unit-cell dimensions

α-GLYGLY was found to be stable to 5.4 GPa. However, the refined parameters of data collected at 5.4 GPa were imprecise and therefore only structural data to 4.7 GPa are reported here and used for comparison with the ambient pressure structure.

The response of the lattice parameters of α-GLYGLY to pressure is anisotropic, with the largest principal component of the strain tensor (Hazen & Finger, 1982[Hazen, R. M. & Finger, L. W. (1982). Comparative Crystal Chemistry, pp. 80-82. New York: John Wiley and Sons.]) formed between the β sheet-like planes, making an angle of 69.22 (6)° with the (10[\overline 1]) plane. The most compressible unit-cell dimension (Fig. 6[link]) is the a axis which decreases by 11.2%, with the b and c axes reducing by 3.8 and 3.6%, respectively, between ambient pressure and 5.4 GPa. The β angle also decreases by 6.61°. Between ambient pressure and 5.4 GPa the volume of α-GLYGLY decreases by 15.2%; most of the compression takes place in the first 1.4 GPa, with a reduction in volume of 8.0%. The gradient of the graph of pressure versus volume (Fig. 6[link]c) decreases markedly under pressure just before the break-up of the crystal.

[Figure 6]
Figure 6
Variation of lattice parameters a, b, c (Å), β (°) and volume (Å3) of α-GLYGLY as a function of pressure (GPa). The variation of a and c are shown on the same graph, with black circles and squares, respectively.

3.3. Conformational analysis of the β sheet motif

The structural analogy between the structure of the layers in α-GLYGLY and β sheet motifs found in proteins was referred to above. Similar observations have been applied to N-formyl-L-Met-L-Val trihydrate (Chatterjee & Parthasarathy, 1984[Chatterjee, A. & Parthasarathy, R. (1984). Int. J. Pept. Protein Res. 24, 447-452.]) and L-His-Gly chloride (Steiner, 1997[Steiner, T. (1997). Acta Cryst. C53, 730-732.]), which form parallel and antiparallel β sheet-like motifs, respectively.

In antiparallel β sheets the conformational angles C(O)—N(H)—Cα—C(O) (φ) and N(H)—Cα—C(O)—N(H) (ψ) adopt typical values of −139 and +135° under ambient pressure conditions, although these values can vary somewhat (Voet & Voet, 1995[Voet, D. & Voet, J. G. (1995). Biochemistry, 2nd ed. New York: Wiley.]). In α-GLYGLY these torsion angles can be defined φ1, ψ1, φ2 and ψ2, leading from the free ammonium end to the free carboxyl end, and correspond to the torsion angles about N1—C1, C1—C2, N2—C3 and C3—C4 (Table 3[link]). φ1 is therefore `unconventional' in the sense that it cannot be defined within the dipeptide molecule; rather, we use the carboxyl O3 atom to which N1 is hydrogen bonded (labelled O3iii in Tables 2[link] and 3[link]). At ambient pressure, φ1 and ψ1 are −154.77 (10) and −152.38 (13)°, respectively, while φ2 and ψ2 measure −155.06 (14) and 169.70 (14)°, respectively.

Table 3
Torsion angles φ and ψ (°) in α-GLYGLY as a function of pressure

For numbering refer to text.

Pressure (GPa) 0 4.7
O3i—N1—C1—C2 (φ1) −154.77 (10) −151.4 (4)
N1—C1—C2—N2 (ψ1) −152.38 (13) −151.3 (6)
C2—N2—C3—C4 (φ2) −155.06 (14) −158.6 (6)
N2—C3—C4—O3 (ψ2) 169.70 (14) 171.9 (5)
Symmetry code: (i) 1+x,y,1+z.

These torsion angles, particularly for ψ, are quite far from those expected for an antiparallel β sheet structure. This is not surprising because of the flexibility of the glycine residues, in particular the ammonium end, which is primarily optimized for hydrogen bonding within the structure. Nevertheless, on increasing the pressure to 4.7 GPa the molecules remain fairly inflexible with both φ1 and ψ1 increasing by +3.4 and +1.1°, respectively, while φ2 and ψ2 decrease and increase by only −3.5 and +2.2°, respectively.

3.4. NH⋯O hydrogen bonds

The variation in hydrogen-bonding parameters between ambient pressure and 4.7 GPa is shown in Table 2[link]. Since all H atoms were placed geometrically, N⋯O distances were used to quantify the relative compressibility of the hydrogen bonds. The most compressible of the NH⋯O hydrogen bonds is the longer interaction in the bifurcated N1H1⋯O2/O3 hydrogen bond, which acts between the β sheet-like layers. The shorter of these bonds, N1H1⋯O2, is the least compressible hydrogen bond in the system. The next most compressible hydrogen bond, N2H6⋯O1, is the interaction between neighbouring peptide groups which act within the β sheet-like layers (Fig. 2[link]a). In a study of the mean geometries of C—H⋯O and N—H⋯O hydrogen-bonding interactions in parallel and antiparallel β sheets (Fabiola et al., 1997[Fabiola, G. F., Krishnaswamy, S., Nagarajan, V. & Pattabhi, V. (1997). Acta Cryst. D53, 316-320.]), the mean distance for this particular N—H⋯O hydrogen bond is 2.89 Å, that is, slightly shorter than observed in α-GLYGLY at ambient pressure. This interaction runs in the same direction as the second largest component of the strain tensor, which is parallel to b and is shown as a red arrow in Fig. 2[link](a).

N1H2⋯O3 shortens more than N1H3⋯O2, even though the latter is the longer bond at ambient pressure. N1H2⋯O3 decreases in length to 2.624 (9) Å at 4.7 GPa. This distance is very short: the shortest NH⋯O(carboxylate) interaction to be observed in ambient-pressure structures of peptides occurs in L-valyl-L-phenylalanine, measuring 2.649 (5) Å (Görbitz, 2002[Görbitz, C. H. (2002). Acta Cryst. B58, 512-518.]). Short NH⋯O hydrogen bonds have also been observed in L-cystine [2.690 (18) Å; Moggach, Allan, Lozano-Casal & Parsons, 2005[Moggach, S. A., Allan, D. R., Lozano-Casal, P. & Parsons, S. (2005). J. Synchrotron Rad. 12, 590-597.]] at 3.7 GPa and ε-glycine at 4.3 GPa [2.59 (4) Å; Dawson et al., 2005[Dawson, A., Allan, D. R., Belmonte, S. A., Clark, S. J., David,W. I. F., McGregor, P. A., Parsons, S., Pulham, C. R. & Sawyer, L. (2005). Cryst. Growth Des. 5, 1415-1427.]].

3.5. CH⋯O hydrogen bonds

The most compressible of the CH⋯O hydrogen-bonding interactions is the bifurcated system, C3H8⋯O2/O3, formed between the β sheet-like layers. The C⋯O distances in this interaction decrease in length by 0.39 and 0.35 Å between ambient pressure and 4.7 GPa, that is, substantially more than any of the NH⋯O bonds.

C1H4⋯O1 decreases by a relatively modest 0.089 Å between ambient pressure and 4.7 GPa, measuring 3.125 (7) Å at 4.7 GPa. In antiparallel β sheets the mean C⋯O distance for this type of interaction is typically 3.27 Å (Fabiola et al., 1997[Fabiola, G. F., Krishnaswamy, S., Nagarajan, V. & Pattabhi, V. (1997). Acta Cryst. D53, 316-320.]), with minimum and maximum values under ambient conditions of 2.91 and 3.50 Å, respectively (3.50 Å being the cut-off distance used in the study).

3.6. C=O⋯C=O interactions

The least compressible of the C=O⋯C=O interactions, C2=O1⋯C2=O1, acts within the β sheet-like layers and decreases in length by 0.178 Å between ambient and 4.7 GPa. This interaction runs in the same direction as the second largest component of the strain tensor and its compression is comparable to that of N2H6⋯O1, which also acts within the layers, between adjacent peptide groups (reducing in length by 0.185 Å). The most compressible C=O⋯C=O interaction is formed between carboxyl groups, C4=O2⋯C4=O2, with d(C⋯O) decreasing by 0.453 Å. This interaction, which measures 2.952 (7) Å at 4.7 GPa acts between the layers and is the most compressible interaction in the structure.

The last of the C=O⋯C=O interactions, C4=O2⋯C2=O1, acts between adjacent carboxyl and carbonyl groups and decreases by 0.365 Å between ambient pressure and 4.7 GPa. This interaction, like that of C4=O2⋯C4=O2, acts between the layers and is the shortest of the three C=O⋯C=O interactions at 4.7 GPa, measuring 2.909 (7) Å.

4. Discussion

4.1. Restrained refinement of GLYGLY at high pressure

Intramolecular bonds are expected to lengthen as intermolecular interactions strengthen with pressure. In paracetamol, for example, the shortening of an intermolecular OH⋯O(O=C) hydrogen bond is accompanied by a small elongation of the C=O bond (0.023 Å at 4 GPa; Boldyreva, 2003[Boldyreva, E. V. (2003). J. Mol. Struct. 647, 159-179.]). Studies of 2-methyl-1,3-cyclopentanedione, dimedone and 1,3-cyclohexanedione also reveal similar variations with pressure (0.02 Å at 3 GPa; Katrusiak, 1992[Katrusiak, A. (1992). J. Mol. Struct. 269, 329-354.]). However, these changes are very small and in most high-pressure structure determinations are within experimental error. In a recent ab initio study on the effect of pressure on pentaerythritol tetranitrate at 23 GPa, changes in calculated bond lengths on compression showed that C—C bonds decrease by 0.05 Å, while CH and CO bonds decreased by only 0.01 Å (Brand, 2005[Brand, H. V. (2005). J. Phys. Chem. B, 109, 13668-13675.]). The largest change in bond angle in this study was 3.7°, while the largest change in torsion angle was 11°.

In high-pressure crystallography, particularly when applied to low-symmetry crystal systems, shading by the pressure cell restricts the volume of reciprocal space that can be sampled. This leads to low data completeness and low data-to-parameter ratios during refinement. During refinement of the high-pressure crystal structures reported here intramolecular bond distances and angles (but not the torsion angles) were restrained to their ambient pressure values in order to alleviate these refinement problems. While such restraints can be justified below about 10 GPa, this approximation is likely to become less accurate at higher pressures.

4.2. Anisotropic compression of α-GLYGLY

In previous pressure studies of L-serine-I and hexagonal L-cystine we have ascribed trends in the relative compressibility of CH⋯O and NH⋯O hydrogen bonds to the closing up of voids within R-type ring motifs, which exist under ambient pressure conditions. These voids are conveniently visualized in α-GLYGLY by comparing space-filling plots of ring motifs between ambient pressure and 4.7 GPa.

In α-GLYGLY there are five R-type ring motifs: all of these contain voids at the ring-centres, and all become smaller as pressure increases. These R motifs can be split into two categories, those within the GLYGLY layers [R22(10) and R44(18)], and those between the layers [R23(6), R22(16) and R44(12)]. The largest voids formed within the layers are those at the centre of the R44(18) ring motifs (Fig. 2[link]) and these are far from being completely closed at 4.7 GPa. Increasing pressure would be expected to close these voids still further, but N1H2⋯O3 measures 2.624 (9) Å at 4.7 GPa, and in amino acids attainment of an NH⋯O distance as short as this preludes a phase transition. This is consistent with the break-up of the crystal which ensues above 4.7 GPa. Of the three hydrogen bonds involved in the formation of the R44(18) rings, the most compressible is N2H6⋯O1, which is also the longest of the three at ambient pressure. Very small voids can also be observed within R22(10) ring motifs which also close up on increasing pressure to 4.7 GPa.

Between the layers, the closure of voids can also be observed within R44(12), R23(6) and R22(16) ring motifs (Fig. 3[link]b/c, 4[link]b/c and 4[link]d/e, respectively). This is achieved by a sliding action of the layers across each other and moving closer together, rather than direct compression of N1H1⋯O2, which is the least compressible of the NH⋯O hydrogen bonds formed. The combination of the sliding of the layers and their movement closer together accounts for the direction of the largest component of the strain tensor, which is illustrated in Fig. 4[link](a). As the layers are compressed together the hydrogen bond about H1 becomes more bifurcated (Fig. 3[link]b/c); as in the case for N2H6⋯O1, described above, this occurs through the compression of a relatively long hydrogen bond (N1H1⋯O3).

The compression of the layers leads to shortening of two C=O⋯C=O interactions. C4=O2⋯C4=O2 decreases by 0.453 Å, while C4=O2⋯C2=O1 compresses to become the shortest of its type in α-GLYGLY, although still substantially longer [2.909 (7) Å] than the shortest value observed under ambient pressure conditions [2.521 (2) Å; Kapplinger et al., 1999[Kapplinger, I., Keutel, H. & Jager, E. G. (1999). Inorg. Chim. Acta, 291, 190-206.]].

Our work on amino acids has shown that compression is accompanied by an increase in the number and strength of CH⋯O contacts. Hence the void in the R24(8) ring motifs formed between C1H4⋯O1 and C1H5⋯O1, which act between the β sheet-like layers, closes up on increasing pressure (Figs. 5[link]b and c). The longest CH⋯O hydrogen bond is the bifurcated interaction C3H8⋯O2/3, which experiences the greatest shortening (Table 2[link]).

To summarize, compression of α-GLYGLY proceeds via the reduction in void sizes. Voids close in such a way as to decrease the distances of stabilizing interactions such as hydrogen bonds and dipolar contacts, but once a contact has become very short (in this case N1H2⋯O3), the crystal begins to break-up, presumably as a result of a phase change. The largest reductions in interaction distances tend to occur for those contacts which are longest at ambient pressure. In α-GLYGLY these longer interactions are formed between the β sheet-like layers and it is understandable therefore that the direction of greatest compression lies in the same direction.

4.3. Hirshfeld surface analysis

Hirshfeld surfaces are constructed by partitioning space within a crystal structure into regions where the electron density from a sum of spherical atoms (the promolecule) dominates over the sum of the electron density of the crystal (the procrystal; McKinnon et al., 2004[McKinnon, J. J., Spackman, M. A. & Mitchell, A. S. (2004). Acta Cryst. B60, 627-668.]). In this study, Hirshfeld surfaces were constructed using the program CrystalExplorer (Wolff et al., 2005[Wolff, S. K., Grimwood, D. J., McKinnon, J. J., Jayatilaka, D. & Spackman, M. A. (2005). CrystalExplorer, Version 1.5. University of Western Australia. http://www.Theochem.uwa.edu.au/crystal_explorer/ .]). Fig. 7[link] shows the distance external to the surface to the nearest nucleus in another molecule (de) mapped onto the surface in two different ranges 0.68–2.31 Å [labelled (i)] and 1.1–1.5 Å [labelled (ii)]. Each surface is shown in three orientations at ambient pressure (top row, ac) and 4.7 GPa (bottom row, df).

[Figure 7]
Figure 7
The Hirshfeld surface of GLYGLY at (a)–(c) ambient temperature and pressure, and (d)–(f) 4.7 GPa. The surfaces at both ambient pressure and 4.7 GPa have been separated into three orientations where (a) and (d) represent the GLYGLY molecule as viewed approximately perpendicular to the (10[\overline 1]) plane. Both (b) and (e), and (c) and (f) represent 90° increment rotations about the vertical axis from (a) and (d). In comparing both the ambient pressure and 4.7 GPa structures, all hydrogen bonds have been normalized to neutron distances (C—H = 1.083 and N—H = 1.009 Å). Surfaces have been mapped over two ranges between [a(i)–f(i)] de, 0.68–2.31 Å and [a(ii)–f(ii)] 1.1–1.5 Å. The molecules beside the surfaces have been added for clarity; for numbers refer to the text. Colour scheme: C grey, N blue, O red and H white.

In Fig. 7[link](a)(i)–(f)(i), red regions on the surface arise from short values of de (i.e. hydrogen-bond acceptors), while flat green regions around the ammonium group and peptide N2H6⋯O1 hydrogen bond correspond to hydrogen-bond donors. Blue regions correspond to long contacts. On increasing the pressure to 4.7 GPa, there are fewer blue regions (longer contacts) and more red regions (short contacts), consistent with the general shortening of contacts at high pressure [Fig. 7[link]a(i)–f(i)]. The decrease in lengths of NH⋯O hydrogen bonds from the ammonium moiety and the peptide hydrogen bond can be seen in Figs. 7(a)(i)/(d)(i) and (b)(i)/(e)(i), as an increase in the size of the red regions labelled 1 and 2. The yellow regions labelled 3 and 4 in Fig. 7[link](a)(i) and (b)(i), which are derived from C1H5⋯O1 and C1H4⋯O1, respectively, become redder in the corresponding regions of Figs. 7[link](d)(i) and (e)(i), indicating a shortening of these contacts at 4.7 GPa. The substantial shortening of the bifurcated hydrogen bond C3H8⋯O2/O3 appears in regions 5 [Fig. 7[link]a(i)/d(i)] and 6 [Fig. 7[link]c(i)/f(i)].

In Fig. 7[link](a)(i)–(c)(i), blue regions on the surfaces correspond to voids in the structure. As these voids become smaller at high pressure the surfaces become greener. For example, the darkest blue region, labelled 7 in Fig. 7[link](a)(i), corresponds to voids in R22(16) ring motifs (cf Fig. 4[link]b) between the β sheet-like layers in the structure. Region 8 [Fig. 7[link]b(i)] corresponds to voids in the middle of R44(18) ring motifs; the reduction in the size of this void can be seen in the corresponding region of Fig. 7[link](e)(i). Notably, this void appears on the surface beside the C3—H7 bond, the only one of its type not involved in the formation of a CH⋯O hydrogen bond, although a contact is formed between C3H7⋯O1, this contact is long, even at 4.7 GPa (3.311 Å). This contact, although it is long, does appear on the surface in Fig. 7[link](c)(i) labelled 9. The region becomes markedly more yellow at 4.7 GPa [Fig. 7[link]f(i)], again clearly representing the compression between the layers.

The region in Fig. 7[link](c)(i) labelled 10 is a close contact between two H atoms attached to the CH2 groups of adjacent ammonium moieties between layers. This region becomes markedly more yellow at 4.7 GPa showing the compression of non-polar side groups of the dipeptide toward each other on increasing pressure.

The compression of the C=O⋯C=O groups is not nearly as clear on the surfaces in Figs. 7[link](a)(i)–(f)(i). In part this is because they are masked by much shorter contacts between NH⋯O and C=O. These contacts can be made clearer by mapping de on the surface over a shorter range [see Fig. 7[link]a(ii)–f(ii)]. This not only enhances the C=O⋯C=O interactions, but makes the increase in strength of CH⋯O and NH⋯O contacts much clearer. However, the regions in which void closure takes place become much more difficult to see, and therefore both sets of surfaces mapped over different ranges are included in Fig. 7[link].

C4=O2⋯C4=O2, the most compressible interaction, appears in region 11 [Fig. 7[link]c(ii)]. The increase in size of the blue/green region in Fig. 7[link](f)(ii) corresponds to the shortening of this interaction on increasing pressure. The final C=O⋯C=O interaction, C4=O2⋯C2=O1, is the shortest of the three C=O⋯C=O interactions at 4.7 GPa, and can be seen in region 12 [Fig. 7[link]a(ii)]. Again, the size of this region increases in Fig. 7[link](d)(ii) and demonstrates the closing up of voids within R22(16) ring motifs between the layers (Fig. 4[link]b/c). Notably, this is the shortest of the C=O⋯C=O interactions at 4.7 GPa and thus accounts for why the C4=O2⋯C2=O1 contact is markedly clearer in appearance on the surface than that formed by C4=O2⋯C4=O2.

4.4. Fingerprint plots

A fingerprint plot is a plot of de against di (the distance from the surface to the nearest atom in the molecule itself). It can be used to encode information on overall packing characteristics (Fig. 8[link]). The number of longer contacts decreases as the points at larger values of de become less frequent at 4.7 GPa: these interactions are formed across the voids within the R-type ring motifs. The overall shortening of these longer contacts is related to the fingerprint plots by a decrease in the maximum values of de between ambient pressure (2.303 Å) and 4.7 GPa (2.196 Å). The two long spikes in both plots represent NH⋯O hydrogen bonds, specifically the shortest de value at 4.7 GPa is caused by N1H2⋯O3, the shortest of the NH⋯O hydrogen bonds at this pressure. In previous studies, such as that of L-cystine, NH⋯O hydrogen bonds have been found to be less compressible than `softer' CH⋯O interactions. This is represented clearly in the fingerprint plot, as the NH⋯O spikes become less pronounced as the rest of the plot moves toward the origin.

[Figure 8]
Figure 8
Two-dimensional fingerprint plots for α-GLYGLY at (a) ambient temperature and pressure and (b) 4.7 GPa.

5. Conclusions

We have described the effect of pressure on the crystal structure of α-GLYGLY. The structure can be considered to consist of layers of GLYGLY molecules which stack perpendicular to the (10[\overline 1]) direction, which are made up of R22(10) and R44(18) ring motifs constructed via NH⋯O hydrogen-bonding interactions. Ring motifs are also formed between layers, again by NH⋯O hydrogen-bonding interactions in R44(12), R22(16) and R23(6) ring motifs. The arrangement of GLYGLY molecules within each layer resembles that of an antiparallel β sheet motif observed in protein structures, where in α-GLYGLY the molecules in the β sheet motif are linked through NH⋯O hydrogen bonds rather than conventional covalent amide links. The conformational changes in the pressure regime studied are quite modest and the same might be expected of β sheets.

The structure was found to be stable to 5.4 GPa, although structural data were only reported to 4.7 GPa. α-GLYGLY undergoes anisotropic compression in which the principal effect is to compress voids in the structure, particularly those between the layers. This compression continued until, at 5.4 GPa, the sample began to break apart and no structural data could be extracted. At 4.7 GPa the length of N1H2⋯O3 decreased in size to the minimum distance usually observed under ambient pressure conditions (ca 2.6 Å) for this type of interaction and it is possible that relief of these close contacts drives the phase transition.

The compression of both NH⋯O and soft CH⋯O interactions are also described using Hirshfeld surfaces. These clearly show the reduction in the sizes of voids and a decrease in length of CH⋯O, NH⋯O and C=O⋯C=O interactions with increasing pressure, both between and within the layers. Hirshfeld surfaces are an effective means to gain an overall view of the environment of molecules at increasing compression in an anisotropic fashion.

Supporting information


Refinement top

199_ALERT_1_C Check the Reported _cell_measurement_temperature 293 K 200_ALERT_1_C Check the Reported _diffrn_ambient_temperature. 293 K

The data collection was at 293 K.

250_ALERT_2_C Large U3/U1 Ratio for Average U(i,j) Tensor ···. 2.30

Principle axes of thermal elipsoids are shown (A**2). All look reasonable.

C2 0.01747 0.01966 0.03013

N2 0.01641 0.01712 0.04362

C3 0.01652 0.02124 0.05680

C4 0.01705 0.02373 0.02706

O2 0.02095 0.02428 0.04673

O3 0.01617 0.04534 0.07004

C1 0.01759 0.02084 0.03478

N1 0.01539 0.02128 0.03334

O1 0.01733 0.02398 0.06416

795_ALERT_4_C C-Atom in CIF Coordinate List out of Sequence.. C1 796_ALERT_4_C O-Atom in CIF Coordinate List out of Sequence.. O1 797_ALERT_4_C N-Atom in CIF Coordinate List out of Sequence.. N1

No action taken.

Computing details top

For all compounds, data collection: SMART (Siemens, 1993); cell refinement: SAINT (Siemens ,1995); data reduction: SAINT (Siemens ,1995). Program(s) used to solve structure: SIR92 (Altomare et al., 1994) for glyg00; USER DEFINED STRUCTURE SOLUTION for glyg14, glyg30, glyg37, glyg47. For all compounds, program(s) used to refine structure: CRYSTALS (Betteridge et al., 2003); molecular graphics: CAMERON (Watkin et al., 1996); software used to prepare material for publication: CRYSTALS (Betteridge et al., 2003).

Figures top
[Figure 1]
[Figure 2]
[Figure 3]
[Figure 4]
[Figure 5]
[Figure 6]
[Figure 7]
[Figure 8]
(glyg00) top
Crystal data top
C4H8N2O3F(000) = 280
Mr = 132.12Dx = 1.516 Mg m3
Monoclinic, P21/cMo Kα radiation, λ = 0.71073 Å
Hall symbol: -P 2ybcCell parameters from 1501 reflections
a = 8.1233 (18) Åθ = 5–56°
b = 9.554 (2) ŵ = 0.13 mm1
c = 7.8224 (17) ÅT = 293 K
β = 107.596 (4)°Block, colourless
V = 578.7 (2) Å30.60 × 0.36 × 0.12 mm
Z = 4
Data collection top
Bruker APEX
diffractometer
1164 reflections with I > 2.00u(I)
Graphite monochromatorRint = 0.027
ω scansθmax = 28.7°, θmin = 2.6°
Absorption correction: multi-scan
SADABS (Siemens, 1996)
h = 106
Tmin = 0.86, Tmax = 0.98k = 1112
3696 measured reflectionsl = 1010
1390 independent reflections
Refinement top
Refinement on F2Primary atom site location: Kvick et al., (1979)
Least-squares matrix: fullHydrogen site location: inferred from neighbouring sites
R[F2 > 2σ(F2)] = 0.049H-atom parameters not refined
wR(F2) = 0.140 w = 1/[σ2(F2) + ( 0.08P)2 + 0.11P]
where P = (max(Fo2,0) + 2Fc2)/3
S = 1.01(Δ/σ)max = 0.000206
1385 reflectionsΔρmax = 0.28 e Å3
82 parametersΔρmin = 0.35 e Å3
0 restraints
Crystal data top
C4H8N2O3V = 578.7 (2) Å3
Mr = 132.12Z = 4
Monoclinic, P21/cMo Kα radiation
a = 8.1233 (18) ŵ = 0.13 mm1
b = 9.554 (2) ÅT = 293 K
c = 7.8224 (17) Å0.60 × 0.36 × 0.12 mm
β = 107.596 (4)°
Data collection top
Bruker APEX
diffractometer
1390 independent reflections
Absorption correction: multi-scan
SADABS (Siemens, 1996)
1164 reflections with I > 2.00u(I)
Tmin = 0.86, Tmax = 0.98Rint = 0.027
3696 measured reflections
Refinement top
R[F2 > 2σ(F2)] = 0.0490 restraints
wR(F2) = 0.140H-atom parameters not refined
S = 1.01Δρmax = 0.28 e Å3
1385 reflectionsΔρmin = 0.35 e Å3
82 parameters
Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å2) top
xyzUiso*/Ueq
C20.51455 (19)0.32926 (16)0.2567 (2)0.0224
N20.38281 (17)0.40729 (13)0.16383 (18)0.0257
C30.2336 (2)0.34438 (17)0.0343 (2)0.0315
C40.13810 (19)0.44681 (17)0.11059 (19)0.0226
O20.17806 (16)0.57319 (12)0.09166 (15)0.0307
O30.02560 (18)0.39389 (16)0.23924 (17)0.0439
C10.6569 (2)0.40541 (16)0.3969 (2)0.0244
N10.82202 (16)0.33096 (13)0.42373 (17)0.0233
O10.52170 (16)0.20188 (12)0.23929 (17)0.0352
H20.90650.37610.50690.0259*
H10.84760.32830.31960.0259*
H30.81260.24310.46110.0259*
H40.66730.50310.35540.0274*
H50.62840.40830.51260.0274*
H60.38580.50050.18120.0276*
H70.27350.26340.02400.0332*
H80.15240.31030.09900.0332*
Atomic displacement parameters (Å2) top
U11U22U33U12U13U23
C20.0237 (7)0.0195 (7)0.0207 (7)0.0007 (5)0.0016 (6)0.0019 (5)
N20.0248 (7)0.0171 (6)0.0271 (7)0.0004 (5)0.0044 (5)0.0007 (5)
C30.0276 (8)0.0222 (8)0.0333 (9)0.0048 (6)0.0080 (6)0.0035 (6)
C40.0230 (7)0.0248 (7)0.0179 (7)0.0009 (5)0.0030 (5)0.0012 (5)
O20.0412 (7)0.0229 (6)0.0232 (6)0.0017 (5)0.0028 (5)0.0014 (4)
O30.0439 (8)0.0443 (8)0.0284 (7)0.0070 (6)0.0115 (6)0.0041 (5)
C10.0254 (7)0.0221 (7)0.0211 (7)0.0025 (5)0.0001 (6)0.0023 (5)
N10.0222 (6)0.0214 (6)0.0210 (6)0.0005 (5)0.0015 (5)0.0013 (5)
O10.0340 (7)0.0177 (6)0.0418 (7)0.0017 (4)0.0066 (5)0.0006 (5)
Geometric parameters (Å, º) top
C2—N21.3263 (19)C4—O21.2474 (19)
C2—C11.517 (2)C4—O31.2440 (19)
C2—O11.2280 (19)C1—N11.4763 (19)
N2—C31.4540 (19)C1—H41.000
N2—H60.900C1—H51.000
C3—C41.521 (2)N1—H20.900
C3—H71.000N1—H10.900
C3—H81.000N1—H30.900
N2—C2—C1116.03 (13)O2—C4—O3126.20 (15)
N2—C2—O1123.62 (14)C2—C1—N1109.45 (12)
C1—C2—O1120.28 (13)C2—C1—H4109.5
C2—N2—C3120.93 (13)N1—C1—H4109.5
C2—N2—H6119.5C2—C1—H5109.5
C3—N2—H6119.5N1—C1—H5109.5
N2—C3—C4112.54 (13)H4—C1—H5109.5
N2—C3—H7108.7C1—N1—H2109.5
C4—C3—H7108.7C1—N1—H1109.5
N2—C3—H8108.7H2—N1—H1109.5
C4—C3—H8108.7C1—N1—H3109.5
H7—C3—H8109.5H2—N1—H3109.5
C3—C4—O2118.59 (13)H1—N1—H3109.5
C3—C4—O3115.21 (14)
(glyg14) top
Crystal data top
C4H8N2O3F(000) = 280
Mr = 132.12Dx = 1.648 Mg m3
Monoclinic, P21/cMo Kα radiation, λ = 0.71073 Å
Hall symbol: -P 2ybcCell parameters from 1234 reflections
a = 7.6428 (3) Åθ = 5–52°
b = 9.3800 (4) ŵ = 0.14 mm1
c = 7.6505 (5) ÅT = 293 K
β = 103.882 (4)°Block, colourless
V = 532.44 (5) Å30.20 × 0.20 × 0.10 mm
Z = 4
Data collection top
Bruker APEX II
diffractometer
360 reflections with I > 2.00u(I)
Graphite monochromatorRint = 0.052
ω scansθmax = 27.2°, θmin = 2.8°
Absorption correction: multi-scan
SADABS (Siemens, 1996)
h = 99
Tmin = 0.85, Tmax = 0.99k = 1111
2911 measured reflectionsl = 55
471 independent reflections
Refinement top
Refinement on F2Primary atom site location: Kvick et al., (1979)
Least-squares matrix: fullHydrogen site location: inferred from neighbouring sites
R[F2 > 2σ(F2)] = 0.076H-atom parameters not refined
wR(F2) = 0.198 w = 1/[σ2(F2) + ( 0.08P)2 + 2.28P]
where P = (max(Fo2,0) + 2Fc2)/3
S = 1.05(Δ/σ)max = 0.000031
455 reflectionsΔρmax = 0.40 e Å3
37 parametersΔρmin = 0.38 e Å3
17 restraints
Crystal data top
C4H8N2O3V = 532.44 (5) Å3
Mr = 132.12Z = 4
Monoclinic, P21/cMo Kα radiation
a = 7.6428 (3) ŵ = 0.14 mm1
b = 9.3800 (4) ÅT = 293 K
c = 7.6505 (5) Å0.20 × 0.20 × 0.10 mm
β = 103.882 (4)°
Data collection top
Bruker APEX II
diffractometer
471 independent reflections
Absorption correction: multi-scan
SADABS (Siemens, 1996)
360 reflections with I > 2.00u(I)
Tmin = 0.85, Tmax = 0.99Rint = 0.052
2911 measured reflections
Refinement top
R[F2 > 2σ(F2)] = 0.07617 restraints
wR(F2) = 0.198H-atom parameters not refined
S = 1.05Δρmax = 0.40 e Å3
455 reflectionsΔρmin = 0.38 e Å3
37 parameters
Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å2) top
xyzUiso*/Ueq
C20.5163 (6)0.3329 (5)0.2639 (10)0.0180 (12)*
N20.3837 (5)0.4101 (4)0.1660 (9)0.0206 (12)*
C30.2365 (7)0.3412 (5)0.0389 (11)0.0225 (13)*
C40.1398 (6)0.4440 (5)0.1066 (9)0.0191 (13)*
O20.1754 (5)0.5737 (4)0.0883 (8)0.0278 (11)*
O30.0287 (5)0.3884 (4)0.2360 (8)0.0360 (13)*
C10.6572 (7)0.4119 (5)0.4032 (11)0.0216 (14)*
N10.8326 (5)0.3369 (4)0.4307 (9)0.0217 (12)*
O10.5253 (5)0.2024 (4)0.2519 (8)0.0292 (12)*
H20.91610.38410.51330.0263*
H10.86670.33300.32620.0263*
H30.82100.24760.47010.0263*
H40.66990.51100.35870.0258*
H50.61900.41610.51850.0258*
H60.38490.50540.17820.0245*
H70.28580.26030.01980.0267*
H80.14840.30400.10520.0267*
Geometric parameters (Å, º) top
C2—N21.322 (7)C4—O21.247 (6)
C2—C11.515 (8)C4—O31.253 (8)
C2—O11.231 (6)C1—N11.483 (6)
N2—C31.450 (8)C1—H41.003
N2—H60.898C1—H50.994
C3—C41.524 (9)N1—H20.899
C3—H71.000N1—H10.899
C3—H80.998N1—H30.902
N2—C2—C1116.7 (4)O2—C4—O3125.7 (5)
N2—C2—O1123.5 (5)C2—C1—N1109.5 (4)
C1—C2—O1119.8 (4)C2—C1—H4109.0
C2—N2—C3120.1 (4)N1—C1—H4109.3
C2—N2—H6119.9C2—C1—H5109.5
C3—N2—H6120.0N1—C1—H5109.9
N2—C3—C4111.7 (4)H4—C1—H5109.7
N2—C3—H7108.9C1—N1—H2109.4
C4—C3—H7108.7C1—N1—H1109.8
N2—C3—H8109.0H2—N1—H1109.6
C4—C3—H8108.9C1—N1—H3109.3
H7—C3—H8109.6H2—N1—H3109.4
C3—C4—O2118.7 (5)H1—N1—H3109.4
C3—C4—O3115.6 (4)
(glyg30) top
Crystal data top
C4H8N2O3F(000) = 280
Mr = 132.12Dx = 1.714 Mg m3
Monoclinic, P21/cMo Kα radiation, λ = 0.71073 Å
Hall symbol: -P 2ybcCell parameters from 1235 reflections
a = 7.4304 (4) Åθ = 6–53°
b = 9.2896 (7) ŵ = 0.15 mm1
c = 7.5943 (9) ÅT = 293 K
β = 102.465 (7)°Block, colourless
V = 511.84 (8) Å30.20 × 0.20 × 0.10 mm
Z = 4
Data collection top
Bruker APEX II
diffractometer
348 reflections with I > 2.00u(I)
Graphite monochromatorRint = 0.048
ω scansθmax = 26.8°, θmin = 2.8°
Absorption correction: multi-scan
SADABS (Siemens, 1996)
h = 98
Tmin = 0.86, Tmax = 0.99k = 1010
2733 measured reflectionsl = 55
451 independent reflections
Refinement top
Refinement on F2Primary atom site location: Kvick et al., (1979)
Least-squares matrix: fullHydrogen site location: inferred from neighbouring sites
R[F2 > 2σ(F2)] = 0.075H-atom parameters not refined
wR(F2) = 0.189 w = 1/[σ2(F2) + ( 0.08P)2 + 1.99P]
where P = (max(Fo2,0) + 2Fc2)/3
S = 1.04(Δ/σ)max = 0.000042
434 reflectionsΔρmax = 0.38 e Å3
37 parametersΔρmin = 0.35 e Å3
17 restraints
Crystal data top
C4H8N2O3V = 511.84 (8) Å3
Mr = 132.12Z = 4
Monoclinic, P21/cMo Kα radiation
a = 7.4304 (4) ŵ = 0.15 mm1
b = 9.2896 (7) ÅT = 293 K
c = 7.5943 (9) Å0.20 × 0.20 × 0.10 mm
β = 102.465 (7)°
Data collection top
Bruker APEX II
diffractometer
451 independent reflections
Absorption correction: multi-scan
SADABS (Siemens, 1996)
348 reflections with I > 2.00u(I)
Tmin = 0.86, Tmax = 0.99Rint = 0.048
2733 measured reflections
Refinement top
R[F2 > 2σ(F2)] = 0.07517 restraints
wR(F2) = 0.189H-atom parameters not refined
S = 1.04Δρmax = 0.38 e Å3
434 reflectionsΔρmin = 0.35 e Å3
37 parameters
Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å2) top
xyzUiso*/Ueq
C20.5186 (6)0.3349 (5)0.2671 (9)0.0183 (12)*
N20.3838 (5)0.4116 (4)0.1676 (8)0.0193 (11)*
C30.2380 (6)0.3406 (5)0.0406 (10)0.0216 (13)*
C40.1405 (6)0.4433 (5)0.1046 (9)0.0172 (12)*
O20.1757 (5)0.5747 (4)0.0868 (7)0.0266 (11)*
O30.0294 (5)0.3870 (4)0.2341 (8)0.0331 (12)*
C10.6579 (6)0.4149 (5)0.4052 (10)0.0206 (13)*
N10.8378 (5)0.3392 (4)0.4331 (8)0.0225 (12)*
O10.5283 (5)0.2027 (4)0.2550 (7)0.0279 (11)*
H20.92160.38670.51570.0273*
H10.87570.33470.32860.0273*
H30.82480.24890.47300.0273*
H40.67200.51480.36010.0250*
H50.61540.41950.52050.0250*
H60.38300.50760.18010.0227*
H70.29210.26030.01890.0255*
H80.14610.30140.10600.0255*
Geometric parameters (Å, º) top
C2—N21.325 (7)C4—O21.250 (5)
C2—C11.501 (7)C4—O31.254 (7)
C2—O11.235 (5)C1—N11.484 (6)
N2—C31.445 (7)C1—H41.003
N2—H60.898C1—H50.994
C3—C41.518 (8)N1—H20.898
C3—H71.001N1—H10.899
C3—H80.996N1—H30.903
N2—C2—C1117.1 (4)O2—C4—O3125.4 (5)
N2—C2—O1122.7 (4)C2—C1—N1109.2 (4)
C1—C2—O1120.1 (4)C2—C1—H4109.0
C2—N2—C3120.1 (4)N1—C1—H4109.3
C2—N2—H6119.7C2—C1—H5109.6
C3—N2—H6120.2N1—C1—H5110.0
N2—C3—C4111.7 (4)H4—C1—H5109.7
N2—C3—H7108.9C1—N1—H2109.5
C4—C3—H7108.4C1—N1—H1109.9
N2—C3—H8109.3H2—N1—H1109.7
C4—C3—H8108.7C1—N1—H3109.2
H7—C3—H8109.7H2—N1—H3109.3
C3—C4—O2118.6 (5)H1—N1—H3109.3
C3—C4—O3115.9 (4)
(glyg37) top
Crystal data top
C4H8N2O3F(000) = 280
Mr = 132.12Dx = 1.758 Mg m3
Monoclinic, P21/cMo Kα radiation, λ = 0.71073 Å
Hall symbol: -P 2ybcCell parameters from 1211 reflections
a = 7.3100 (15) Åθ = 6–53°
b = 9.232 (2) ŵ = 0.15 mm1
c = 7.550 (3) ÅT = 293 K
β = 101.51 (3)°Block, colourless
V = 499.3 (3) Å30.20 × 0.20 × 0.10 mm
Z = 4
Data collection top
Bruker APEX II
diffractometer
332 reflections with I > 2.00u(I)
Graphite monochromatorRint = 0.048
ω scansθmax = 26.9°, θmin = 2.8°
Absorption correction: multi-scan
SADABS (Siemens, 1996)
h = 98
Tmin = 0.84, Tmax = 0.99k = 1010
2678 measured reflectionsl = 55
435 independent reflections
Refinement top
Refinement on F2Primary atom site location: Kvick et al., (1979)
Least-squares matrix: fullHydrogen site location: inferred from neighbouring sites
R[F2 > 2σ(F2)] = 0.068H-atom parameters not refined
wR(F2) = 0.163 w = 1/[σ2(F2) + ( 0.05P)2 + 2.18P]
where P = (max(Fo2,0) + 2Fc2)/3
S = 1.04(Δ/σ)max = 0.000042
419 reflectionsΔρmax = 0.31 e Å3
37 parametersΔρmin = 0.30 e Å3
17 restraints
Crystal data top
C4H8N2O3V = 499.3 (3) Å3
Mr = 132.12Z = 4
Monoclinic, P21/cMo Kα radiation
a = 7.3100 (15) ŵ = 0.15 mm1
b = 9.232 (2) ÅT = 293 K
c = 7.550 (3) Å0.20 × 0.20 × 0.10 mm
β = 101.51 (3)°
Data collection top
Bruker APEX II
diffractometer
435 independent reflections
Absorption correction: multi-scan
SADABS (Siemens, 1996)
332 reflections with I > 2.00u(I)
Tmin = 0.84, Tmax = 0.99Rint = 0.048
2678 measured reflections
Refinement top
R[F2 > 2σ(F2)] = 0.06817 restraints
wR(F2) = 0.163H-atom parameters not refined
S = 1.04Δρmax = 0.31 e Å3
419 reflectionsΔρmin = 0.30 e Å3
37 parameters
Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å2) top
xyzUiso*/Ueq
C20.5201 (6)0.3365 (5)0.2673 (9)0.0185 (12)*
N20.3840 (5)0.4127 (4)0.1685 (8)0.0180 (11)*
C30.2390 (6)0.3411 (5)0.0401 (10)0.0197 (12)*
C40.1420 (6)0.4432 (5)0.1037 (9)0.0163 (12)*
O20.1770 (5)0.5760 (4)0.0861 (7)0.0259 (10)*
O30.0294 (5)0.3866 (4)0.2322 (8)0.0300 (11)*
C10.6588 (6)0.4168 (5)0.4061 (10)0.0198 (13)*
N10.8408 (5)0.3403 (4)0.4349 (8)0.0202 (11)*
O10.5306 (5)0.2029 (4)0.2570 (7)0.0266 (11)*
H20.92460.38810.51790.0249*
H10.88200.33570.33030.0249*
H30.82660.24960.47480.0249*
H40.67460.51740.36090.0242*
H50.61310.42170.52130.0242*
H60.38120.50910.18210.0210*
H70.29660.26140.02010.0228*
H80.14500.30030.10490.0228*
Geometric parameters (Å, º) top
C2—N21.321 (7)C4—O21.253 (5)
C2—C11.501 (8)C4—O31.255 (7)
C2—O11.239 (5)C1—N11.484 (6)
N2—C31.446 (7)C1—H41.004
N2—H60.897C1—H50.993
C3—C41.504 (8)N1—H20.899
C3—H71.001N1—H10.900
C3—H80.994N1—H30.903
N2—C2—C1117.3 (4)O2—C4—O3125.3 (5)
N2—C2—O1122.9 (4)C2—C1—N1109.2 (4)
C1—C2—O1119.6 (4)C2—C1—H4109.1
C2—N2—C3120.3 (4)N1—C1—H4109.2
C2—N2—H6119.7C2—C1—H5109.6
C3—N2—H6120.0N1—C1—H5110.0
N2—C3—C4112.0 (4)H4—C1—H5109.7
N2—C3—H7108.8C1—N1—H2109.6
C4—C3—H7108.3C1—N1—H1109.9
N2—C3—H8109.2H2—N1—H1109.5
C4—C3—H8108.7C1—N1—H3109.3
H7—C3—H8109.9H2—N1—H3109.3
C3—C4—O2118.7 (5)H1—N1—H3109.2
C3—C4—O3116.0 (4)
(glyg47) top
Crystal data top
C4H8N2O3F(000) = 280
Mr = 132.12Dx = 1.780 Mg m3
Monoclinic, P21/cMo Kα radiation, λ = 0.71073 Å
Hall symbol: -P 2ybcCell parameters from 1070 reflections
a = 7.2437 (8) Åθ = 6–52°
b = 9.2083 (13) ŵ = 0.15 mm1
c = 7.5328 (17) ÅT = 293 K
β = 101.214 (14)°Block, colourless
V = 492.86 (14) Å30.20 × 0.20 × 0.10 mm
Z = 4
Data collection top
Bruker APEX II
diffractometer
318 reflections with I > 2.00u(I)
Graphite monochromatorRint = 0.052
ω scansθmax = 27.2°, θmin = 2.9°
Absorption correction: multi-scan
SADABS (Siemens, 1996)
h = 98
Tmin = 0.75, Tmax = 0.98k = 1010
2669 measured reflectionsl = 55
437 independent reflections
Refinement top
Refinement on F2Primary atom site location: Kvick et al., (1979)
Least-squares matrix: fullHydrogen site location: inferred from neighbouring sites
R[F2 > 2σ(F2)] = 0.072H-atom parameters not refined
wR(F2) = 0.187 w = 1/[σ2(F2) + ( 0.08P)2 + 2.23P]
where P = (max(Fo2,0) + 2Fc2)/3
S = 1.03(Δ/σ)max = 0.000038
422 reflectionsΔρmax = 0.35 e Å3
37 parametersΔρmin = 0.33 e Å3
17 restraints
Crystal data top
C4H8N2O3V = 492.86 (14) Å3
Mr = 132.12Z = 4
Monoclinic, P21/cMo Kα radiation
a = 7.2437 (8) ŵ = 0.15 mm1
b = 9.2083 (13) ÅT = 293 K
c = 7.5328 (17) Å0.20 × 0.20 × 0.10 mm
β = 101.214 (14)°
Data collection top
Bruker APEX II
diffractometer
437 independent reflections
Absorption correction: multi-scan
SADABS (Siemens, 1996)
318 reflections with I > 2.00u(I)
Tmin = 0.75, Tmax = 0.98Rint = 0.052
2669 measured reflections
Refinement top
R[F2 > 2σ(F2)] = 0.07217 restraints
wR(F2) = 0.187H-atom parameters not refined
S = 1.03Δρmax = 0.35 e Å3
422 reflectionsΔρmin = 0.33 e Å3
37 parameters
Fractional atomic coordinates and isotropic or equivalent isotropic displacement parameters (Å2) top
xyzUiso*/Ueq
C20.5214 (6)0.3376 (5)0.2692 (10)0.0177 (13)*
N20.3849 (6)0.4133 (4)0.1709 (9)0.0181 (12)*
C30.2395 (7)0.3405 (5)0.0407 (11)0.0195 (13)*
C40.1426 (6)0.4434 (5)0.1027 (10)0.0183 (13)*
O20.1782 (5)0.5760 (4)0.0852 (8)0.0252 (11)*
O30.0300 (5)0.3862 (4)0.2332 (8)0.0301 (12)*
C10.6607 (7)0.4177 (5)0.4085 (11)0.0198 (14)*
N10.8432 (6)0.3422 (5)0.4362 (9)0.0203 (12)*
O10.5317 (5)0.2038 (4)0.2573 (8)0.0262 (12)*
H20.92700.39010.51970.0244*
H10.88460.33950.33100.0244*
H30.82940.25100.47460.0244*
H40.67580.51900.36570.0237*
H50.61450.42070.52520.0237*
H60.38140.51030.18420.0217*
H70.29850.26040.01870.0235*
H80.14400.29880.10590.0235*
Geometric parameters (Å, º) top
C2—N21.314 (7)C4—O21.250 (6)
C2—C11.501 (8)C4—O31.264 (8)
C2—O11.239 (6)C1—N11.472 (6)
N2—C31.456 (8)C1—H41.000
N2—H60.900C1—H51.000
C3—C41.504 (9)N1—H20.900
C3—H71.000N1—H10.900
C3—H81.000N1—H30.900
N2—C2—C1117.6 (4)O2—C4—O3125.3 (5)
N2—C2—O1122.4 (5)C2—C1—N1109.3 (4)
C1—C2—O1119.8 (4)C2—C1—H4109.5
C2—N2—C3120.1 (4)N1—C1—H4109.5
C2—N2—H6119.9C2—C1—H5109.5
C3—N2—H6120.0N1—C1—H5109.5
N2—C3—C4111.7 (4)H4—C1—H5109.5
N2—C3—H7108.9C1—N1—H2109.5
C4—C3—H7108.9C1—N1—H1109.5
N2—C3—H8108.9H2—N1—H1109.5
C4—C3—H8108.9C1—N1—H3109.5
H7—C3—H8109.5H2—N1—H3109.5
C3—C4—O2118.8 (5)H1—N1—H3109.5
C3—C4—O3115.9 (4)

Experimental details

(glyg00)(glyg14)(glyg30)(glyg37)
Crystal data
Chemical formulaC4H8N2O3C4H8N2O3C4H8N2O3C4H8N2O3
Mr132.12132.12132.12132.12
Crystal system, space groupMonoclinic, P21/cMonoclinic, P21/cMonoclinic, P21/cMonoclinic, P21/c
Temperature (K)293293293293
a, b, c (Å)8.1233 (18), 9.554 (2), 7.8224 (17)7.6428 (3), 9.3800 (4), 7.6505 (5)7.4304 (4), 9.2896 (7), 7.5943 (9)7.3100 (15), 9.232 (2), 7.550 (3)
β (°) 107.596 (4) 103.882 (4) 102.465 (7) 101.51 (3)
V3)578.7 (2)532.44 (5)511.84 (8)499.3 (3)
Z4444
Radiation typeMo KαMo KαMo KαMo Kα
µ (mm1)0.130.140.150.15
Crystal size (mm)0.60 × 0.36 × 0.120.20 × 0.20 × 0.100.20 × 0.20 × 0.100.20 × 0.20 × 0.10
Data collection
DiffractometerBruker APEX
diffractometer
Bruker APEX II
diffractometer
Bruker APEX II
diffractometer
Bruker APEX II
diffractometer
Absorption correctionMulti-scan
SADABS (Siemens, 1996)
Multi-scan
SADABS (Siemens, 1996)
Multi-scan
SADABS (Siemens, 1996)
Multi-scan
SADABS (Siemens, 1996)
Tmin, Tmax0.86, 0.980.85, 0.990.86, 0.990.84, 0.99
No. of measured, independent and
observed [I > 2.00u(I)] reflections
3696, 1390, 1164 2911, 471, 360 2733, 451, 348 2678, 435, 332
Rint0.0270.0520.0480.048
(sin θ/λ)max1)0.6750.6430.6350.637
Refinement
R[F2 > 2σ(F2)], wR(F2), S 0.049, 0.140, 1.01 0.076, 0.198, 1.05 0.075, 0.189, 1.04 0.068, 0.163, 1.04
No. of reflections1385455434419
No. of parameters82373737
No. of restraints0171717
H-atom treatmentH-atom parameters not refinedH-atom parameters not refinedH-atom parameters not refinedH-atom parameters not refined
Δρmax, Δρmin (e Å3)0.28, 0.350.40, 0.380.38, 0.350.31, 0.30


(glyg47)
Crystal data
Chemical formulaC4H8N2O3
Mr132.12
Crystal system, space groupMonoclinic, P21/c
Temperature (K)293
a, b, c (Å)7.2437 (8), 9.2083 (13), 7.5328 (17)
β (°) 101.214 (14)
V3)492.86 (14)
Z4
Radiation typeMo Kα
µ (mm1)0.15
Crystal size (mm)0.20 × 0.20 × 0.10
Data collection
DiffractometerBruker APEX II
diffractometer
Absorption correctionMulti-scan
SADABS (Siemens, 1996)
Tmin, Tmax0.75, 0.98
No. of measured, independent and
observed [I > 2.00u(I)] reflections
2669, 437, 318
Rint0.052
(sin θ/λ)max1)0.642
Refinement
R[F2 > 2σ(F2)], wR(F2), S 0.072, 0.187, 1.03
No. of reflections422
No. of parameters37
No. of restraints17
H-atom treatmentH-atom parameters not refined
Δρmax, Δρmin (e Å3)0.35, 0.33

Computer programs: SMART (Siemens, 1993), SAINT (Siemens ,1995), SIR92 (Altomare et al., 1994), USER DEFINED STRUCTURE SOLUTION, CRYSTALS (Betteridge et al., 2003), CAMERON (Watkin et al., 1996).

Selected geometric parameters (Å, º) for (glyg00) top
C2—N21.3263 (19)C3—C41.521 (2)
C2—C11.517 (2)C4—O21.2474 (19)
C2—O11.2280 (19)C4—O31.2440 (19)
N2—C31.4540 (19)C1—N11.4763 (19)
N2—C2—C1116.03 (13)C3—C4—O2118.59 (13)
N2—C2—O1123.62 (14)C3—C4—O3115.21 (14)
C1—C2—O1120.28 (13)O2—C4—O3126.20 (15)
C2—N2—C3120.93 (13)C2—C1—N1109.45 (12)
N2—C3—C4112.54 (13)
Selected geometric parameters (Å, º) for (glyg14) top
C2—N21.322 (7)C3—C41.524 (9)
C2—C11.515 (8)C4—O21.247 (6)
C2—O11.231 (6)C4—O31.253 (8)
N2—C31.450 (8)C1—N11.483 (6)
N2—C2—C1116.7 (4)C3—C4—O2118.7 (5)
N2—C2—O1123.5 (5)C3—C4—O3115.6 (4)
C1—C2—O1119.8 (4)O2—C4—O3125.7 (5)
C2—N2—C3120.1 (4)C2—C1—N1109.5 (4)
N2—C3—C4111.7 (4)
Selected geometric parameters (Å, º) for (glyg30) top
C2—N21.325 (7)C3—C41.518 (8)
C2—C11.501 (7)C4—O21.250 (5)
C2—O11.235 (5)C4—O31.254 (7)
N2—C31.445 (7)C1—N11.484 (6)
N2—C2—C1117.1 (4)C3—C4—O2118.6 (5)
N2—C2—O1122.7 (4)C3—C4—O3115.9 (4)
C1—C2—O1120.1 (4)O2—C4—O3125.4 (5)
C2—N2—C3120.1 (4)C2—C1—N1109.2 (4)
N2—C3—C4111.7 (4)
Selected geometric parameters (Å, º) for (glyg37) top
C2—N21.321 (7)C3—C41.504 (8)
C2—C11.501 (8)C4—O21.253 (5)
C2—O11.239 (5)C4—O31.255 (7)
N2—C31.446 (7)C1—N11.484 (6)
N2—C2—C1117.3 (4)C3—C4—O2118.7 (5)
N2—C2—O1122.9 (4)C3—C4—O3116.0 (4)
C1—C2—O1119.6 (4)O2—C4—O3125.3 (5)
C2—N2—C3120.3 (4)C2—C1—N1109.2 (4)
N2—C3—C4112.0 (4)
Selected geometric parameters (Å, º) for (glyg47) top
C2—N21.314 (7)C3—C41.504 (9)
C2—C11.501 (8)C4—O21.250 (6)
C2—O11.239 (6)C4—O31.264 (8)
N2—C31.456 (8)C1—N11.472 (6)
N2—C2—C1117.6 (4)C3—C4—O2118.8 (5)
N2—C2—O1122.4 (5)C3—C4—O3115.9 (4)
C1—C2—O1119.8 (4)O2—C4—O3125.3 (5)
C2—N2—C3120.1 (4)C2—C1—N1109.3 (4)
N2—C3—C4111.7 (4)
 

Footnotes

1Supplementary data for this paper are available from the IUCr electronic archives (Reference: GP5004 ). Services for accessing these data are described at the back of the journal.

Acknowledgements

We would like to thank Dr Josh McKinnon for his help with the program CrystalExplorer, the EPSRC and The University of Edinburgh for funding.

References

First citationAllen, F. H. (2002). Acta Cryst. B58, 380–388.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationAllen, F. H., Baalham, C. A., Lommerse, J. P. M. & Raithby, P. R. (1998). Acta Cryst. B54, 320–329.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationAllen, F. H. & Motherwell, W. D. S. (2002). Acta Cryst. B58, 407–422.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationBernal, J. D. (1931). Z. Kristallogr. Kristallgeom. Kristallphys. Kristallchem. 78, 363–369.  CAS Google Scholar
First citationBernstein, J., Davis, R. E., Shimoni, L. & Chang, N.-L. (1995). Angew. Chem. Int. Ed. Engl. 34, 1555–1573.  CrossRef CAS Web of Science Google Scholar
First citationBetteridge, P. W., Carruthers, J. R., Cooper, R. I., Prout, K. & Watkin, D. J. (2003). J. Appl. Cryst. 36, 1487.  Web of Science CrossRef IUCr Journals Google Scholar
First citationBoldyreva, E. V. (2003). J. Mol. Struct. 647, 159–179.  Web of Science CrossRef CAS Google Scholar
First citationBoldyreva, E. V., Ivashevskaya, S. N., Sowa, H., Ahsbahs, H. & Weber, H.-P. (2004). Dokl. Phys. Chem. 396, 111–114.  Web of Science CrossRef CAS Google Scholar
First citationBoldyreva, E. V., Kolesnik, E. N., Drebushchak, T. N., Ahsbahs, H., Beukes, J. A. & Weber, H.-P. (2005). Z. Kristallogr. 220, 58–65.  Web of Science CSD CrossRef CAS Google Scholar
First citationBrand, H. V. (2005). J. Phys. Chem. B, 109, 13668–13675.  Web of Science CrossRef PubMed CAS Google Scholar
First citationBruker–Nonius (2002). SMART. Bruker–Nonius, Madison, Wisconsin, USA.  Google Scholar
First citationBruker–Nonius (2004a). SAINT, Version V7.12A. Bruker–Nonius, Madison, Wisconsin, USA.  Google Scholar
First citationBruker–Nonius (2004b). APEX-II, Version V1. Bruker–Nonius, Madison, Wisconsin, USA.  Google Scholar
First citationChatterjee, A. & Parthasarathy, R. (1984). Int. J. Pept. Protein Res. 24, 447–452.  CrossRef CAS PubMed Web of Science Google Scholar
First citationCrystal Impact (2004). DIAMOND, Version 3.0. Crystal Impact GbR, Postfach 1251, 53002 Bonn, Germany. http://www.crystalimpact.com/diamondGoogle Scholar
First citationDawson, A., Allan, D. R., Belmonte, S. A., Clark, S. J., David,W. I. F., McGregor, P. A., Parsons, S., Pulham, C. R. & Sawyer, L. (2005). Cryst. Growth Des. 5, 1415–1427.  Web of Science CSD CrossRef CAS Google Scholar
First citationDawson, A., Allan, D. R., Clark, S. J., Parsons, S. & Ruf, M. (2004). J. Appl. Cryst. 37, 410–416.  Web of Science CSD CrossRef CAS IUCr Journals Google Scholar
First citationDerewenda, Z. S., Lee, L. & Derewenda, U. (1995). J. Mol. Biol. 252, 248–262.  CrossRef CAS PubMed Web of Science Google Scholar
First citationDesiraju, G. R. & Steiner, T. (1999). The Weak Hydrogen Bond in Structural Chemistry and Biology. IUCr Monographs on Crystallography No. 9. Oxford Univerity Press.  Google Scholar
First citationFabiola, G. F., Krishnaswamy, S., Nagarajan, V. & Pattabhi, V. (1997). Acta Cryst. D53, 316–320.  CrossRef CAS Web of Science IUCr Journals Google Scholar
First citationFarrugia, L. J. (1999). J. Appl. Cryst. 32, 837–838.  CrossRef CAS IUCr Journals Google Scholar
First citationGirard, E., Kahn, R., Mezouar, M., Dhaussy, A.-C., Lin, T., Johnson, J. E. & Fourme, R. (2005). Biophys. J. 88, 3562–3571.  Web of Science CrossRef PubMed CAS Google Scholar
First citationGörbitz, C. H. (1989). Acta Cryst. B45, 390–395.  CrossRef Web of Science IUCr Journals Google Scholar
First citationGörbitz, C. H. (2002). Acta Cryst. B58, 512–518.  Web of Science CSD CrossRef IUCr Journals Google Scholar
First citationHazen, R. M. & Finger, L. W. (1982). Comparative Crystal Chemistry, pp. 80–82. New York: John Wiley and Sons.  Google Scholar
First citationHughes, E. W. & Moore, W. J. (1949). J. Am. Chem. Soc. 71, 2618–2623.  CSD CrossRef CAS Web of Science Google Scholar
First citationJeffrey, G. A. & Maluszynska, H. (1982). Int. J. Biol. Macromol. 3, 173–185.  CrossRef Web of Science Google Scholar
First citationKapplinger, I., Keutel, H. & Jager, E. G. (1999). Inorg. Chim. Acta, 291, 190–206.  Web of Science CSD CrossRef CAS Google Scholar
First citationKatrusiak, A. (1990a). High Press. Res. 4, 496–498.  CrossRef Google Scholar
First citationKatrusiak, A. (1990b). Acta Cryst. B46, 246–256.  CSD CrossRef CAS Web of Science IUCr Journals Google Scholar
First citationKatrusiak, A. (1992). J. Mol. Struct. 269, 329–354.  CSD CrossRef CAS Web of Science Google Scholar
First citationKatrusiak, A. (2004). High-Pressure Crystallography, edited by A. Katrusiak & P. F. McMillan, pp. 513–520. Dordrecht: Kluwer Academic Publishers.  Google Scholar
First citationKatrusiak, A. & Nelmes, R. J. (1986). J. Phys. C Solid State Phys. 19, L765–L772.  CSD CrossRef CAS Web of Science Google Scholar
First citationKvick, Å., Karaghouli, A. R. & Koetzle, T. F. (1977). Acta Cryst. B33, 3796–3801.  CSD CrossRef CAS IUCr Journals Web of Science Google Scholar
First citationMaccallum, P. H., Poet, R. & Milner-White, J. E. (1995). J. Mol. Biol. 248, 361–373.  CrossRef CAS PubMed Web of Science Google Scholar
First citationMerrill, L. & Bassett, W. A. (1974). Rev. Sci. Instrum. 45, 290–294.  CrossRef Web of Science Google Scholar
First citationMcKinnon, J. J., Spackman, M. A. & Mitchell, A. S. (2004). Acta Cryst. B60, 627–668.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationMoggach, S. A., Allan, D. R., Lozano-Casal, P. & Parsons, S. (2005). J. Synchrotron Rad. 12, 590–597.  Web of Science CSD CrossRef CAS IUCr Journals Google Scholar
First citationMoggach, S. A., Allan, D. R., Morrison, C. A., Parsons, S. & Sawyer, L. (2005). Acta Cryst. B61, 58–68.  Web of Science CSD CrossRef CAS IUCr Journals Google Scholar
First citationMoggach, S. A., Allan, D. R., Parsons, S., Sawyer, L. & Warren, J. E. (2005). J. Synchrotron Rad. 12, 598–607.  Web of Science CSD CrossRef CAS IUCr Journals Google Scholar
First citationParsons, S. (2004). SHADE. The University of Edinburgh, Scotland.  Google Scholar
First citationPiermarini, G. J., Block, S., Barnett, J. D. & Forman, R. A. (1975). J. Appl. Phys. 46, 2774–2780.  CrossRef CAS Web of Science Google Scholar
First citationSheldrick, G. M. (1997). XP. University of Göttingen, Germany.  Google Scholar
First citationSheldrick, G. M. (2004). SADABS. University of Göttingen, Germany.  Google Scholar
First citationSpek, A. L. (2003). J. Appl. Cryst. 36, 7–13.  Web of Science CrossRef CAS IUCr Journals Google Scholar
First citationSteiner, T. (1997). Acta Cryst. C53, 730–732.  CSD CrossRef CAS Web of Science IUCr Journals Google Scholar
First citationVoet, D. & Voet, J. G. (1995). Biochemistry, 2nd ed. New York: Wiley.  Google Scholar
First citationWolff, S. K., Grimwood, D. J., McKinnon, J. J., Jayatilaka, D. & Spackman, M. A. (2005). CrystalExplorer, Version 1.5. University of Western Australia. http://www.Theochem.uwa.edu.au/crystal_explorer/Google Scholar

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