ARTICLE pubs.acs.org/crystal
Three-Dimensional Water Channel Embedded in an r,γ-Cyclic Octapeptide-Derived Organic Porous Material Manuel Amorín,† Antonio L. Llamas-Saiz,‡ Luis Castedo,† and Juan R. Granja*,† †
Departamento de Química Organica y Unidad Asociada al C.S.I.C. Centro Singular de Investigacion en Química Biologica y Materiales Moleculares (CIQUS), Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain ‡ Unidad de Rayos X; RIAIDT Edificio CACTUS, Universidad de Santiago de Compostela, 15782 Santiago de Compostela, Spain
bS Supporting Information ABSTRACT: A dual behavior for water is described, in which the water molecules play an active role in inducing a cyclic peptide to fold and assemble to produce a novel three-dimensional porous organic solid without any interpeptide hydrogen bonds, and at the same time, the water molecules fill the voids left by the cyclic peptide (CP) aggregate to form highly ordered 3D water channels at room temperature through large interconnected water clusters. Once the crystal is taken out of the mother liquor, it slowly loses its water content while increasing its crystal symmetry from P21 to I2.
’ INTRODUCTION Liquid water is one of the most important and mysterious substances in our world as a result of its fundamental importance in practically every area of human activity and the fascinating array of unusual properties that it exhibits.1,2 Many of the anomalous properties of liquid water are attributed to its unique structure, which comprises a random and fluctuating threedimensional network of hydrogen bonds that link the water molecules.3 To understand the bulk water structure would not only explain the water properties but also gain a better insight into the world of many biomolecules, which achieve their function by interacting with structured water.4 Structural studies on discrete water clusters, most of the time captured within the lattice of a crystal host, have significantly advanced our knowledge toward the first step of understanding the behavior of bulk water.5 In order to increase our understanding of the structure of water it is necessary to grow larger water clusters and determine how they link to form large networks, a situation that is the bridge between clusters and bulk water, in a well-defined environment of appropriate dimensionality, such us within carbon nanotubes, zeolites, and other porous materials.6 Porous materials are of scientific and technological interest because of their ability to interact with atoms, ions, and molecules not only at their surface but throughout the bulk material.7 Thus those materials might be of interest because it has been assumed that the water structure confined in nanoscale spaces would be different from that of the bulk. In addition the interaction of the ordered water with biological-related materials such as organic porous materials is also of essential significance because it might shed light on protein folding or pressure-induced unfolding processes in which water transport out of and into the protein interior is playing an important role.8 Particularly intriguing is the conjecture that matter within the narrow confines of hydrophobic nanopores r 2011 American Chemical Society
might exhibit a solid liquid critical point beyond which the distinction between solid and liquid phases disappears.9 11 Herein, we report a dual behavior for water: on the one hand, the water molecules may play an active role in inducing a cyclic peptide to fold and assemble to produce a novel three-dimensional porous organic material without any direct hydrogen bonds among CP molecules, and on the other hand, the water molecules interconnect the CP units to form highly ordered 3D water channels inside the crystal at room temperature. The resulting water structure is made of several different interconnected water clusters that could help to better understand how the clusters are linked to form large networks. We believe that the water structure described here sheds light on yet another novel mode of cooperative association between water molecules and the relation between biopolymer folding and water structure.4,8
’ EXPERIMENTAL SECTION Peptide Synthesis. Peptide cyclo[(D-MeN-Ala-L-γ-Ach)4 ] (r,γ-
CP1a) was prepared following the synthetic strategy described previously.12
Preparation of Peptide Single Crystals for X-ray Analysis. Different crystallizations were carried out. HPLC-purified r,γ-CP1a (2 3 mg) was dissolved in CHCl3 (0.5 mL) and equilibrated by vaporphase diffusion against hexanes (5 mL). This resulted in spontaneous crystallization after 2 5 days. Similar crystallization trials gave rise to a mixture of two types of crystals that were indistinguishable by optical microscopy but displayed very different structures: one with planar cyclopeptides that formed dimers and another with twisted monomers that led to a water channel structure. Peptide r,γ-CP1a (2 3 mg) was dissolved in CHCl3 (0.5 mL), dried over Na2SO4, and equilibrated by Received: August 25, 2010 Revised: June 14, 2011 Published: June 20, 2011 3351
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Scheme 1. Structures of r,γ-Cyclic Octapeptides (r,γ-CP1a, r,γ-CP1b, and r,γ-CP1c) and Their Corresponding SPN (r,γ-SPN1c) and Dimers (r,γ-D1a and r,γ-D1b), Illustrating the Two β-Sheet Structures Present in the Nanotubea
a
For clarity, some amino acid side chains have been omitted in the representations of the nanotube and dimers.
vapor-phase diffusion against hexanes (5 mL). This resulted in spontaneous crystallization after 2 3 days. These crystals had a dimeric structure in all cases.12 Alternatively, a solution of r,γ-CP1a (2 3 mg) in wet CHCl3 (0.5 mL), after shaking with H2O, was equilibrated by vapor-phase diffusion against hexanes (5 mL). This process resulted in spontaneous crystallization after 3 5 days of the water channel structure in all cases. Crystals of the monomeric form grown in wet CHCl3 were found presenting either space group P21 or I2 with very similar unit cell parameters; they contained four r,γ-CP1a cyclic peptides and up to 66 water molecules in the unit cell. X-ray Crystallographic Analysis. The first two crystals were taken from the same crystallization trial. Diffraction data for the first crystal were collected soon after sizable crystals appeared in the vapor diffusion equilibrium (crystal A). Data for the second crystal were measured 30 days later with the vial open to air in the refrigerator and all of the mother liquor evaporated (crystal B). Data collection was performed with a Nonius FR591 Kappa CCD2000 diffractometer with Cu KR radiation (λ = 1.54178 Å) and a confocal multilayer mirror monochromator for crystal A and a Bruker Kappa APEXII with Mo KR radiation (λ = 0.71073 Å) and a graphite monochromator for B. Crystal cell constants were calculated by least-squares global refinement. Raw images were integrated using HKL200013 or APEX2,14 and the resulting intensities were scaled and corrected from absorption using SADABS.15 The structures were solved by direct methods with SIR200416 and refined by constrained full least-squares on F2 with SHELXL.17 Crystal data for A: 2(C44H72N8O8) 3 30.10H2O, colorless block, 0.50 0.35 0.23 mm3, monoclinic, space group P21, a = 14.3497(4), b = 26.8857(6), c = 16.5038(4) Å, β = 105.869(1), V = 6124.5(3) Å3, Z = 2, F(000) = 2424, T = 100(2) K, μ(Cu KR) = 0.808 mm 1, 4.6 e 2Θ e 130.5; 62 528 reflections measured, 10 653 independent reflections (Rint =0.0963, Friedel pairs merged), 1452 parameters, 1814 restraints; final R1[I > 2σ(I)] = 0.1055, wR2 (all data) = 0.3246, min/max difference electron density 0.77/0.86 e Å 3. Crystal data for B: 2(C44H72N8O8) 3 31.12H2O, colorless prism, 0.35 0.30 0.22 mm3, monoclinic, space group I2, a = 14.2481(5), b = 26.9980(6), c = 16.4923(3) Å, β = 106.211(1), V = 6091.9(3) Å3, Z = 2, F(000) = 2484, T = 100(2) K, μ(Mo KR) = 0.100 mm 1, 3.0 e 2Θ e 56.7; 61 302 reflections measured, 7720 independent reflections (Rint = 0.0374, Friedel pairs merged), 788 parameters, 1007 restraints; final R1 [I > 2σ(I)] = 0.0780, wR2 (all data) = 0.2486, min/max difference electron density 0.65/0.71 e Å 3. Crystallographic details for crystal A collected at T = 150 K and T = 200 K and those for crystals C, D, E, F, G, and H
are included in Supporting Information. These data can be obtained free of charge from the Cambridge Crystallographic Data Centre via http://www. ccdc.cam.ac.uk/data_request/cif (accession numbers are CCDC-762589 to CCDC-762597 for crystals A, A (T = 150 K), A (T = 200 K), B, C, D, E, F, and G, respectively, and CCDC-781764 for H).
’ RESULTS AND DISCUSSION Recently, we started a program aimed at the development of functional self-assembling peptide nanotubes (SPNs) from cyclic peptides containing cyclic γ-amino acids such as 3-aminocyclohexanecarboxylic acid (γ-Ach) (Scheme 1).11,18 Our original studies concerned simple dimeric models, based on N-methylated CPs, that mimic the β-sheet type hydrogen-bonding interactions present in R,γ-SPNs with the aim of establishing the structural and thermodynamical requirements for nanotube formation.12,19,20 For example, cyclic octapeptides r,γ-CP1a and r,γCP1b form the corresponding dimers r,γ-D1a and r,γ-D1b in nonpolar solvents,12 with the second system (r,γ-D1b) at least 3 orders of magnitude more stable than the dimer (r,γ-D1a) that interacts through its γ-face. Although the formation of these systems was attributed mainly to the steric repulsion between the N-methyl groups and carbonyl oxygens of the R-amino acids,12,21 DFT calculations showed that r,γ-CP1a tends to adopt conformations that deviate from planarity, such as the horse-chair-like conformation (Figure 1a-left), in which the formation of intramolecular hydrogen bonds between the carbonyl and NH groups of each γ-Ach contributes to shift the equilibrium toward the monomeric form.22 The dimeric structure r,γ-D1a was finally confirmed by X-ray crystallography of single crystals obtained by crystallization from CHCl3/CCl4.12 Interestingly, a new crystal type (A crystal) was obtained from CHCl3/hexanes when wet chloroform was used. Under these conditions, the CP is folded into a distorted structure that has C1 point group symmetry and is packed in the P21 space group with two complete CP molecules in the asymmetric unit. In this case, neither intra- nor intermolecular hydrogen bonds were formed between the NH and carbonyl groups of the CP (Figure 1a, right), with these groups instead hydrogen bonded to 14 water molecules, four through the amide protons and ten to the carbonyl groups, thus forming the first hydration 3352
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Table 1. Crystal history, Estimated Water Content and Molecular Distortion Data for the Eight Analyzed Crystalsa space
cryst
age
group
trial
(days)
solventb
WCIc
I/σ(I)d
rms
e
A Ae
P21 I2
1 1
1 1
+ +
18.189 16.442
0.67 0.67
0.1924
Af
P21
1
1
+
18.313
0.76
0.1995
Ag
P21
1
1
+
18.462
0.66
0.1768
Be
I2
1
30
15.331
0.29
Be
P21
1
30
14.243
0.29
0.0930
Ce
P21
1
31
15.791
0.58
0.2030
Ce
I2
1
31
16.228
0.58
Dh Dh
P21 I2
2 2
4 4
+ +
18.862 17.509
0.76 0.76
0.1458
Eh
P21
3
1
+
21.083
0.94
0.3588
Eh
I2
3
1
+
21.412
0.94
Fe
P21
4
1
+
16.760
0.50
Fe
I2
4
1
+
14.416
0.50
Ge
I2
5
79
13.995
0.12
Ge
P21
5
79
13.219
0.12
0.0463
He
P21
6
1
21.951
0.96
0.3792
crystal
Figure 1. (a) Molecular conformation of the CP obtained by DFT ab initio calculations (left). Black dashed lines indicate intramolecular hydrogen bonds (left). Overlay of the molecular structure of the CP in the crystal (right) corresponding to one molecule of crystal A (P21 space group) in red and one molecule of crystal B (I2 space group) in green. (b) CP-derived porous materials displayed along the a (left), the b (center), and the c (right) unit cell axes of crystal A. Water network omitted for clarity. Molecular surfaces colored according atom colors: N (blue), O (red), molecule 1 C (green), and molecule 2 C (cyan). (c) Water network displayed along the a (left), the b (center), and the c (right) unit cell axes of crystal A.
shell of each CP molecule in the asymmetric unit. The folded peptides pack to form an organic porous material (Figure 1b) made of 3D-intersecting channels filled with a network of hydrogen bonded water molecules (Figure 1c). Two of the channels are straight and run parallel to the crystallographic a and c axes, respectively, while the third one, along the b axis, is sinuous and as narrow as the one along c. Pore dimensions have been evaluated using the algorithms implemented in Caver23 with a probe sphere of 1.4 Å radius. The channel along the a axis displays maximum and minimum radii of 3.2 and 2.0 Å, respectively, while the channels along b and c are narrower and present approximately the same maximum and minimum radii of 2.5 and 1.5 Å. The peptide packing in the crystal is based on the hydrophobic contacts between the methyl and cyclohexyl groups and a network of hydrogen-bonded water molecules that stabilize the whole crystal packing acting as a “molecular glue”. All NH and the carbonyl groups of γ-Ach point toward the channel along the a axis, while the carbonyl of the R-Aa point toward the channel along c. In addition to the first hydration shell, there are another ten water molecules in the asymmetric unit that are not directly bonded to the CP backbone, but these are saturating hydrogen bonding water coordination and stabilizing the CP second hydration shell structure. The resulting water network (31 main locations for water molecules in the crystallographic asymmetric unit, 7 of them disordered in more than one position) is formed by interconnected small cyclic clusters that create larger clusters, which in turn form the 3D interconnected water channels, vide infra. In order to improve the global quality of the structure, a new set of data was collected on a 30 day old crystal stored in the refrigerator (Table 1). To our surprise, a new, yet very similar, crystal structure was obtained (B crystal), and this has a molecular and crystal structure with higher symmetry (I2 space group).
mean
+
0.1680
a
Plots are in Figure 2. b Crystal taken from its mother liquor (+) or after all solvent evaporated ( ). c WCI: Normalized water content index (see text). d Average I/σ(I) for systematically extinct reflections in I centered crystal lattice (h + k + l = odd). e Data collected at 100 K. f Data at 150 K. g Data at 200 K. h Data at 120 K.
The cyclic peptide molecules are arranged around the crystallographic 2-fold axis with a C2 point group symmetry (two halfmolecules in the asymmetric unit). The small differences in the peptide backbone structure found in the two crystals are shown in Figure 1a, right. In addition, the water network changes, displaying 32 locations for the water molecules in the asymmetric unit (one more than for crystal A) and a higher level of disorder (16 disordered positions versus 7 in crystal A). The first hydration shell of both CP structures is quite different; while all NH groups are always bonded to one water molecule, the hydration of the carbonyl groups is different. In the first structure, five carbonyl groups are hydrogen bonded to two water molecules, ten to one and one to none, while in the second structure six carbonyls are bonded to two waters, eight to one and, finally, two carbonyl groups are not hydrated. This behavior is quite intriguing and demonstrates a different stability for the water molecules and their effects on the folding and packing of the CP in the crystal structure. In order to study these phenomena, we decided to extend our studies to other crystals varying their aging (i.e., time spent from crystal formation to data collection) and storing conditions (kept in mother liquor vapor diffusion equilibrium or open to air). The results of this study are shown in Table 1. Eight crystals from six crystallization trials were analyzed by single-crystal X-ray diffraction, and all of the samples had fairly ordered water content. Two crystals (B and G) display the highest symmetry (I2 space group) as suggested by ÆI/σ(I)æ values lower than 2.0 for the h + k + l = odd reflections. The lowest symmetry was the P21 space group (two complete cyclic peptides in the asymmetric unit), and this was found in crystals A, C, D, E, F, and H.24 To distinguish between these two very similar crystal structures, the diffraction data from all crystals were processed and the structures solved 3353
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Figure 2. Correlation plots. The linear regression and correlation coefficient are in the top right corner. (a) Mean I/σ(I) for the systematically absent reflections in the centered I crystal lattice (h + k + l = odd) vs the normalized water content index; (b) rms deviation along the pseudo-2-fold axes through the cyclic peptide center in P21 vs the normalized water content index.
and refined in both space groups. Experimental crystallographic details for one representative structure of each space group, crystals A and B, are reported above (for more details, see the Supporting Information). Three complete data sets for crystal A (collected at 100, 150, and 200 K) did not show significant differences in crystal packing and the presence of temperaturedependent solid-state phase transitions were ruled out. To explain the different degrees of distortion of the peptide structures, a systematic study of the crystal water content was performed. The positions of all water molecules were included and refined using the “Automatic Water Divining” procedure (SHELXWAT) implemented by Sheldrick25 starting from the first water molecule manually placed at the highest peak in the difference Fourier synthesis. In order to bring the water content in different crystals into a common scale and to minimize small differences in crystal quality or other experimental conditions, a normalized water content index (WCI) was formulated as follows: WCI = ∑(occ/ADP)water/Æ(occ/ADP)CPæ, “occ” being the atomic occupancy and “ADP” the isotropic equivalent of the corresponding anisotropic atomic displacement parameter. The symmetry of the crystals was estimated using the values of ÆI/σ(I)æ for the systematic absent reflections in the I centered crystal lattice (h + k + l = odd). The molecular symmetry was evaluated by means of the rms parameter, root mean square deviation between pairs of pseudo-symmetry-equivalent atoms. The point group symmetry of isolated molecules was determined by following the SYMMOL algorithm26 (Table 1 and Figure 2). The calculated parameters from all crystals (Table 1 and Figure 2) were combined and a clear correlation between the water content in the structure and the symmetry of the CP was established. Good correlation coefficients were obtained either using the diffraction intensity of the systematic extinct reflections
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to check the crystal symmetry (Figure 2a) or the local pseudosymmetry in the refined structure of each CP molecule (Figure 2b). The higher water content implies lower symmetry, that is, more distorted CPs. We found that crystal H has the highest water content; therefore it has been used for all figures unless otherwise stated and to describe the overall structure of the water network. It is formed by 33 main locations for water molecules in the crystallographic asymmetric unit. Some of these waters are disordered in more than one position depending on the crystal analyzed, ranging from five partially occupied positions in E to 16 in B. The water network is formed by interconnected small cyclic clusters (four- to seven-membered rings) that create two larger clusters depicted in Figure 3b, which in turn form the 3D interconnected network, Figure 3a. For example, in the junction of the channels along the a and c axes, there is a cluster (WC1) formed by three cyclic pentamers that share two connected water molecules (Figure 3b, left). One of the pentamers shares three water molecules with two spiro-tetramers inside the channel along the c axis (the vector defined by O_58 and O_60 points along c), while the other two pentamers share four water molecules that, together with two additional ones, form a chair-shaped cyclic hexamer included inside the channel along the a axis (the O_39, O_44 vector points along a). A second large cluster (WC2, Figure 3b, right) is formed adjacent to the first, and this shares one water molecule (O_44) with WC1 to form a spiro-pentamer system on one side and shares two additional ones (O_38, O_39) on the side that runs parallel to the channel along a. In the channel along c, there is one water molecule (O_60) that is shared by both large clusters forming a spiro [5.4]-type bicyclic system; meanwhile O_57 from WC2 and O_58 from WC1 are interconnected. WC2 is also molded by several smaller clusters, the aforementioned cyclic pentamer shares three water molecules with a hexamer, and both clusters use jointly three water molecules (two of each cluster) with an additional seven-water ring cluster. The central hexamer also shares two water molecules with a cyclic tetramer and hexamer. Finally, this former hexamer has in common three water molecules with the five-water ring cluster that contains the O_60 water molecule. Both clusters together contain all water molecules involved in small cyclic cluster except O_50, which is hydrogen-bonded to only one water molecule in WC2 (O_46) and to one amino and one carbonyl group of two different CP molecules. In these clusters, there are several water molecules (O_33, O_35, O_36, O_52, and O_55) that are tetracoordinated to four other waters and are located at the apexes of three different cyclic clusters. In addition, there are two water molecules (O_44, O_60) that are also linked to four other waters, but these are spiro-centers that form part of the two different ring clusters that share them. The averaging of the WCI parameter for each individual water position over all crystal structures shows that in general the more stable water molecules are those in the first hydration shell, although the two water molecules with lowest WCI values (O_61 and O_62, red colored in Figure 4) belong to this shell. However, it should be noted that these waters are hydrogen bonded to a disordered carbonyl group of the CP and to two disordered water molecules (O_63 and O_59). All these water are sited in WC2 forming the last mentioned [5.6]-bicyclic system. Most water molecules in the structure (71%) are involved in four hydrogen-bonding interactions. The third less stable water, O_31, is only hydrogen bonded to another two 3354
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Figure 3. (a) Network of hydrogen-bonded water molecules displayed along the a (left) and the c (right) unit cell axes on crystal H. (b) View of the two water clusters (WC1, left, and WC2 ,right) that constitute the 3D water network. Oxygen atoms forming the clusters are colored red. Atom labeling and oxygens in yellow indicate how the water clusters are interconnected. For clarity purposes only one of the mutually exclusive disordered water positions is displayed for each disordered site.
Figure 4. View of the crystal packing down the a (left) and c (right) unit cell axes. Water molecules shown as small spheres (first hydration shell) and large spheres (second hydration shell) colored according to the calculated WCI for each water averaged over all crystals (dark blue to red correspond to atomic positions from highest to lowest occupancy).
water molecules. The next least stable water molecules are tetracoordinated, but most of them belong to the second hydration shell and are connected to one another. It is possible that the loss of the initial molecules from this shell opens up space
for subsequent molecules to move away, thus facilitating the loss of further water molecules from this environment. In summary, most of the water molecules that fill the channel along the c axis are the ones that are lost first, while the water molecules that fill 3355
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Crystal Growth & Design the channel along the a axis are the most stable (Figure 4), perhaps due to the different dipolar moment generated by the peptide folding and crystal packing inside each type of channel (see above for channel description). With respect to the water clusters defined above, WC1 is mainly in the channel along a and remains almost invariable, while the second cluster (WC2) loses some water molecules (O_61, O_62, or O_63) in several of the crystal structures reported here. Furthermore, 7 of the first 10 most mobile water molecules according their WCI parameters are part of WC2.
’ CONCLUSIONS In summary, there is a clear indication that the crystal structure of the cyclic peptide reported here is able to include higher water contents despite losing its intramolecular symmetry. Once the crystal is taken out of the mother liquor (humid chloroform), it slowly loses its water content and increases its symmetry.26 This results in a change of the crystal space group from P21 to I2, which implies shifting from molecular point group C1 to C2. These changes in structure require the loss of some water molecules and are independent of temperature. The X-ray crystallographic study revealed that the supramolecular assembly is the result of cooperative hydrogen-bonding interactions between water molecules and between water molecules and the CPs to give water-filled three-dimensional porous materials in which the water molecules are ordered and at the same time form bridges to hold the complete 3D molecular assembly. The water network is made of large interconnected clusters. A study of the properties of these water filled channels has the potential to provide information about the structure of bulk water. ’ ASSOCIATED CONTENT
bS
Supporting Information. Summary of experimental crystal data (crystallization, data collection, processing, and refinement), ORTEP view of CP molecule, analysis of water content and correlation with molecular and crystal symmetry, normalized water content indexes (WCI) calculated for each water position and occupancy, atomic displacement parameters (ADP), and calculated normalized water content index (WCI) for each crystal in space groups I2 or P21. This material is available free of charge via the Internet at http://pubs.acs.org.
’ AUTHOR INFORMATION Corresponding Author
*E-mail:
[email protected].
’ ACKNOWLEDGMENT This work was supported by the Spanish Ministry of Education and Science and the ERDF [(SAF2007-61015, and Consolider Ingenio 2010 (CSD2007-00006)], by the Xunta de Galicia (PGIDIT08CSA047209PR and GRC2006/132), and European project Magnifyco (NMP4-SL-2009-228622). M.A. thanks the Spanish MICINN for his Ramon y Cajal contract. ’ REFERENCES (1) (a) Ball, P. H2O: A Biography of Water; Weidenfeld & Nicolson: London, 1999. (b) Ludwig, R. Angew. Chem., Int. Ed. 2001, 40, 1808. (c) Ball, P. ChemPhysChem 2008, 9, 2677.
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