Structural Transformation of Guanine Coordination Motifs in Water

Jun 15, 2018 - Structural Transformation of Guanine Coordination Motifs in Water Induced by Metal Ions and Temperature. Wei Li†‡ , Jing Jin† , X...
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Structural Transformation of Guanine Coordination Motifs in Water Induced by Metal Ions and Temperature Wei Li,†,‡ Jing Jin,† Xiaoqing Liu,† and Li Wang*,† †

Department of Physics, Nanchang University, Nanchang 330031, P. R. China Department of Science, Nanchang Institute of Technology, Nanchang 330099, P. R. China



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S Supporting Information *

ABSTRACT: The transformation effects of metal ions and temperature on the DNA base guanine (G) metal−organic coordination motifs in water have been investigated by scanning tunneling microcopy (STM). The G molecules form an ordered hydrogenbonded structure at the water−highly oriented pyrolytic graphite interface. The STM observations reveal that the canonical G/9H form can be transformed into the G/(3H,7H) tautomer by increasing the temperature of the G solution to 38.6 °C. Moreover, metal ions bind with G molecules to form G4Fe13+, G3Fe32+, and the heterochiral intermixed G4Na1+ metal−organic networks after the introduction of alkali-metal ions in cellular environment.



INTRODUCTION Deoxyribonucleic acid (DNA) molecules (and more specifically, the sequence of bases in the DNA) store, reproduce, and transmit genetic information necessary for biological processes.1−5 Because of the intimate environmental association with nucleic acids, many metal ions (such as Na+, K+, Ca2+, Fe3+, etc.) can help to improve the stability of the structure of nucleic acids.6 There is now mounting evidence that shows that these metal ions play an important role in the biosynthesis, conformation maintenance, function play, and regulation of nucleic acid.7−10 At the same time, the metal in the protein can also regulate the transcription and translation of nucleic acid.11−13 Recent bioinformatic studies have shown that the biologic functions associated with organometallic compounds make these structures appealing targets for drug development or intracellular imaging.14 Hence, it is fundamentally important to understand the biochemical nature of interactions between metal ions and nucleic acid bases. The guanine base has been investigated under various environments in the past few years, including pioneering studies in air and organic solvents,15−18 demonstrating selfassembly into two-dimensional ordered structures, and detailed ultrahigh vacuum (UHV) scanning tunneling microcopy (STM) studies,19−22 revealing the formation of metal−organic coordination motifs with metals on surface. Despite the many studies on the self-assembled structures and the interactions of metal−guanine molecules, the biological functions of guanine bases in the homologous biological liquid system environments were still unrevealed. To tackle this problem, water, which is vital for life as a solvent, was recognized to be a favorable template to investigate the guanine bases under the similar biological system.23−25 Moreover, the interaction between © XXXX American Chemical Society

metal ions and the nucleic acid bases in homologous biological liquid environment is the base of discovery of antitumor drugs and development of nanometer scale DNA-based device technology. In this study, the ordered hydrogen-bonded structure of guanine was constructed at the water−highly oriented pyrolytic graphite (HOPG) interface. The STM images demonstrate that increasing the temperature of the G solution to 38.6 °C causes the transformation of canonical G/9H form into the G/(3H,7H) tautomer. Furthermore, owing to the valence states of the metal ions, G4Fe13+, G3Fe32+, and the heterochiral intermixed G4Na1+ metal−organic frameworks were formed with the incorporation of the metal ions in similar biological environment.



RESULTS AND DISCUSSION

Figure 1a shows the schematic model of the adsorption of G molecules from water solution onto the highly oriented pyrolytic graphite (HOPG) substrate as water molecules volatilize from the surface. Further adsorption of G molecules to the nucleus results in the expansion of molecular domains, which subsequently coalesce into self-assembled monolayers. When a droplet of G−water solution (2.2 × 10−5 M) was dropped on a fresh HOPG surface, the formation of a thin film with stripelike structures was observed by STM, as shown in Figure 1b. Because of the adsorption competition between water and G molecules, water molecules escape from the Received: April 17, 2018 Revised: June 13, 2018 Published: June 15, 2018 A

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Figure 1. (a) Schematic model of G molecular self-assembly at the water−solid interface showing guanine adsorption and water desorption as water escapes. A series of STM images (5 nm × 5 nm, I = 0.72 nA, V = −0.15 V) of guanine structures change with water volatilization: (b) 0 h, (c) 1 h, (d) 2 h, (e) 3 h, and (f) 4 h when all of the water molecules had been replaced by guanines, and the sample is exposed to air. (g) DFTcalculated structure proposed to explain the observed STM image with complete water volatilization (the green dashed circles show the adsorption of G molecules from the solution).

surface as G molecules fill their spaces. Appearance of some bright spots was observed in the stripes after 1 h, indicating the adsorption of G molecules. The STM images (Figure 1c−e) taken at different time stages show that G molecules have replaced more water molecules over a 4 h time period. The bright spots filled all of the stripes in 4 h, indicating that all of the water had volatilized. This structure is the same as that observed in ultrahigh vacuum (Figure S1). The evolvement of

the assembled structures in Figure 1a−e with time suggests that these structures are kinetically controlled due to the evaporation of water. However, the consistency between Figures 1f and S1 confirms that the finally observed structure is indeed thermodynamically stable. This model calculated by density functional theory (DFT) in Figure 1g shows that each G molecule inside the monolayer interacts with its four neighboring molecules via six hydrogen bonds with varied B

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Figure 2. (a) STM image (I = 0.74 nA, V = −026 V, 35 nm × 35 nm) of the zigzag structure of G (highlighted by white dash lines) after heating the solution to 37.5 °C. (b) STM image (I = 0.72 nA, V = −0.30 V, 30 nm × 30 nm) showing the coexistence of zigzag structures (highlighted by white dash lines) and six-membered ring network structures (highlighted by green dash circles) after annealing the G solution at 41.0 °C for 2 h. (c) Overview image (I = 0.89 nA, V = −0.15 V, 60 nm × 60 nm) and (c,i) high-resolution image (I = 0.74 nA, V = −0.26 V, 20 nm × 20 nm) of the structure after heating the solution to 58.0 °C. (d) High-resolution STM image of G/9H zigzag network. The corresponding DFT-optimized structural model is superimposed on the STM image. H: white; C: gray; N: blue; O: red. (e) High-resolution STM image of six-membered ring structure. The DFT-optimized model is superimposed on the STM image in (e). H: white; C: gray; N: blue; O: red. (f) Graph of the changes in the number of G/(3H,7H) structures with changes in temperature. (g) Graph of the changes in percentages of G/(3H,7H) structures with changes in temperature.

proposed unit cell with a = 1.0 ± 0.1 nm, b = 1.9 ± 0.1 nm, and α = 88 ± 2°. This interesting result opens up the possibility of guiding the formation of large-scale molecular

strength. The distances of hydrogen bonds N−H···N, N−H··· O, and CO···H are 2.08, 1.73, and 1.89 Å, respectively. The experimentally obtained unit cell is superimposed on the C

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Figure 3. (a) STM image of structures I and II co-adsorbed on the graphite surface (50 nm × 50 nm, I = 0.93 nA, V = −0.45 V). The dashed lines indicate phase-separated boundaries between G network and G4Na1+ structures. (b) STM topography image (15 nm × 15 nm, I = 0.63 nA, V = −0.25 V) of the heterochiral intermixed metalosupramolecular G-quartet network. (c) High-resolution STM image (5 nm × 5 nm, I = 0.70 nA, V = −0.18 V) of the G4Na1+ network. (d) DFT-proposed model of the G4Na1+ network superimposed on the close-up STM image.

membered ring networks arise when the G molecules are converted into their rare tautomeric G/(3H,7H) form in the water. Figure 2b shows the STM image of the mixture of zigzag structure with six-membered ring structure after the G−water solution was heated up to 41.0 °C for 2 h. Figure 2e shows the submolecular resolved STM images with the corresponding DFT-optimized structural model superimposed. The model for the network is inserted in the lower right corner of Figure 2c,i to further verify the rationality of the model for the sixmembered ring structure. The zigzag structures (highlighted by white dash lines) are consistent with G/9H phase, and sixmembered ring structures agree with the G/(3H,7H) phase (highlighted by green dash lines). Both formations are stabilized by the adoption of intermolecular N−H···N and N−H···O hydrogen bonds. Figure 2c further shows that the increase of the temperature to 58.0 °C obviously destroys the zigzag structures and promotes the formation of the sixmembered ring structures. Figure 2f shows the changes in the numbers of G/9H and G/(3H,7H) molecules with temperature. Interestingly, the numbers of G/9H and G/(3H,7H) vary with temperature in a nonlinear way. Figure 2g shows the changes in the percentage of G/(3H,7H) with different temperatures. The calculations show that the canonical G/ 9H form begins to transform into the tautomeric G/(3H,7H) form at 38.6 °C, and the process follows a nonlinear thermal activation behavior with an activation energy of −4.2 V. Owing to the advantage of coordination selectivity and diversity with respect to different alkali metals, various static

networks, leading to important atomic-scale insights into the chemical and biological properties of G molecules and their applications. As previously shown,26−28 G could have various tautomeric forms under different environments and at high temperatures. Recently, the tautomerization of G molecules from the canonical G/9H form to the rare tautomer G/(3H,7H) form has been experimentally observed on Au(111) surface by introducing water molecules into the UHV system.29,30 Theoretical investigations have shown that the water could significantly enhance the stability of different DNA base tautomers by reducing the energy barrier of tautomeric conversions and thus favoring the formation of some rare base tautomers.31,32 To verify the influence of temperature on the process of tautomeric recognition in aqueous solution, a series of droplets of G−water solutions heated to various temperatures were deposited on clean HOPG surfaces, which were held at room temperature. In Figure 2a, an STM image for the G−water solution heated to 37.5 °C, the stripe phase can be clearly observed from the high-resolution STM image with the superimposed DFT model shown in Figure 2d. In this phase, the G molecules form a zigzag structure (highlighted by the white dash lines) via hydrogen bonds. When the G solution was heated to 39.0 °C for about 2 h, surprisingly, the disordered phase is converted into chain structures together with six-membered ring network structures, and the number of six-membered ring network structures increases with further heating, as shown in Figure S2. On the basis of the STM images and previous reports,30,32,33 it is considered that the sixD

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Figure 4. (a) Coexistence of G4Fe13+ structures I and G self-assembled network II (30 nm × 30 nm, I = 0.68 nA, V = −0.34 V). The dashed line indicates phase-separated boundary between structures I and II. (b) High-resolution STM image (7 nm × 7 nm, I = 0.68 nA, V = −0.22 V) of the G4Fe13+ network. (c) Close-up STM image of the G4Fe13+ motif superimposed with the DFT-optimized gas-phase structural model. (d) STM topography image (30 nm × 30 nm, I = 0.63 nA, V = −0.25 V) of the G3Fe32+ network. (e) High-resolution STM image (7 nm × 7 nm, I = 0.62 nA, V = −0.25 V) of the G3Fe32+ network. (f) Close-up STM image of the G3Fe32+ motif superimposed with the DFT-optimized gas-phase structural model.

indicated by the green square in Figure 3d. From the optimized model superimposed on the enlarged STM image cut out from the region highlighted in Figure 3c, it can be identified that Na+ is located in the center of the G-quarter and there are two kinds of interactions: hydrogen bonding (N−H··· N and N−H···O) and metal−ligand bonding (Na−O) to stabilize the G4Na1+ network. It is worth noting that each G4Na1+ motif binds to the neighboring ones through double N−H···N hydrogen bonds. Similar metal coordination bond network can be also achieved by depositing a mixture of G molecules and Fe3+ with a concentration of 5 × 10−6 M on HOPG surface, as shown in Figure 4a. Two distinct structures indicating different phases labeled as I and II on the same surface area are separated by the white dash line. A close examination of Figure 4a reveals that the structure I is self-assembled by G molecules and that the structure II stands for G-quartet structure. With the increase of the Fe3+ concentration to 1 × 10−5 M, all G molecules form the G-quartet coordination structures with Fe3+ ions, as shown in Figure S4. The high-resolution STM image in Figure 4b shows that the building block for this new structure is a G-quartet network structure. On the basis of the high-resolution STM image, we have performed DFT optimization and found that the G-quartet−Fe3+ is the most energetically favorable model, as the STM image overlaid on Figure 4c. By virtue of coordination diversity, further

G−metal coordination frameworks can be fabricated, and furthermore these structures could be responsive to metal/ molecule stoichiometric ratios, coverage, the valences of metal ions, and/or temperatures resulting in structural transformations.34−36 Hence, to explore the possibility of forming the G−metal coordination structures at water−solid interface, mixtures of G molecules and metal ions were deposited on HOPG surface. As shown in Figure 3a, when the water solution containing G molecules and Na+ was deposited on HOPG surface, three distinct structures labeled as I, II, and III were separated by the white lines, which can be observed on the same area. Obviously, the structure III is the HOPG surface. Figure S3 reveals that the structure I represents the self-assembled network structure formed by G molecules and that the structure II is the metallosupramolecular G-quartet network motif. As experienced with coordination schemes between DNA bases and transition metals,37,38 we assign this quartet motif to G4Na1+ metal−organic structure. From the high-resolution STM image (Figure 3c), we can identify that the network structure is composed of two enantiomers (marked R and L). The heterochiral intermixed G4Na1+ metal−organic network structure contains the same amounts of chiral R and L forms as G molecules. Such an arrangement exhibits a characteristic pattern of the intermixed G quartets with alternating chirality, forming oval stripes running at 90° to each other throughout the G4Na1+ metal−organic network, as E

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were fully relaxed until the residual force on each atom was less than 0.01 eV/Å. The graphite surfaces were not included in the optimization due to the heavy calculation burden.

deposition of the water solution containing G molecules and Fe2+ metal ions on HOPG surface at room temperature leads to the formation of well-ordered trimer structures array, as shown in Figure 4d. From the high-resolution STM image (Figure 4e), we found that the molecular rings are composed of trimers, as depicted by the oval contours. It is worth nothing that this structure is formed by three homochiral G molecules in coordination with three Fe2+ ions by occupying all of the available O and N sites simultaneously in the superimposed DFT-optimized model, where the tri-iron cluster (Fe2+) is resolved as a bright spot, and there are no potential intermolecular hydrogen bonds within the motif, as shown in Figure 4f.



ASSOCIATED CONTENT

S Supporting Information *

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.langmuir.8b01263. G structure in ultrahigh vacuum (UHV); effect of temperature on the tautomeric G/(3H,7H) structures and the self-assembly of G molecules structure at water− solid interface; and STM images of all of the G molecules form the G4Fe13+ coordination structures with Fe3+ ions when the Fe3+ concentration increases to 1 × 10−5 M (PDF)



CONCLUSIONS In conclusion, the ordered hydrogen-bonded structures of guanine have been investigated at the water−HOPG interface. From the interplay of high-resolution STM images and density functional theory (DFT) calculations, the experimental results showed that the canonical G/9H form can be transformed into the G/(3H,7H) tautomer by increasing the G solution temperature to 38.6 °C. Furthermore, the hydrogen-bonded structures of G have been significantly transformed to G4Fe13+, G3Fe32+, and the heterochiral intermixed G4Na1+ metal− organic coordination network structures after the introduction of the metal ions in similar biological environment. The results presented here can aid answering some fundamental questions about the nature of the interaction of a nucleobase with metal ions in water, which could have basic and clinical uses.





AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. ORCID

Li Wang: 0000-0001-6919-1712 Notes

The authors declare no competing financial interest.



ACKNOWLEDGMENTS This study was financially supported by Natural Science Foundation of China (Grant Nos. 61474059, U1432129, and 11504158) and National Key Basic Research Program of China (2013CB934200). L.W. acknowledges Jiangxi Provincial Innovation Talents of Science and Technology (20165BCB18003).

EXPERIMENTAL SECTION

Sample Preparation. Guanine molecules and metal chloride (NaCl, FeCl2, and FeCl3) used in this work were not further purified after purchased from Tokyo Chemical Industry (TCI). The solvent used in this work was ultrapure water (Merck), with a resistivity of 18.2 MΩ̇ cm at 25.0 °C. G molecules were dissolved in ultrapure water with the concentration less than 2.0 × 10−5 M and were sonicated in an ultrasonic bath for about 5 min. The mole ratio of G to metal chloride (NaCl, FeCl2, and FeCl3) in the final product was controlled by both the concentrations and the volumes that were deposited. G solutions were heated to different temperatures (37.5, 39.0, 40.0, 41.0, 42.0, 50.0, and 58.0 °C) in a water bath. A piece of highly oriented pyrolytic graphite (HOPG, grade SPI-2) substrate was freshly cleaved using adhesive tape. First, about 50 μL of these heated G solutions was deposited on HOPG substrate. Then, the samples were kept for about 4 h, during which water molecules volatilize from the surface to form the ultrathin film. Finally, the samples were investigated by STM. STM Measurements. All STM experiments were performed with a Pico-SPM (Molecular Imaging, Agilent Technology) scanning tunneling microscope in constant-current mode under ambient conditions. STM tips were mechanically cut from 0.25 mm Pt/Ir (80/20) wires (California Fine Wire Co., Grover Beach, CA) and tested on the freshly cleaved HOPG surface. All STM images provided raw data, which were calibrated by referring the underlying graphite lattice. All samples were tested repeatability and to make sure that there were no artifacts caused by interactions between the tip and the sample. Details of tunneling conditions are provided in the corresponding figure captions. Constructed and Computational Details. Theoretical calculations of the superstructures were performed using DFT, as implemented in the Vienna ab initio simulation package in this work. The Perdew−Burke−Ernzerhof generalized gradient exchange and correlation function was applied in exchange−correlation energy. The optB86b-vdw method was employed to describe the van der Waals interaction. Adopting a 1 × 1 × 1 k-point mesh, all structures



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