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Scanning Tunneling Microscopy Image Contrast as a Function of Scan Angle in Hydrogen-Bonded Self-Assembled Monolayers Stephen J. Sowerby,† Michael Edelwirth, Michael Reiter, and Wolfgang M. Heckl* Ludwig Maximilians Universita¨ t Mu¨ nchen, Institu¨ t fu¨ r Kristallographie, Theresienstr. 41, 80333 Mu¨ nchen, Germany Received November 13, 1997. In Final Form: May 26, 1998 Scanning tunneling microscopy (STM) has been performed on monolayers of the nucleic acid base, adenine, adsorbed to molybdenum disulfide (MoS2) surfaces. Analysis of the real space images of the adsorbates, together with molecular mechanics simulations suggest that the molecules form monolayers stablized by cyclic hydrogen bonds. We present data showing the effect on image contrast of varying scan angles of the STM tip. These indicate an anisotropic response of components of the monolayer to the scan direction and support a structural model implicating cyclic hydrogen bonds in both the stability of the monolayer and in the STM image contrast mechanism.
Introduction The application of scanning tunneling microscopy (STM)1 has proved particularly well suited to study the molecular arrangement of close-packed adsorbate structures physisorbed on the surfaces of inert layered compounds such as graphite and molybdenum disulfide (MoS2). Relevant examples include cyclic aromatic compounds,2 long chain alkane derivatives,3 and cyanobiphenyl liquid crystal derivatives.4 The physisorption of the purine base adenine (6aminopurine) and other nucleic acid bases onto solid surfaces has only recently been demonstrated.5-16 In addition to van der Waals interactions, monolayer formation involves specific adsorbate-adsorbate interactions mediated through intermolecular hydrogen bonding. In situ electrochemical STM techniques for studying adenine monolayer formation on graphite11,12,14 and gold † Present address: Department of Biochemistry, University of Otago, P.O. Box 56, Dunedin, New Zealand. * Telephone: +49 89 2394 4331. Fax: +49 89 2394 4331. E-mail:
[email protected].
(1) Binnig, G.; Rohrer, H.; Gerber, C.; Weibel, E. Phys. Rev. Lett. 1982, 49, 57. (2) Ludwig, C.; Gompf, B.; Petersen, J.; Strohmeier, R.; Eisenmenger, W. Z. Phys. 1994, B93, 365. (3) Cyr, D. M.; Venkataraman, B.; Flynn, G. B. Chem. Mater. 1996, 8, 1600. (4) Smith, D. P. E.; Heckl, W. M.; Klagges, H. A. Surf. Sci. 1992, 278, 166. (5) Allen, M. J.; Balooch, M.; Subbiah, S.; Tench, R. J.; Siekhaus, W.; Balhorn, R. Scanning Microsc. 1991, 5, 625. (6) Boland, T.; Ratner, B. D. Langmuir 1994, 10, 3845. (7) Heckl, W. M.; Smith, D. P. E.; Binnig, G.; Klagges, H.; Ha¨nsch, T. W.; Maddocks, J. Proc. Natl. Acad. Sci. U.S.A. 1991, 88, 8003. (8) Sowerby, S. J.; Heckl, W. M.; Petersen, G. B. J. Mol. Evol. 1996, 43, 419. (9) Sowerby, S. J.; Petersen, G. B. J. Electroanal. Chem. 1997, 433, 85. (10) Srinivasan, R.; Murphy, J. C.; Fainchtein, R.; Pattibiraman, N. J. Electroanal. Chem. 1991, 312, 293. (11) Srinivasan, R.; Murphy, J. C. Ultramicroscopy 1992, 42-44, 453. (12) Srinivasan, R.; Gopalan, P. J. Phys. Chem. 1993, 97, 8770. (13) Tao, N. J.; DeRose, J. A.; Lindsay, S. M. J. Phys. Chem. 1993, 97, 910. (14) Tao, N. J.; Shi, Z. J. Phys. Chem. 1994, 98, 1464. (15) Tao, N. J.; Shi, Z. Surf. Sci. Lett. 1994, 301, L217. (16) Freund, J.; Edelwirth, M.; Kro¨bel, P.; Heckl, W. M. Phys. Rev. B 1997, 55, 5394.
surfaces6,13 and atomic force microscopy (AFM) on graphite surfaces14 have demonstrated a propensity for adenine to spontaneously condense at the solid-liquid interface. A previous STM study of adenine monolayers formed on MoS2 surfaces indicated the presence of two oblique mirror symmetric structures.8 The spontaneous self-assembly of such structures at the solid-liquid interface has been invoked in a model for the emergence of life.8,17 The application of low-energy electron diffraction (LEED) to the adenine monolayers formed on graphite by sublimation techniques, showed that the adsorbate molecules were arranged in a P2gg plane group on the graphite surface.16 The application of molecular mechanics to trial structures of this monolayer system enabled discrimination between different close-packed models on the basis of energy minimization arguments and convergence criteria. In the final energy-minimized configuration,18 the most favored structure positioned the adenine molecules lying with their planar ring systems flat on the graphite surface with a maximized van der Waals interaction. This structure also satisfied the adsorbate symmetry requirements and realized the maximum number of possible intermolecular hydrogen bonds between adjacent molecules. Although consistent lattice dimensions have been observed for these structures formed in ultrahigh vacuum,16 in liquid,14 and by evaporation of aqueous solution5,8,19 and suggest a common adsorbate structure, alternative packing arrangements have been proposed. It has been proposed that hydrogen bonding might be implicated in the STM image contrast mechanism of guanine7 and adenine18 on graphite surfaces and uracil monolayers on MoS2 surfaces.9 In this paper, we show the response of the STM image contrast of adenine monolayers on MoS2 surfaces to the scan direction of the STM tip. Our motivation for performing these types of experiments has been the observed effect on STM contrast of the adsorbate orientation with respect to the STM scan direction. These effects resulted in markedly different (17) Sowerby, S. J.; Heckl, W. M. Origins Life Evol. Biosph. 1998, 28, 283. (18) Edelwirth, M.; Freund, J.; Sowerby, S. J.; Heckl, W. M. Surf. Sci., in press, 1998. (19) Reiter, M.; Edelwirth, M.; Heckl, W. M.; Sowerby, S. J. Probe Microsc., in press.
S0743-7463(97)01235-3 CCC: $15.00 © 1998 American Chemical Society Published on Web 08/15/1998
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STM images of the molecular adsorbate, which were highlighted at grain boundaries and exemplified by the nonreproducibility of STM image contrast and interpretation between different authors. Furthermore, the conspicuous absence of such a study in the literature necessitates a specific examination of this effect, which may be extendible to other monolayer systems under investigation by STM. These studies indicate that hydrogen-bonding interactions and the orientation of the adsorbates to the STM scan direction play a dominant role in the STM image contrast of these monolayer structures. Methods Scanning Tunneling Microscopy. The adsorbate structures were prepared by evaporation of saturated aqueous solutions of adenine, as previously described for nucleic acid bases.5,7 STM measurements were performed with a home-built STM using electrochemically (2 N KOH) prepared polycrystalline tungsten tips. The measurements were made at bias voltages between (100 and (1000 mV and tunneling currents between 10 pA and 1 nA in the constant current mode. Scan angle variation was achieved in ≈30° increments by applying an electronic two-dimensional clockwise rotation matrix
(
cos R Ω(R) ) sin R
- sin R cos R
)
This mixed oscillation input signals to generate the output signals applied to the x and y electrodes of the piezoelectric tube scanner to which the STM tip was fixed. The sample was kept immobilized. Variation in the scan angle with this system did not constitute a rotation of either the tip or the sample. Nonlinearities of the piezoelectric scanner were corrected in the adsorbate images by assuming a perfect 3-fold symmetry for the atoms of the underlying crystal substrate surface, which were imaged by piercing the tip through the adsorbate crystal after reducing the gap resistance. Geometric corrections and fast Fourier transform analysis were performed on the STM images using Image SXM a spin-off of the public domain NIH Image program. Molecular Mechanics Simulations. Molecular mechanics was applied to models of adenine monolayers on the surface of MoS2 with the program Cerius2 running on a Silicon Graphics Indigo II workstation. For the energy minimization calculations, we used the Dreiding II force field,20 which has been parametized for organic, biological, and main group inorganic molecules and has an explicit hydrogen-bonding term. The potential energy (ET) of the adsorbate monolayer system is the sum of the two-, three-, and four-body terms in the energy expression, which is implemented by Cerius2, ET ) Ebond + Eangle + Etorsion + Einversion + EvdW + ECoulombic + EH The expression can be divided into two terms. The valence terms, Ebond (bond stretching), Eangle (angular distortions), Etorsion (dihedral angle torsions), and Einversion (umbrella inversions), relate to specific bond and atomic orientations of the molecular structure and were modeled by classical mechanics expressions fitted to reproduce spectroscopic and crystallographic data. The nonbond terms, EvdW (van der Waals), ECoulombic (electrostatic), and EH (hydrogen bonding), relate to intermolecular interactions. The van der Waals term was modeled using a Lennard-Jones 12-6 potential, whereas the hydrogen bond applies the LennardJones 12-10 potential and includes an angle dependent cosθ term. Electrostatic interactions took the form of a Coulombic point charge interaction between atom-centered partial charges. Longrange electrostatic and van der Waals interactions were treated with the Ewald summation technique. The two-dimensional monolayer systems were modeled as a molecular solid of infinite dimensions using periodic boundary conditions in a three-dimensional crystal model space of P1 symmetry, as previously described.18,21-23 The three Cartesian (20) Mayo, S. L.; Olafson, B. D.; Goddard, W. A., III J. Phys. Chem. 1990, 94, 8897. (21) Bondi, C.; Baglioni, P.; Taddei, G. Chem. Phys. 1985, 96, 277.
vectors a, b, and c corresponded to the two surface mesh vectors and third dimension, respectively. We modeled the adsorption of adenine molecules to the surface of MoS2 in a method similar to that described for adenine on graphite18 and uracil on graphite and MoS2 surfaces.23 Electrostatic potential derived partial atomic charges, the starting geometry of the atoms of adenine molecules, and the adenine dipole moment were calculated by the semiempirical AM1 method using the public domain software “MOPAC”, accessible through Cerius2. The substrate model surface was the (0001) surface of MoS2, the top layer of the 2HMoS2 bulk crystal model.24 The partial atomic charges of the Mo and S atoms of the MoS2 substrate were set to zero. Convergence calculations were used to determine the depth of the model bulk solid, which corresponded to a three-layer slab. The length of the cell perpendicular to the surface (c) was extended to 15 nm to ensure no artifactual effects of the adjacent cells generated by ghost molecules from the periodic boundary conditions. The model surface mesh dimensions (a, b) were that of the adsorbate coincident mesh determined by comparison of the real space STM images of the adsorbate and of the underlying substrate. The minimizations were terminated when the total energy of the potential energy hypersurface reached an RMS force gradient e0.03 kcal/mol/Å.
Results and Discussion Scanning Tunneling Microscopy. Inspection by STM of monolayers of adenine formed on the surface of MoS2 showed the presence of large (>500 nm in most cases) domains of planar crystalline material with periodicities inconsistent with images of the bare MoS2 surface. In stable regions of the adsorbate and at constant scan direction, the image contrast was not responsive to changes in the magnitude of the applied bias voltage between the ranges of -0.18 and -1.0 V. The images were exclusively obtained with the STM at negative tip bias, which corresponds to electrons flowing from the occupied states of the tip into the unoccupied states of the sample. Images of the adsorbate at STM tip positive were generally unstable and short-lived, although images of the MoS2 substrate were routinely obtained (0.3-0.4 V) with this polarity. The resolution and image contrast was sensitive to the quality of the STM tips and was often observed to change throughout the duration of continuous experiments, presumably as a result of spontaneous geometric/ electronic modifications at the tip-sample tunnel junction. With stable tips and at specific scan directions, periodicities within the adsorbate images of individual domains were resolved equivalently as discrete units with centerto-center dimensions (0.6-0.9 nm), consistent with that of individual adenine molecules (Figure 1A,B). Congruent lattice dimensions were observed in images containing grain boundaries where domains of differing orientation lay juxtaposed in the image (Figure 1). Measurements of the angles between consistent lattice features showed values (60°, 120°) that represented the P6 symmetry of the underlying MoS2 substrate and indicated heteroepitaxial registration. The contrast difference between such adjacent domains could not be accounted for by a simple geometric operation of one image onto the other or by spontaneous tip changes and necessitated a further understanding of the STM data acquisition mechanism. Analysis of the image contrast as a function of scan angle (Figure 2) showed marked variation in the apparent adsorbate structure. Consistent periodicities within each adsorbate image could be used to define the adsorbate lattice mesh dimensions. These were resolved for all (22) Seidel, C.; Awater, C.; Liu, X. D.; Ellerbrake, R.; Fuchs, H. Surf. Sci. 1997, 371, 123. (23) Sowerby, S. J.; Edelwirth, M.; Heckl, W. M. Appl. Phys. A 1998, 66, S549. (24) Dickinson, R. G.; Pauling, L. J. Am. Chem. Soc. 1923, 45, 1466.
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Figure 1. (A) STM image of an ordered array of adenine molecules adsorbed to the surface of MoS2 (imaging parameters, bias voltage ) -1.0 V, tunnel current ) 20 pA) showing a grain boundary between two domains. The double-headed arrow indicates the fast scan direction of the STM tip. Equivalent lattice directions on each of the domains are indicated by the black lines and intersect at an angle of 60°, indicating epitaxial registration with the underlying substrate. (B, C) Enlarged portions of each of the domains in (A) delineated by the white rectangle. On each image, the adsorbate mesh is described by the black dashed line parallelograms of dimensions 2.28 × 0.84 nm.
orientations of scan direction and the dimensions were invariant. Despite the images being obtained at different scan angles, the resulting contrast changes were not a simple geometric rotation of the observed contrast features, as was the case for the uppermost S atoms of the underlying MoS2 substrate. For these images of the adsorbate (Figure 2), contrast variation due to changes in the geometry of the STM tip could be excluded because of the reproducibility of the image contrast following recursive examination of the sample. Similarly, the reproducibility of the image contrast in separate experiments with different tips supported these observations, as did images of differently oriented domains obtained at grain boundaries (Figure 1). A striking feature was an apparent smearing of the individual molecular features in which the discrete units were blended together into bands of comparatively high STM contrast. Comparison of the images as a function of scan direction shows that images obtained at scan angles related by 180°, showed the same dominant periodicities of smeared bands. Small differences in the contrast can be accounted for as the images are not fully symmetric as a function of scan angle. This is because the in-plane components of the applied electric field from the STM tip are vectorial and can polarize electronic components of the adsorbate differently. Although the molecular adsorbate has P2 symmetry, it electronically interacts with the substrate and has the reduced P1 symmetry. These quantum electronic variations are observed directly by STM. Additionally, the mechanism that effects scan angle variation is imperfect due to nonlinearities in the operation of the piezoelectric ceramic and in the electronic scan rotator; so true 180° scan angle variations were not possible in all cases. Similarly, the STM tip collected electronic information only in one direction of the fast scan. Comparison of many images as a function of scan angle suggests that the contrast of the adsorbate can be broadly classified into subgroups. Parts D, E, K, and J of Figure 2 were acquired with the same scan direction and form one class of image contrast that resolve banding that extends diagonally, in one direction across the STM image. Analysis of Figure 1C suggests that this is also the case.
These constitute the majority of STM images obtained in experiments that did not consider scan angle. The remaining contrast patterns show a large anisotropy with bands horizontal in the STM images. At certain scan orientations, the stability of the monolayer was reduced and tip-induced rupture was often observed (Figure 2G). The weaker orientations tended to be when the fast scan of the STM tip was 60-120° to the horizontally resolved banding pattern (Figure 2A,B,F,G,H,L). Consequently, these were rarely resolved in experiments that did not consider scan angle and were only obtained by trial and error in experiments with stable STM tips and well-tuned tunneling parameters. The scan angle dependent effects were inconsistent with artifactual oscillations generated by excess gain on the feedback loop that controls the vertical position of the STM tip. This is supported by images of grain boundaries (Figure 1), where domains of different orientation lie juxtaposed at different orientations to the STM tip. The findings of a scan angle dependency on STM image contrast do not appear to be consistent with published images of alkane derivatives at grain boundaries,3,25,26 where adsorbate-adsorbate interactions are predominantly of the van der Waals type. Analysis of the adsorbate and corresponding substrate data in both the real space and the reciprocal space of a number of STM images, suggested the presence of two symmetrically equivalent structures related only by a reflection in the plane perpendicular to the substrate. This was in agreement with earlier observations that suggested a chiral symmetry break by the formation of enantiomorphic monolayer domains.8 For the symmetrically equivalent adsorbate structures, both the real-space and fast Fourier transform (FFT) analysis (Figure 3) resolved the two primitive mesh vectors with dimensions of |a| ) 2.20 ( 0.2 nm, |b| ) 0.85 ( 0.2 nm, and g ) 93 ( 1° for both the “left” and “right” hand configurations. Comparison of both adsorbate structures with that of their respective underlying substrates shows (25) Rabe, J. P. Ultramicroscopy 1992, 42-44, 41. (26) Cyr, D. M.; Venkataraman, B.; Flynn, G. B.; Black, A.; Whitesides, G. M. J. Phys. Chem. 1996, 100, 13747.
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Figure 2. STM images (A-L) of an ordered array of adenine molecules adsorbed to the surface of MoS2 (imaging parameters, bias voltage ) -0.85 V, tunnel current ) 106 pA) at varying scan angle. Each image is accompanied by a double-headed arrow that corresponds to the fast scan direction of the STM tip. The images have been placed in the wagon wheel configuration and rotated into equivalent orientations to allow the reader easy comparison of the images. The adsorbate images were all individually geometrically corrected with their corresponding substrate images (not all shown) and subjected to a low-frequency band-pass filter in their respective Fourier space. Center, an STM image of the underlying MoS2 showing the uppermost S atoms, 0.316 nm apart. The image was obtained directly beneath the adsorbate structure (C) and at the same scale and orientation (imaging parameters, bias voltage ) +0.39 V, tunnel current ) 900 pA).
that equivalent lattice features are in registry with the substrate (Figure 3). Coincident lattices were observed that can be described by matrices in terms of the substrate vectors,
() (
a 2 ) b -3
)( )
g1 8 -1 g2
for the “left-hand” configuration (Figure 3A) and
() (
a 3 ) b -2
)( )
2 g1 6 g2
|g1| ) |g2| ) 0.316 nm for the “right-hand” configuration (Figure 3B). By comparing the direction of the primitive mesh vectors of both adsorbates with those of the underlying substrate, we can understand the enantiomorphic behavior of the adsorbate in terms of the heteroepitaxy with the substrate. The oblique meshes are related by an equal but opposite misalignment of (14° of the adsorbate a vector with the substrate g2 vector (Figure 3). Additional information from the LEED analysis of adenine on graphite showed the presence of two glide reflections with the adsorbate molecules oriented in a P2gg space group. However, deviation of the adsorbate mesh from rectangular to oblique reduces the adsorbate sym-
metry from P2gg to P211 and allows for the formation of two mirror structures on MoS2, but in addition, through the electronic interaction of the adsorbate with the substrate crystal, the overall symmetry is further reduced to P1. Molecular Mechanics Simulation. In the present calculation, the partial atomic charges of the Mo and S atoms of the MoS2 substrate were set to zero. The electrochemical evidence for adenine monolayer formation on graphite,11 gold,13 and mercury27 electrodes showed monolayer formation when the charge density on the electrode surface was at zero charge. In the previous calculations of adenine adsorption on graphite, the Lennard-Jones component was determined to play the dominant role in the adsorbate-substrate interaction. This suggested that neglect of the electrostatic component would not seriously affect molecular model building where van der Waals interactions dominate.18 Similarly, the geometric analysis of the STM images suggests that the adenine molecules are lying planar to the surface. The restriction of the adsorbate molecules to the observed coincident mesh was modeled by the imposition of periodic boundary conditions. The measured mesh dimensions are the only empirical parameter that we have placed on the adsorbate-substrate interaction. This restriction (27) Vetterl, V. Collect. Czech. Chem. Commun. 1966, 31, 2105.
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Figure 3. (A) STM image of an ordered array of adenine molecules adsorbed to the surface of MoS2 (imaging parameters, bias voltage ) -0.75 V, tunnel current ) 27 pA). The adsorbate primitive mesh that is coincident with the underlying substrate is shown by the black parallelogram and described by the adsorbate mesh vectors a and b. Adjacent, STM image of the underlying MoS2 showing the uppermost S atoms, 0.316 nm apart. The image was obtained directly beneath the adsorbate structure and at the same scale and orientation (imaging parameters, bias voltage ) +0.40 V, tunnel current ) 390 pA). The substrate primitive mesh vectors (g1 and g2) are shown in white. The white dashed-line parallelogram shows the adsorbate primitive mesh that is coincident with the underlying substrate, and the matrix is described in the text. Below, the composite reciprocal space analysis of the adsorbate and substrate images enlarged 3×. The primitive mesh vectors a and b marked in the adsorbate image are represented in the FFT by a* and b*, as are the substrate vectors g1 and g2 (g1* and g2*). (B) STM image of an ordered array of adenine molecules adsorbed to the surface of MoS2 that is related to (A) by a reflection in the plane perpendicular to the substrate (imaging parameters, bias voltage ) -0.85 V, tunnel current ) 106 pA). Adjacent, STM image of the underlying MoS2. The image was obtained directly beneath the adsorbate structure and at the same scale and orientation (imaging parameters, bias voltage ) +0.39 V, tunnel current ) 900 pA). Below, the composite reciprocal space analysis of the adsorbate and the substrate. The descriptions and relationship of the FFT to the adsorbate and substrate images are the same as for (A). The adsorbate images were both individually geometrically corrected with their corresponding substrate images and subjected to a low-frequency band-pass filter in their respective Fourier space.
simulates the effects of both the adsorbate-adsorbate and the adsorbate-substrate interactions in the two-dimensional plane of the adsorbate and not the specific adsorbate-substrate interaction that a lone molecule would experience on the surface. This approach has been previously applied to uracil monolayers formed on graphite and MoS2 surfaces.23 Although this approximation is crude and fails to account for the electrostatic component of the cleaved MoS2 surface and its interaction with polar molecules, the method seemed to reasonably simulate the molecular packing of the uracil monolayer structures and allowed discrimination between competing structural models. To test possible adsorbate lattice structures, we used trial mesh dimensions and trial packing configurations. The trial mesh dimensions were derived from the nearest neighbor substrate atoms of the observed adsorbate coincident mesh and included both enantiomorphic possibilities. The trial packing structures included the configurations that had previously been proposed for adenine monolayers on graphite5,8,14,16,18 and MoS2.8 Of the trials, only the simulations with both of the STMderived dimensions shown here and the packing configuration determined for adenine on graphite by LEED analysis and molecular mechanics simulation16,18 converged with the lowest energy minima (Figure 5). Both enantiomorphic structures behaved similarly during their minimization calculations.
The dimensions determined for the adenine adsorbate on MoS2 are similar to those observed for the adenine adsorbate structures prepared on graphite surfaces (|a| ) 2.21 nm, |b| ) 0.85 nm, and g ) 90°) determined by both STM5,8,14 and LEED studies.16 These observations are analogous with the comparative STM studies of the nucleic acid purine, guanine7 and the pyrimidine, uracil9 on MoS2 and graphite surfaces. These also show similar lattice dimensions with rectangular adsorbate structures on graphite and oblique structures on MoS2. Examination of the pyrimidine adsorbates was also supported by X-ray crystal studies of the bulk state. Unfortunately, however, we have been unable to locate any literature on the crystal structure of pure adenine, which has only been crystallized as a hydrochloride,28-30 hydrochloride hemihydrate,31 or dihydrochloride32 or within mixed component complexes and complicated biological compounds.33 Consequently, a direct comparison of the adenine monolayer structures with that of the bulk state has not been straightforward. The small deviations in adsorbate mesh structure from (28) Broomhead, J. M. Acta Crystallogr. 1951, 4, 92. (29) Broomhead, J. M. Acta Crystallogr. 1948, 1, 324. (30) Cochrane, W. Acta Crystallogr. 1951, 4, 81. (31) Kistenmacher, T. J.; Shigematsu, T. Acta Crystallogr. 1974, B30, 166. (32) Kistenmacher, T. J.; Shigematsu, T. Acta Crystallogr. 1974, B30, 1528. (33) Saenger, W. Principles of nucleic acid structure; Springer-Verlag New York Inc.: New York, 1984.
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Figure 4. Energy-minimized model of the adenine monolayer (right-hand configuration) on the surface of MoS2. A centrosymmetric dimer with a 180° rotational axis (black ellipse) is shown together with the calculated dipoles of the individual molecules (black arrows ) 2.18278 D). Intermolecular hydrogen bonds are shown by dashed lines between the proton donors and acceptors of adjacent molecules. The adsorbate primitive mesh vectors (|a| ) 2.276 nm, |b| ) 0.836 nm) describe the adsorbate structure that is coincident with the underlying substrate (|g1| ) |g2| ) 0.316 nm).
rectangular on graphite to oblique on MoS2 are suggestive of an adsorbate-substrate interaction that influenced the molecular packing. For uracil monolayers on graphite, the primitive mesh dimensions were indistinguishable from that of the bulk solid and suggested that a larger adsorbate-substrate interaction on MoS2 caused the subsequent skewing of the uracil adsorbate structure on MoS2.23 Differences in site-specific adsorption energies have also been determined in calculations comparing the adsorption of benzene on graphite and MoS2 surfaces.34 The ability of the adsorbate structures to accommodate their substrate dependent conformations is due to the flexibility of the hydrogen-bonding interactions, which are soft and weakly directional.33 In the energy-minimized model of the adenine adsorbate on MoS2 (Figure 4), the proposed structure of the adsorbed layer satisfies the maximum number of possible intermolecular hydrogen bonds. The three proton donor and acceptor moieties of each adenine molecule are involved in cyclic hydrogen bonds with the adjacent molecules on three sides. The cyclic hydrogen bonds are similar to those seen in nucleic acids35 and similarly would be stabilized by π-cooperativity, enhanced through resonance-assisted electronic contributions to the cyclic structure. The structure proposed here is a packing configuration different from that previously proposed for adenine on MoS2,8 which failed to converge in these energy minimization (34) Fisher, A. J.; Blo¨chl, P. E. Phys. Rev. Lett. 1993, 70, 3263. (35) Jeffrey, G. A.; Saenger, W. Hydrogen bonding in biological structures; Springer-Verlag: Berlin, 1994.
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calculations. Although this earlier model similarly satisfied all intermolecular hydrogen bonds, we propose a misinterpretation of the STM data that was complicated by the scan direction dependency on image contrast. Central to the adsorbate structure (Figure 4) is the formation of centrosymmetric dimers that electrically neutralize the strong dipole moments of individual molecules. These dimers are linked to adjacent dimers through nonsymmetrical cyclic hydrogen bonds in a P211 configuration. The symmetry is further reduced to P1 by the electronic interaction of the adsorbate with the substrate. The overall structure is one of a two-dimensional network of continuously linked cyclic motifs, alternating between the aromatic-like character of the adenine heterocycles and the cyclic hydrogen bonds. In the model, there are three orientations that would give rise to continuously linked cyclic motifs. The direction of the adsorbate lattice b vector would describe one of these directional motifs and is composed of a bimolecular row of adenines. In each row, the adenines are in a linear configuration. The molecules within each row are each asymmetrically hydrogen bonded through equivalent cyclic hydrogen bonds to two molecules in the adjacent row. The other two orientations involve inequivalent hydrogen-bonding interactions between adjacent pairs of centrosymmetric dimers. The adsorbate structure proposed here for adenine on MoS2 and previously for adenine on graphite surfaces18 would also account for the observed stability of the adsorbate structure, which was consistently compromised at certain scan directions by forces exerted by the STM tip (Figure 2G). Variations in adsorbate stability can be interpreted in terms of the unsymmetrical nature of the adenine molecules and the inequivalency in the energies of the different intermolecular hydrogen bonds.18 These anisotropic adsorbate-adsorbate interactions were particularly noticeable at the edges of monolayer clusters, which often showed the formation of straight edges (not shown) and had also been observed during adenine monolayer growth and dissolution processes on graphite surfaces.14,19 Examination of the STM images of adenine on MoS2 supports the proposed model in terms of the changing image contrast in response to the STM scan direction. The observed smearing and the subsequent formation of bands could be interpreted as resolving the intermolecular hydrogen bonds as well as the molecular component of the adsorbate. π-Bond cooperativity, which contributes to the stability of cyclic hydrogen bonds between complementary base pairs in nucleic acids, requires that adjacent hydrogen bonding functional groups are linked by bonds with π-electron character.35 The commonly reproduced resonance structures, indicating the π-bond character in adenines (amino tautomer), are shown in the proposed model of the monolayer system (Figure 4) and provide a mechanism for π-electron cooperativity. Overlaying the proposed model directly onto the STM images (Figure 5) shows how the band structure might be constructed from alternating between the adenine heterocycles and the cyclic hydrogen bonds. Molecular Basis of Scan Dependent Image Contrast. The scanning action of the STM tip plays two roles in these experiments. First, quantum electron tunneling between occupied and unoccupied states of the tip extremities and the sample surface provide a mechanism for the real-space imaging of the surface structure. The exact mechanism is not known, but there is an empirical relationship between increasing the relative STM image contrast of submolecular components of organic adsorbates and atomic polarizability, which suggests an image
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Figure 5. STM images (A-D) of an ordered array of adenine molecules adsorbed to the surface of MoS2 (imaging parameters, bias voltage ) -0.85 V, tunnel current ) 106 pA) at varying scan angle. Each image is accompanied by a double-headed arrow that corresponds to the fast scan direction of the STM tip. Overlaid on each image is the proposed lattice model of the adsorbate structure with intermolecular hydrogen bonds shown in white.
contrast mechanism dependent on distortion of the electronic system.26 Second, the potential difference applied across the tunnel junction results in an electric field between the tip and the sample. A dipole moment in a polarizable adsorbate may be permanent or can be induced by the electric field of the tip. The resulting modulation of the barrier to tunneling or the substrate sample’s work function can explain the contrast of different molecular functionalities.37 Polarizable molecular functionalities have been correlated to STM image contrast with brighter regions being assigned to more polarizable groups such as π-electron rich aromatic moieties.37 This would account for the contrast attributed to the adenine molecules assigned in the models (Figure 5), which remained essentially unaltered as a function of changing scan angle. The physical basis for the observed scan angle dependent contrast changes can be explained by proton polarizability and depends, in a highly anisotropic way, on the scanning angle of the applied electric field and its interaction with the cyclic hydrogen bonds between adjacent adenine molecules. There are three inequivalently oriented inplane cyclic hydrogen bond structures within the adenine monolayer (Figure 4). Protons within the cyclic hydrogen bond structures can move within a symmetrical potential well, with either double minima or a single broad minimum. Proton displacement is highly anisotropic, along the axis of the hydrogen bond. Their polarizability is known to be high and small changes in their environment can shift their equilibria.36 For the protons in the adenine monolayer, the applied electric field of the STM tip, on the order of 107 V/m, is sufficient to displace them. The electric field results in an in-plane dipole in the adsorbate, which induces the tautomeric shift of the protons in the hydrogen bond. This causes a simultaneous shift in the electrons. As the cyclic hydrogen bonds are π-electron stabilized and the protons have a high polarizability, their contribution to the STM image is often observed (Figures 2 and 5), but not always (Figure 1A,B). Although the coupling mechanism between the applied electric field and the monolayer is not well understood, it seems likely that components of the applied electric field would influence the anisotropic displacement of the (36) Zundel, D. In Studies in physical and theoretical chemistry; Mu¨ller, A., Ratajczak, H., Junge, W., Diemann, E., Eds.; Elsevier: Amsterdam, 1992; Vol. 78, p 313. (37) Spong, J. K.; Mizes, H. A.; LaComb, L. J., Jr.; Dovek, M. M.; Frommer, J. E.; Foster, J. S. Nature 1989, 338, 137.
protons in an angle dependent fashion because the electric field, its induced in-plane dipole, and the hydrogen bonds are vectorial in nature. At a single scan direction this effect is not always noticeable, except when two or more domains of differing orientation lie juxtaposed in the same STM image frame (Figure 1). Clearly, the temporal way in which the in-plane dipole is scanned across the hydrogen bonds is changed with changing orientation of the adsorbate. When the scan angle is changed, the direction of the electric field is not changed, but the angle with which the electric field interacts with the adsorbate is. Similarly, the temporal way in which the in-plane dipole is scanned across the hydrogen bond is changed with changing scan angle and simulates the case of differing domain orientation. This would be manifested as scan angle dependent changes in image contrast and is what we have observed (Figure 2). The applied electric field will polarize each of the oriented in-plane hydrogen bond motifs differently because each of the hydrogen bond motifs is vectorially distinct. In addition to the perpendicular electric field component of the STM tip, there are, in practice, additional planar components to the electric field that arise due to the asymmetric shape of the tip, so the coupling mechanism of the applied electric field from the STM tip with the adsorbate is not known and an exact relationship between the scan angle and the observed contrast pattern cannot be accurately described. As a first-order approximation, we assume that the best coupling occurs when the STM image contrast of the hydrogen bonds is greatest. There are several scan angle dependent variations that we have observed for the contrast of adenine monolayers on MoS2. The most simple case resolves all molecules in the adsorbate equivalently (Figure 1B); however, this contrast is not commonly observed in single experiments where scan angle is not considered. More typical are images that resolve the molecules together with one or more of their hydrogen-bonding interactions. The most predominantly resolved interaction is the cyclic hydrogen bond between dimers in the centrosymmetric configuration (Figure 5A). A variation of this also resolves one of the nonsymmetrical interactions. Linking of these results in the banding pattern (Figure 5B). The equivalent but opposite banding pattern is also seen but not shown. These anisotropic banding patterns are the most commonly resolved contrasts, as they are observed at scan angles that are most stable to the adsorbate. Images with only
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nonsymmetrical hydrogen bonds (Figure 5C) or all hydrogen bonds (Figure 5D) are rarely resolved, as scanning the STM tip in these orientations typically resulted in destruction of the monolayer. Consistent with this interpretation is the location of the darkly contrasted regions seen in all of the STM images, assigned to the interstitial space between molecules where no molecular or hydrogen bond electronic components would be expected to contribute to the image contrast. Summary The STM analysis of monolayers of adenine formed on MoS2 surfaces shows a marked and anisotropic response of the STM image contrast to the scan direction of the STM tip. Energy-minimized computer models of the adsorbate lattice structure, based on the STM images and the previously determined structure of adenine monolayers on graphite, have been prepared. This analysis provides an interpretation of the image contrast that is dependent on electronic distortion of the substrate barrier to tunneling by the polarizability of the adenine molecules and their intermolecular hydrogen bonds. In our model (Figures 4 and 5), we have attributed the constant features of high contrast to the adenine molecules and the darker regions to the interstitial spaces between them. These do not change markedly with changing scan angle. Only the parts attributed to the cyclic hydrogen bonds are scan angle dependent. The scan angle dependency on image contrast was interpreted in terms of tautomeric proton displacements mediated by an in-plane dipole moment, induced by the electric field of the STM tip.
Sowerby et al.
The proposed structure and the STM image contrast are suggestive of “conductive bands” formed from organic heterocycles with π-electron contributions linked by cyclic hydrogen bonds. The two-dimensional networks of these electrically linked organic heterocyclic structures suggests that the monolayer may have interesting optoelectronic and energy transducing properties. The coupling of three conduction bands in the adenine adsorbate would result in a continuous two-dimensional network throughout the monolayer domain structure. The abiotic synthesis of adenine and subsequent self-assembly into monolayer structures may even provide a prebiotic mechanism to mimic the modern function of adenine as a component in energy transduction. These studies indicate how the scan direction can influence the observed STM contrast in STM images. Model building that can accommodate all of the observed lattice features as a function of varying scan direction provides a self-consistent method for the interpretation of STM images of organic monolayer systems. Acknowledgment. S.J.S. thanks the Alexander von Humboldt-Stiftung for a postdoctoral research fellowship. Support was from the Deutsche Forschungsgemeinschaft through He 1617/3-1/3-2/6-1. Supporting Information Available: Another example of scan angle dependent STM image contrast of an ordered array of adenine molecules as described in Figure 2 (1 page). Ordering information is given on any current masthead page. LA9712350
