Simulating a Molecular Machine in Action - The Journal of Physical

Article pubs.acs.org/JPCA

Simulating a Molecular Machine in Action Tim Raeker,† Niss Ole Carstensen,† and Bernd Hartke*,† †

Institut für Physikalische Chemie, Christian-Albrechts-Universität, Olshausenstraße 40, D-24098 Kiel, Germany ABSTRACT: Using QM/MM methods, we have simulated the action of a simple molecular machine, a cilium. It consists of a platform for surface mounting, a photochemical motor unit, and a tail-like effector that amplifies the small-scale conformational change of the motor unit into a larger-scale beating motion usable for molecular transport. In this proof-of-principle application, we show that the techniques used here make it possible to perform such simulations within reasonable real time, if the device action is sufficiently fast. Additionally, we show that this molecular device actually works as intended for one isomerization direction. For the other direction, results are inconclusive, possibly because the total propagation times we can afford are too short to capture the complete event.

1. INTRODUCTION Molecular machines1,2 are a hot topic of current research. There are unidirectional molecular rotors with a MHz rotation rate3 that can even be made to switch their rotation sense.4 There are molecular cars5 that have to be pushed around on a surface, and more recent designs6 that may eventually be able to propel themselves forward. Most of the molecular design of these items is done by traditional chemical insight. Clearly, theory can provide important design input. One central problem of molecular machines is the connection from their subnanometer scale to the macroscopic scale, not only in terms of work performed or of material processed but already in detecting their action at all, as exemplified by the attempts to make molecular rotation visible macroscopically.7 Again, theory can come to the rescue and reveal directly if the designed molecular machine actually moves as intended. Since a few years, artificial cilia are an important topic in microfluidics. Electro-statically actuated polymer structures8 have been used to drive fluid flow and mixing, all-polymer microdevices have been fabricated using inkjet printing technology in combination with self-organizing liquid-crystal network actuators9 and were driven by light, and magnetically actuated cilia have been proposed theoretically10 for microswimming. In contrast to those approaches, we simulate here an artificial cilium at the subnanometer scale. The design originates in the Herges group;11 it consists of a surface mount, a photochemical motor unit, and a cilium tail, all integrated into a single molecule. The design hope is that with appropriate photochemical triggering, the motor unit will undergo small-amplitude cis↔trans isomerizations, and these will be translated into large-amplitude cilium beating movements that may then be employed for transport (either of extra particles placed atop an array of these cilia, or of a nanoparticle to which these cilia are attached). Such a simulation, however, is challenging because (a) molecular machines are large molecules from the viewpoint of © 2012 American Chemical Society

theory, (b) photochemical driving (as in this case) enforces a treatment of electronically excited states, and (c) ensuing system action has to be followed over a considerable time interval. All this severely cuts down on the theoretical methods that can be used in practice. Therefore, we build upon our previous work on diazocine.12 There we have shown that the semiempirical floatingoccupation configuration interaction (FOCI) approach by Granucci and Persico13 is fast enough to be practical but still sufficiently accurate to correctly capture photochemical dynamics of azobenzene-based molecular switches, when compared with ab initio calculations (CASSCF/CASPT2) on the one hand and with detailed femtochemical experiments on the other hand.14 Here we employ the QM/MM extension of this approach, also implemented by Granucci and Persico,15,16 to investigate if the intended cilium action actually happens. The remainder of this contribution is organized as follows: The setup of the molecular system is explained in subsection 2.1. Technical details for the employed methods are listed in subsection 2.2, followed in subsection 2.3 by benchmark results of this approach for the present system. Section 3 presents the results of the actual dynamics simulation, followed by conclusions in section 4.

2. MOLECULAR SYSTEM AND COMPUTATIONAL APPROACH 2.1. System Setup. As pointed out in the introduction, mounting reversibly switching molecular functions (for example, molecules that undergo a photoisomerization process) onto a surface is one of the key steps in the design of future nanodevices. Among other difficulties in this field, one of the Special Issue: Jörn Manz Festschrift Received: May 30, 2012 Revised: August 22, 2012 Published: August 23, 2012 11241

dx.doi.org/10.1021/jp305258b | J. Phys. Chem. A 2012, 116, 11241−11248

The Journal of Physical Chemistry A

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azobenzene molecule, resulting in 10 newly optimized parameter values for the nitrogen atoms and 11 for the carbon atoms, respectively.23 This new parameter set was employed in a variety of studies on azobenzene derivatives, including, for example, naked azobenzene, a bridged azobenzene-derivative, and QM/MM studies on azobenzophane or a peptidic derivative of azobenzene. In all cases the parameters were used without further reparametrization and yielded an overall qualitative agreement with both experiment and ab initio data.12,23−25 In our workgroup, we have also employed this parameter set, for a tightly bridged azobenzene derivative,12 again in good agreement with ab initio data and with experimental results. Since the molecular setting in the present study does not differ more strongly from the parent molecule azobenzene (for which the parameters were generated) than it does in those previous examples, we expected it to also perform well here. For all our calculations we used a special version of the MOPAC program package,26 modified by Persico et al. to include direct classical-mechanical dynamics with FOCI-AM1 forces, combined with the fewest switching surface hopping method by Tully.27 To further cut down on computational expense, we employed a QM/MM approach. Besides the azobenzene core the QM part also contains the branched octenyl cilium chain. This is because we used the connection atom (CA) ansatz, where the frontier atom is handled by the force field and is embedded in the QM wavefuntion via its point charge and van der Waals parameter. So having the cilium in the MM part would mean cutting through an electronic conjugation, which would have adverse effects on the quality of the QM wave function. This also allows us to check whether the bigger π-electron system has an influence on the nitrogen bonding in the azobenzene and therefore on the isomerization process as a whole. For the MM part, that is, the TATA platform, we used the TINKER package28 (already linked in MOPAC) with the OPLSAA-L forcefield29 with some minor modifications. These included adding in missing parameters for the carbon−carbon triple bond and the tertiary amines of the TATA platform.30 For all calculations the floating ocupation width parameter13 was set to 0.1 au. All FOCI-AM1 calculations were carried out with a CAS-CI of six electrons in four orbitals plus single excitations from the seven highest occupied to the six lowest unoccupied orbitals for a total of 94 determinants in the CI space. This corresponds to the setup of the FOCI-AM1 semiempirics employed for reparametrization of azobenzene (AB) and was used without further modification. The geometry optimizations were performed with FOCIAM1/OPLSAA-L QM/MM and also with a density functional theory (DFT) calculation for comparison purposes, with tight convergence criteria. During all dynamic runs, ground or excited states, all 336 degrees of freedom were active. Apart from representing the platform with a classical force field no further model asumptions were made. UV spectra were calculated from Brownian dynamic runs at a temperature of 298.15 K, with a total propagation time of 15 ps and a time step of 0.1 fs. The initial structures for the excited states dynamics were also taken from these trajectories by randomly choosing structures that are within a certain energy range to the S1 state, that is, 440 ± 40 nm for both isomers, to create starting structures corresponding to the excitation energy of the n → π*-peak in the UV spectra. The trajectories for the excited

key problems appears to be preserving the functionality of the adsorbed molecules. Requirements for preserving molecular functionality are both of sterical nature (sufficient space for the isomerization process, avoidance of direct contact between substrate and functional group) and of electronic nature (coupling between the photoswitchable moiety and the substrate may render the molecule unswitchable). An elegant way of overcoming these problems is the concept of a molecular platform17,18 with a defined adsorption geometry to which the target functional molecule can be attached. Upon self-assembly from solution, these functionalized platforms are capable of forming an ordered monolayer at a surface,17,18 with the functional molecules standing upright. The artificial cilium in this study is one possible candidate for such a functionalized platform. The platform itself consists of a triazatriangulenium unit (TATA) with an ethinyl spacer, while the switching functionality is provided by an azobenzene unit, following the experimental approach of Herges et al.17,18 For completion of this artificial cilium, we added a hydrocarbon chain to the azobenzene, as effector tail of the cilium. In a smaller project prior to the present study,19 this hydrocarbon chain was optimized for maximum momentum transfer and impact stability, with classical molecular dynamics simulations employing the reactive force field reaxFF20,21 in its implementation within the ADF program package.22 Although the reaxFF approach is able to handle breaking and formation of chemical bonds, also including the azobenzene photoisomerization into such a simulation would require further extensive assumptions and modeling. Hence, we employ a QM/MM approach in the present study to simulate the photoisomerization of the complete artificial cilium, consisting of platform, linker, azobenzene, and hydrocarbon chain, in the gas phase (ignoring the surface mount via the platform, and possibly present solvent molecules). Within the QM/MM simulations we have set the QM part to contain the azobenzene and the hydrocarbon chain, while the platform is taken to be the MM part (Figure 1). Technical details about the simulation of the excited state dynamics, composition of QM and MM parts, and the linking of both are presented in section 2.2. 2.2. Methods. As the method of choice for the calculations in this work we used a floating-occupation configuration interaction (FOCI) method with semiempirical AM1 orbitals.13 The AM1 parameters in this approach were reoptimized by Persico et al. against high-level ab initio data, specifically for the

Figure 1. Schematic structure of the simulated molecular machine in this work and assignments for each part: QM = quantum mechanics, MM = molecular mechanics. 11242



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Table 1. Comparison of Optimized Geometries: DFT(TPSS/TZVPP) versus QM/MM(FOCI-AM1/OPLS-AA-L)a transDFTb transQM/MMc cisDFTb cisQM/MMc

CNNC

NNCCT

NNCCD

NNCT

NNCD

CNT

CND

NN

179.8 179.8 14.6 0.5

0.2 0.4 45.1 2.9

0.7 0.8 42.8 89.1

114.3 118.7 124.0 130.8

115.1 120.3 124.4 131.3

1.409 1.439 1.426 1.430

1.405 1.449 1.422 1.446

1.273 1.280 1.257 1.254

a

The subscripts label the direction towards the TATA-platform (T) or the top of the cilium (D). bThis work, TPSS/TZVPP. cThis work, FOCIAM1/OPLS-AA-L.

Figure 2. Ground state structures resulting from geometry optimizations on DFT (TPSS/TZVPP) and QM/MM (FOCI-AM1/OPLS-AA-L) level of theory.

Figure 3. Comparison of calculated and experimental UV spectra. Panel (a) shows the experimental azo-TATA spectra taken from ref 18 while panel (b) shows the calculated QM/MM spectra of the cilium. A direct comparison is shown in panels (c) and (d). No shift was applied to the spectra (see text for details).

comparison of our QM/MM structures was carried out against the optimized Tao, Perdew, Staroverov, and Scuseria functional and triple-ζ valence plus polarization basis set (TPSS/TZVPP) ground state structures of both isomers. The characteristic degrees of freedom for these optimized structures are shown in Table 1. While the optimized structures of DFT and QM/MM for the trans-isomer show only subtle differences, well within expect-

states dynamics of both isomers were propagated for 3.25 ps with a time step of 0.1 fs, starting from the S1 state and only taking this first excited state into account. In total we calculated 200 surface-hopping-trajectories for both the cis→trans- and the trans→cis-photoisomerization. 2.3. Benchmarks. Because of the size of the cilium on the TATA, excited state calculations of benchmark quality level of theory become very challenging. For this reason a first 11243



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Note that none of the spectra were artificially shifted to improve the match. Although the overall intensities differ from the experimental ones, the relative intensities still show satisfactory agreement with experiment, even though the transition dipole moments were not part of the reparametrization procedure. While the transition dipole moments reflect the intensities of the UV peaks, the peak positions reflect the shapes of the surfaces around the Franck−Condon region. Note that within the actual surface hopping dynamics the transition dipole moments are of no importance in contrast to the shapes of the surfaces. Another effect not included in our spectra is the mixing of both isomers in experiment. In our case the cis-UV-spectrum results from the cis-isomer only, while the experimental spectrum contains a mixture of trans- and cis-isomers, which is clearly visible in the remaining shoulder at 330 nm. We consider this to be a promising result encouraging the following calculation of surface hopping dynamics with the aim of gaining qualitative insight into the excited states dynamics.

ation range for a QM/MM-approach, the cis-isomers seem to differ more significantly. A closer look at the listed degrees of freedom reveals differences mainly in NNCC-dihedral angles and less prominently in the CNNC-dihedral angle. A possible explanation is visible in Figure 2 where both DFT and QM/ MM optimized structures are shown. The cis-QM/MM-structure seems to form an attractive interaction between the H-atom of the lower phenyl ring and the π-system of the upper phenyl ring, resulting in a shorter distance between H-atom and phenyl ring. This effect is missing in the optimimized DFT-structure. It is difficult to decide whether the QM/MM-approach is overestimating this interaction or DFT is underestimating it. Since this is a proofof-principle application, and since we achieved very good agreement in the simulation of experimental spectra, we leave this question for future planned ab initio calculations. So far the only available information about the excited states of azo-TATA is an experimental UV spectrum.18 For this reason a direct comparison of QM/MM-FOCI-AM1 UVspectra of the full cilium (TATA-azo-tail) against the corresponding experimental spectra of azo-TATA is an important quality criterion. The UV-spectra were calculated from two 15 ps ground state trajectories with Brownian motion at 298.15 K following the procedure of Persico et al.23,24 Figure 3 shows overall spectral features typical for azobenzene compounds, although both isomers show a characteristic shift in higher excitations. This shift is most prominent in the S0 → S2-excitation of the trans-isomer (see Table 2 for details). In direct comparison against experimental

3. RESULTS The photodynamics of trajectories starting from the cis-isomer on the first excited state show a rapid decay to the ground state, which can be seen from Figure 4 where 50% of the trajectories are back on the ground state surface after ≈42 fs, with the average time of the return to the ground state being 53.5 fs. During the short excited state dynamics the CNNC dihedral changes most dramatically, with Δ(CNNC) = 45° on average (see Table 3 for this and other average coordinate changes; in this table, we have averaged the starting values of the corresponding degree of freedom on the S1 surface and the values upon first return to the S0 surface, over all trajectories. In contrast to Figure 5, in this table dihedral angles are shown without signs (after averaging). Dihedral angle differences and changes all remain within the interval [0°, 180°]). Since the NNC angles show only a slight increase during the dynamics on the S1-surface, the coordinates which are considered to be of further importance are the NNCC dihedral angles; they have to close to form the trans-structure. The NNCC dihedral pointing toward the cilium's tail appears to be the one with the bigger relative change during the excited state dynamics, although both keep on changing steadily to form the cis-isomer on the ground state surface. As can be seen from the angle velocities in Table 3, all degress of freedom listed experience a significant increase in angle velocities on the excited state surface, suggesting a rather steep shape of the excited state surface.

Table 2. Comparison of Experimental Azobenzene (AB), FOCI-AM1-Azobenzene and FOCI-AM1-TATA-Cilium Vertical Excitation Energiesa exp. ABcisb exp. ABtransb FOCI-AM1 ABcisc FOCI-AM1 ABtransc FOCI-AM1 Ciliumcisd FOCI-AM1 Ciliumtransd

S0 → S1

S0 → S2

S0 → S3

433.5 442.8 429.0 438.1 426.1 441.2

283.1 314.7 255.1 283.7 291.7 353.2

227.9 263.2 281.8 279.2

a

All values are given in nanometers (nm). bRef 23. cRef 31. dThis work, FOCI-AM1/OPLS-AA-L.

spectra our simulated spectra show very good agreement. Characteristic points and peak positions are captured nicely.

Figure 4. Population of states (as fraction of trajectories on current state) averaged over all trajectories. Panel (a) shows the S0 and S1 populations resulting from n → π* excitation of the cis-isomer, panel (b) shows the corresponding populations of the trans-isomer. 11244



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far larger trajectory sampling. In contrast to the initial photochemical S1 events that are over after about 50 fs, the time scale for the ensuing ground state movements is on the order of a few picoseconds. A cartoon-like picture of the cis→trans isomerization process is given in Figure 6. Apparently, the photochemically driven

Table 3. Surface Hopping Results for cis→trans and trans→ cis Photodynamics upon n → π* Excitationa

CNNC CNNT CNND NNCCT NNCCD dCNNC/dt dCNNT/dt dCNND/dt dNNCCT/dt dNNCCD/dt return to S0 [fs]

cis→trans, start

cis→trans, end

trans→cis, start

trans→cis, end

5.17 127.53 128.44 116.13 95.70

50.09 130.84 131.40 109.95 94.18

177.31 118.52 117.94 169.94 18.99

173.78 130.68 139.24 175.61 31.71

0.035 0.033 0.025 0.043 0.039

0.613 0.134 0.127 0.357 0.321 53.5

0.018 0.128 0.123 0.019 0.041

0.387 0.315 0.215 0.343 0.474 135.63

The change dX/dt of coordinate X is given at the first two steps on the S1 surface (start) and at the first two steps after return to the ground state S0 (end). Additional subscripts label the direction towards the TATA-platform (T) or the top of the cilia (D). All values are averaged over all trajectories. Units are fs and degrees or Å, accordingly. a

Apparently, this is most pronounced for the CNNC dihedral, indicating a very efficient switching from cis to trans. Incidentally, the steepness of the S1 surface also is in line with the short lifetimes mentioned above. Following the trajectory data over a much longer time interval (cf. Figure 5) indicates that the photochemical events (in the sense of what happens on the S1 surface) only are the initial trigger for much more pronounced molecular movements after the system has returned to the electronic ground state. (Note that the definition of the dihedral angles stayed the same for all trajectories. Signs in dihedral angles indicate different directions during the dynamics. Also note that deviations from the optimized ground state geometries given in Table 1 are due to the dynamics. Especially the NNCC dihedrals can rotate rather freely.) When looking at the state populations depicted in Figures 4 and 5 for the trans→cis isomerization, it should be noted that these trajectories were showing a greater diversity in behavior than those of the cis→trans isomerization. This less clear-cut behavior may be part of the problems encountered during the simulation of the trans→cis isomerization, as it would require a

Figure 6. Snapshots taken from a reactive cis→trans trajectory. The sketch marks the change of CNNC- and both NNCC-angles (see text for details).

conformational switch of the azobenzene chromophore is successfully translated into a large-scale flapping motion of the artificial cilium tail appended to it, and this happens on the slower ps time scale mentioned above. This is exactly the effect intended by this molecular setup, and hence it confirms the molecular design which was done in a static, abstract fashion, prior to the present dynamics test. This may seem to be a rather trivial finding, until other possible outcomes are considered: The photochemical action is triggered in the central NN azo unit and manifests itself at first only as an impulsive change in the CNNC dihedral,12 that is, as a very localized, fast, and mode-specific movement. The cilium tail, however, and in the present setup also the TATA platform on the other end of the azobenzene unit, together constitute a comparatively large molecular system that offers

Figure 5. First 1500 fs of two typical (reactive) trajectories starting on the Franck−Condon-Region of the S1 surfaces of the trans and cis isomers respectively. Gray shaded backgrounds mark that the system is on the S1 surface. See text for details. 11245



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twice as slow, or even slower. This is beyond the total propagation times we can afford with our hardware. Further complications manifest themselves in the state populations depicted in Figures 4 and 5. As already pointed out, the trajectories show diverse behavior and exhibit many surface hops. To define a S1 decay more clearly, one would have to distinguish between the initial dynamics and the repopulation of the excited state. It might be possible to explain the long time trapping in the excited state with the existence of an S1 minimum, which could have an impact on the excited state decay. In fact, it is often seen in the photochemistry of azobenzene derivatives and other photoactive compounds that the S1 surface possesses minima in close vicinity to conical intersection seam minima. However, since excited systems usually exhibit a large amount of excess kinetic energy, barrier crossings or a surface hopping to the groundstate are likely to appear within a few vibrational excursions. In either case, the trappings are limited in time. The effects on the dynamics are usually a delayed decay and a possible lowering of quantum yields. We expect this to be the case in the present study as well. Nonetheless this remains a hypothesis since even a few vibrational excursions of our cilia system exceed the power of our current hardware. The computed quantum yields, that is, the fractions of reactive trajectories, are listed in Table 4. The quantum yields

very many degrees of freedom into which to dissipate initial impulsive kicks. Of course, many modes of this dissipation are slow compared to photochemical events like the present one, but the central issue to be tested here is whether such an ultrafast event can be translated into one specific intended movement of a larger molecular arrangement. Since such a larger movement is of the same basic nature as other molecular ground-state movements, it happens on the very same time scale and hence is in competition with them. The intended movement is a very specific one, whereas all other possible movements of similar speed obviously are far more numerous. So, on second thought, the prospects for photochemically triggered but specific molecular action seems to be bleak. Therefore, a properly chosen molecular design has to ensure that the intended specific movement really happens, in face of all the other possibilities. Apparently, this was successfully realized here. With other molecular designs, very different outcomes can be envisioned and, in fact, may be more likely: A more flexible cilium tail may start to coil up on itself after an initial impulse, or it may wrap around the azobenzene unit or become tangled up with the platform. A heavier and/or longer cilium may display too much inertia so that the azobenzene motor unit turns out to be too weak to induce appreciable motion of such a cilium. Our initial, abstract testing of only the cilium tail in several forms19 also involved considerably stronger initial movement impulses which then lead to dissociative events in various places of the molecular setup. None of all that happens here, which indicates a balanced molecular design, appropriate for the desired task. From the reactive trajectories we calculated an average velocity of 8 × 10−3 Å/fs for the C-atom marked with a circle in Figure 6. From our previous cilium tests19 we know that such a velocity is well within the interval that leads to significant transport when the cilium hits a (sub)nanoscale object like a C60 buckyball, without causing rupture of the cilium or of the object to be transported. While the trajectories starting from the cis-isomer show complete switching, and translation of this initial impulse into large-amplitude cilium motion, during our simulations of the first 3.25 ps of the trans→cis dynamics the cis-isomer was not completely reached. A simple but strong reason for this may be that the trans→cis-dynamics takes too long to be observable within this maximum time frame that we can afford computationally. For the parent compound AB, it is known from both simulations23 and femtosecond time-resolved spectroscopy32 that the photoreaction from the trans- to the cis-isomer takes about twice as long as in the opposite isomerization direction. This is corroborated by our findings for the present system: We did see the initiation of the expected behavior, namely, a rotation-based reaction mechanism with a prominent change in the CNNC-dihedral (see Figure 5; note that this figure shows two single trajectories; hence, not all features are present in all other trajectories). However, the data in Table 3 demonstrate that the initial CNNC angular velocity and in particular also the final one on the S1 state (at the initial movement away from the Franck−Condon point, and directly after the S1 → S0 surface hop, respectively) are much smaller than for the cis→trans isomerization direction, by a factor of about two. As described above, this CNNC action on the S1 surface only is the kick-start for a possibly ensuing largeamplitude cilium movement on a much longer time scale. If the initial trigger for this latter movement only is half as intense, it is to be expected that the large-scale cilium movement also is

Table 4. Simulated (Cilium) and Experimental (Naked AB) Quantum Yields for cis→trans- and trans→cisPhotoisomerization upon n → π*-Excitation sim.a Φcis→trans Φtrans→cis a

exp.b c

0.57 (±0.04) ≤0.27 (±0.03)c

FOCI-AM1/OPLSAA-L, this work. [Φ(1−Φ)/Nt]1/2.

b

0.40−0.75 0.20−0.36

Taken from ref 23. cσ =

appear to be well within the range of naked azobenzene quantum yields deduced from experiment. It should be noted that the quantum yields for the trans→cis-isomerization are upper limits in that the trajectories did not fully reach the cisisomer within simulation time. To arrive at quantum yield values nevertheless, we applied the assumption that reactive trajectories will undergo a CNNC-torsion-like mechanism, similar to naked azobenzene, and that only trajectories reaching a CNNC-dihedral of 90° are capable of proceeding to the cisisomer. Following the reasoning of this assumption we approximated the upper limit of the quantum yield of the trans→cis-isomerization as the fraction of trajectories reaching a CNNC-dihedral angle of 90°. One should take into account that adding a solvent will most likely lower the isomerization quantum yields, but then the given number would still be an upper limit. If, however, the above mechanism assumption does not hold, this upper-limit property may be lost. In comparing to experiment, also note that we are not capable of simulating a photostationary equilibrium as it will probably be achieved in an experimental setup, and that according to experiment this photostationary equilibrium for azo-TATA (without a cilium tail) contains a rather high amount (73%) of cis-isomer at room temperature in [D8]toluene.18 The existence of this cis−trans mixture in a photostationary state of a closely related molecule provides evidence that both photoisomerization directions are possible experimentally. As our group has already demonstrated in 11246



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previous work,33 addition of suitable substituents in a fully automated, global optimization approach can be used to “tune” the excitation wavelengths for the cis- and the trans-isomer to predefined values, which in turn can be exploited to arrive at purer photostationary states, that is, at more complete photoswitching processes.

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4. CONCLUSIONS Using QM/MM direct dynamics, we have shown that a preconceived molecular cilium setup, consisting of a surfacemount TATA platform, an azobenzene photochemical motor unit, and a conjugated, branched hydrocarbon chain (dynamically designed previously), displays exactly the desired mode of action: Photochemical excitation to the S1 state induces an ultrafast cis→trans isomerization at the central azobenzene CNNC moiety. This is then amplified into a large-amplitude beating motion of the attached cilium tail, which is operative on a time scale of a few ps, that is, long after the return of the whole system into the electronic ground state. Judged from the cilium velocity, this beating motion could indeed induce transport on the (sub)nanometer scale. Unfortunately, we could not observe a complete trans→cis back-isomerization of the azobenzene unit. This may lead to a back-stroke of the cilium, completing a full operative cycle, driven by two laser pulses of different wavelengths. From our partial results on this isomerization direction we deduce that the coupled azobenzene-cilium action presumably is too slow to be captured within the limited simulation time we can afford. Future work on these and similar systems will also include the surface to which the TATA platform is attached. This will allow to test if this physisorption is strong enough to hold the system during action or if the platform will dissociate from the surface at one of the first cilium beats. Further tests will check if azobenzene isomerizations also lead to cilium beatings if the starting conformation of the cilium is far from its equilibrated one. Success in both tests is necessary for the intended transport action of the cilium. The transport itself will also be directly investigated by adding a target molecule to the MM part of the model. An experimentally realizable setup that also can perform macroscopically useful transport will have to involve large ensembles of many copies of such cilium systems. A direct simulation of such a setup is well beyond current QM/MM capabilities, but it may be amenable to a purely MM treatment, using reactive force fields fitted to QM ground- and excited states. For such a fitting, the present QM/MM simulation will serve as a valuable benchmark. Work along these lines is also under way in our lab.

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AUTHOR INFORMATION

Corresponding Author

*E-mail: [email protected]. Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS It is a pleasure for us to thank Dr. G. Granucci and Prof. M. Persico (Univ of Pisa, Italy) for valuable advice and for permission to use a modified MOPAC program for FOCI-AM1 surface-hopping dynamics. This work was inspired by the collaborative research project SFB 677 “Function by Switching”. 11247



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(33) Carstensen, N. O.; Dieterich, J. M.; Hartke, B. Phys. Chem. Chem. Phys. 2011, 13, 2903.

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Simulating a Molecular Machine in Action - The Journal of Physical

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