COMMENTARY

Supermolecules steer electrons down a wrong- way street COMMENTARY Malcolm D. E. Forbesa,b,1

The controlled movement of electrons is of paramount reaction centers was understood in detail by the 1970s importance for solving current technological problems (7). When the crystal structure of a reaction center that will have broad societal impact. Batteries for became available in 1984 (8), many structure−reactivity electric vehicles, quantum computers, efficient solar relationshipsinphotosynthesisweremoreclearly energy conversion devices, and nanoscale machines elucidated. A key feature of the ET cascade was its for biomedical applications represent just a handful of pronounced directionality: Despite 2 sets of pigments

such possible advances. A current research thrust is to arranged in an approximate C2 symmetry inside the better understand and control the rate and direction- membrane-bound protein, the multistep reaction ality of electron transfer (ET) reactions. The problem of went in only one direction. This observation stimu- ET directionality has long fascinated scientists and lated many scientists to attempt to mimic the process engineers (1), and researchers in the field of electron in solution, and to develop artificial photosynthetic donor (D)–acceptor (A) interactions are now deeply systems (9). immersed in developing methods to exert control The desire for a deeper understanding of photo- over electron motion in molecules, metamaterials, synthesis in plants, to mimic nature’s processes for and bulk materials on micrometer and nanometer solar energy conversion, and for the generation of scales. The PNAS paper by Polizzi et al. (2) reports re- solar fuels, led chemists to develop a special class of sults on directional ET reactions in so-called “supermo- molecule called a donor–spacer–acceptor (DSpA). lecules,” inspired by the ET cascade found in the The Sp moiety is (typically) electronically inert, and the photosynthetic reaction center of plants and certain D and A are covalently (chemically) bonded to each bacteria. This fundamental work is certain to enhance other through Sp. The syntheses of DSpAs were not and stimulate new research in the field. trivial, and were driven by a desire to confirm or refute the solution phase ET theory of R. A. Marcus (10), first Early History proposed in 1956. Marcus predicted a nonlinear de- It is easy to surmise that our ancestors watched light- pendence of the ET reaction rate with respect to the ning strike and wondered why it always came from the free-energy difference between D and A. In particular, sky to the ground instead of the other way around (the it was predicted that ET rates would decrease at large properties of lightning, wind, and sunlight were good free-energy differences (so-called “inverted” behavior), cause for humans to regard Earth’s sky as something whichupsettheconventional wisdom at the time. It special) (3). In the 18th century, Benjamin Franklin’s (4) became clear by about 1980 that experiments in liquids, early experiments with keys and kites (some of the where D and A were free to move with respect to each earliest documented D−A interactions), as well as other, caused problems in verifying the theory (11). In- Joseph Priestley’s (5) observations on oxygen evolu- termolecular diffusion became rate-limiting no matter tion in photosynthesis, stimulated research on the how large the free-energy difference between D and A. nature of the electron and its connection to light inter- In the early 1980s, at Argonne National Laboratory acting with matter (photoredox reactions). Twentieth and the University of Chicago, 2 great intellects col- century chemists such as Ciamician (6) noted the im- lided at the cutting edge of the field. Gerhard Closs, a portance of these connections. highly skilled physical organic chemist, and John Photosynthesis soon became a dominant topic in Miller, a visionary experimental chemist who pioneered the fields of biology and botany. Through collaborations a unique method for measuring thermal ET rates using a with chemists, biochemists, and physicists, the mech- pulsed electron beam (12), began a fruitful collabo- anism of the ET cascade in bacterial photosynthetic ration where they designed, synthesized, and measured

aDepartment of Chemistry, Bowling Green State University, Bowling Green, OH 43403; and bCenter for Pure & Applied Photosciences, Bowling Green State University, Bowling Green, OH 43403 Author contributions: M.D.E.F. wrote the paper. The author declares no conflict of interest. Published under the PNAS license. See companion article 10.1073/pnas.1901752116. 1Email: [email protected].

www.pnas.org/cgi/doi/10.1073/pnas.1908872116 PNAS Latest Articles | 1of3 Downloaded by guest on October 1, 2021 ET rates for a series of DSpA molecules where the diffusion between “wrong-way street”). These 2 distinct states can be selectively

D and A was absent in free solution. The result was a landmark prepared using blue (S3) or red (S1) femtosecond light pulses. 1983 paper that showed, for the first time, the Marcus inverted re- In most photoinduced ET reactions, the primary competition gion in solution at room temperature (13). This work helped earn for deactivation of excited singlets (1D*A) is between charge + – Marcus the 1992 Nobel Prize in Chemistry, and simultaneously cre- separation to singlet radical ion pairs (1D*A to 1[D A ]) and in- ated a cottage industry within the field to build DSpA molecules tersystem crossing (ISC; 1D*A to 3D*A, from which, eventually, the + – that could answer more questions about ET reactions beyond the triplet radical ion pair 3[D A ] arises). The ISC process, which pro- free-energy dependence: orientation of D with respect to A, duces low-energy triplet states and the ensuing triplet radical ion temperature, solvent, spin densities, and, of course, directionality. Collaborations flourished between previously divergent fields of The problem of directionality in photoinduced science (14). ET reactions has been directly addressed by There are many strategies for controlling the directionality of Polizzi et al. using a cleverly designed set of ET. The natural phenomenon of lightning might be called the simple mechanism: a high electric potential of the D (charges in clouds) molecules and highly sophisticated ultrafast above A (the ground). On a smaller scale, assembling an organic spectroscopy. material with a unique electric polarization can ensure electron flow in only one direction (15). Smaller still, molecular conformations (e.g., pairs, is one of the primary deactivation pathways that limit the stereochemistry) can be manipulated to control directionality (16). efficiencies of solar energy conversion devices. By reversing the Oneofthefirstexamplesofdirectional control in a DSpA complex polarization of the singlet state in RuPZn, a remarkable damping came from Fox and Gallopini (17), where the net dipole direction of a of ISC is observed when the “U-turn” ET pathway takes place. In peptide Sp was inverted to show different charge separation rates. In fact, for the “one-way” ET reaction, ultrafast ISC to the triplet + – semiconductor diodes and transistors, on which all of the ones and stifles the formation of the desirable 1(D A ) intermediate. Con- zeroes in our laptops depend, the use of polarization and electric versely, with the “U-turn” ET reaction, the ISC process is sup- + – fields is common, but we are approaching size limitations in such pressed, and the high-energy 1(D A ) photoproduct is selectively materials that will impact future computational speed limits. Mole- realized. The authors hypothesize that, by reversing the polari- cules are the answer, and a major effort is now underway to precisely zation, the orbital overlap (and therefore the ISC rate) between control charge and spin motion on the subnanoscale (18, 19). 1D*A and 3D*A is strongly affected. Scientific and technical challenges in this field depend on the To bring this story full circle, it is worth revisiting the structure and scales involved, from small molecules to bulk materials. For ex- spectroscopy of bacterial photosynthetic reaction centers, which, to ample, a long-standing truism in the field of photocatalysis is that begin with, sparked 4 decades of research on DSpA molecules. One the materials can be cheap, robust, and efficient, but you may only of the most complete studies of Rhodobacter sphaeroides wild type choose 2. At the core of the efficiency issue in these devices is the and mutated reaction centers is by Moore et al. (20) in 1999, using presence of other deactivation pathways. The spin-allowed pho- Stark effect spectroscopy measurements. This work advanced the toexcited singlet states of organic molecules can show complex concept of an asymmetric excited singlet state in the so-called behavior as either Ds or As, and control over their properties is “special pair” of photosynthetic reaction centers, deduced its po- much more difficult. They have many deactivation pathways larization, and demonstrated that the special pair singlet excited available beside ET: fluorescence, internal vibrational relaxation, state is polarized opposite to the direction in which charge flows (a and intersystem crossing to excited triplet states. This situation is “U-turn” ET mechanism). In 2012, it was revealed, through solid-state true for molecules, supermolecules, and more complex systems chemically induced nuclear spin polarization experiments by such as photosynthetic reaction centers. Thamarath et al. (21), that the excited triplet states of the same reaction centers have opposite polarizations to the excited singlet states. The Main Result Polizzi et al.’s (2) model system establishes the photophysical The problem of directionality in photoinduced ET reactions has basis for a previously unrecognized but important fact regarding been directly addressed by Polizzi et al. (2) using a cleverly the reaction center special pair: The opposing singlet and triplet- designed set of molecules and highly sophisticated ultrafast state polarizations serve to curtail ISC and preserve high-energy spectroscopy. The work provides significant insight into a process intermediates throughout the cascade. This work strongly sug- one might call “polarization filtering,” where careful choice of gests that “polarization filtering” is a mechanism by which the which excited state is involved as the D can dictate a strong directionality of ET reactions may be controlled, and that oppo- preference for fast charge separation in a particular direction. The sitely polarized singlet and triplet states are responsible for the molecule under examination consists of a Ruthenium (II) poly- selective, unit quantum yield initial ET event of photosynthesis. It pyridyl compound (Ru for simplicity), connected to a Zn porphyrin is remarkable that we now have a simpler analog from which to moiety (PZn) via an acetylene Sp, as the D. The A, which is directly draw even further insight into such a delicate, but critical, feature attached to the porphyrin ring, is naphthalene diimide, which is of successful photosynthetic materials, both natural and artificial. attached to the porphyrin ring such that there is minimal pertur- The title of this Commentary borrows phrasing from the great bation of the RuPZn ground state. A key property of RuPZn for poet and guitarist Mark Knopfler, and is gratefully acknowledged selective preparation of the D excited state is that its dipole mo- (22). No one has ever seen a “wrong-way street,” and yet most of

ment has opposite directions for the S1 vs. S3 excited singlet us know exactly what that looks like. It is the perfect metaphor for states. For the S3 excited singlet, the dipole favors “one-way” ET, the broader intellectual twists and turns required to appreciate pulling electron density away from the D and toward the A (i.e., this far-reaching and thought-provoking study of photoinduced

“normal” behavior). However, in the S1 excited singlet, the dipole ET reactions. This work is notable for establishing a design prin- is reversed, which can be described as “U-turn” ET (i.e., the ciple for organic molecular electronics, which should provide a

2of3 | www.pnas.org/cgi/doi/10.1073/pnas.1908872116 Forbes Downloaded by guest on October 1, 2021 strategic advantage for researchers seeking to maximize charge research represents a great leap forward at the cutting edge of ET separation efficiencies, and to help prolong the lifetime of high research and should be regarded as one of the most beautiful energy intermediates that can be used for redox catalysis, solar experiments in physical chemistry of the 21st century. power, dye sensitized solar cells, or spin/charge communication. The results lean heavily on the shoulders of the giants whose work Acknowledgments is discussed above but also bring DSpA molecules to a high level I acknowledge the US National Science Foundation for continued support of my of sophistication for the precise control of electron motion. This research program through Grant CHE–1464817.

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