C O M M U N I C A T I O N S
proton activity, to move the oxidizing equivalent from the sensitizer
at the semiconductor surface to a mediator. Key features of the
construct are that a considerable fraction of the high potential of
the porphyrin radical cation is maintained in the phenoxyl radical
and the notoriously irreversible phenoxyl/phenol redox couple is
instead chemically reversible (an imperative for a mediator).
Acknowledgment. This work was supported by the U.S.
Department of Energy (FG02-03ER15393 and DE-AC02-
06CH11357). T.A.M. acknowledges the Blaise Pascal Research
Chairs for support of work in biomimetic solar energy conversion
in collaboration with groups at Universite´ Paris-Sud, Orsay, and
CEA Saclay. We thank Ally Aukauloo, A. William Rutherford,
and Sun Un for their insightful suggestions.
Supporting Information Available: Synthesis and structural char-
acterization, electrochemical data, TiO2 preparation, EPR data. This
References
(1) The term PCET is used here to denote all regimes of coupling from stepwise
to concerted.
(2) (a) Stubbe, J.; Nocera, D. G.; Yee, C. S.; Chang, M. C. Y. Chem. ReV.
2003, 103, 2167–2201. (b) Faller, P.; Goussias, C.; Rutherford, A. W.;
Un, S. Proc. Natl. Acad. Sci. U.S.A. 2003, 100, 8732–8735. (c) Mayer,
J. M. Annu. ReV. Phys. Chem. 2004, 55, 363–390.
(3) (a) Barry, B. A.; Babcock, G. T. Proc. Natl. Acad. Sci. U.S.A. 1987, 84,
7099–7103. (b) Debus, R. J.; Barry, B. A.; Babcock, G. T.; McIntosh, L.
Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 427–430. (c) Yachandra, V. K.;
Sauer, K.; Klein, M. P. Chem. ReV. 1996, 96, 2927–2950. (d) McEvoy,
J. P.; Brudvig, G. W. Chem. ReV. 2006, 106, 4455–4483.
Figure 1. (a) Experimental photoinduced X-band (9.5 GHz) EPR spectrum,
at 4.2 K, of an acetonitrile suspension of TiO2 and 1. (b) Experimental
photoinduced D-band (130 GHz) EPR spectrum, at 13 K, of an acetonitrile
suspension of TiO2 and 1 (red line), simulated 2•+ (green line), simulated
3•+ (purple line), and the sum of simulations [(2•+) + (3•+)] (black line).
The experimental spectra were recorded as the magnetic field dependence
of the two-pulsed electron spin echo intensity. The dotted lines connecting
panels a and b indicate the region of the spectrum investigated by D-band
(4) (a) Mamedov, F.; Sayre, R. T.; Styring, S. Biochemistry 1998, 37, 14245–
14256. (b) Hays, A.-M. A.; Vassiliev, I. R.; Golbeck, J. H.; Debus, R. J.
Biochemistry 1999, 38, 11851–11865. (c) Diner, B. A. Biochim. Biophys.
Acta 2001, 1503, 147–163. (d) Debus, R. J. Biochim. Biophys. Acta 2001,
1503, 164–186. (e) Ferreira, K. N.; Iverson, T. M.; Maghlaoui, K.; Barber,
J.; Iwata, S. Science 2004, 303, 1831–1838. (f) Loll, B.; Kern, J.; Saenger,
W.; Zouni, A.; Biesiadka, J. Nature 2005, 438, 1040–1044.
(5) (a) Hoganson, C. W.; Babcock, G. T. Science 1997, 277, 1953–1956. (b)
Tommos, C.; Babcock, G. T. Biochim. Biophys. Acta 2000, 1458, 199–
219. (c) Meyer, T. J.; Huynh, M. H. V.; Thorp, H. H. Angew. Chem., Int.
Ed. 2007, 46, 5284–5304.
(6) (a) Maki, T.; Araki, Y.; Ishida, Y.; Onomura, O.; Matsumura, Y. J. Am.
Chem. Soc. 2001, 123, 3371–3372. (b) Benisvy, L.; Bill, E.; Blake, A. J.;
Collison, D.; Davies, E. S.; Garner, C. D.; Guindy, C. I.; McInnes, E. J. L.;
McArdle, G.; McMaster, J.; Wilson, C.; Wolowska, J. Dalton Trans. 2004,
n/a, 3647–3653. (c) Costentin, C.; Robert, M.; Save´ant, J.-M. J. Am. Chem.
Soc. 2006, 128, 4552–4553. (d) Rhile, I. J.; Markle, T. F.; Nagao, H.;
DiPasquale, A. G.; Lam, O. P.; Lockwood, M. A.; Rotter, K.; Mayer, J. M.
J. Am. Chem. Soc. 2006, 128, 6075–6088.
•-
EPR. In panel b, the TiO2 signal is not shown.
resulting holes are localized on the phenol and 5% on the porphyrin.
Following illumination at 4.2 K, only 48% of the holes are localized
on the phenol and 52% on the porphyrin. Raising the temperature
from 4.2 to 80 K results, once again, in localization of 95% of the
holes on the phenol. The holes remain localized on the phenol
moiety when the temperature is cycled back to 4.2 K.
The observed temperature dependence of the charge shift is
attributed to restricted nuclear motion at low temperature. At 4.2
K approximately half of the molecules are trapped in a high-energy
state, and only relax to a lower energy state upon warming to 80
K. This situation is reminiscent of the observation of a trapped
high-energy state in natural photosynthetic systems.2b,10 The present
data, complicated by heterogeneity11 in the frozen sample, are
insufficient to resolve a detailed relaxation mechanism. However,
the model system reduces the variables present in the natural system
that affect the redox behavior, and thereby sets the stage for a better
understanding of the critical role of the phenol-imidazole H-bond
in water oxidation.
In conclusion, a model for the donor side of PSII, which includes
a chlorophyll-like photoactive species, has been prepared and
characterized. The presence of a final charge separated state
involving a phenoxyl radical is demonstrated using low temperature
photoinduced D-band EPR spectroscopy. This construct models the
TyrZ-His190 mediator coupling of P680•+ to the water-oxidizing
unit (OEC) in the reaction center of PSII and provides a built in
high-potential mediator thermodynamically capable of coupling the
dye-sensitized anode of a photoelectrochemical cell12 to an ap-
propriate water-oxidation catalyst.13 The construct uses a bioinspired
concept, a stepwise electron transfer process with tight control of
(7) (a) Hung, S.-C.; Macpherson, A. N.; Lin, S.; Liddell, P. A.; Seely, G. R.;
Moore, A. L.; Moore, T. A.; Gust, D. J. Am. Chem. Soc. 1995, 117, 1657–
1658. (b) Burdinski, D.; Wieghardt, K.; Steenken, S. J. Am. Chem. Soc.
1999, 121, 10781–10787. (c) Sjo¨din, M.; Styring, S.; Åkermark, B.; Sun,
L.; Hammarstro¨m, L. J. Am. Chem. Soc. 2000, 122, 3932–3936. (d)
Lachaud, F.; Quaranta, A.; Pellegrin, Y.; Dorlet, P.; Charlot, M.-F.; Un,
S.; Leibl, W.; Aukauloo, A. Angew. Chem., Int. Ed. 2005, 44, 1536–1540.
(8) (a) Land, E. J.; Porter, G.; Strachan, E. Trans. Faraday Soc. 1961, 57,
1885–1893. (b) Richards, J. A.; Whitson, P. E.; Evans, D. H. J. Electroanal.
Chem. 1975, 63, 311–327. (c) Rappaport, F.; Lavergne, J. Biochemistry
1997, 36, 15294–15302.
(9) (a) Blankenship, R. E.; Babcock, G. T.; Warden, J. T.; Sauer, K. FEBS
Lett. 1975, 51, 287–293. (b) Gilchrist, M. L., Jr.; Ball, J. A.; Randall, D. W.;
Britt, R. D. Proc. Natl. Acad. Sci., U.S.A. 1995, 92, 9545–9549. (c)
Svistunenko, D. A.; Cooper, C. E. Biophys. J. 2004, 87, 582–595.
(10) In the present work, no temperature dependent change in the gx tensor of
the phenoxyl radical was observed. For TyrD• in Mn-depleted PSII, a change
in gx upon warming from 1.8 to 77 K is mainly attributed to either
deprotonation of a histidinyl cation or movement of the uncharged histidine
away from the tyrosyl radical.2b In 1 the lack of a secondary proton acceptor
and the covalent attachment of the benzimidazole base likely preclude such
changes to the local electrostatic environment of the phenoxyl radical.
(11) Heterogeneity encompasses various frozen conformations and tautomeric
structures of 1.
(12) (a) Gra¨tzel, M. Nature 2001, 414, 338–344. (b) Meyer, G. J. Inorg. Chem.
2005, 44, 6852–6864. (c) Hambourger, M.; Gervaldo, M.; Svedruzic, D.;
King, P. W.; Gust, D.; Ghirardi, M.; Moore, A. L.; Moore, T. A. J. Am.
Chem. Soc. 2008, 130, 2015–2022.
(13) (a) Hoertz, P. G.; Kim, Y.-I.; Youngblood, W. J.; Mallouk, T. E. J. Phys.
Chem. B 2007, 111, 6845–6856. (b) Cady, C. W.; Crabtree, R. H.; Brudvig,
G. W. Coord. Chem. ReV. 2008, 252, 444–455.
JA803015M
9
J. AM. CHEM. SOC. VOL. 130, NO. 32, 2008 10467