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J. Phys. Chem. B 2000, 104, 6668-6673
Effect of Terminal Groups, Polyene Chain Length, and Solvent on the First Excited Singlet States of Carotenoids Zhangfei He,† David Gosztola,‡ Yi Deng,† Guoqiang Gao,† Michael R. Wasielewski,§ and Lowell D. Kispert*,† Department of Chemistry, The UniVersity of Alabama, Tuscaloosa, Alabama 35487-0336; Chemistry DiVision, Argonne National Laboratory, Argonne, Illinois 60439; and Department of Chemistry, Northwestern UniVersity, EVanston, Illinois 60208 ReceiVed: March 2, 2000; In Final Form: May 10, 2000
The effect of terminal groups, polyene chain length, and solvent on the first excited singlet states (S1) of carotenoids was studied by steady-state and transient optical absorption spectroscopy, and AM1 semiempirical molecular orbital calculations. The carotenoids studied were ethyl 8′-apo-β-caroten-8′-oate (I), ethyl 6′-apoβ-caroten-6′-oate (II), ethyl 4′-apo-β-caroten-4′-oate (III), 8′-apo-β-caroten-8′-nitrile (IV), 6′-apo-β-caroten6′-nitrile (V), 4′-apo-β-caroten-4′-nitrile (VI), 8′-apo-β-caroten-8′-al (VII), and 6′-apo-β-caroten-6′-al (VIII). Solvents were 3-methylpentane (3-MP) and MeCN. The effect of solvent on the S1 absorption maxima is similar to that on the ground state (S0) absorption maxima, which suggests that both effects stem from the same type of interaction, i.e., the dispersive interaction between carotenoids and solvents. Carotenoids with terminal CHO groups have S1 absorption maxima at longer wavelenths than those with terminal CN or CO2Et groups. The S1 absorption maxima are red-shifted with increasing polyene chain length. In the nonpolar solvent 3-MP, the S1 lifetimes of carotenoids depend mainly on the polyene chain length. With a one CdC bond increase, the S1 lifetime decreases by a factor of ca. 2 (ca. 24 ps for I, IV, and VII; 12 ps for II, V, and VIII; and 7 ps for III and VI). Terminal groups have little effect on the S1 lifetimes in 3-MP. However, in the polar solvent MeCN, carotenoids with terminal CHO groups have decreased S1 lifetimes (ca. 8 ps for VII and 6 ps for VIII), while carotenoids with terminal CN and CO2Et groups have essentially unchanged S1 lifetimes. This observation, along with the data of β-carotene and 7′-apo-7′,7′-dicyano-β-carotene, suggests that polar solvents could decrease the S1 lifetimes of carotenoids, when, and only when, there is considerable charge transfer character in their excited states.
Introduction Carotenoids are found in photosynthetic systems. The most important roles that they play are photoprotection and light harvesting.1-4 They can protect photosynthetic systems either by quenching (bacterio)chlorophyll ((B)chl) triplet states, to prevent their reaction with molecular oxygen (which results in the formation of the damaging singlet oxygen), or by directly reacting with singlet oxygen to detoxify it. Carotenoids can also play the photoprotection role by dissipating excess energy. They serve as light-harvesting antennae by absorbing light energy in the visible region of the spectrum, where (B)chls are not efficient absorbers, and then transferring energy for use in photochemical events. It has been suggested that carotenoids carry out energy transfer with the special pair of (B)chls via monomeric (B)chls,5 but the path is not fully understood. According to the currently accepted theory, energy transfer can occur between the S1 states (first excited singlet states, 2Ag-) of carotenoids and the Qy states of (B)chls, and between the S2 states (second excited singlet states, Bu+) of carotenoids and the Qx states of (B)chls. Energy transfer from the S2 state of spirilloxanthin to the Qy state of Bchl was also recently proposed.6 One important * To whom correspondence should be addressed. † The University of Alabama. ‡ Argonne National Laboratory. § Northwestern University.
aspect in the study of the energy transfer of carotenoids is the determination of the energy levels of the S1 and S2 states of carotenoids. The energy levels of the S2 states can be readily determined from ground state optical absorption spectra, because transition from the S0 (ground state, 1Ag-) to S2 is optically allowed. However, the energy levels of the S1 states cannot be determined directly from ground state optical absorption spectra, because the transition from S0 to S1 is optically forbidden. Although the S1 states of several carotenoids have been estimated by fluorescence and Raman spectroscopy, the precise energy levels of their S1 states are not known. Furthermore, the S1 energy levels of many carotenoids have not even been estimated. More information about the S1 energy levels is needed to understand the energy transfer of carotenoids. Another important aspect in the study of the energy transfer of carotenoids is the measurement of the S1 lifetimes. Since the first measurement of S1 lifetimes of carotenoids (β-carotene, canthaxanthin, and 8′-apo-β-caroten-8′-al) in 1986,7 the S1 lifetimes of some other carotenoids have been measured more recently. The S1 lifetimes of β-carotene series8 (β-carotene and other compounds which have the same molecular structure except the polyene chain length) and a spheroidene series9 (similar study) show strong S1 lifetime dependence on polyene chain length. As the polyene chain length increases, S1 lifetime decreases. The S1 lifetime of 7′-apo-7′,7′-dicyano-β-carotene has been found to be sensitive to the solvent polarity (from 11.7
10.1021/jp0008344 CCC: $19.00 © 2000 American Chemical Society Published on Web 06/24/2000
First Excited States of Carotenoids CHART 1
ps in 3-methylpentane to 1.9 ps in MeCN), whereas that of β-carotene is essentially insensitive to the solvent polarity.10 The reason for this difference is not clear. In our current study, the effect of terminal groups, polyene chain length and solvent on S1 states of 3 series of carotenoids is examined. We propose that the charge transfer character in the S1 states of some carotenoids is the major reason for their S1 lifetime sensitivity to solvent polarity. The structures of carotenoids studied, together with those of 7′-apo-7′,7′-dicyano-β-carotene and β-carotene, are shown in Chart 1. Experimental Section Ethyl 8′-apo-β-caroten-8′-oate (I) was a gift from HoffmannLa Roche, Basel, Switzerland. Ethyl 6′-apo-β-caroten-6′-oate (II), ethyl 4′-apo-β-caroten-4′-oate (III), 8′-apo-β-caroten-8′nitrile (IV), 6′-apo-β-caroten-6′-nitrile (V), 4′-apo-β-caroten4′-nitrile (VI), 6′-apo-β-caroten-6′-al (VIII), and 7′-apo-7′,7′dicyano-β-carotene (IX) were synthesized in our lab by Dr. Elli S. Hand. 8′-Apo-β-caroten-8′-al (VII) was obtained from Roche Vitamins and Fine Chemicals, Nutley, NJ; β-carotene (X) was from Fluka. All carotenoids were all-trans, except VI, which contained ca. 15% of the 5′-cis isomer. All carotenoids were kept at -16 °C, stored over Drierite and wrapped with Parafilm and aluminum foil to avoid exposure to moisture and light. Just prior to use, they were allowed to warm to room temperature. 3-Methylpentane (3-MP, 99+%) was from Aldrich. MeCN (99.9%) was from Fisher Scientific. Molecular sieves were added to both solvents to remove residual water. For facile comparison, optical absorption spectra shown in the same figure are normalized to the same absorbance. Ground state absorption spectra were determined in a 1 mm optical path length cuvette with a double-beam Shimadzu Model 1601 UVPC Spectrophotometer. The first excited singlet state absorp-
J. Phys. Chem. B, Vol. 104, No. 28, 2000 6669 tion spectra and the kinetics were recorded using a previously described amplified titanium:sapphire laser system pumping a tunable optical parametric amplifier (OPA).9,11 Briefly, the output from a continuous wave intracavity doubled Nd:YVO4 laser (Spectra Physics Millennia) pumped a self-mode-locked titanium:sapphire oscillator operating at 840 nm. The 50 fs, 840 nm output was chirped-pulse-amplified in a regenerative titanium:sapphire amplifier pumped with the output from a 1 kHz Nd: YLF (Quantronix, 527 DP-S). The compressed output (150 fs) of the amplifier was split, and about 5% was used to create a stable white light continuum probe beam by focusing it into a 2 mm thick sapphire window. The remaining amplified light was frequency doubled yielding 60-100 µJ, 420 nm pulses. The doubled light was used to pump a two-stage OPA, which was tunable from 475 to 750 nm. Samples were typically excited using a 490 nm, 0.18 ps laser pulse focused to 1 mm. The pulse powers are indicated in the figure captions. During measurements, samples were stirred continuously. Excited state lifetimes were obtained by iterative deconvolution of kinetic data using the Levenberg-Marquardt algorithm. AM1 (Austin Model 1) semiempirical molecular orbital calculations12 were carried out using HyperChem software on a Gateway (Pentium III) personal computer. Results and Discussion 1. Ground State and the First Excited Singlet State Absorption Spectra. Figure 1 shows the ground state optical absorption spectra (S0 f S2) of I-III in 3-MP and MeCN. In the nonpolar solvent 3-MP, the absorption spectra of all three carotenoids exhibit well-resolved vibrational structures. In the strongly polar solvent MeCN, the absorption bands become broader, but their vibrational structures can still be clearly observed, although they are not as well resolved as in 3-MP. Carotenoids with terminal CN groups (IV-VI) exhibit the same band structural change with solvent as I-III, which have terminal CO2Et groups. However, VII and VIII, which have terminal CHO groups, exhibit different band structural changes from I-VI, as shown in Figure 2. In MeCN, the ground state absorption bands of VII and VIII are broader than I-VI, and their vibrational structures totally disappear, which suggests that more charge transfer character is mixed into their excited states than those of I-VI.10 The ground state absorption maxima (S0 f S2) of I-VIII are listed in Table 1. For all eight carotenoids studied, a large solvent polarity change from 20 °C 1.913 (3-MP) to 37.513 (MeCN) has small, if any, effect on their absorption maxima. For I-IV and VII, there is actually no change. For VI and VIII, there are 7 and 5 nm blue shifts, respectively. It is wellknown that the absorption maximum of a carotenoid depends mainly on the solvent polarizability ((n2 - 1)/(n2 + 2), where n is the refractive index of the solvent).14,15 In a solvent of larger n, carotenoids have longer absorption maxima. Although the two solvents have very different polarity, they have similar polarizability. At 20 °C, n is 1.376 for 3-MP, and 1.344 for MeCN.13 Thus, the absorption maxima of I-VIII change little when the solvent is changed from 3-MP to MeCN. As the polyene chain length of carotenoids increases, the absorption maxima are red-shifted. From the number of CdC bonds equal to 9 to 10, there is ca. 20 nm red shift; from CdC bonds 10 to 11, there is ca. 11 nm red shift. At the same polyene chain length, carotenoids with terminal CHO groups have longer absorption maxima than those with terminal CN or CO2Et groups in both solvents. For example, in 3-MP, VII has an absorption maximum at 454 nm, whereas I and IV absorb at 442 and 445 nm, respectively.
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Figure 2. Optical absorption spectra of S0 f S2 transitions of (a) VII and (b) VIII in 3-MP (solid line) and MeCN (dotted line).
TABLE 1: Optical Absorption Maxima (nm) of S0 f S2 and S1 f Sn Transitions of Carotenoids 3-MP
Figure 1. Optical absorption spectra of S0 f S2 transitions of (a) I, (b) II, and (c) III in 3-MP (solid line) and MeCN (dotted line).
Table 1 also lists the first excited singlet state optical absorption maxima (S1 f Sn) of I-VIII in 3-MP and MeCN. When the solvent is changed and the polyene chain length increases, these absorption maxima exhibit behavior very similar to those of the ground state absorption. Changing the solvent from 3-MP to MeCN has only a small, if any, effect on these absorption maxima. The shift of the S1 absorption maxima with solvent change from 3-MP to MeCN is less than 7 nm. This similarity suggests that the solvent effect on the S1 absorption maxima stems mainly from the same type of interaction as on S0 absorption maxima, i.e., the dispersive interaction between carotenoids and solvents. In both solvents, when the polyene chain length increases, the S1 absorption maximum is redshifted. With a one CdC bond increase, the S1 absorption maximum increases by about 20 nm. At the same polyene chain length, the carotenoids with terminal CHO groups have S1 absorption maxima at longer wavelength than those with terminal CN or CO2Et groups. For example, in 3-MP, VII has an S1 absorption maximum at 544 nm, whereas both I and IV absorb at 535 nm. Those with terminal CN and CO2Et groups have almost the same S1 absorption maxima (except III and VI in MeCN). The S1 transient absorption spectra of I-III in 3-MP and MeCN are shown in Figure 3. 2. First Excited Singlet State Lifetimes. Figure 4 shows the transient absorption kinetics of the S1 states of I-III in
I II III IV V VI VII VIII
MeCN
S0 f S2
S1 f Sn
S0 f S2
S1 f Sn
442 461 472 445 468 480 454 472
535 555 573 (552a) 535 556 (534a) 555 (578a) 544 568
443 461 472 444 456b 473 453 467
536 558 579 534 557 569 551 567
a The next absorption maximum. b Because of the weak absorption, this value may not be accurate.
3-MP upon laser pulse excitation. Deconvolution of these kinetic data shows that the decays are single exponential, and that the S1 lifetimes of I, II, and III are 24.1, 12.4, and 6.2 ps, respectively. As the number of CdC bonds increases by 1, the S1 lifetime decreases by a factor of ca. 2. In MeCN, the decay of the S1 states of I-III is also single exponential, and has similar lifetimes to those in 3-MP (the difference is less than 8%, see Table 2), which shows that solvent polarity has little effect on the S1 lifetimes of I-III. Deconvolution of the kinetic data of IV-VIII in 3-MP and MeCN shows that the decay of the S1 states of these carotenoids is also single exponential in both solvents. The S1 lifetimes are given in Table 2. In 3-MP, I, IV, and VII have similar S1 lifetimes; II, V, and VIII have similar S1 lifetimes; and III and VI have similar lifetimes. The S1 lifetime of all-trans 7′-apo-7′,7′-dicyano-β-carotene (IX), which has the same polyene chain length as II, V, and VIII, is 11.7 ps in 3-MP,10 very close to those of II (12.4 ps), V (12.2 ps), and VIII (12.0 ps). These comparisons suggest that in the nonpolar solvent 3-MP terminal substituents have little effect on the S1 lifetimes of carotenoids. The major factor, which determines the S1 lifetimes of carotenoids, is the polyene chain length. This lack of S1 lifetime dependence on the terminal groups of carotenoids suggests that terminal groups have little effect
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Figure 3. Optical absorption spectra of S1 f Sn transitions of I (chained line), II (dotted line), and III (solid line) in (a) 3-MP; (b) MeCN following a 490 nm, 0.5 µJ, 0.18 ps laser pulse. 1 mm optical path length.
on the energy levels of S1 states in nonpolar solvents. The S1 energy levels are determined primarily by the polyene chain length, and decrease with an increase of the chain length. According to the energy gap law,16,17 the smaller the energy difference between the S1 and S0 states, the faster the radiationless decay from S1 to S0. Our current observations agree with the earlier conclusion that, as the number of CdC bonds of a carotenoid increases, the energy level of the S1 state of the carotenoid decreases.11,18,19 From their lifetimes, the S1 energy levels of carotenoids I-VIII can be estimated by comparison with the S1 lifetimes of carotenoids with known S1 energy levels.20 The estimated S1 energies of I-VIII are listed in Table 2. For I, IV, and VII (9 CdC bonds), the S1 states are at ca. 655 nm; for II, V, and VIII (10 CdC bonds), at ca. 694 nm; for III and VI (11 CdC bonds), at ca. 728 nm. As shown in Table 2, IV-VI, which have terminal CN groups, have S1 lifetimes in MeCN similar to those in 3-MP. This behavior is similar to those of carotenoids with terminal CO2Et groups (I-III). However, the S1 lifetimes of VII and VIII, which have terminal CHO groups, are sensitive to the solvent. As the solvent is changed from 3-MP to MeCN, the S1 lifetime of VII decreases from 26.4 to 8.4 ps, and that of VIII decreases from 12.0 to 6.3 ps. The S1 transient absorption kinetics of VII in both solvents are shown in Figure 5. The decrease of the S1 lifetimes of VII and VIII in MeCN compared to those in 3-MP is not due to the change of their S1 energy levels in MeCN. Because of the low oscillator strength of transition between S1 and S0, S1 energy levels are hardly affected by solvents.21 Furthermore, the polarizability of the two solvents is very similar, which results in similar dispersive interaction with the carotenoids. Thus, like I-VI, the S1 energy levels of VII and VIII should have little change when the solvent is changed from 3-MP to MeCN. To investigate if the dipole-dipole interaction between S1 states of carotenoids and the solvent is the major reason for the decrease of VII and VIII S1 lifetimes in MeCN, we used the AM1 method to calculate
Figure 4. S1 state decay kinetic of (a) I at 534 nm, (b) II at 555 nm, and (c) III at 573 nm in 3-MP following a 490 nm, 0.5 µJ, 0.18 ps laser pulse. The circles are the experimental data; the solid line is the best fit to the experimental data. 1 mm optical path length.
TABLE 2: S1 State Lifetimesa (ps) and Energy Levels (nm) of Carotenoids I II III IV a
3-MP
MeCN
S1 energy
24.1 12.4 6.2 23.9
23.8 11.4 6.0 23.9
656 694 733 656
V VI VII VIII
3-MP
MeCN
S1 energy
12.2 7.3 26.4 12.0
11.2 6.0 8.4 6.3
694 722 653 694
The uncertainty could be ( 5%.
the gas-phase dipole moments of S0 and S1 states of I-VIII. The results are listed in Table 3. When the polyene chain length increases, the gas phase dipole moments of both S0 and S1 states increase slightly, and S1 states have larger dipole moments than S0 states. At the same polyene chain length, carotenoids with terminal CN or CHO groups have larger S0 and S1 dipole moments than those with terminal CO2Et groups (the difference in dipole moment is ca. 2 D). Those with CHO groups have almost the same S0 and S1 dipole moments as those with CN groups. Furthermore, the eight carotenoids have similar dipole moment differences between the S1 and S0 states (ca. 2.6 D). Thus, the gas phase dipole moments cannot explain the fact that the S1 lifetimes of only VII and VIII decrease in MeCN, whereas the S1 lifetimes of IV-VI do not change.
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Figure 6. Optical absorption spectra of S0 f S2 transitions of X in 3-MP (solid line) and MeCN (dotted line).
Figure 5. S1 state decay kinetic of VII in (a) 3-MP at 555 nm; (b) MeCN at 550 nm following a 490 nm, 0.5 µJ (a) or 0.4 µJ (b), 0.18 ps laser pulse. The circles are the experimental data; the solid line is the best fit to the experimental data. 1 mm optical path length.
TABLE 3: Dipole Moments (debyes) of S0 and S1 States of Carotenoids and Their Differences I II III IV
S0
S1
∆S (S1-S0)
2.72 2.91 3.04 4.79
5.22 5.50 5.50 7.49
2.51 2.59 2.46 2.70
V VI VII VIII
S0
S1
∆S (S1-S0)
4.92 5.04 4.65 4.97
7.71 7.75 7.47 7.83
2.78 2.71 2.82 2.86
However, in strongly polar solvents, dipole-dipole interactions of carotenoids with the solvents may result in enhanced charge transfer character in the excited states of carotenoids, which may change the dipole moments and accelerate the decay of the excited states.10 In the ground state absorption spectrum of IX, the vibrational structure is well resolved in 3-MP but disappears in MeCN and EtOH. The disappearance of the vibrational structure due to the broadening of the absorption bands is characteristic of mixing the charge transfer character into the excited states.10 The S1 lifetime of IX decreases from 11.7 ps10 in 3-MP to 1.9 ps10 in MeCN and 2.4 ps in EtOH. However, the S1 lifetime of β-carotene (X) is almost independent of solvents. In 3-MP, it is 8.1 ps;22 in toluene, it is 8.4 ps;7 in EtOH, it is 9.2 ps. In its ground state absorption spectrum, the vibrational structure is well resolved in both nonpolar solvent 3-MP and polar solvent MeCN, as shown in Figure 6, although it is not as well-resolved in MeCN as in 3-MP. In toluene and EtOH, the vibrational structure of X is also well resolved. The well-resolved vibrational structure of X indicates that there is little charge transfer character in its excited states. In our current study, I-VI have similar S1 lifetimes in 3-MP and MeCN, and their vibrational structures are still resolved in the ground state absorption spectra in MeCN. Their behavior is very similar to that of X; VII and VIII have decreased S1 lifetimes in MeCN, and their vibrational structures totally disappear in ground state absorption spectra in MeCN. These observations strongly suggest that there is a relationship between the disappearance of vibrational structure in ground state absorption spectra and
the decrease of the S1 lifetime of carotenoids, i.e., the charge transfer character in the S1 states is the major reason for the decrease of S1 lifetimes. The decreased S1 lifetimes of VII and VIII in MeCN compared to those in 3-MP are thus attributed to the existence of considerable charge transfer character in their S1 states. In I-VI, little charge transfer character exists in their S1 states. Their S1 lifetimes have very small, if any, decrease in MeCN. A very recent study suggested that the presence of a charge transfer state can cause the large decrease of the S1 lifetimes of carotenoids with solvent polarity increase.21 It was observed that when the solvent is changed from cyclohexane to MeCN, the S1 lifetime of peridinin decreases from 172 to 9 ps. In the ground state optical absorption spectrum of peridinin, the vibrational structure is well resolved in nonpolar solvents (e.g., cyclohexane), but the vibrational structure totally disappears in polar solvents (e.g., MeCN). In the cases of VII, VIII, and IX, the S1 lifetime changes are not as large as that of peridinin. The charge transfer state may be absent. There is only some extent of charge transfer character in the excited states of VII, VIII, and IX. The extent of the charge transfer character in the excited states of carotenoids is different from one carotenoid to another as reflected in the different S1 lifetime sensitivity to solvent polarity. The S1 lifetime of IX decreases by a factor of 6 when the solvent is changed from 3-MP to MeCN. Those of VII and VIII decrease by a factor of ca. 3 and 2, respectively, from 3-MP to MeCN. Carotenoids VII and VIII appear to have less charge transfer character in their excited states than IX, but more than I-VI and X. Conclusions Our results suggest that the solvent effect on the first excited singlet state absorption maxima of carotenoids stems from the same type of interaction as on the ground state absorption maxima, i.e., the dispersive interaction between carotenoids and solvents. In nonpolar solvents, the S1 lifetimes of carotenoids depend primarily on the polyene chain length. With a one Cd C bond increase, the S1 lifetime decreases by a factor of ca. 2. The S1 energy levels of carotenoids are thus indicated to depend mainly on the polyene chain length, according to the energy gap law. Terminal groups (CHO, CN, CO2Et) have little effect in nonpolar solvents. However, carotenoids with different terminal groups could have different S1 lifetime sensitivity to solvent polarity, because of a different extent of charge transfer character in their excited states. Polar solvents decrease the S1 lifetimes of carotenoids, when, and only when, there is considerable charge transfer character in their excited states. Acknowledgment. We thank Dr. Elli S. Hand for helpful discussions and synthesis of carotenoids II-VI and VIII. This
First Excited States of Carotenoids work is supported by the Division of Chemical Science, Office of Basic Energy Sciences, Office of Energy Research, U.S. Department of Energy, under Grant Nos. DE-FG02-86-ER13465 (L.D.K.) and DE-FG02-99-ER14999 (M.R.W.), and contract No. W-31-109-Eng-38 (D.G.). References and Notes (1) Goedheer, J. C. Annu. ReV. Plant Physiol. 1972, 23, 87. (2) Koyama, Y. J. Photochem. Photobiol. 1991, 139, 265. (3) Frank, H. A.; Cogdell, R. J. Photochem. Photobiol. 1996, 63, 257. (4) Razi Naqvi, K.; Melø, T. B.; Bangar Raju, B.; Ja´vorfi, T.; Simidjiev, I.; Garab, G. Spectrochim. Acta, A 1997, 53, 2659. (5) Frank, H. A.; Violette, C. A. Biochim. Biophys. Acta 1989, 976, 222. (6) Okamoto, H.; Ogura, M.; Nakabayashi, T.; Tasumi, M. Chem. Phys. 1998, 236, 309. (7) Wasielewski, M. R.; Kispert, L. D. Chem. Phys. Lett. 1986, 128, 238. (8) Andersson, P. O.; Bachilo, S. M.; Chen, R. L.; Gillbro, T. J. Phys. Chem. 1995, 99, 16199. (9) Frank, H. A.; Desamero, R. Z. B.; Chynwat, V.; Gebhard, R.; van der Hoef, I.; Jansen, F. J.; Lugtenburg, J.; Gosztola, D.; Wasielewski, M. R. J. Phys. Chem. A 1997, 101, 149.
J. Phys. Chem. B, Vol. 104, No. 28, 2000 6673 (10) O’Neil, M. P.; Wasielewski, M. R.; Khaled, M. M.; Kispert, L. D. J. Chem. Phys. 1991, 95, 7212. (11) Frank, H. A.; Cua, A.; Chynwat, V.; Young, A.; Gosztola, D.; Wasielewski, M. R. Photosynth. Res. 1994, 41, 389. (12) Dewar, M. J. S.; Zoebisch, E. G.; Healy, E. F.; Stewart, J. J. P. J. Am. Chem. Soc. 1985, 107, 3902. (13) Lide, D. R. Handbook of Chemistry and Physics, 78th ed.; CRC Press: Boca Raton, FL, 1997-1998. (14) Andersson, P. R.; Gillbro, T.; Ferguson, L.; Cogdell, R. J. Photochem. Photobiol. 1991, 54, 353. (15) Nagae, H.; Kuki, M.; Cogdell, R. J.; Koyama, Y. J. Chem. Phys. 1994, 101, 6750. (16) Englman, R.; Jortner, J. Mol. Phys. 1970, 18, 145. (17) Bixon, M.; Jortner, J.; Cortes, J.; Heitele, H.; Michel-Beyerle, M. E. J. Phys. Chem. 1994, 98, 7289. (18) DeCoster, B.; Christensen, R. L.; Gebhard, R.; Lugtenburg, J.; Farhoosh, R.; Frank, H. A. Biochim. Biophys. Acta 1992, 1102, 107. (19) Snyder, R.; Arvidson, E.; Foote, C.; Harrigan, L.; Christensen, R. L. J. Am. Chem. Soc. 1985, 107, 4117. (20) Chynwat, V.; Frank, H. A. Chem. Phys. 1995, 194, 237. (21) Bautista, J. A.; Connors, R. E.; Raju, B., B.; Hiller, R. G.; Sharples, F. P.; Gosztola, D.; Wasielewski, M. R.; Frank, H. A. J. Phys. Chem. B 1999, 103, 8751. (22) Wasielewski, M. R.; Johnson, D. G.; Bradford, E. G.; Kispert, L. D. J. Chem. Phys. 1989, 91, 6691.
