J. Phys. Chem. 1987, 91, 4831-4835
4831
Pulse Radiolytic and Electrochemical Investigations of Intramolecular Electron Transfer in Carotenoporphyrins and Carotenoporphyrin-Quinone Triads Edward J. Land2 Doris Lexa,t R e d V. Bensasson,s Devens Gust,*l Thomas A. Moore,l Ana L. Moore,l Paul A. Liddell,l and Gregory A. Nemethl Paterson Institute for Cancer Research, Christie Hospital and Holt Radium Institute, Manchester M20 9BX, U.K.; Laboratoire d'Electrochimie Moleculaire Universite de Paris VII, 75221 Paris Cedex 05, France; Laboratoire de Biophysique, Museum National d'Histoire Naturelle, INSERM U.021, CNRS UA.481, 75700 Paris, France; Department of Chemistry, Arizona State University, Tempe, Arizona 85287 (Received: January 20, 1987: In Final Form: May 4, 1987)
Thermodynamic and kinetic aspects of intramolecular electron-transfer reactions in carotenoporphyrin dyads and carotenoid-porphyrin-quinone triads have been studied by using pulse radiolysis and cyclic voltammetry. Rapid (< 1 ps) electron transfer from carotenoid radical anions to attached porphyrins has been inferred. Carotenoid cations, on the other hand, do not readily accept electrons from attached porphyrins or pyropheophorbides. Electrochemical studies provide the thermodynamic basis for these observations and also allow estimation of the energetics of photoinitiated two-step electron transfer and two-step charge recombination in triad models for photosynthetic charge separation.
Introduction Carotenoid polyeneshave recently been found to act as electron donors in carotenoid-porphyrin-quinone (C-P-Q) triad molecules.'" These molecules mimic the multistep electron-transfer reactions of photosynthesis which lead to long-lived, high-energy charge-separated states. Excitation of the porphyrin to yield C-'P-Q is followed by electron transfer to the quinone to give C-P'+-Q'-. A second electron-transfer step yields C'+-P-Q'-, which has a lifetime on the microsecond time scale. In order to understand the electron-transfer role of the carotenoid in the triad systems, one must have a basic knowledge of the static and dynamic aspects of the redox behavior of the carotenoid and of the associated porphyrin and quinone moieties. The results of pulse radiolysis studies, described below, yield such information. Although pulse radiolysis cannot, of course, be used to study primary photochemical events, the dynamics of subsequent processes involving electron-transfer reactions can be elucidated very conveniently via this technique when the results are interpreted in light of electrochemical potentials from cyclic voltammetric studies. In addition to aiding in the interpretation of the pulse radiolysis data, the electrochemical results also allow an estimation of the energetics of the various electron-transfer states in the triads.
4
R,
i
CH3,
Rz = k. R,
=
CH,.
i(,
= H,
=
I
6 RI
=
R,
1
p \..
Experimental Section Materials. The syntheses of carotenoid derivatives 1-3, car0=
2: R
=
H
3: R + Paterson
* f
=
1
'NH~
Institute. UniversitE de Paris VII. Musium National d'Histoire Naturelle. Arizona State University.
(1) Moore, T. A,; Gust, D.; Mathis, P.; Mialocq, J. C.; Chachaty, C.; Bensasson, R. V.; Land, E. J.; Doizi, D.; Liddell, P. A.; Nemeth, G. A.; Moore, A. L. Nature (London) 1984, 307, 630-632. (2) Gust, D.; Mathis, P.; Moore, A. L.; Liddell, P. A,; Nemeth, G. A.; Lehman, W. R.; Moore, T. A.; Bensasson, R. V.; Land, E. J.; Chachaty, C. Photochem. Photobiol. 1983, 37S, S46. (3) Moore, T. A.; Mathis, P.; Gust, D.; Moore, A. L.; Liddell, P. A.; Nemeth, G. A,; Lehman, W. R.; Bensasson, R. V.; Land, E. J.; Chachaty, C. In Aduances in Photosynthesis Research; Sybesma, C., Ed.; Nijhoff/Junk: The Hague, 1984; pp 729-732. (4) Gust, D.; Moore, T. A. J. Photochem. 1985, 29, 173-184. (5) Seta, P.; Bienvenue, E.; Moore, A. L.; Mathis, P.; Bensasson, R. V.; Liddell, P. A,; Pessiki, P. J.; Joy, A.; Moore, T. A,; Gust, D. Nature (London) 1985, 316, 653-655. (6) Liddell, P. A.; Barrett, D.; Makings, L. R.; Pessiki, P. J.; Gust, D.; Moore, T. A. J. Am. Chem. SOC.1986, 108, 5350-5352.
0022-3654/87/2091-4831~01.50/0 0 1987 American Chemical Society
4832
The Journal of Physical Chemistry, Vol. 91, No. 18, 1987
Land et al.
h
L'
w
17 and were used as received, with the exception of dichloromethane, which was stored over sodium carbonate in order to remove traces of acid. For the electrochemical measurements in dichloromethane, the solvent containing the supporting electrolyte, (CH3CHJ4NC104, (CH3CH2CH2CH2)4NC104, or (CH3CH2CH2CH*),NPF6, was dried over freshly dried neutral alumina prior to each experiment. Pulse Radiolysis. The pulse radiolysis equipment has been described." Benzene solutions were argon-flushed and irradiated in 1-cm quartz cells with 20-ns, N 10-Gy pulses of 9-12-MeV electrons from a Vickers electron linear accelerator. Resulting changes in light absorption were monitored as a function of time at each wavelength by using photoelectric detection. For wavelengths below 690 nm, EM1 7983R or Hamamatsu R928 photomultipliers were used, in the 600-1 100-nm range a U.D.T. PIN 10 diode was employed, and detection at >1100 nm was provided by a Philco Ford L4521 diode. Cyclic Voltammetry. A three-electrode configuration contained in a conical amber glass cell equipped with a water jacket was used with a solution volume of 5 mL. The temperature of all experiments was 17 f 1 "C. The solutions were purged with argon and an argon atmosphere was maintained during the experiments. The counter electrode was a platinum wire and the reference a NaC1-saturated calomel electrode (SCE). All potentials are referred to this electrode. NaCl was used instead of KCl to prevent the precipitation of KC104 (when a perchlorate was used as supporting electrolyte) in the pores of the glass frit separating the reference electrode compartment from the bridge containing the same solvent and supporting electrolyte as the solution under investigation. The potential of the NaCl SCE is 5.5 mV negative of that of the KC1 SCE. The Eo of ferrocene/ferrocenium couple was measured under our experimental conditions as -0.44 V/SCE. The working electrode was a glassy carbon disk electrode obtained by sealing a 3-mm-diameter carbon rod in a glass holder. The carbon disk was frequently polished with diamond pastes of decreasing sizes (7, 3, l pm) followed by ultrasonic washing with ethanol and drying. The instrumentation consisted of a home-built potentiostat equipped with positive feedback IR compen~ation,'~ a PAR Model 175 function generator, an IFFELEC I F 2502 XY pen recorder and a SCHLUMBERGER A 220 digital voltmeter. The peak potentials were measured with an accuracy of about &3 mV.
II
0
otenoporphyrins 4-7 and 15, carotenopyropheophorbide (8), triads 9-11, porphyrin derivatives 13, 14, 16, and 19, and quinone 17 have been reported previous1y.'-I2 Compounds 12 and 18 were prepared by standard methods. Solvents were spectroscopic grade ~
(7) Dirks, G.; Moore, A. L.; Moore, T.A,; Gust, D. Photochem. Photobiol. 1980, 32, 277-280. ( 8 ) Moore, A. L.; Dirks, G ; Gust, D.;Moore, T. A. Photochem. Photobiol 1980, 32, 691-695. (9) Moore, A . L.; Joy, A.; Tom, R.; Gust, D.; Moore, T. A.; Bensasson, R. V.; Land, E. J. Science (Washington D.C.) 1982, 216, 982-984. (10) Gust, D.; Moore, T.A,; Bensasson, R. V.; Mathis, P.; Land, E. J.; Chachaty, C.; Moore, A . L.; Liddell, P. A,; Nemeth, G. A. J. Am. Chem. SOC. 1985, 107, 3631-3640. (1 1 ) Liddell, P. A.; Nemeth, G . A.; Lehman, W. R.; Joy, A . M.; Moore, A. L.; Bensasson, R. V.; Moore, T.A,: Gust, D. Photochem. Photobiol. 1982, 36, 641-645. (12) Gust, D.; Moore, T.A.; Liddell, P. A.; Nemeth, G. A,; Makings, L. R.; Moore, A. L.; Barrett, D.; Pessiki, P. J.; Bensasson, R. V.; Rougge, M.; Chachaty, C ; De Schryver, F. C.; Van der Auweraer, M.; Holzwarth, A. R.; Connolly, J S . J . Am. Chem. SOC.1987, 109, 846-856.
Results Pulse Radiolysis. Pulse radiolysis of carotenoid polyene 1 in benzene solution yielded the spectra shown in Figure 1. On the basis of previous experiment^,'^,'^ the spectrum 2 ps after the pulse (A,, 975 nm) may be attributed mainly to the rapidly formed radical anion of 1 and the spectrum 8 ps after the pulse (Ama 1025 nm) to about equal concentrations of the radical anion and the more slowly formed radical cation. The anionic component was found to be suppressed by the electron scavenger N 2 0 which prevented electron capture by the carotenoid. The polyene radical anion and cation spectra of 2, similarly obtained, are shown in Figure 2. Although the differences between the absorption profiles of the two transient spectra of Figure 2 are not as great as in Figure 1, they are still significant. Confirmation that both car(13) Keene, J. P. J. Sci. Instrum. 1964, 41, 439-496. (14) Garreau, D.; Saveant, J. M. J. Electroanal. Chem. 1977, 99, 2786. (15) Dawe, E. A.; Land, E. J . J. Chem. SOC.,Faraday Trans. 1 1975, 7 1 . 2162-2169. -. .- -....
(16) Lafferty, J.; Truscott, T. G.; Land, E. J. J. Chem. SOC.,Faraday Trans. I 1978, 7 4 , 2760-2762.
The Journal of Physical Chemistry, Vol. 91, No. 18, 1987 4833
Electron Transfer in Carotenoporphyrins
2.01
2.0
0
1.5-
-
X >I
.-
fn
C
P a,
-m 2
a
1.0-
.-C
E
m 0
a, 0
t m
t m
0
0
0.5-
0 5-
0
800
1000
1200
800
Wavelength (nm)
Figure 1. Transient absorption spectrum ( 0 )2 ps and (0)8 ps after M 1 in argon-flushed benzene. pulse radiolysis of 2.0 X
1200
Figure 3. Transient absorption spectrum ( 0 ) 2 ps and (0) 8 ps after M 4 in argon-flushed benzene. pulse radiolysis of 2.8 X
spectrum, and the absorption profiles of the two spectra were identical (A, 1025 nm). Thus, only the carotenoid radical cation spectrum was detected at both times. The failure to observe the carotenoid radical anion of 4, even though it is likely to be produced under the radiolysis conditions, suggests relatively rapid (((1 ps) electron transfer from the carotenoid moiety to the porphyrin: c*--p + c - p (1)
2.5
2.0
Tetrapyrrole radical ions are known to absorb only very weakly above 900 nmI7 by comparison with the high extinctions in this region for carotenoid ions ( E > lo5 dm3 mol-' cm-' at A,, in the infrared).l5-I7 Thus, the absorption of the C-P'- species formed in eq 1 is not apparent in Figure 3. Similar results were obtained for carotenoporphyrins 5-7. Only the radical cation of the carotenoid moiety was observed after pulse radiolysis in benzene. The rise time of the cation absorption (8-10 ps) was similar for all of these carotenoporphyrins. In the pulse radiolysis experiment, the solvent is oxidized to solvent cation So+ in the primary radiation chemical event. Thus, the source of the carotenoid radical cations might be either carotenoid electron donation to a porphyrin cation radical (formed via S*+)
z 1.5 X >I
.-fn
a, 0
-m
: . 1.0 a
.-C 0 al
m
6
1000 Wavelength (nm)
0.5
0
c-p*+ + c*+-p or a donation to solvent cations
-s +
(2)
(SO'):
800
1000 Wavelength (nm)
1200
Figure 2. Transient absorption spectrum ( 0 )4 ps and (0) 18 ps after pulse radiolysis of 2.5 X M 2 in argon-flushed benzene.
otenoid radical cations and carotenoid radical anions contribute to the spectra of Figure 2 is provided by kinetic considerations. Solute radical anions are normally formed much faster than solute radical cations in hydrocarbon^.'^ Thus, in both Figures 1 and 2, the peaks of the earlier spectra, due mainly to rapidly formed (2.-, are more intense that the peaks of the later spectra which are due both to slowly formed C'+ and C*-, some of which have already decayed. It will be noted that the wavelength maximum of the cation of 2 in benzene (1025 nm) is strongly shifted compared to the cation position in dichloromethane (970 nm), as determined by pulse radiolysis of 2 and 10. Pulse radiolysis ofcarotenoporphyrin ester 4 in benzene solution yielded transient spectra in the infrared region (Figure 3) observed 2 and 8 ps after the radiolysis pulse. In this case, the pepk of the earlier spectrum was much less intense than that of the later
S'+
+ c-P
c'+-P
(3)
The importance of this latter process is suggested by the fact that the growth rate of the C'+ spectra in the C-P solutions and solutions of polyene 1 are very similar. Pulse radiolysis of 8, in which the porphyrin moiety has been replaced by pyropheophorbide a, in benzene also yields only the spectrum of the carotenoid radical cation. Electrochemical Measurements. The observation of reaction 1, and possibly (2), by pulse radiolysis has implications for the and P'-in the covalently linked relative stabilities of C", C*-, P'+, bichromophoric species. Therefore, a-cyclic voltammetric study of the redox potentials of the molecules under investigation was undertaken. The solvent was dichloromethane containing 0.1 M (CH3CH2),NC104,(CH3CH2CH2CH2),NC1O4, or (CH3CH,CH,CH,),NPF, as supporting electrolytes. The results are collected ~
(17) Bensasson, R. V.; Land, E. J.; Truscott, T. G. Flash Photolysis and Pulse Radiolysis: Contributions to the Chemistry of Biology and Medicine; Pergamon: New York; 1983; p 33.
4834 The Journal of Physical Chemistry, Vol. 91, No. 18, 1987
Land et al.
TABLE I: Oxidntion-Reduction Potentials"in Dichloromethaw at 17 OC reduction E O , V vs SCE
compd methyl pyropheophorbide a porphyrins
QRZ
QRI
(18)
PRI -1.11
-1.20 -1.20 -1.18
12 13 14
carotenoids @-carotene
oxidation E O , V vs SCE pR 2
cR I
quinones p-benzoquinone 17 dyads and triads carotenoporphyrin 15 triad 11 porphyrin quinone 19
4.51 -0.57
-1.01 -1.03
-0.51 4.48
-1.05 -1.00
-1.20 -1.20 -1.30
Po2
-1.35
0.83
-1.49 -1.52 -1.52
0.93
1.16
0.80 adsorbed 0.95
1.14
-1.75 (2e irrev) -1.47
3
Po I
COI
0.72
0.64 (irrev)
-1.53 (irrev)
-1.55 (irrev) -1.65
0.66 (irrev) 0.65 (irrev)
"All the oxidation and reduction potentials correspond to single electron reversible waves, except when otherwise stated, and were measured with a potential sweep rate of 0.2 V/s. The value of the oxidation potential of @-carotenewas measured at I O OC and 5 V/s. In the case of irreversible waves, the potential value corresponds to the anodic peak in oxidation and to the cathodic peak in reduction. a.
4 A
4
reduction step. A similar small increase was observed for the first oxidation wave of 14 vs. 12. Porphyrin 13, on the other hand, adsorbs strongly on the electrode in oxidation; only one wave was observed, and the potential given is not as accurate as the others. Turning to the carotenoids, @-caroteneis reduced in two oneelectron waves, the standard potentials of which are very c10se.l~ The first wave is shifted 280 mV to positive potential when the carotene is modified by addition of an aryl ring and electronwithdrawing group in 3. @-Caroteneis oxidized reversibly by a one-electron wave at 0.72 V. i n the case of 3, this wave is not reversible even at high sweep rates and low temperature (10 "C). An anodic peak at 0.64 V is observed, followed at more positive potentials by other oxidation waves which must correspond to the further oxidation of the decomposition products made during the first wave.19 The potentials reported for the quinone moieties in Table I were obtained with tetra-n-butylammonium hexafluorophosphate as supporting electrolyte. The two (reversible) one-electron-reduction waves found for 1,4-benzoquinone are similar to those previously reported in acetonitrile.20 The first reduction wave for quinone 17 was found at -0.57 V. This shift to a more negative potential is as expected for a quinone substituted with an electron-donating alkyl group. We turn now to the electrochemistry of the dyads and triads. The results for 15, which consists of a carotenoid analogous to 3 covalently linked to a porphyrin analogous to 13, show that the potential of the first reduction wave of the porphyrin is not changed. The second reduction wave is more complex: its height is about three electrons, and it is irreversible. This seems to be due to overlapping of the second reduction ( P R 2 )wave of the porphyrin (one electron) and the CRlwave of the carotenoid (two electrons). In oxidation, we observed the same irrevesible carotenoid wave as was found for 3. In Figure 4b, reporting the voltammogram of PQ dyad 19, it is interesting to note that there is no overlap of the reversible reduction waves of the quinones with those of the porphyrins. The oxidation waves are irreversible and accurate potentials could not be obtained, as was the case for 13. Both overlap of the oxidation waves of the porphyrin with those of semiquinone impurities produced on the electrodes and oxidation of the -NH2 group may contribute to the problem. The voltammogram of C-P-Q triad 11 shows the reduction waves of the three components. &I is at -0.51 V, Q R 2 is at -1.05 V, the P,, wave (which still seems reversible) is at -1.20 V, and the second P,, wave is like the corresponding wave observed for 15. In oxidation, the carotene is still oxidized irreversibly at 0.65 V.
tF:2 VvsSCE
Figure 4. Cyclic voltammograms obtained in dichloromethane containing 0.1 M (CH3CH2CH2CH2),NPF6, on a glassy carbon electrode at 0.2 V/s for (a) pyropheophorbide a (18), the one-electron waves 3,3' and 4.4' corresponding to the reductions and the wave 5,5' to the first oxidation; (b) PQ dyad 19, the one-electron waves 1,l' and 2,2' corresponding to the reductions of the quinone, and 3,3' and 4,4' to the reductions of the
porphyrin. in Table I. In this table, Q R i and QR2represent the first and second reduction waves of the quinones and quinone moieties in the dyad and triad systems. CRIand Co, represent the first reduction and oxidation waves of the carotenes, and PRI,p R 2 , Pol, Poz denote the corresponding waves for the porphyrins and pyropheophorbide a. Figure 4 shows two examples of cyclic voltammograms. The shapes of the voltammogram obtained for the porphyrins 12 and 14 are very similar to that for pyropheophorbide 18 shown in Figure 4a. With respect to the porphyrins 12-14, it is clear that replacing two of the methyl groups of 12 with amino groups (13) has little effect upon reduction potentials in spite of the fact that these two groups differ in their electron donating abilities (Hammett substituent constants up = -0.17 for -CH3 and -0.66 for -NH2).I8 The substitution of acetamido groups for the amino groups of 14 leads to a slightly (20 mV) less negative potential for the first (18)
Zuman, P.Substitutent
New York, 1967; p 46.
Effects in Organic Polarography; Plenum:
Discussion The pulse radiolysis results show that the cation observed in (19) Park, S. M. J . Electrochem. SOC. 1978,125, 216-222 (20)Peover, M. E. J . Chem. Sac. 1962, 4540-4549.
The Journal of Physical Chemistry, Vol. 91, No. 18, 1987 4835
Electron Transfer in Carotenoporphyrins the carotenoporphyrin species is basically carotenoid in character and is not delocalized over the entire molecule: the cation spectra obtained for 1 and 4 are essentially identical and are similar to those previously obtained for carotenoid^.'^^'^^^^-^^ This observation is consistent with previous photophysical studies of carotenoporphyrins'-I2 which show only slight, if any, perturbations of ground-state and triplet absorption and fluorescence emission spectra for such molecules. In addition, the results suggest that, in the carotenoporphyrin and triad species, C'--P rapidly (
