3754
J. PhyS. Chem. 1982, 86, 3754-3759
Solvent and Structural Effects on PIcosecond Electron Transfer Reactions in Diporphyrin Models of the Photosystem I 1 Reaction Center of Green Plants I. FuJtta, J. Fajer, Department of Energy and Environment, Brookhaven Netionel Laboratcny, Upton, New York 11973
C.-K. Chung, C.4. Wang, Depertment of Chemistry, Michlgan State University, East Lansing, Mlchigen 48824
M. A. Bergkamp, and 1. L. Neirel’ Deperbnent of chemlsby. Brookhaven Metlormi Lsbcfatcny, Upton, New York 11973 (Received November 30, 198 1; In Final Form: April 26, 1982)
Picosecond absorbance measurements on doubly linked diporphyrins, comprising magnesium and free base subunits (Mg-H,), were made to assess the sensitivity of their light-driven electron transfer (ET) reactions to solvation and structural changes. Solvents vary the lifetime of the ET product (Mg+.-Hz--) in the 0.2-1.3-11s range and have no observable effect on the rate of formation of the ET product from the initial excited state (k > 10” s-l). The lifetime of the Mg+.-H2-. ET product thus can be manipulated to approach the 2-4-11s lifetime of the primary photoproducts in photosystem I1 of green plants. Kinetic results on a noncofacial diporphyrin (“slippedstructure”) show that the relative orientation of the macrocycles plays a measurable role in controlling ET reactions within diporphyrins. The results are discussed in terms of excited-state couplings in Mg-H2 diporphyrins.
Introduction The conversion of light into the chemical energy that drives photosynthesis in green plants and algae takes place in two chlorophyll-mediated systems which oxidize water (photosystem 11, PSII) and reduce carbon dioxide (PSI). In PSI, a chlorophyll “special pairn1 effects the energy transduction by transferring an electron to another chlorophyll, in a picosecond time domain. In PSII, pheophytin, a demetallated chlorophyll, acta as the acceptor2p3 and a monomeric chlorophyll is the postulated electron donor! Phohynthetic bacteria, on the other hand, utilize a dimeric bacteriochlorophyll d o n ~ r , (BChU2, ~,~ and a bacteriopheophytin acceptor,’+’ BPheo, possibly preceded by a bacteriochlorophyll.l0J1 To ascertain whether a dimeric donor is required to stabilize charge separation from excited singlet states of porphyrin derivatives and to assess the influence of redox potential differences in controlling electron transfer (ET) kinetics, we previously investigated12J3 the photochemistry of cofacial di(1) Katz, J. J.; Norris, J. R.; Shipman, L. L.; Thurnauer, M. C.; Wasielewski, M. R. Annu. Rev. Biophys. Bioenerg. 1976, 7, 393. (2) Fajer, J.; Davis, M. S.; Forman, A.; Kilmov, V. V.; D o h , E.; Ke, B. J . Am. Chem. SOC.1980.102. 7143. ~. (3) klimov, V. V.; Klevhik, A.V.; Shuvalov, V. A.; Krasnovski, A. A. KEBS Lett. 1977,82, 183. (4) Davis, M. S.: Forman, A.: Fajer, J. R o c . Natl. Acad. Sci. U.S.A.
1979, 76, 4170. (5) Norris, J. R.; Uphaus, R. A.; Crespi, H. L.; Katz, J. J. R o c . NatE. Acad. Sci. U.S.A. 1971,68,625. (6) McElrov. J. D.: Feher, G.: Mauzerd, D. C. Biochim. Biophys. . . Acta 1972; 267, 363.’ (7) Kaufman, K. J.; Dutton, P. L.; Netzel, T. L.; Leigh, J. S.;Rentzepis, P. M. Science 1975,188,1301. (8) Rockley, M. G.; Windsor, M. W.; Cogdell, R. J.; Parson, W. W. R o c . Natl. Acad. Sci. U.S.A. 1975, 72, 2251. (9) Fajer, J.; Brune, D. C.; Davis, M. S.; Forman, A.; Spaulding, L. D. Roc. Natl. Acad. Sci. U.S.A. 1975, 72, 4956. (10) Shuvalov, V. A.; Krakhmaleva, I. N.; Klimov, V. V. Biochim. Biophys. Acta 1976, 449, 597. (11) Holtan, D.; Hoganson, C.; Windsor, M. W.; Schenck, C. C.; Parson, W. W.; Migus, A.; Fork, R. L.; Shank, C. V. Biochim. Biophys. Acta 1980, 592, 461.(12) Netzel, T. L.; Kroger, P.; Chang, C.-K.;Fujita, I.; Fajer, J. Chem. Phys. Lett. 1979, 67, 223. ’
0022-3854182120863754$0 1.2510
Scheme I
I
I
1‘
I
porphyrins with center-to-center separations of -4 A (structure I). We found that a diporphyrin comprising
IC2
f
RI
I
magnesium and free base porphyrin subunits linked by five atom chains, Mg-H2(5), displayed optical changes consonant with electron transfer from the magnesium porphyrin to the free base within 6 ps of excitation. In methylene chloride (CH2C12),the E T product decayed to both the ground state and a long-lived state, X (dX) = 4-9 ns). These relaxations are summarized in Scheme I. This behavior differed from that of the symmetric diporphyrins, Mg-Mg(5) and H,-H,(5), which provided no spectral evidence of ET and exhibited excited-state lifetimes much longer than 5 ns. When Mg-H2(5) was dissolved in tet(13) Netzel, T. L.; Bergkamp, M. A.; Chang, C.-K.J.Am. Chem. SOC. 1982,104, 1952.
0 1982 American Chemlcal Society
The Journal of phvsical Chemistry, Vol. 86, No. 19, 1982 3755
Electron Transfer Reactlons in Diporphyrln Models
rahydrofuran (THF), the optical spectrum of its photoproduct appeared to be more like those of the symmetric diporphyrins than that attributed to Mg+.-Hp. Therefore, the first observable photoproduct of Mg-H2(5) in T H F was assigned to an excited r,a* singlet state (S1).12 These assignments are supported by recent work13which demonstrated that high concentrations of p-benzoquinone (BQ) (>0.25 M) quenched the r,r* states of Mg-H2(5) in THF in subnanosecond times, whereas under similar conditions the ET product state of Mg-H2(5) in CH2Clz yielded separated ionic products that survived >15 ns and resulted from the reaction Mg+--H2-- + BQ Mg+.-H2 BQ-e. Here, we report the results of studies designed to explore spacial and environmental effects on E T reactions in diporphyrins. We varied (1)the solvent, (2) the length of the covalent linking bridges, and (3)the relative orientation of the porphyrin subunits. While changing the solvent did not alter the rate at which the E T product was formed from S1 (>loll s-l), its lifetime was lengthened and approached that found for the primary E T product in PSII.14J5 Results for a noncofacial diporphyrin further indicate that the molecular architecture of the donors and acceptors also plays a significant role in controlling their ET reactions.
+
-
(fwhm) white probe pulse. The energy dependence of the AA spectra of Mg-H2(5) in THF and CH2C12showed that they varied linearly with energy for pulses < 0.25 mJ and were invariant for pulses > 1mJ. For the pulse energies used in this study, 1-2 mJ, the AA spectra also varied linearly with the sample concentration (5 X 10-5-4 X lo4 M). Thus, it was possible to quantitatively compare the AA spectra of different samples. Time-resolved emission measurements were made with a Varian VPM-152 photomultiplier tube coupled to a Tektronix 7904 oscilloscope. The overall time response of this detection system was 1.0 f 0.1 ns. A "front surface" geometry was used to detect emission and the 527-nm light scattered from the 6-ps excitation pulse was absorbed by red filters (Hoya 0-56 and R-60). Emission and excitation spectra were measured on a Perkin-Elmer MPF-4 spectrofluorimeter equipped with a Hamamatsu R-446 multialkali photomultiplier tube and an automatic emission corrector. Redox potentials were measured by cyclic voltammetry.20 The anion radical of free base octaethylporphyrin (H20EP)was generated by controlled potential electrolysis in tetrahydrofuran, and the cation of magnesium octaethylporphyrin (MgOEP) in methylene chloride.20
Results Solvent Effects. Theoretical treatments of ET processes indicate that ET rates should depend on the nature of the solvent. Four possible causes of this sensitivity are (1) alteration of the shapes of the potential energy surfaces of the reactants and produ~ts,2l-~~ (2) alteration of the electronic coupling, V, of the product and reactant wave R, = - C H , - C - N ( ~ ~ b ~ t ~ l ) ~ C H , ~ C H , ~ functions,26-B(3)variation of the free energy change, AGO, II of the r e a ~ t i o n , ~ ~and ~ ~ (4) " ~ variation ~ " - ~ ~ of the electron0 vibration ~ o u p l i n g . ~ ~ - " ~To * ~explore ~ solvent effects, we and the R1 groups are n-octyl chains. For H,-H2(4) the investigated the excited-state dynamics of Mg-H2(5) in linking chains are N,N-dimethylformamide (DMF) and N-methylacetamide (NMA). These results supplement the data previously R, = -CH,-C-N-CH,obtained in CH2C12and THF.12J3 Table I lists redox po/I I O H tentials and excited-state energies for Mg-H2(5) in these solvents. For a given porphyrin ligand, the free base and the R1 groups are n-pentyl chains. Replacement of complex is harder to oxidize and easier to reduce than the the two central H atoms by a Mg atom in one porphyrin magnesium complex. Thus, in a Mg-H2 diporphyrin, ET subunit yields Mg-H2(4) or Mg-H2(5). H2-H2(5S) comprises one 2,7,12,17-tetramethyl-3,13-di-n-pentylporphine to yield an oxidized Mg porphyrin and a reduced free base is energetically favored over the reverse reaction. For joined to a second porphyrin with the ammine ends of the solvents in which the free energy change required by this two covalent bridges, R2, attached at carbons 8 and 18. The second porphyrin is 3,7,12,18-tetramethyl-13,17-di- redox process, estimated from the oxidation and reduction potentials of the diporphyrin is less than the enn-pentylporphine with the acid ends of the two covalent ergy available from the lowest excited single state (E(&)), bridges attached at carbons 2 and 8. Again, Mg-H2(5S) such a light-driven ET process should be thermodynamdiffers only in the substitution of a Mg atom for two ically allowed.12 (Note that the excited-state energy is an central H atoms in one porphyrin subunit. enthalpy change and can be compared to a free energy The picosecond laser apparatus used to measure changes change only if the entropy changes associated with the in absorbance (AA)has been described elsewhere.'&19 The formation of the excited state are small.) Inspection of the samples (2 X 104-4 X lo4 M) were degassed with three data in Table I suggests that E T from the lowest excited freeze-pump-thaw cycles and sealed under vacuum in 2-mm path length cells. These samples were excited at 527 (20) Fajer, J.; Brune, D. C.; Davis, M. S.; Forman, A,; Spaulding, L. nm with a 6-ps laser pulse (1-2 mJ) and the AA spectra D. Proc. Natl. Acad. Sci. U.S.A. 1975, 72,4596. of the resulting photoproducts were measured with an &ps (21) Jortner, J. J. Chem. Phys. 1976, 64, 4860. Materials and Methods The syntheses of the cofacial diporphyrins are described in detail el~ehwere.'~J' Structure I is the free base-free base diporphyrin, Hz-H2(n). For H,-H2(5) the linking chains are
(14) Shuvalov, V. A.; Klimov, V. V.; Dolan, E.; Parson, W. W.; Ke, B. FEES Lett. 1980,118, 279. (15) Ke, B.; Klimov, V. V.; Dolan, E.; Shaw, E. R.; Shuvalov, V. A.; Parson, W. W.; Fajer, J.; Davis, M. S.; Forman, A. "Proceedings of the 5th International Congress on Photosynthesis", Halkidiki, Greece, in press. (16) Chang, C.-K. J. Heterocycl. Chem. 1977, 14, 1285. (17) Wang, C.-B.; Chang, C.-K., in preparation. (18) Creutz, C.; Chou, M.; Netzel, T. L.; Okumura, M.; Sutin, N. J. Am. Chem. SOC. 1980,102,1309. (19) Bergkamp, M. A.; Dalton, J.; Netzel, T. L. J. Am. Chem. SOC. 1982,104, 253.
(22) Hopfield, J. J. Proc. Natl. Acad. Sci. U.S.A. 1974, 71, 3640. (23) Warshel, A. Proc. Natl. Acad. Sci. U.S.A. 1980, 77, 3105. (24) Jortner, J. J. Am. Chem. SOC. 1980, 102, 6676. (25) Jortner, J.; Rice, S. A. "Physics of Solids at High Pressures"; Tomizuka, C. T., Emrich, R. M., Eds.; Academic Press: New York, 1975. (26) Hush, N. S. Trans. Faraday SOC. 1961,57,557. (27) Reynolds, W. L.; Lumry, R. W. 'Mechanisms of Electron Transfer"; Ronald Press: New York, 1966. (28) Levich, V. G. Adu. Electrochem. Eng. 1966,4, 249. (29) Brunshcwig, B. S.; Logan, J.; Newton, M.; Sutin, N. J . Am. Chem. SOC.1980,102,5798. (30) Sutin, N. Annu. Rev. Nucl. Sci. 1962, 12, 285. (31) Marcus, R. A. Discuss. Faraday SOC. 1960,29, 21. (32) Marcus, R. A. Annu. Reu. Phys. Chem. 1964,15, 155.
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The Journal of physical Chemistty, Vol. 86, No. 19, 1982
Fujita et al.
TABLE I: Thermodynamic and Lifetime Data for Mg-H,(5) solventa
E @ , )Ib
CH,CI,
eV 1.80e 2.03e 1.86 >1.88h
1.95 1.95 1.95 1.95
THF DMF NMA a
AEl,z,c
eV
ns
T ! m d
0.20
?
O.Olf
g
1.3 * 0 . 1 0.85 i 0.05
04r
0.1 M tetraethylammonium perchlorate was used as
Energy of the long wavethe supporting electrolyte. Sum o f the length edge of the first absorption band. free energy changes (negatives of the half-wave potentials) for the one-electron oxidation and reduction of Mg-H,(5). Lifetime of t h e Mg+.-H,-.(5) electron transfer product observed immediately after photolysis. e Reference 1 2 . f References 1 3 and 33. R In THF, only ~ T , R *states are observed (see text). Reduction of Mg-H,(5) in NMA is electrochemically irreversible.
L
2
M g - 4,151 i n
I
.,I-
ma
& ""':
L
-02 2
L-L--
~
63b
665nm
NMA
hALE-EfuGTH
-
820
700 pmr
Flgure 2. Changes in absorbances for 2.0 X lo-' M Mg-H2(5) in N-methylacetamkle at the indicated times after excitation. The insert shows a kinetic plot of these data with the AA value at 5 ns taken as the asymptote of the initiiel decay process.
41 -0 10L 500
M g - H 2 ( 5 ) IN DMF I.
~
l
600
1
I
650 700 750 WAVELENGTH ( n m )
!
000
Figure 1. Changes In absorbance for 2.08 X lo4 M Mg-H,(5) in N,Ndimethylformamkle at the indicated times after excitation at 527 nm with a &ps laser pulse. The insert shows a kinetic plot of these data with the AA value at 5 ns taken as the asymptote of the initial decay process. The rapid decrease in AA between 0 and 120 ps probably reflects solvent reorganization about the newly formed photoproduct. Such processes usually are complete in C20 ps.
singlet state is energetically unfavorable only for THF. (The case for E T in NMA is unclear because electrochemical reduction of the diporphyrin is not reversible in that solvent.) Figures 1 and 2 show the AA spectra and kinetic plots for Mg-H,(5) in DMF and NMA. Although the lifetimes of the initial transients differ, the early (0.97 (NMA) eV. These are plausible values for solvent reorganization energies; additionally, X-raSp76 and Raman data3' on neutral and ionic porphyrins suggest that the inner-sphere reorganization energy should be small. However, comparison of the aEllz values with these A's shows that AGO < -A. In this situation a classical model cannot be used to describe the reverse ET. This conclusion supports our earlier de~cription'~ of the reverse ET (Mg+.-Hp(5) Mg-H2(5)) as a nonadiabatic reaction due to an avoided crossing between the reactant and product potential energy surfaces. (Assuming that an effective or critical nuclear displacement coordinate governs ET rates in diporphyrins, the reactions can be discussed in terms of potential energy functions along this coordinate.) Since the avoided crossing occurs between two steeply rising potential energy curves, small changes in medium reorganization energy or AGO are likely to affect its location and alter the rate of the reverse ET. That the lifetimes of the E T products range between 0.2 and 1.3 ns with solvent variation agrees qualitatively with this nonadiabatic model. (The long-lived state (T = 5-15 ns) formed on decay of the ET product can only shorten the lifetime of Mg+*-Hp and thus cannot explain the slowness of the reverse E T to re-form S,,.) In contrast to the variable rate of reverse ET, the forward reaction in the above three solvents (Table I) is always >lO1's-l. This agrees qualitatively with our earlier proposal13that the potential energy curves for the SI and E T states are likely to cross near the minimum of the S1 potential energy curve. In this situation small variations 2 or, in medium in free energy change, AGO = U I j-E&), reorganization energy, are unlikely to alter significantly the ET rates, since it will remain nearly activationless. Temperature-dependent studies would test this possibility. The rate of a truly activationless ET process is calculated to be proportional to (1/7')ll2and therefore to have an apparent negative activation energy.24 We studied Mg-H2(4) and Mg-H2(5S) to learn about the variability of E T reaction rates due to alterations of the relative distance and orientation of the donor and acceptor macrocycles. Although the shorter linking chain in MgH2(4)should strain the diporphyrin by doming the macrocycles according to molecular models, the kinetics and spectral results for Mg-H2(4) were nearly indistinguishable from those of Mg-H2(5). Whether the rates of forward ET in CH2C12were actually altered could not be determined because the rates for both compounds were faster than the instrumental resolution, >lo" s-l. The results for Mg-H2(5S) in THF imply T,T* excitedstate decay without ET. In CH2C12,some conformations of Mg-Hz(5S) transfer electrons from their excited singlet states in 610 nm. This is not true for the excitation spectrum of shorterwavelength emidon. Thus,some impurity is present. Small amounts of impurities do not contribute to AA spectra (within error), unless their Ae for excited-state formation is much greater than the Ae for the sample's excited-state formation. This is not generally the case. In contrast, a small amount of an emitting impurity can be detected easily if ita emission spectrum is not identical with the sample's. (35) Several rates of singlet-state ET are possible, since the NMR spectrum of H*-H2(5S) (Chang, C.-K.;Wang, C.-B., unpublished data) shows that a molecule with the same carbon and nitrogen skeleton as Mg-H2(5S) has multiple conformations that are stable for at least 1 ms at room temperature. In accord with this NMR result, the triplet ESR spectrum of Cu-Cu(5S) at low temperature (Davis, M. S., private communication) shows that it also has more than one conformation.
(36) Spaulding, L. D.; Eller, P. G.; Bertrand, J. A.; Felton, R. H. J.Am. Chem. SOC.1974,96,982. (37) Felton, R. H.; Yu, N.-T. 'The Porphyrins";Dolphin, D.; Ed.; Academic Press: New York, 1978; Vol. 111, p 347.
J. Php. Chem. lQ82, 86, 3759-3767
decay also illustrates the complexity that flexible models introduce into ET studies. A series of donor-acceptor complexes with different but rigid relative orientations and distances is required for quantitative study of how such alterations affect ET reactions. Construction of such models constitutes a major synthetic challenge, however. In summary, the studies of solvent variation support our model of nearly activationless ET from the S1state of the diporphyrin followed by nonadiabatic reverse ET to reform the ground ~ t a t e . ' ~ The $ ~ chief reason the reverse E T step is so much slower than the forward one is that the ET product and ground-state potential energy curves nest and avoid crossing each other. In this case an adiabatic E T to re-form the ground state is not possible. Such molecular rectification seems to be a key process in natural
3759
photosystems, and Mg-Hz(5) and Mg-Hz(4) appear to simulate it well. The upper range of lifetimes for Mg+.H2--(5)as a function of solvent approaches that observed for the primary E T product of PSII (2-4 ns). Thus, the Mg-H2 diporphyrins afford reasonable biomimetic models of the primary donor-acceptor pair of PSII of green plants14 and illustrate the environmental and structural parameters that may control E T in vivo.
Acknowledgment. This work was supported by the Office of Basic Enegy Sciences of the U.S. Department of Energy, Washington, DC (Contract No. DE-AC0276CH00016) at Brookhaven National Laboratory and by the Research Corp. and the National Science Foundation (Grant CHE-7815285) at Michigan State University.
Measurement of the Kinetics of Ligand Motion about Rare-Earth Ions in Liquids and Glass-Forming Fluids Steven Brawer Lawrence Llvermore Netbnal Laboratory, L i v e r " , Callfornla 94550 (Received: December 3, 1981; I n Final Form: Merch 22, 1982)
We show how the technique of fluorescence line narrowing spectroscopy may be used to study the kinetics of ligand rearrangement about rare-earth ions in a liquid or glass-forming fluid. The equations relating the optical properties to the frequency-dependenttime autocorrelation function are derived under very general conditions. They are illustrated for the case of a Gaussian random process. A full qualitative discussion of the expected behavior is given. It is shown that at higher temperatures it is possible to observe narrow emission lines even in a system with considerable inhomogeneous broadening, due to motional narrowing.
Introduction In this article we describe how the technique of fluorescence line narrowing (FLN)' can be used to study the kinetics of ligand rearrangement about some optically active ions in liquids. FLN involves selective excitation of ions in an inhomogeneously broadened spectral profile by narrow-band, usually laser, radiation. The relevant equations describing the optical properties are derived, and a qualitative discussion is given of the nature and meaning of experimental results to be expected in various temperature regions. For purposes of this article our results will be concerned with rare-earth (RE) ions, particularly Eu3+. The results can also be applied to ion rearrangement in the vicinity of an organic molecule possessing an intrinsically narrow emission band. One of the problems addressed by this article concerns results similar to those of Figure 1. This is the broad-band 6Do-7Foemission of Eu3+ in an aqueous nitrate solution. The remarkable feature of this result is the very narrow width of the band, less than 6 cm-'.This is to be compared with the homogeneous width of this transition in oxide crystals, which is about 2 cm-', or the inhomogeneous width of the transition in oxide glaases,2of the order of 50 cm-'. Similar narrow bands in the absorption of Nd3+ in aqueous solutions have been observed by S v o r ~ n o s . ~ (1)W. M.Yen and P. M. Selzer, Eds., 'Laser Spectroscopy of Solids", Springer-Verlag, West Berlin, 1981. (2) See, for example: M. J. Weber in ref 1; S. A. Brawer and M. J. Weber, Phys. Rev. Lett., 46,460 (1980);J. Chem. Phys. 75,3516 (1981). (3)M.Svoronos, C.N.R.S., Meudon, France, private communication. 0022-365418212086-3759$0 1.2510
There appear to be two possible explanations for such a narrow band as shown in Figure 1. One is that the RE forms a very regular molecular complex in the solution, so each RE has the same environment, the same type of site (assuming that for some reason the second coordination sphere is not important in the inhomogeneous broadening). This would presumably eliminate the inhomogeneous broadening of the type found in glasses, where each rare earth is in a different type of site. Another possible explanation is that the spectrum of Figure 1 is motionally narrowed. Motional narrowing arises when the ligands move very rapidly relative to the inhomogeneous broadening (divided by h). In this case, the RE emission line is narrower than the full inhomogeneous width of the energy levels doing the emitting. This phenomenon is very well-known in NMR4 where it is observed frequently. In that case, the width of the absorption l i e s of spin levels are much narrower for spins in solution than in glasses in polycrystals. To my knowledge, true motional narrowing of optical emission lines in liquids has not been reported in the literature. (It has been discussed (4)P. W. Anderson and P. R. Weiss, Rev. Mod. Phys., 25,269(1953). (5) S.Hunklinger and W. Arnold, 'Physical Acoustics", Vol. 12, W. P. Maeon, Ed., Academic Press, New York, 1976. (6)S.A. Brawer, submitted to Phys. Rev. (7)S. K. Lyo and R. Orbach, Phys. Reu. B , 22, 4223 (1980);T.L. Reinecke, SoZid State Commun., 32,1103(1979);J. Hegarty and W. M. Yen, Phys. Reu. Lett., 43,1126 (1979);P.M.Selzer, D. L. Huber, D. S. Hamilton, W. M. Yen, and M. J. Weber, ibid., 36, 813 (1976). (8)D. L. Huber, in ref 1. (9)M.Goldstein, J. Chem. Phys., 51,3728 (1969);G. P. Johani and M.Goldstein, ibid., 53,2372 (1970). (IO) P.W. Anderson, B. J. Halperin, and C. M. Varma, Philos. Mag., 25, 1 (1972).
0 1982 American Chemical Society
