6440
J. Phys. Chem. B 1998, 102, 6440-6447
Fast Photoinduced Electron Transfer from Polyalkyl- to Polyfluoro-Metalloporphyrins in Lipid Bilayer Membranes Kai Sun and David Mauzerall* The Rockefeller UniVersity, 1230 York AVenue, New York, New York 10021 ReceiVed: April 22, 1998
Direct electrochemical evidence shows that photoinduced electron transfer from excited Mg-octaethylporphyrin (MgOEP) to a Mg (or Zn) complex of tetrakis(pentafluorophenyl)porphyrin (TFPP) in lipid bilayers occurs with a second-order rate constant g108 M-1 s-1. This reaction is ∼100 fold faster than the reported intermolecular rate between porphyrins, and occurs even under aerobic conditions. Electron transfer from the ground state of MgOEP to excited ZnTFPP is observable under anaerobic conditions, but the rate is ∼10-fold slower. Time-resolved photoconductivity of the lipid bilayer with the mixed metalloporphyrins suggests that the charge recombination times (τ) of the geminate ion pairs in the MgTFPP-MgOEP and ZnTFPP-MgOEP systems are 20 and 38 µs, respectively. The MgTFPP- anion reduces O2 with a secondorder rate constant of ∼107 M-1 s-1, but the oxidation of ZnTFPP- anions by O2 is very slow. The differences between the two systems may arise from different redox potentials of ZnTFPP and MgTFPP. These data prove that, even containing Mg, the least electronegative element which can be stably chelated, a metalloporphyrin with poly electron-withdrawing groups is a good electron acceptor. Our results suggest that such electronegative porphyrins are useful molecular parts for assembling of porphyrin-based biomimetic energy conversion devices.
Introduction Photoinduced electron transfer in condensed phases is the basis of biological photosynthesis and artificial solar energy conversion. The primary electron donor and acceptor1-3 of the photosynthetic bacteria and green plants are porphyrin-based pigments in cell membranes. To mimic photosynthesis and develop porphyrin-based photoelectronic devices, a large number of porphyrins4 and covalently linked porphyrin assemblies5-9 have been synthesized and studied over past decades. Magnesium and zinc complexes of porphyrins have attracted special interest because of their high photochemical activity and closer relation to photosynthetic processes than other metalloporphyrins. They are usually stronger electron donors in their excited states and more lipophilic than corresponding free-base porphyrins. These advantages may be why only magnesium1 and, under special acidic conditions, zinc10 have been selected by evolution as the chelated metals in known photosynthetic organisms. Although the first step of charge separation in photosynthetic processes occurs between porphyrin-like pigments2,3 and quinones are the secondary electron acceptors, quinones and other small molecules have been extensively used as the primary acceptor in reported biomimetic systems.5 This is partly because few magnesium, zinc, or even free-base porphyrins have been found to be good electron acceptors in ground or excited states, although interporphyrin ion formation has been demonstrated by sensitive methods.11,12 In recent years, more efforts to find artificial systems with interporphyrin electron transfer has been made. Most covalently linked porphyrin assemblies have resulted in significant excitation energy transfer, but not electron transfer,9 although fast intramolecular electron transfer between * To whom correspondence should be addressed. FAX: 212-327-8853. E-mail:
[email protected].
porphyrin groups have been reported in some dimers.6-8 The porphyrin anions formed in these dimers have lifetimes of 1.0 V shift of the reduction potential of metalloporphyrins at electrode surfaces.15 Gust et al.8 have shown by transient spectroscopy that free-base polyhaloporphyrin can rapidly accept an electron from a covalently linked electrondonating porphyrin on light excitation. Up to now, however, there has been no evidence that intermolecular electron transfer between the two porphyrin monomers can occur effficiently on excitation. ZnTFPP has been found to be hardly oxidized by O2 in its excited state.16 Further photochemical studies of metal complexes of polyhaloporphyrins have not yet been reported. Earlier studies11,17 have shown that photoformed geminate ion pair in the liquid phase can be monitored by measuring changes of dc conductivity caused by dielectric dependent escape of the ions. We now provide direct electrochemical evidence for photoinduced porphyrin anion-cation charge separation between MgTFPP (or ZnTFPP) and MgOEP (magnesium octaethylporphyrin). The electron transfer from excited MgOEP to the ground state of MTFPP (M represents metal) in
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TABLE 1: Comparison of Maximum Absorption Wavelengths (λmax, nm) and Coefficients (E, mM cm-1) between TFPP, ZnTFPP, MgTFPP, and MgOEP in Chloroform TFPP ZnTFPP MgTFPP MgOEP
λmax
λmax
λmax
λmax
at 590
at 620
412 414 419 411
483 400 698 372
505 542 556 543
37.8 16.8 20.6 15.0
584 578 589 580
12.0 5.3 2.8 12.7
656 624 628
10.8 4.9 5.1
9.5 1.3 2.6 2.1
1.6 4.1 2.9
lipid bilayers has a faster rate than the intermolecular reactions in earlier reported systems.11,12 This reaction in the present system occurs even under aerobic conditions. The geminate charge recombination in the photoformed porphyrin ion pair takes many microseconds, depending on the metal chelated in TFPP. Materials and Methods 1,2-Diphytanoyl-3-sn-phosphatidylcholine was obtained from Avanti Polar Lipids. Glucose oxidase and D-glucose were from Sigma Chemical Co. Magnesium octaethylporphyrin (MgOEP) and 5,10,15,20-tetrakis(pentafluorophenyl)-21H,23H-porphyrin (TFPP) were from Aldrich Chemical Co. Magnesium and zinc chelates of TFPP were prepared from TFPP. MgTFPP is a previously unreported compound. We prepared it by the magnesium insertion method reported recently by Lindsey and Woodford.18 TFPP (200 mg) was dissolved in 25 mL of CHCl3 in a round bottom flask. Triethylamine (0.8 mL) was added into the flask followed by 1.3 g of MgBr2‚O(Et)2. The mixture was stirred magnetically at the refluxing temperature. The occurrence of magnesium insertion reaction into TFPB was directly seen from the color change of yellowish brown to purplish red. The reaction progress was monitored by UV-vis absorption measurements of the solution. After 4 h, the strongest adsorption bands of free-base TFPP at 412, 505, and 656 rim became hardly observable, and new bands appearing at 419, 556, and 628 nm did not further increase with time. The mixture was diluted with 80 mL CHCl3, washed with 100 mL of 5% NaHCO3 three times, dried with Na2SO4, and filtered. The filtrate was concentrated to ∼10 mL by evaporating the solvent and purified by passing through a chromatographic column (3 × 50 cm) filled with alumina (Fisher A540) in CH2Cl2. The sample was eluted with CH2Cl2, producing 193 mg of MgTFPP (∼95% yield). Table 1 is a comparison of the absorption properties of MgTFPP, ZnTFPP, TFPP, and MgOEP. Detailed descriptions of the lipid bilayer-forming method and the apparatus for time-resolved photoelectric measurements were published earlier.19 In this study, membrane forming solutions contained 20 mM diphytanoylphosphatidylcholine and one or two kinds of porphyrin at 0.1-4.0 mM in n-decane. Lipid bilayer membranes were formed in a 1.5 mm diameter hole in a thin Teflon partition of a polyethylene cell and bathed in aqueous solution of 0.1 M NaCl and 0.01 M Hepes buffer (pH 7.8). They had a capacitance of 6 nF and a resistance of g109 Ω. The presence of MgOEP in the lipid bilayer affected neither the membrane capacitance nor the membrane resistance. The addition of MgTFPP or ZnTFPP in the lipid bilayer caused e10fold decrease of the resistance, when the concentration is e2 mM, and no significant changes of the capacitance. However, the addition of free-base TFPP at 2 mM in the lipid solution reduced the membrane resistance by up to 3 orders of magnitude depending on pH of the bathing solution. Because complicated proton transfers were involved when TFPP was present, the photoelectrochemical signals of the TFPP-MgOEP system were not simply comparable to those of the MTFPP-MgOEP systems. When used, ferrocyanide, ferricyanide, anthraquinone-
2-sulfonate (AQS-) or methyl viologen (MV2+), and glucose oxidase in aqueous solutions were added into the bathing electrolyte solution of the membrane. Light was incident on the lipid membrane through a glass window of the cell. A 1 µs pulse of light (590, Rhodamine 6G, or 620 nm, Rhodamine B3) was from a pulsed dye laser (Candela MDL-1P). Typically, the porphyrins in lipid bilayers were excited by a pulse with ∼2 mJ energy. Currents were monitored across the membrane through two calomel electrodes with saturated KCl bridges immersed in the bathing solutions and by a fast operational amplifier (Teledyne #1021) with a homemade feedback circuit of adjustable gain and time constant. The time constant was 1-100 µs depending on the gain (105107 V/A) set for measuring different currents. dc voltages were applied between the same calomel electrodes across the membrane by a variable voltage source connected in series to the ground input of the amplifier. To keep the symmetry of the lipid bilayer, voltages with opposite signs were alternatively applied for the same time ( millisecond scale) and its total charge (i.e. the time integral of current) is strikingly decreased. These changes suggest that O2 at air concentration oxidizes the porphyrin anions in the geminate ion pairs within 10 µs, producing free porphyrin cations and O2anions. The slow movement of the former under applied voltage produces the aerobic slow-phase current. Details are given in the Discussion. The weak photocurrent in the presence of MgOEP alone (curve c in Figure 2A) possibly arises from voltage-induced asymmetric electron transfer across the two interfaces from the excited MgOEP to aqueous glucose oxidase. This enzyme is a weak electron acceptor.23 It is known that O2 can quench the triplet excited state of porphyrins on the microsecond time scale, but cannot significantly oxidize excited porphyrins.11,22 Clearly the striking O2 sensitivity of the photocurrent does not arise from the quenching of the excited porphyrin, since this will cause less total photoformed charges, opposite to the observed increase in mobile charges (Table 2). These results show that the interporphyrin electron transfer has a faster rate than the O2 quenching reaction of the excited porphyrin under aerobic conditions. MTFPP is an Efficient Electron Acceptor. When ZnTFPP instead of MgTFPP is present with MgOEP in lipid bilayers, a photocurrent with a 3-4-fold larger amplitude on the microsecond time scale occurs on excitation of 590 rim (curve a in Figure 3A), but its magnitude of ∼10 pA on the 100 ms scale
Figure 2. Changes of the photocurrents caused by removing O2 from the lipid bilayer system on excitation respectively at 590 nm (A, both MgTFPP and MgOEP excitation) and 620 nm (B, exclusively MgTFPP excitation). (a) The bilayer containing both MgTFPP and MgOEP at air-saturated O2 concentration. (b) The O2 concentration in (a) is reduced g103-fold in the presence of 120 µg/mL glucose oxidase and 0.01 M D-glucose on both sides of the bilayer. (c, d) The bilayer containing MgOEP or MgTFPP alone under anaerobic conditions.
TABLE 2: Maximum Magnitude, Half-Life, and Total Charge of the Photocurrent under the Typical Conditions for Various Systems aerobicity MgTFPP-MgOEP compounds 590 nm Imax (nA) t1/2 (µs) q (pC) 620 nm Imax (nA) t1/2 (µs) q (pC)
O2 38 130 1200 ∼2 ∼50 ∼0.1
-O2 235 35 15 20 30 0.6
ZnTFPP-MgOEP O2
-O2
140 70 18
255 80 32
5 ∼50 ∼0.3
78 90 10
is ∼100-fold weaker than that of the Mg-Mg system under aerobic conditions. In the absence of O2 (curve b in Figure 3A), the photocurrent amplitude of the Zn-Mg system is comparable to that of the Mg-Mg system, but the current rise and decay rates of the former are significantly slower. The large fast-phase current confirms that the interporphyrin electron transfer occurs in the Zn-Mg system. Note that the relative numbers of charges photoformed in the Zn-Mg and Mg-Mg
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Figure 4. Changes of the fast-phase photocurrent amplitude under anaerobic conditions with increase of excitation energy at (A) 590 nm and with concentration of (B) MgTFPP. The excitation energies are those measured before the light passes through the glass window of the membrane-containing cell. The dotted curve shows the fit of a square-root function to the data. The photocurrent of ZnTFPP-MgOEP system has a similar dependence on the concentration of ZnTFPP.
Figure 3. Photocurrent of the lipid bilayer with ZnTFPP and MgOEP under the typical conditions of excitation at 590 nm (A) and 620 nm (B). (a) O2 is present. (b) O2 is removed. The bilayer contains both ZnTFPP and MgOEP. The dotted curve shows the fit of a linear combination (f ) 1.33a(A) + b(B)) of the traces a in A and b in B to the trace b in A. This suggests that the anaerobic current at 590 nm includes a contribution of charge separation between the excited ZnTFPP and ground MgOEP. (c, d) The bilayer contains only ZnTFPP in the presence or absence of O2.
systems cannot be estimated simply from the ratio of their current amplitudes, because the dissociation constant of the geminate ion pairs may be different. In the Zn-Mg system O2 has less effect on the photocurrent than in the Mg-Mg system. The small total charge of the aerobic current in the former (Table 2) indicates that few porphyrin cations have been freed by oxidation of the coformed anions. These results suggest that the MTFPP- anions, whose properties alter with the chelated metal, are formed in the lipid bilayer. The lesser sensitivity of ZnTFPP- anions to O2 most likely arises from its higher oxidation potential than that of MgTFPP-. Thus intermolecular electron transfer occurs in the direction from MgOEP to MTFPP. The excited state of MgOEP is known to be an efficient electron donor.19-22 This supports the direction of electron transfer inferred from the higher oxidation potential of MTFPP and proved by the O2 effects on the photocurrents. A photocurrent with a comparable rise-time and amplitude have been observed from a lipid bilayer with free-base TFPP and MgOEP, but the interference of proton transfer in the system complicates the current decay (data not shown).
For both the Mg-Mg and Zn-Mg systems, the amplitude of photocurrent is roughly linear to changes of porphyrin concentrations and excitation energy in the lowest ranges (Figure 4, not shown for the Zn-Mg system). The amplitude increases sublinearly with further increase of the concentration and the energy, approximately as the square root of the variable. These data suggest that the active states of porphyrins are their monomers and that the electron transfer occurs from an excited state to a ground state, not between excited sates. Are the Excited States of Both Porphyrins Active? Because both MTFPP and MgOEP have absorption at 590 nm (Table 1), the active excited state in the interporphyrin electron transfer cannot be known from only the data on excitation at 590 nm. Figures 2B and 3B show the photocurrent induced by a saturating pulse of light at 620 nm, where the absorption by MgOEP is negligible and the absorption of both MgTFPP and ZnTFPP is greater than that at 590 nm (Table 1). Under aerobic conditions, the excitation at 620 nm causes at most 5% of the photocurrent observed at 590 nm for both the Mg-Mg and ZnMg systems. Thus the excited state of MTFPP has very small contribution to the aerobic photocurrent possibly because of more extensive quenching of the excited state. The excited MgOEP must be the active electron donor for the fast electron transfer on excitation at 590 nm. Intermolecular energy transfer between MTFPP and MgOEP was not observed by fluorescence measurements of thin porphyrin-doped lipid films on a glass surface. Both porphyrins showed their respective fluorescence. The electron transfer may occur from the triplet states, see Discussion. The system with MTFPP alone has little photocurrent on excitation of 620 nm under both aerobic and anaerobic conditions, indicating that electron transfer between the excited and
6444 J. Phys. Chem. B, Vol. 102, No. 33, 1998
Figure 5. The fit of a single exponential function to the decay of the fast-phase photocurrent under anaerobic conditions. The slow-phase is removed by adding ferrocyanide at 5 mM to both sides of the lipid bilayer. Other conditions are typical. (a) The MgTFPP-MgOEP system. (b) The ZnTFPP-MgOEP system. The dotted curves are the fit of a single exponential function (I ) Imax exp(-t/τi)) to the current decay traces.
ground states of MTFPP can hardly occur. In the anaerobic Zn-Mg system, however, a significant photocurrent is induced by the same excitation (curve b in Figure 3B). This current arises most likely from the oxidation of ground state MgOEP by the triplet state of ZnTFPP. Its slow rise time (t1/2 ≈ 10 µs) shows that this reaction is much slower than the electron transfer from excited MgOEP to ground ZnTFPP (t1/2 < 1 µs), similar to the intramolecular electron transfer in the covalently linked dimers reported by Gust et al.8 The sensitivity of the current to O2 (Figure 3B) suggests that the electron transfer from the ground state of MgOEP to the triplet state of ZnTFPP is slower than the quenching of triplet ZnTFPP by O2. The contribution of such a slowly-rising current component may be the main cause for the higher amplitude and slower rise and decay rates of the anaerobic than aerobic photocurrents at 590 nm. This explanation is supported by a fit of the linear combination of curve b in Figure 3B and curve a in Figure 3A to the curve b in Figure 3A. The Charge Recombination of Geminate Porphyrin Ion Pairs. It is unlikely that the currents observed are caused by the orientation of the ion pair in the applied electric field. If so, a corresponding negative current would be observed as the charges in the oriented pairs recombined. The anaerobic experiment indicates the recombination occurs on the
