Support from model studies for the proposed existence of an S?1 oxidation level in the manganese assembly of the photosynthetic water oxidation centre (original) (raw)
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Modeling the photosynthetic water oxidation center. Preparation and properties of tetranuclear manganese complexes containing [Mn4O2]6+,7+,8+ cores, and the crystal structures of Mn4O2(O2CMe)6(bipy)2 and Mn4O2(O2CMe)7(bipy)2
Journal of the American Chemical Society, 1989
An inorganic model approach to the photosynthetic water oxidation enzyme has been initiated, and synthetic entry into tetranuclear Mn complexes containing \Mn402]6+~7+~8+ cores has been achieved. They have been obtained by bipyridine (bipybmediated conversion of trinuclear [Mn30]-containing species, with the product oxidation level governed by the exact identity of the [Mn30] reagent employed. Treatment of Mn3O(O,CMe),(py), with -3 equiv of bipy in MeCN yields Mn402(02cMe),(bipy), (1) in 91% yield. Complex 1.2CHCl3 crystallizes in triclinic space group Pi with (at -160 "C) a = 13.883 (3) A, b = 10.592 (2) A, c = 8.848 (1) A, a = 91.18 (l)", / 3 = 72.14 (I)", y = 71.44 (l)", V = 1163.84 A3, and Z = 1. A total of 3064 unique data with F > 3u(F) were refined to values of R and R,of 3.23 and 3.75%, respectively. The molecule lies on an inversion center and contains a planar Mn4 rhombus with two p 3 -0 atoms, one above and one below the Mn4 plane. The resulting [ M I I , O~]~+ core is mixed valence (2Mn", 2Mn"') and can be considered as fusion of two M n 3 0 units by edge-sharing. Peripheral ligation is by six p2-02CMe and two terminal bipy groups to yield a complex with imposed C, symmetry. Treatment of Mn3O(o,CR),(py),(H2o) (R = Ph, 3-Me-Ph) with -3 equiv of bipy in MeCN yields Mn4O2(O2CR),(bipy), (R = Ph (2) or 3-Me-Ph (3)) containing Mn", 3Mn"'. Similarly, treatment of [Mn30(02CR),(py)3](C104) (R = Me, Et, Ph) with -3 equiv of bipy in MeCN yields [Mn4O2(0,CR),(bipy),](C1O4) (R = Me (4), Et (8), Ph (9)) containing 4Mn"'. Use of 4,4'-Mez-bipy instead of bipy results in the corresponding complex [Mn402(02CMe)7(4,4'-Mez-bipy),l(C104)
Inorganic Chemistry, 1996
Synthetic procedures are described that allow conversion of [Mn 4 O 2 (OAc) 6 (py) 2 (dbm) 2 ] (1, dbmH ) dibenzoylmethane) to [Mn 4 O 3 X(OAc) 3 (dbm) 3 ] (X ) Cl, 2; X ) Br, 3). Treatment of 1 with NBu n 4 Cl in CH 2 Cl 2 or hot MeCN leads to 2 in 5-8% and 35-43% yields (based on dbm), respectively. A higher yield (∼88%) is obtained by treating 1 with 4 equiv of Me 3 SiCl in CH 2 Cl 2 . An analogous procedure with 4 equiv of Me 3 SiBr in CH 2 Br 2 gives 3 in 55% yield. Complexes 2 and 3 are isomorphous, monoclinic space group P2 1 /n, T ) -155°C, Z ) 4. For 2, a ) 13.900(3), b ) 22.038(5), and c ) 16.518(5) Å and ) 107.80(1)°; for 3, a ) 13.644(2), b ) 22.190(4), and c ) 16.548(3) Å, and ) 106.64(1)°. The structures were solved by direct methods (MULTAN78) and refined on F to R(R w ) values of 7.85 (7.38) and 7.37 (6.89)% using 2267 and 2809 unique reflections with F > 2.33σ(F) for 2 and 3, respectively. Treatment of [Mn 3 O(OAc) 6 (py) 3 ](ClO 4 ) in MeCN with Me 3 SiCl followed by addition of H 2 O and acetic acid results in crystallization of (pyH) 3 [Mn 4 O 3 Cl 7 (OAc) 3 ]‚2MeCN (4) in 75% yield (based on Mn). Complex 4 crystallizes in monoclinic space group C2/c with the following cell parameters at -157°C: a ) 37.420(5), b ) 13.752(1), and c ) 16.139(2) Å, ) 110.33(1), V ) 7787.9 Å 3 , and Z ) 8. The structure was solved by direct methods (MULTAN78) and refined on F to R(R w ) values of 5.74 (5.78)% using 2612 unique reflections with F > 3.0σ(F). The complexes possess a [Mn 4 (µ 3 -O) 3 (µ 3 -X)] distorted cubane core and a 3Mn III ,Mn IV trapped-valence oxidation-state description. Three AcOgroups bridge each Mn III Mn IV pair, and a chelating dbm -(2 and 3) or two Clions (4) on each Mn III complete peripheral ligation. The pyridinium cations of 4 are involved in hydrogen-bonding interactions with the µ 3 -O 2and the terminal Clions of the anion. Variable-temperature solid-state magnetic susceptibility studies show that the magnetic properties of 2 and 3 are very similar: µ eff values steadily rise from ∼9 µ B at room temperature to ∼10 µ B at 30.0 K and then drop rapidly to ∼9.5 µ B at 5 K. Fitting of the experimental data for the two complexes to the appropriate theoretical equation yield the following fitting parameters, in the format 2/3: J ) J(Mn III ‚‚‚Mn IV ) ) -28.4/-30.1 cm -1 , J′ ) J(Mn III ‚‚‚Mn III ) ) +8.3/+7.4 cm -1 , and g ) 1.98/2.03. Both 2 and 3 have S ) 9 / 2 ground states that are well-separated (∼180 cm -1 ) from an S ) 7 / 2 first excited state. The ground state was confirmed by magnetization vs magnetic field studies at several fields and temperatures; fitting of the data allowed the zero-field splitting parameter D to be determined for both complexes. The magnetochemical properties of 4 are very similar to those of 2 and 3, and the fitting parameters were J ) -29.1 cm -1 , J′ ) +10.2 cm -1 , and g ) 1.97, giving an S ) 9 / 2 ground state and showing that the hydrogen-bonding interactions of the µ 3 -O 2ions do not cause a significant change to the exchange parameters or to the electronic structure of the [Mn 4 O 3 Cl] 6+ core. 1 H NMR spectra of 2-4 in CDCl 3 or CD 3 CN solution at ∼23°C are similar and show that the Mn 4 complexes retain their solid-state structure on dissolution in this solvent. X-band EPR spectra of 2 and 3 in CH 2 Cl 2 /toluene (1:1) glasses at 5 K are also extremely similar, with three main features at g ) 11.0, 5.2, and 1.96. Cyclic voltammetry at 100 mV/s and differential pulse voltammetry at 5 mV/s show that both 2 and 3 support a reversible oxidation and two reductions, the first of which is reversible. The reversible processes are at 1.09/1.06 and -0.25/-0.21 V vs ferrocene and show that the [Mn 4 O 3 X] core can exist at three oxidation levels spanning the 4Mn III to 2Mn III , 2Mn IV range. The combined results from 2 and 3 show that the identity of X has minimal influence on the resultant structures, magnetic properties, 1 H NMR and EPR spectral properties, or the redox behavior. Such observations are of interest with regard to the ability of Brto successfully substitute for Clat the photosynthetic water oxidation center and thus maintain the activity of the tetranuclear Mn aggregate toward oxygen evolution. † Present address:
Photochemistry and Photobiology, 1999
The water-oxidizing complex of chloroplast photosystem I1 is composed of a cluster of four manganese atoms that can accumulate four oxidizing redox equivalents. Depletion of manganese from the water-oxidizing complex fully inhibits oxygen evolution. However, the complex can be reconstituted in the presence of exogenous manganese in a process called photoactivation. In the present study, mononuclear manganese complexes with ligands derived from either nitrosonaphthol and ethylenediamine (Niten) or from diaminohexane and salicylaldehyde (Salhxn) are used in photoactivation experiments. Measurements of photoinduced changes of chlorophyll fluorescence yield, thermal dissipation using photoacoustic spectroscopy, photoreduction of 2,6-dichorophenolindophenol and oxygen evolution in manganese-depleted and in reconstituted photosystem I1 preparations demonstrate that photoactivation is more efficient when Niten and Salhxn complexes are used instead of MnCI,. It is inferred that the aromatic ligands facilitate the interaction of the manganese atoms with photosystem 11. The addition of CaCI, and of the extrinsic polypeptide of 33 kDa known as the manganese-stabilizing protein during photoactivation further enhances the recovery of electron transport and oxygen evolution activities. It is proposed that mononuclear manganese complexes are able to contribute to reconstitution of the water-oxidizing complex by sequential addition of single ions similarly to the current model for assembly of the tetranuclear manganese cluster and that these complexes constitute suitable model systems to study the assembly of the water-oxidizing complex.
Inorganic Chemistry, 1996
Synthetic procedures are described that allow conversion of [Mn 4 O 2 (OAc) 6 (py) 2 (dbm) 2 ] (1, dbmH ) dibenzoylmethane) to [Mn 4 O 3 X(OAc) 3 (dbm) 3 ] (X ) Cl, 2; X ) Br, 3). Treatment of 1 with NBu n 4 Cl in CH 2 Cl 2 or hot MeCN leads to 2 in 5-8% and 35-43% yields (based on dbm), respectively. A higher yield (∼88%) is obtained by treating 1 with 4 equiv of Me 3 SiCl in CH 2 Cl 2 . An analogous procedure with 4 equiv of Me 3 SiBr in CH 2 Br 2 gives 3 in 55% yield. Complexes 2 and 3 are isomorphous, monoclinic space group P2 1 /n, T ) -155°C, Z ) 4. For 2, a ) 13.900(3), b ) 22.038(5), and c ) 16.518(5) Å and ) 107.80(1)°; for 3, a ) 13.644(2), b ) 22.190(4), and c ) 16.548(3) Å, and ) 106.64(1)°. The structures were solved by direct methods (MULTAN78) and refined on F to R(R w ) values of 7.85 (7.38) and 7.37 (6.89)% using 2267 and 2809 unique reflections with F > 2.33σ(F) for 2 and 3, respectively. Treatment of [Mn 3 O(OAc) 6 (py) 3 ](ClO 4 ) in MeCN with Me 3 SiCl followed by addition of H 2 O and acetic acid results in crystallization of (pyH) 3 [Mn 4 O 3 Cl 7 (OAc) 3 ]‚2MeCN (4) in 75% yield (based on Mn). Complex 4 crystallizes in monoclinic space group C2/c with the following cell parameters at -157°C: a ) 37.420(5), b ) 13.752(1), and c ) 16.139(2) Å, ) 110.33(1), V ) 7787.9 Å 3 , and Z ) 8. The structure was solved by direct methods (MULTAN78) and refined on F to R(R w ) values of 5.74 (5.78)% using 2612 unique reflections with F > 3.0σ(F). The complexes possess a [Mn 4 (µ 3 -O) 3 (µ 3 -X)] distorted cubane core and a 3Mn III ,Mn IV trapped-valence oxidation-state description. Three AcOgroups bridge each Mn III Mn IV pair, and a chelating dbm -(2 and 3) or two Clions (4) on each Mn III complete peripheral ligation. The pyridinium cations of 4 are involved in hydrogen-bonding interactions with the µ 3 -O 2and the terminal Clions of the anion. Variable-temperature solid-state magnetic susceptibility studies show that the magnetic properties of 2 and 3 are very similar: µ eff values steadily rise from ∼9 µ B at room temperature to ∼10 µ B at 30.0 K and then drop rapidly to ∼9.5 µ B at 5 K. Fitting of the experimental data for the two complexes to the appropriate theoretical equation yield the following fitting parameters, in the format 2/3: J ) J(Mn III ‚‚‚Mn IV ) ) -28.4/-30.1 cm -1 , J′ ) J(Mn III ‚‚‚Mn III ) ) +8.3/+7.4 cm -1 , and g ) 1.98/2.03. Both 2 and 3 have S ) 9 / 2 ground states that are well-separated (∼180 cm -1 ) from an S ) 7 / 2 first excited state. The ground state was confirmed by magnetization vs magnetic field studies at several fields and temperatures; fitting of the data allowed the zero-field splitting parameter D to be determined for both complexes. The magnetochemical properties of 4 are very similar to those of 2 and 3, and the fitting parameters were J ) -29.1 cm -1 , J′ ) +10.2 cm -1 , and g ) 1.97, giving an S ) 9 / 2 ground state and showing that the hydrogen-bonding interactions of the µ 3 -O 2ions do not cause a significant change to the exchange parameters or to the electronic structure of the [Mn 4 O 3 Cl] 6+ core. 1 H NMR spectra of 2-4 in CDCl 3 or CD 3 CN solution at ∼23°C are similar and show that the Mn 4 complexes retain their solid-state structure on dissolution in this solvent. X-band EPR spectra of 2 and 3 in CH 2 Cl 2 /toluene (1:1) glasses at 5 K are also extremely similar, with three main features at g ) 11.0, 5.2, and 1.96. Cyclic voltammetry at 100 mV/s and differential pulse voltammetry at 5 mV/s show that both 2 and 3 support a reversible oxidation and two reductions, the first of which is reversible. The reversible processes are at 1.09/1.06 and -0.25/-0.21 V vs ferrocene and show that the [Mn 4 O 3 X] core can exist at three oxidation levels spanning the 4Mn III to 2Mn III , 2Mn IV range. The combined results from 2 and 3 show that the identity of X has minimal influence on the resultant structures, magnetic properties, 1 H NMR and EPR spectral properties, or the redox behavior. Such observations are of interest with regard to the ability of Brto successfully substitute for Clat the photosynthetic water oxidation center and thus maintain the activity of the tetranuclear Mn aggregate toward oxygen evolution. † Present address:
Intermediates of a polynuclear manganese center involved in photosynthetic oxidation of water
Proceedings of the National Academy of Sciences, 1981
Electron paramagnetic resonance of spinach chloroplasts given a series of laser flashes, n = 0, 1, ..., 6, at room temperature and rapidly cooled to -140°C reveals a signal possessing at least 16 and possibly 21 or more hyperfine lines when observed below 35 K. The spectrum is consistent with a pair of antiferromagnetically coupled Mn ions, or possibly a tetramer of Mn ions, in which Mn(III) and Mn(IV) oxidation states are present. The intensity of this signal peaks on the first and fifth flashes, suggesting a cyclic change in oxidation state of period 4. The multiline signal produced on the first flash is not affected by the electron transport inhibitor 3-(3,4-dichlorophenyl)-1,l-dimethylurea but is abolished by agents that influence the state of bound manganese, such as incubation with alkaline Tris, or dithionite, and by extraction with cholate detergent in the presence of ammonium sulfate. These results indicate that the paramagnetic signal is monitoring oxidation state changes in the enzyme involved in oxidation of water.
Inorganic Chemistry, 1999
The compound [Mn III 2 OL 2 ](ClO 4) 2 .2.23CHCl 3 .0.65CH 2 Cl 2 where Lis the monoanionic N,N-bis(2-pyridylmethyl)-N′-salicyliden-1,2-diaminoethane ligand, has been synthesized. The complex dication [Mn III 2 OL 2 ] 2+ contains a linear Mn(III)-O-Mn(III) unit with a Mn-Mn distance of 3.516 Å. The pentadentate ligand Lwraps around the Mn(III) ion. Electrochemically, it is possible to prepare the one electron oxidized trication [Mn 2 OL 2 ] 3+ which crystallizes as [Mn 2 OL 2 ](ClO 4) 2.37 (PF 6) 0.63 ‚1.5CH 3 CN. The complex trication [Mn 2 OL 2 ] 3+ contains a Mn(III)-O-Mn(IV) unit with a Mn-Mn distance of 3.524 Å and a Mn-O-Mn angle of 178.7(2)°. The contraction of the coordination sphere around the Mn(IV) is clearly observed. The [Mn 2 OL 2 ] 2+ dication possesses a S) 0 electronic ground state with J)-216 cm-1 (H)-JS 1 ‚S 2), whereas the [Mn 2 OL 2 ] 3+ trication shows a S) 1 / 2 ground state with J)-353 cm-1. The UV-visible spectrum of [Mn 2 OL 2 ] 3+ exhibits an intense absorption band () 3040 M-1 cm-1) centered at 570 nm assigned to a phenolate f Mn(IV) charge-transfer transition. The potentials of the redox couples determined by cyclic voltammetry are E°([Mn 2 OL 2 ] 3+ /[Mn 2 OL 2 ] 2+)) 0.54 V/saturated calomel electrode (SCE) and E°([Mn 2 OL 2 ] 4+ /[Mn 2 OL 2 ] 3+)) 0.99 V/SCE. Upon oxidation at 1.3 V/SCE, the band at 570 nm shifts to 710 nm () 2500 M-1 cm-1) and a well-defined band appears at 400 nm which suggests the formation of a phenoxyl radical. The [Mn 2 OL 2 ] 3+ complex exhibits a 18-line X-band electron paramagnetic resonance (EPR) spectrum which has been simulated with rhombic tensors |A 1x |) 160 × 10-4 cm-1 ; |A 1y |) 130 × 10-4 cm-1 ; |A 1z |) 91 × 10-4 cm-1 ; |A 2x |) 62 × 10-4 cm-1 ; |A 2y |) 59 × 10-4 cm-1 ; |A 2z |) 62 × 10-4 cm-1 and g x) 2.006; g y) 1.997; g z) 1.982. This EPR spectrum shows that the 16-line paradigm related to a large antiferromagnetic exchange coupling and a low anisotropy can be overcome by a large rhombic anisotropy. Molecular orbital calculations relate this rhombicity to the nature of the orbital describing the extra electron on Mn(III). This orbital has a majority but not pure d z 2 contribution (with the z axis perpendicular to the Mn-Mn axis). Low-temperature resonance Raman spectroscopy on an acetonitrile solution of [Mn 2 OL 2 ] 4+ prepared at-35°C indicated the formation of a phenoxyl radical. This suggests that the ligand was oxidized rather than the Mn(III)Mn(IV) pair to Mn(IV)Mn(IV), which illustrates the difficulty to store a second positive charge in a short range of potential in a manganese mono-µ-oxo pair. The relevance of these results to the study of the photosynthetic oxygen evolving complex is discussed.