Horizontal and Vertical Push Effects in Saddled Zinc Porphyrin

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Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX

Horizontal and Vertical Push Effects in Saddled Zinc Porphyrin Complexes: Implications for Heme Distortion Jinjin Zhang, Min Tang, Dilong Chen, Binghua Lin, Zaichun Zhou,* and Qiuhua Liu* Key Laboratory of Theoretical Organic Chemistry and Functional Molecules, Ministry of Education, and School of Chemistry and Chemical Engineering, Hunan University of Science and Technology, Xiangtan 411201, China

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S Supporting Information *

ABSTRACT: A heme oxygen binding behavior was described through a unique geometric and electronic comparison of zinc porphyrin complexes. In this work, a charge transfer model for saddled metalloporphyrin complexes outlined the push effects of the ring nonplanarity and axial imidazole, and the pull effect of the axial dioxygen. The origin and role of the horizontal (ring nonplanarity) push effect and its relationship to the vertical (axial ligand) push/pull effect and its contribution to dioxygen binding were considered from the perspectives of crystal structures, theoretical calculations, and bathochromic shifts. Single-point energy and molecular orbital calculations starting from crystal structures were used to obtain the electronic structures of zinc porphyrin complexes. This study not only revealed that the electronic behavior of metalloporphyrins is driven by ring nonplanarity and axial ligation but also afforded new insight into the oxygen carrier mechanism in heme.

1. INTRODUCTION Several properties unique to heme enzyme bound by histidine (His), tyrosine, or cysteine are attributed to a so-called “push effect” of the axial imidazole,1 phenolate,2 or thiolate3 ligands, respectively. O−O bond cleavage in heme is facilitated by preorganized hydrogen bonding interactions formed through the pull effect of the distal arginine (Arg) and His, and donation of a charge density from the push effect of the proximal His, which is called the Poulos−Kraut mechanism.4,5 For instance, the formation of Compound I in horseradish peroxidase depends on the push effect of His170 as well as the “pull effect” of Arg38. Similar axial ligation plays a dominant role in determining the electronic structure and reactivity of iron porphyrin active sites and synthetic models. These observations suggest the strength of push and/or pull effects is modulated in each class of heme enzymes like peroxidases.6 However, a direct comparison of these effects has not been reported because of the absence of a spectroscopic or similar measurement technique that is sensitive to both effects.7 Knowledge of the molecular mechanism that controls the formation rate of compound I is essential to understand peroxidase function at a molecular level. Generally, the axial push effect originating from the ligation of axial amino acid residues is not strong enough alone to drive charge (or electron) transfer from the heme ring to the axial ligand. This indicates that the activation of metalloporphyrins including the relevant natural analogues to dioxygen (O2) should not depend only on this vertical effect (Figure 1, left). One advantage of porphyrin rings is that they are highly flexible and can adopt a range of nonplanar conformations that © XXXX American Chemical Society

Figure 1. Schematic representation of the potential horizontal push effect. A saddled porphyrin is used to display the geometric changes as a representative of distorted metalloporphyrin, and the green structure represents a regular metalloporphyrin.

are necessary for a variety of biological functions.8 Recently, we demonstrated that the core contraction derived from the deformations of porphyrin rings can induce conversion of the electronic structure of coordinated iron(III),9−11 cobalt(II),12−14 copper(II),15 and zinc(II).16 Core contraction causes horizontal compression and should also exert a push force on the central metal. In this way, the metal is activated from both the horizontal and vertical directions (Figure 1, right). A unique Zn−O2 complex in a highly saddled porphyrin was observed and characterized.16 In this complex, strong charge Received: November 17, 2018

A

DOI: 10.1021/acs.inorgchem.8b03219 Inorg. Chem. XXXX, XXX, XXX−XXX

Article

Inorganic Chemistry

functional B3LYP of DFT, as implemented in Gaussian 09,22 and three X-ray crystal structures were used as the starting point of calculations. Single-point energy was obtained on the ground-state spin multiplicity.23 The 6-31G(d) and The 6-311G(d) basis set was used for all atoms.24 The information on d (Zn) and p (N) orbital energies, d → π* back bonding, and partial atomic charge assignments were obtained using the pop=NBO keyword, where NBO represents natural bond orbital procedure. All calculations were performed under Cs symmetry constraints. Additionally, mass spectroscopy was performed with a Waters Xevo Q-TOF-electronic spray Ion mass spectrometer. Absorption spectroscopy of the neutral complexes was recorded on a PerkinElmer Lambda 35 spectrophotometer.

feedback behavior from the zinc center to the axial O2 component maintains the stability of the oxygen adduct. It is well-known that charge transfer (CT) is inevitably accompanied by varying degrees of energy transfer in many photofunctional systems,17−20 where the energy required by the CT process originates from the ring distortion. In this work, we report the origin and role of the horizontal push effect in three saddled zinc porphyrin complexes and the relationship of the horizontal effect to the vertical effect and its contribution to binding with O2. Using single-point energy calculations starting from crystal structures rather than the optimized ones allows us to directly probe the electronic information in the ground-state molecules. A CT model is established to describe the predicted CT relationship of the saddled zinc porphyrin complexes.

3. RESULTS AND DISCUSSION 3.1. Synthesis. The synthesis and interconversion of three complexes containing zinc are outlined in Scheme 1.

2. EXPERIMENTAL SECTION Scheme 1. Zinc Porphyrin Complexes and Their Interconversiona

2.1. General Synthesis. Zinc Porphyrin (1-Zn). Free base porphyrin 1-H2 (20 mg, 0.021 mmol) was fully dissolved in dichloromethane (6 mL) under inert gas atmosphere, and the saturated methanol solution of zinc acetate (0.2 mL) was injected into the above solution and fluxed for 30 min. And then the solvent was removed under reduced pressure. The residue solid was separated by silica gel column chromatography with CH2Cl2/PE (1:1, v/v) to give the violet solid 21 mg (1-Zn) in yield 96.0%. 1H NMR (CDCl3, 500 MHz) δ: 8.96 (s, 4 H), 8.49 (d, 8 H, J = 2.5 Hz), 7.64 (dd, 4 H, J1 = 8.5 Hz, J2 = 2.0 Hz), 6.92 (d, 4 H, J = 8.5 Hz), 4.11 (dd, 4 H, J1 = 11.0 Hz, J2 = 6.0 Hz), 3.43 (dd, 4 H, J1 = 11.0 Hz, J2 = 6.0 Hz), 1.71 (s, 36 H); 13C NMR δ: 157.26, 151.90, 150.95, 142.52, 131.91, 131.48, 131.40, 129.08, 126.01, 113.34, 111.00, 65.71, 34.52, 31.94; UV−vis (chloroform, 293 K) λmax: 450, 573, 641 nm; ESI-high resolution mass spectrum (HR MS) calcd. for [C64H64N4O4Zn] [M]+: 1016.4214, found: 1016.4216. Zinc-Imidazole Porphyrin Complex (1-Zn-Im). Zinc porphyrin 1Zn (10 mg, 0.01 mmol) was dissolved in dichloromethane of 3 mL under inert gas atmosphere, and 1-H-imidazole (7 mg, 0.1 mmol) was added into the above solution and was stirred for 10 min at the room temperature. And then the solvent was removed under reduced pressure. The residue solid was washed by methanol three times and recrystallized in chloroform/methanol solution to give the violet solid 10 mg (1-Zn-Im) in yield 99.0%. %. 1H NMR (CDCl3, 500 MHz) δ: 8.88 (d, J = 2.5 Hz, 4 H), 8.38 (s, 4 H), 8.29 (s, 4 H), 7.60 (dd, 4 H, J = 8.5, 2.5), 7.39 (bs), 6.89 (d, 4 H, J = 8.5), 6.87 (bs), 4.10 (dd, 4 H, J = 11.0, 6.0), 4.10 (dd, 4 H, J = 11.0, 6.0), 2.0 (s, 2 H), 1.66 (s, 36 H), 1.26 (m, 3-H); 13C NMR (CDCl3, 500 MHz) δ: 157.4, 152.1, 151.5, 142.7, 134.9, 131.8, 131.6, 130.3, 129.3, 125.9, 121.6, 113.1, 111.2, 65.7, 60.5, 53.4, 34.5, 31.9, 14.2; UV−vis (chloroform, 293 K) λmax: 469, 588, 633, 695 nm; ESI-high resolution mass spectrum (HR MS) calcd. for [C67H67N6O4Zn] [M − H]−: 1083.4521, found: 1083.4533. The synthesis and characterization of 1-H2 and 1-Zn-O2 are discussed in the recent report.16 2.2. Crystal Structure Determination. A suitable single crystal of each compound was carefully selected and glued to a thin glass fiber with cyanoacrylate glue. Structural determination was performed by X-ray diffraction with a Bruker SMART 1000 CCD diffractometer equipped with a normal focus 2.4-KW sealed-tube X-ray source using monochromatic CuKα (λ = 1.54184 Å) radiation. The SMART program package was used to determine the unit-cell parameters and for data collection. All the structures were solved by direct methods and refined on F2 by full-matrix least-squares using the SHELXT-97 program system.21 For all compounds, the positional parameters for the zinc, N, and O atoms were located by direct methods. All the hydrogen positions were placed geometrically and refined by riding on their respective O and C atoms. The final positions of all nonhydrogen atoms were refined anisotropically. The procedure of the single crystal growth was provided in Supporting Information p S9. 2.3. Electronic Structure Calculation. The calculations of single point energy were performed using the hybrid exchange-correlation

a

Note: (a) Zn(AcO)2, dichloromethane/methanol; (b) Zn(AcO)2, acetic acid, refluxed for 2 h in air. (c) imidazole (Im); (d) in the presence of acetic acid and air. Symbols x- and y- represent the two perpendicular directions of N1−N3 and N2−N4 in the core, respectively.

Compound 1-Zn was obtained using the classic metal insertion method under anaerobic conditions.25 Actually, one of the axial positions of 1-Zn is ready to bind to a ligand, which is methanol here, because of the five-coordinate nature of the zinc center in this complex.26 Sample 1-Zn will preferentially form the Zn−O2 component under acidic and aerobic conditions, so the 1-Zn-O2 complex can be directly formed by Adler−Longo condensation27 in the presence of zinc and oxygen sources.16,28 Alternatively, the 1-Zn-O2 complex can also be obtained by metal insertion into 1-H2 under the same conditions, where the metal-free material 1-H2 can be prepared in an acceptable yield by a recently published modular synthesis strategy.29 Complex 1-Zn-Im was directly transformed from its counterpart 1-Zn or 1-Zn-O2 by adding excess imidazole and recrystallization from chloroform/methanol solution. More planar materials 2-Zn and 3-Zn used as references were synthesized according to our previous report.16 The target complexes were directly characterized by X-ray B


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Inorganic Chemistry

Figure 2. Crystal structures of three zinc porphyrin complexes. Axial ligands are labeled in square brackets; LNN and LZnN shown in the bottom of each structure represent the distances of diagonal N−N and Zn−N atoms in the core, respectively; ANZnN is the bond angle of the central N−Zn− N components, and symbols x- and y- represent the two perpendicular directions of N1−N3 and N2−N4 in the core, respectively.

diffraction, ultraviolet−visible and nuclear magnetic resonance spectral methods, and high-resolution mass spectrometry. 3.2. Size Effect between the Metal and Ligands. The diameters of metal ions will change with the porphyrin core size,9−15 but this change is not static because changes in the metal (for example, a change in oxidation state) can exert a counteracting effect on core size.15,30,31 Three complexes of zinc porphyrin, 1-Zn-O2, 1-Zn-Im, and 1-Zn, and the relative free-base material 1-H2 were combined to track this interaction between the metal and core. As for 1-H2, its core is not affected by a metal ion, so it can be used as a reference to evaluate the influence of metal species on the porphyrin core. The relevant crystal structures and selected structural parameters are presented in Figure 2 and Table 1. Figure 3. Comparison of the core size (LNNx and LNNy) in two perpendicular directions for the porphyrins. ΔL1, ΔL2, and ΔL3 are the deviations of 1-Zn, 1-Zn-Im, and 1-Zn-O2 from LNN of 1-H2 in the x-direction, respectively.

Table 1. Selected Structural Parameters of Zinc Porphyrin Complexes material parameter a

LNNx (/Å) LNNy (/Å) LZnNx (/Å)a LZnNy (/Å) ANZnNx (/deg) ANZnNy (/deg) LZnL (/Å)b

1-Zn-O2

1-Zn-Im

1-Znc

1-H2d

3.932(6) 4.121(6) 2.011(6) 2.074(6) 155.7 167.1 2.078(6) (Zn−O)

3.904(3) 4.137(3) 2.022(3) 2.088(3) 149.8 164.4 2.100(9) (Zn−N)

3.706(11) 4.098(13) 1.891(12) 2.051(10) 156.9 174.8 2.167(11) (Zn−O)

3.878(6) 4.131(6)

The changes in core diameter induced by ring geometry act as a switch to tune the electronic behavior of the central metal and macrocycle.9−16 These changes should originate from a balance between the push effects of the metal and core in the horizontal direction. It is well-known that there are two types of deformations of a porphyrin ring, in-plane and out-of-plane (Figure 1),34 and the in-plane deformation responsible for core contraction is correlated with the out-of-plane deformation if the effect of the metal on the ring is not considered.29 For the current complexes, however, the effect of the out-of-plane deformation is constant because the complexes have the same straps, which indicates that the observed change of core size (Figure 3) is only derived from the change in electronic behavior of the central metal. Additionally, the axial ligand can also exert different electronic effects, which are manifested by the different geometries of the complexes, such as the shortened Zn−O bond and elongated O−O bond in the Zn−O2 component and unchanged Zn−N bond in the Zn-Im one (Figure 2).35 Next, single-point energy calculations were conducted using the experimental crystal structures to determine the energy levels and charge occupancies of the zinc 3d orbitals and porphyrin ring with different geometries and axial ligation, to further evaluate the strength, direction, and shift of these push effects in three complexes. 3.3. Electronic Structures of Metal and Porphyrin Rings. The density functional theory (DFT) method was used here because of its ability to investigate the molecular and electronic structures of metalloporphyrins and related complexes.36,37 Researchers have been able to obtain broad theoretical pictures of the ground-state structures and orbital information of various important classes of metalloporphyrin complexes via empirical and semiempirical calculations.38

a

LNNx, LNNy, LZnNx, and LZnNy are defined in Figure 2. bLZnL is the bond length of Zn to the coordinating atom of the axial ligand. cThe axial ligand of 1-Zn is methanol. dStructural parameters of 1-H2 are extracted from ref 29. The symbol “−” represents no relevant value.

The macrocycles in the three complexes are strapped by two short ether straps, O(CH2)2O, which compels these macrocycles to adopt a classic saddle-type deformation. The axial ligands O2, Im, and MeOH are located on the same side as the straps. The complexes differ in their core size and metal deviation from the N4 core plane. (i) The core size changes even though the straps are the same, as shown by the comparison of LNNx and LNNy (Figure 3). The core geometry maintains a rhombus shape, and LNNx is smaller than LNNy, just like in reference 1-H2, but both LNNx and LNNy fluctuate obviously,32 especially ΔL1, which decreases by 0.17 Å in 1-Zn compared with that of 1-H2. Additionally, the increases of ΔL2 and ΔL3 of 0.02 and 0.05 Å, respectively, in the other two complexes are also not negligible. (ii) The metal deviation from the N4 core plane is considerable, as supported by the bond angles (ANZnNx) of 157° for 1-Zn, 156° for 1-Zn-O2, and 150° for 1-Zn-Im in the x-direction, which are much smaller than those in regular zinc porphyrin.33 C


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Inorganic Chemistry Table 2. Relative Energy Levels (Ed) and Charge Occupancies (Cd) of Zinc d Orbitals in Porphyrin Complexes parameter 1-Zn-O2 a

1-Zn-Im

1-Zn

2-Zn

3-Zn

orbital

Ed

Cd

Ed

Cd

Ed

Cd

Ed

Cd

Ed

Cd

dx2−y2 dz2 dxy dxz dyz

−10.58 −10.77 −10.69 −10.89 −10.81

1.986 1.962 1.981 1.988 1.980

−10.02 −10.14 −10.12 −10.22 −10.18

1.988 1.977 1.981 1.986 1.977

−10.28 −10.48 −10.38 −10.58 −10.53

1.986 1.970 1.974 1.989 1.976

−10.35 −10.55 −10.46 −10.62 −10.60

1.991 1.975 1.979 1.990 1.981

−10.42 −10.58 −10.46 −10.65 −10.63

1.988 1.975 1.983 1.987 1.986

a

The unit of Ed is eV.

However, purely theoretical explorations of porphyrins remain rather inadequate because of too many condition limitations.39,40 To investigate the push effects of these distorted zinc porphyrin complexes, we used crystal structure data as a starting point for calculations, which allowed us to directly probe the electronic states of the ground-state molecules, and employed the single-point energy method to extract molecular pictures and orbital energies. The calculated results were used to quantify and compare the origin and role of the push effects in the complexes 1-Zn, 1-Zn-O2, and 1-Zn-Im; complexes 2Zn and 3-Zn with more planar structures than that of 1-Zn were used as references with more planar structure. All calculations were based on crystal structures and implemented in Gaussian 09.22 The single-point energy and molecular energy-level calculations were performed using B3LYP/631G(d)41 and B3LYP/6-311G(d)42 basis sets in the DFT method, respectively. The partial atomic charge assignments were obtained using the pop = NBO keyword, where NBO is the natural bond orbital procedure. The calculation results are presented in Tables 2 and 3 and Figures 4, 5, and 6. To

Figure 5. Schematic representation of the proposed charge transfer model of heme.

3.3.1. Electronic Structures of Metal Centers. The electronic behavior of the current zinc(II) ion in the complexes can be tuned by the ring nonplanarity and axial ligation. The parameters that best reflect this behavior are the energy level (Ed) and charge occupancy (Cd) of each 3d orbital because the changes of Ed and Cd can effectively indicate the potential and direction of charge (or electron) transfer. The Ed and Cd values of the zinc porphyrin complexes are shown in Table 2 and Figure 4. The energy level (Ep) and charge occupancy (Cp) values of the 2p orbitals of coordinated atoms in axial ligands are shown in Table S2 in Supporting Information. As seen in Figure 4a, the changes of the central metal are mainly manifested in two ways: one is the geometric effect caused by the ring nonplanarity (arrow I), and the other is the electronic effect caused by the axial ligation (arrows IIa and IIb). The ring nonplanarity is reflected by the in-plane core contraction. Inspection from 3-Zn to 1-Zn shows that Ed increases as the core size (illustrated by LNNx) shrinks from 4.04 to 3.71 Å. The Ed increase can be safely attributed to the core contraction originating from the geometric differences between the complexes because they have the same chemical environment except for core size. This geometric effect can be

Table 3. Energy Levels of the LUMO (ELUMO) and HOMO (EHOMO) of Porphyrin Rings structure

ELUMO

EHOMO

ΔEMOa

1-Zn-O2 1-Zn-Im 1-Zn 2-Zn 3-Zn

−2.389 −1.841 −2.319 −1.968 −2.207

−4.566 −4.205 −4.569 −4.536 −4.681

2.177 2.364 2.250 2.568 2.574

ΔEMO represents the gap between EHOMO and ELUMO

a

separately show the effects of ring distortion and axial ligation on the central metal and porphyrin rings, the electronic behaviors of metal and rings are discussed individually.

Figure 4. Comparison of d orbitals of complexes in terms of (a) energy level (Ed) and (b) charge occupancies (Cd). Symbols ΔCd1 and ΔCd2 denote the Cd deviation of the dz2 orbital in 1-Zn after binding with Im and O2, respectively. D


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Inorganic Chemistry

Figure 6. Frontier molecular orbitals of porphyrin rings. Values denote the energy levels of the lowest unoccupied (LUMO) or highest occupied (HOMO) molecular orbitals, and the pink arrows represent the out-of-plane deformations of the molecular orbitals; The inserted “S”, “M”, and “W” denote a strong, moderate, and weak distortion, respectively.

requirement for oxygen fixation and activation in heme catalysis. It appears that the horizontal effect first accumulates the potential for the metal, and then the vertical effect reaches the threshold for electron transfer to occur. Also note that because of the unique five-coordinate nature of zinc(II) in porphyrins, it is suitable to independently examine the push role of imidazole or pull role of O2; however, it is unsuitable to examine the synergistic effect originating from these two ligands in the same molecule. This synergy should be present in heme because of the flexible interconversion of iron species between the five- and sixcoordinate forms.49 The single-point energy comparison also provides important information about the abnormal energy level alternation of the complexes (Figure 4a). On the one hand, unlike the orbital splitting between the antibonding d orbitals (dγ) and bonding ones (dε) described by the Jahn−Teller effect,50 the relative Ed between zinc dγ and dε is almost unchanged during the push/ pull processes induced by the geometric and/or electronic effects, but almost either rises or falls simultaneously, which means that the five d orbitals jointly participate in a redistribution of the accumulated charge. When a metal ion is simultaneously subjected to the strong push effects from both horizontal and axial directions, the open-shell coordination environment required by the Jahn−Teller effect does not exist;51 instead, a closed-shell environment is present. The benefits of the common rise or fall of the five d orbitals are obvious; these orbitals together act as a charge memory,52 just like a rechargeable capacitor.53,54 In contrast, an overlap was observed between the dxy and dz2 orbitals in each complex, and Ed of the bonding dxy orbital as well as that of the antibonding dx2−y2 one became higher than those in planar metalloporphyrin because of a strong horizontal compression, which indicates that the push effect in the current zinc complexes mainly

defined as a push effect, which raises Ed by increasing the charge density in the horizontal direction (Figure 5). The axial ligation effect is more complicated than that of the above geometric effect; the two ligands exert opposite electronic effects (Figure 4a). Compared with Ed of 1-Zn, the coordination of imidazole raises Ed of 1-Zn-Im (IIb), whereas O2 visibly lowers Ed of 1-Zn-O2 (IIa). Obviously, the ligation of imidazole affords an additional push effect at the axial position, which is probably similar to the push effect of the proximal imidazole in heme.1 Considering the different origins and directions of the two push effects, we divided the influences of ring nonplanarity and axial ligands into the “horizontal push effect” and “vertical push effect”, respectively. The ligation of imidazole raised the 3d energy further from the increase of Ed induced by ring nonplanarity; conversely, O2 binding with a pull role fully absorbed the energy accumulated by ring nonplanarity. From these results, a CT model considering the oxygen fixation mechanism of heme was proposed (Figure 5). This model can reasonably describe the origin and mutual relationship of the horizontal and vertical push effects. We can reasonably envision that the horizontal and vertical push effects vary during the heme cycle.43 The horizontal effect is responsible for charge accumulation in the metal in the oxygen fixation stage. In this stage, the metal only needs to accumulate the feedback charge to satisfy the formation of MO2 component, as supported by plenty of M-O2 complexes with ring distortion, such as M = Mn,44 Fe,45 Co,46 and Zn (this work).16 The vertical effect is responsible for the potential electron transfer in the oxygen activation stage through a trans effect.47,48 As seen Figure 4b, Cd of the axial dz2 orbitals shows a different trend; specifically, the coordination of imidazole causes a slight increase of Cd (ΔCd1), while that of O2 lowers Cd (ΔCd2). This trend indicates that imidazolyl ligation makes a unique contribution to axial metal-to-ligand CT. In brief, the horizontal and vertical push effects together meet the charge E


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Inorganic Chemistry

Figure 7. Comparison of the (a) LUMO (ELUMO) and HOMO (EHOMO), and (b) LUMO−HOMO gap (ΔEMO) of zinc porphyrin complexes.

in porphyrins. In general, both ring nonplanarity16,68 and axial ligation69 cause red shifts of absorption spectra because they increase the energy of the molecular ground state of metalloporphyrins. Therefore, the strength of the push (or pull) effect raising (or lowering) the energy of the molecular ground state by increasing (or decreasing) the d orbital energy level can be roughly quantified according to the magnitude of the red shift. The absorption spectra of the three complexes of 1 are shown in Figure 8, along with that of 3-Zn as a reference planar zinc porphyrin.

depends on that in the horizontal direction, which is induced by nonplanarity.55 3.3.2. Electronic Structures of Porphyrin Rings. The electronic structures of porphyrin rings are also affected by the ring geometry and axial ligation, which have rarely been considered in previous reports.56,57 In catalytic processes involving heme-containing enzymes,58 a putative oxidant is usually thought to be an iron(IV)-oxo porphyrin radical cation termed Compound I.59 The stability and activity of the radical delocalized in the π-system are closely related to the electronic structures of the rings.60 Schematics of the molecular orbitals and a comparison of orbital energy levels are provided in Figure 6 and Table 3, respectively. The effects of ring geometry and axial ligation on the complexes are mainly reflected by three characteristics. (i) The molecular orbitals are visibly deformed as the degree of distortion increases from 3-Zn to 1-Zn, as shown by the pink arrows in Figure 6; these deformations change the conjugation of porphyrin rings, which can result in a switch of the highest occupied molecular orbital (HOMO) from a2u to a1u in the πring (Figure 7a).61,62 The a1u state is at a lower energy than a2u, which makes it advantageous for stabilizing radicals like Compound I. A radical signal of the 1−Zn-O2 complex was also observed (see Supporting Information Figure S5), which should be a zinc porphyrin π radical cation.63 (ii) The axial electronic effect can transfer to the porphyrin ring mediated by the central metal. Specifically, the changes of HOMO and lowest unoccupied molecular orbital (LUMO) can be judged according to the push or pull effect of the axial ligand (Figure 7a). For example, the binding of imidazole increases the HOMO of 1-Zn by about 0.3 eV (ΔEHOMO1), while that of O2 slightly lowers it (ΔEHOMO2). This point is of great interest to understand the electron transfer of heme radicals,64 the unidirectionality of heme ring current,65 and the role of proximal His ligands in heme performance.1,6 (iii) The ring distortion and axial pull effect can narrow the HOMO−LUMO gap (ΔEMO), as manifested by the decreases of ΔEMO from 2.57 eV for 3-Zn to 2.25 eV for 1-Zn and from 2.25 eV for 1Zn to 2.18 eV for 1−Zn-O2 (Figure 7b). It is thought that the orbital deformation induced by ring nonplanarity can enhance the electronic polarization, thus delocalizing the electronic distribution and decreasing ΔEMO.66,67 In summary, as the important components of heme, the changes in the electronic structure of the π-ring are indispensable for the performance of heme even though the changes of the metal ion are the most critical factor. 3.4. Comparison of Absorption Spectra. The bathochromic shift of absorption spectra is a simple but effective way to evaluate the role and contribution of push or pull effects

Figure 8. Absorption spectra of zinc(II) porphyrin complexes. The concentrations of 1-Zn, 1-Zn-O2, 1-Zn-Im, and 3-Zn were 2−4 × 10−5 M in CHCl3 at 293 K. Inset is a magnified view of the Q bands and a list of the absorption maxima (λmax). Spectral red shifts are labeled as Δλ1 (3-Zn to 1-Zn), Δλ2 (1-Zn to 1-Zn-Im), and Δλ3 (1Zn to 1−Zn-O2); their values are indicated in the figure.

Figure 8 shows three spectral red shifts, labeled as Δλ1 (3Zn to 1-Zn), Δλ2 (1-Zn to 1-Zn-Im), and Δλ3 (1-Zn to 1-ZnO2), which correspond to the horizontal and vertical push effects and the pull effect described above, respectively. First, stronger distortion typically results in a higher ground-state energy level, which agrees with previous reports.16 As illustrated by Δλ1, the red shift of 20.5 nm from 3-Zn to 1Zn is equivalent to an increase of the molecular energy level (ΔE) of 12.7 kJ/mol, which is completely dependent on the geometric effect responsible for the horizontal push effect. Such a red shift further proves that the geometric effect is indeed an electron-donating push effect on the central zinc ion. Second, axial ligation also leads to the increase of ΔE of the metalloporphyrins, which partly depends on the strength of the coordination.70 The coordination of imidazole generally causes F


Article

Inorganic Chemistry a red shift of ∼9 nm (ΔE = 6.0 kJ/mol) for regular zinc porphyrin.71 For 1-Zn, imidazole coordination caused a red shift of 17.8 nm (Δλ2) equivalent to an increase of ΔE of 10.1 kJ/mol. It was also found that this shift amplitude was little affected by the type and bonding strength of ligands; Δλ was 18.5 nm for pyridine, 20.7 nm for aniline, and 15.0 nm for 5bromopyrimidine (see the Supporting Information Figure S1) Therefore, compared to the bathochromic shift in the more planar Zn-Im porphyrin systems, this additional bathochromic shift induced by axial ligation is completely dependent on the electronic effect producing the vertical push effect. Such a shift also indicates that the electronic effect of imidazole is electrondonating. The reported M-Im components show that bond length of M-N (Im) varies in the range of 1.99−2.18 Å, which indicates that the charge feedback in 1-Zn-Im is very weak from the Zn to Im (see the Supporting Information Figure S5). Third, O2 binding caused a red shift of just 2.2 nm (Δλ3; ΔE = 1.3 kJ/mol), which is anomalous considering the geometric and electronic effects described above. It is well-known that the formation of an M-O2 complex benefits from the presence of effective charge feedback from M to O2 as well as weak σcoordination from O2 to M.72 Therefore, this small red shift is the result of a charge balance between π-feedback and σcoordination, and the π-feedback plays a strong pull role. Therefore, the trend observed in the absorption spectra is consistent with that obtained by the calculations. Experiments involving ligand exchange to determine the axial affinity of the 1-Zn complex were carried out,73 and titrations to measure the ligand exchange and affinity were performed as previously described.70 Stock solutions of ∼40 μM 1-Zn-O2 or 1-Zn in chloroform were freshly prepared, and the binding titrations were performed at 298 K with stirring. For each concentration, ligand was added to both the sample and reference cells and stirred for about 30 s before difference spectra were recorded. Axial binding was quantified based on a differential absorption peak at 452 nm for 1-Zn-O2 and 450 nm for 1-Zn. The change in absorption (ΔA) was plotted against zinc porphyrin concentration to determine the association constant (ka) using nonlinear fitting treatment, as shown in Figure 9. The titration results show that the ligand exchange of imidazole with O2 in 1-Zn-O2 can occur, as manifested by the appearance of a peak at 568 nm and the clear isosbestic point in Figure 9. This suggests that the oxygen

dissociation of heme is possibly related to the ligation of heme proximal ligands.1−3 Interestingly, the ligand exchange titration using 1-Zn-O2 was very similar to direct binding of imidazole to 1-Zn, as supported by the same ka value of 1.8 × 104 M−1. Note that O2-binding affinity of 1-Zn could not be determined under the current titration conditions.70,74 Additionally, stability tests of the 1-Zn-O2 complexes were also performed using different N-containing ligands, acetic acid, and neutral conditions (see the Supporting Information Figures S1−S2). The results showed that the Zn−O 2 component is stable under acidic conditions, which is consistent with its synthesis conditions. The O2 ligand slowly dissociated under neutral conditions and was quickly replaced by N-containing organic ligands such as pyridine, aniline, and substituted pyrimidine.

4. CONCLUSIONS The horizontal push effect was identified by comparing the molecular geometries, electronic structures, and spectral changes of three complexes of a highly saddled zinc porphyrin. The origin and role of the horizontal push effect and its relationship to vertical push/pull effects were discussed. A CT model was established to explain the CT relationships between the push and pull effects. This study not only revealed that the electronic behavior of metalloporphyrins is driven by these geometric and electronic effects but also affords new insight into the oxygen carrier mechanism in heme.

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ASSOCIATED CONTENT

* Supporting Information S

The Supporting Information is available free of charge on the ACS Publications website at DOI: 10.1021/acs.inorgchem.8b03219. Additional results, stability tests of the 1-Zn-O2 complex, computational results, mass spectral and NMR characterization (PDF) Accession Codes

CCDC 1878277−1878278 contain the supplementary crystallographic data for this paper. These data can be obtained free of charge via www.ccdc.cam.ac.uk/data_request/cif, or by emailing [email protected], or by contacting The Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge CB2 1EZ, UK; fax: +44 1223 336033.

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AUTHOR INFORMATION

Corresponding Authors

*E-mail: [email protected] (Z.Z.). *E-mail: [email protected] (Q.L.). ORCID

Zaichun Zhou: 0000-0003-2075-8241 Notes

The authors declare no competing financial interest.

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ACKNOWLEDGMENTS

This study was supported by the National Natural Science Foundation of China (No. 21602054) and China Scholarship Council (201708430033, 201709480009) is also acknowledged.

Figure 9. Titration of imidazole binding to zinc(II) porphyrin 1-ZnO2. Inset is a plot of the changes of absorption maxima against concentration and the association constant (ka) determined based on these titrations. G


Article

Inorganic Chemistry

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