Redox Potentials and Electronic States of Iron Porphyrin IX Adsorbed

Mar 6, 2018 - Jason A. BennettDaniel P. MillerScott M. SimpsonMarcela RodriguezEva Zurek. Langmuir 2018 34 (38), 11335-11346. Abstract | Full Text ...
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Redox Potentials and Electronic States of Iron Porphyrin IX Adsorbed on Single Crystal Gold Electrode Surfaces ling zhang, Kasper P. Kepp, Jens Ulstrup, and Jingdong Zhang Langmuir, Just Accepted Manuscript • DOI: 10.1021/acs.langmuir.8b00163 • Publication Date (Web): 06 Mar 2018 Downloaded from http://pubs.acs.org on March 7, 2018

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Redox Potentials and Electronic States of Iron Porphyrin IX Adsorbed on Single Crystal Gold Electrode Surfaces Ling Zhang, Kasper P. Kepp, Jens Ulstrup*, Jingdong Zhang* Department of Chemistry, Technical University of Denmark, Building 207, Kemitorvet, DK−2800 Kgs. Lyngby, Denmark. ABSTRACT: Metalloporphyrins are active sites in metalloproteins and synthetic catalysts. They have also been studied extensively by electrochemistry as well as being prominent targets in electrochemical scanning tunneling microscopy (STM). Previous studies of FePPIX adsorbed on graphite and alkylthiol modified Au electrodes showed a pair of reversible Fe(III/II)PPIX peaks at about -0.41 V (vs. NHE) at high solution pH. We recently used iron protoporphyrin IX (FePPIX) as an intercalating probe for long-range electrochemical electron transfer through a G-quadruplex oligonucleotide (DNAzyme); this study disclosed two, rather than a single pair of voltammetric peaks with a new and dominating peak, shifted 200 mV positive relative to the ≈ -0.4 V peak. Prompted by this unexpected observation, we report here a study of the voltammetry of FePPIX itself on single-crystal Au(111), (100), and (110) and poly-crystal Au electrode surfaces. In all cases the dominating pair of new Fe(III/II)PPIX redox peaks, shifted positively by more than 200 mV compared to those of previous studies appeared. This observation is supported by density functional theory (DFT) which show that strong dispersion forces in the FePPIX/Au electronic interaction drive the midpoint potential towards positive values. The FePPIX spin states depend on interaction with the Au(111) interface, converting all the Fe(II)/(III)PPIX species into low-spin states. These results support electrochemical evidence for the nature of the electronic coupling between FePPIX and Ausurfaces, and the electronic states of adsorbate molecules, with a bearing also on recent reports of magnetic FePPIX/Au(111) interactions in ultra-high vacuum (UHV). 1. Introduction Metalloporphyrins are the active sites of a broad range of hemoproteins including cytochromes, hemoglobin and myoglobin, and enzymes, involved in electron transfer (ET), oxygen storage and transport, and biochemical catalysis.1-4 Modifications of porphyrin axial ligands and side groups also enable mapping the catalysis of a variety of oxidative processes of hydrocarbons and sulfides.5-7 The unique electronic properties of the metalloporphyrins, rooted in subtle ligand field control between low- (LS) and high-spin (HS) states, have inspired development of artificial enzymes, as well as electrocatalysts via л-л electron conjugation or intercalation.1,8,9 Surface assembly of metalloporphyrins has, further been reported extensively using electrochemistry and electrochemical scanning tunneling microscopy (in situ STM) on single−crystal gold, copper, and highly oriented pyrolytic graphite (HOPG) surfaces.10-12 The midpoint potential (E1/2) of metalloproteins is a “ruler” of protein ET thermodynamics.13-15 The local environments and axial coordination of metalloporphyrins thus affect strongly E1/2.16,17 Axial ligand fields also promote transitions between LS and HS states.18,19 Electron paramagnetic resonance spectroscopy shows for example that LS has a higher redox potential than HS heme b cytochrome in the bacterial terminal oxidase cyt cbb3.20 Axial ligation and spin states are therefore crucial in heme ET thermodynamics.

Gold surfaces and gold nanomaterials are widely used in electrochemistry, fuel cells, biosensors, and drug transport.21,22 The Au-surfaces affect the electronic properties of adsorbed molecules and biomolecules. Such interactions have been mapped in detail for Au-S surface linked molecules and biomolecules23-28 and apply broadly.29 Studies that directly compare different surfaces using voltammetry combined with in situ single−molecule structural mapping and computational support seem, however, needed to obtain a coherent view of the complex metalloporphyrin adsorption on metallic surfaces.10,12 We have recently reported voltammetry/in situ STM of the heme group stacked onto a 12-guanine DNA quadruplex (DNAzyme) immobilized on Au(111) via a thiol linker9. The voltammetry was unusual, first with high conductivity through the quadruplex and secondly, with two rather than a single voltammetric signal as otherwise broadly known. In an attempt to explore this phenomenon further and to map the electronic structures of directly adsorbed iron protoporphyrin IX (FePPIX) we report here a voltammetric study of FePPIX using all the three low-index Au(111), Au(100), and Au(110) single−crystal electrodes. Atomically planar electrodes ensure highest possible voltammetric resolution. Carbon electrodes such as basal plane (BPG) and edge plane graphite (EPG), and glassy carbon (GC) are employed as a comparison. The data disclose more subtle voltammetry than hitherto reported, also with

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Figure 1. CVs of Au(111) (A) and BPG (C) electrodes in 10 µM FePPIX solution. 5 mM NaClO4, pH 11.7. Scan rates, 0.2, 0.3, 0.4, 0.5, -1 0.7, and 1.0 V s . Anodic and cathodic peak current densities (j) versus scan rates of FePPIX on Au(111) (B) and BPG (D) elec-1 trodes. (E) CVs of FePPIX on Au(111) at different pH. Scan rates, 0.4 V s . (F) Plots of E1/2 vs. pH for the two pairs of redox peaks.

two local structure dependent voltammetry peaks instead of only a single pair as in many previous reports.8,30-32 Density Functional Theory (DFT) calculations indicate further that the difference is caused by strong dispersion forces between FePPIX and the Au surfaces driving the Fe(III/II)PPIX half potential to higher values. Particularly the FePPIX/Au interaction transfers FePPIX spin onto the Au-surface. This resembles what could be denoted as magnetic electrochemical Kondo features as in recent observations for FePPIX and related molecules on Au(111) and ferromagnetic surfaces at low temperatures in ultrahigh vacuum (UHV).33-35 Other implications of the study are i) that the specific surface binding of the complex target molecule such as FePPIX crucially controls the voltammetric patterns. This applies both to direct target molecular adsorption and perhaps also to intercalation of target molecules and long-range ET triggering as in DNAzymes9; ii) dispersioncorrected hybrid DFT can offer important insight and data rationalization regarding spin changes and electrochemical potential shifts as noted below. 2. Results 2.1 Midpoint potentials of FePPIX adsorbed on Au(111)− and BPG electrode surfaces FePPIX adsorbs on single−crystal gold surfaces from basic solution, pH 11.7, where both the pendant propionate groups and axial water ligands are fully deprotonated. FePPIX adsorbed on Au(111) showed consistently two pairs of voltammetric peaks in the potential range -0.7 to 0.1 V (vs. NHE), Figure 1A. The dominating pair appears at

-0.193 ± 0.007 V (the “high−potential peaks”, or Potential 1) with small peak separation (< 22 mV) and a half−width of 90~120 mV at scan rates v = 0.2−1.0 V s-1 (Table S1), indicative of reversible one−ET.36 The anodic and cathodic peak currents depend linearly on v (Figure 1B), also reflecting FePPIX adsorption. The second, “low−potential pair” or Potential 2 with only about a tenth of the peak currents of Potential 1 is observed at -0.425 ± 0.009 V, also with peak separation about 23 mV and half−widths 80~100 mV at 0.2−1.0 V s-1 (Table S1). As a comparison, FePPIX adsorbed on basal−plane pyrolytic graphite (BPG) surfaces exhibits only a single pair of well-defined peaks at -0.386 ± 0.006 V, close to Potential 2 on Au(111) (Figure 1C and D). The half−widths are 90~140 mV (0.2−1.0 V s-1), again according with confined one−ET processes (Table S2) and with reported E1/2 values ≈ -0.40 V (pH 11.7, Table S3).8,30-32,37 The new “highpotential” peaks at -0.193 V are attributed to coupling and possibly magnetic interactions of FePPIX with Au(111) surface atoms, Sections 2.5 and 3. This is different from FePPIX п−stacking on the BPG surface and reflects different electronic states of high-potential FePPIX on Au(111) compared with low-potential FePPIX on Au(111) and BPG. 2.2 Nernstian pH−dependence on Au(111) The one−ET half-reaction potential of Fe(III/II)PPIX depends on pH as the axial OH2 ligand(s) are deprotonated at pH > 7. The pendant propionic acid groups are fully ionized in this whole pH-range. FePPIX was brought to adsorb onto Au(111) at pH 11.7, and the FePPIX modified 2

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Au(111)−electrodes tested in blank solutions at variable

pH.

Figure 2. (A) CVs of FePPIX on Au(100), Au(110), and Au(poly) electrodes in 10 µM FePPIX, 5 mM NaClO4, pH 11.7 . Scan rates, −1 1.0 V s . (B) 3-dimensional model of Au-atom organization in a face-centered cubic lattice, exposing (111), (100), and (110) facets. (C) Total coverages of electroactive FePPIX adsorbed on different Au electrode surfaces (black lines) and the ratio between Potential 2 and 1 coverages (red line). (D) Possible configuration of FePPIX adsorbed on atomically planar (a) and rough edge sites (b) of single crystal Au surfaces. (E) In situ STM image of (oxidized) FePPIX monolayer on Au(111) surface with large terraces. 0.01 M sodium hydroxide solution, pH 11.7. Sample potential, 0.2 V (vs. NHE). Tip potential, 0.36 V. Tunneling current, 0.04 nA.

Table 1. E1/2and Electroactive Coverages of FePPIX Adsorbed on the Different Electrodes. 5 mM NaClO4, pH 11.7. Electrodes

High−potential Au(111)

−2

E1/2, V vs. NHE −0.193 ± 0.007

Г, mol cm , and Ratio to Full Monolayer*

Low−potential −0.425 ± 0.009

High−potential

Low−potential

-11

5.1(± 1.5) × 10 , 3.0%

-11

-12

2.7(± 1.7) × 10 , 1.5%

-11

5.5(± 1.5) × 10 , 3.0%

3.7(± 0.6) × 10 , 20%

-12

Au(100)

−0.197 ± 0.004

−0.433 ± 0.010

4.0(± 0.6) × 10 , 25%

Au(110)

−0.035 ± 0.004

−0.430 ± 0.004

2.7(± 0.5) × 10 , 15%

Au(poly)

−0.146 ± 0.021

−0.427 ± 0.012

1.3(±0.2) × 10 , 7.6%

8.7(±0.2) × 10 , 5.1%

BPG

−

−0.386 ± 0.006

−

1.8(±0.8) × 10 , 100%

-12

-11

-12

-12

-12

EPG

−

−0.386 ± 0.007

−

2.0(±0.5) ×10 , 100%

GC

−

−0.401 ± 0.024

−

1.3(± 0.2) ×10 , 80%

-10

*Theoretical dense monolayer, 1.7 × 10

-2

-10

2

mol cm assuming closest packing of 1.0 × 1.0 nm FePPIX molecules.

Both high− and low−potential Au(111) FePPIX peaks are shifted positively when pH is decreased from 11.7 to 8.0 (Figure 1E and F). The slopes of the E1/2−pH correlations, −0.062 and −0.068 V/pH for Potential 1 and 2 accord roughly with −0.059 V/pH for a coupled single-electron, single−proton transfer process,

Fe(III)PPIX(OH−) + e- + H+Fe(II)PPIX + H2O.30 2.3 Surface structural effects on the FePPIX redox peaks The new voltammetric properties of FePPIX induced by interactions with Au(111)-surfaces were consolidated by FePPIX voltammetry at Au(110) and (100) electrodes which gives a pattern resembling that of Au(111), i.e. two pairs of reversible peaks (Figure 1A and 2A) with a domi3

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nating high-potential peak. The linear peak current versus scan rate again reflects adsorbed FePPIX (Figure S1). The high−potential E1/2 on Au(100) (-0.197 ± 0.004 V) is about the same as for Au(111) but 200 mV higher (− 0.035 ± 0.004 V) for Au(110), giving a 400 mV peak separation between the high− and low−potential pairs instead of 200 mV as for Au(111) and Au(100), Table 1. The similar redox behavior of FePPIX adsorbed on Au(100) and Au(111), (Table 1 and S4) is paralleled by the close-packed planar and regular surface atomic structures and largely similar packing FePPIX modes on both these surfaces. Au(110) and Au(poly) surfaces are much rougher and complex, and structurally less compatible with the planar FPPIX structure. FePPIX interaction with gold atoms is therefore weaker, and broader high-potential peaks and notable peak potential shifts compared with Au(111) and Au(100) can therefore be expected, as also observed. The observed high-potential peak widths on Au(110) are close to 200 mV for 1 Vs-1 (Figure 2A and Table S4), which as noted reflects a distribution of configurations of FePPIX on multiple adsorption sites. These could involve both “loose” and firmer attachment on the more open and complex, “missing row” Au(110) surface compared with Au(111) and Au(100) (Figure 2B).38,39 The similar high-potential FePPIX peak on polycrystalline Au, poly(Au) as for Au(110) supports this view (Figure 2A and Table S4). In contrast to the high-potential peaks, E1/2 and peak widths of the low-potential FePPIX peaks are independent of the Au-surface structure. The low-potential peak is assigned to interfacial ET of “loosely” bound FePPIX where the FePPIX molecules are in less direct contact with the electrode surfaces. The low-potential peak potential is therefore less sensitive to the surface structure of the Au-electrode surfaces. The coverage ratio of the low- to high-potential peak, however, increases significantly on the rough Au(poly) surface, and the total FePPIX coverages decrease as Au(111) ≈ Au(100) > Au(110) > Au(poly) (Figure 2C and Table 1). This indicates that the electronic states of FePPIX are sensitive to the adsorption sites (Figure 2D and E). We attribute the high-potential peaks to FePPIX adsorbed parallel to the planar terraces on the Au electrode surfaces with close packing (Figure 2D, panel a). The low-potential peaks could then be associated with FePPIX adsorption on terrace edge sites with the porphyrins pointing away from the Au surface and therefore keeping roughly the same electronic states as the free molecules. The same behavior as for free FePPIX also dominates at EPG and GC with amorphous surfaces (Figure S2, Table 1, S2 and S5), giving E1/2 close to that of the low-potential FePPIX peaks on Au and of FePPIX on graphite8,30,31 and on alkylthiol modified Au electrodes32. This suggests that л-л stacking on the carbon surfaces does not affect the electronic states of FePPIX (Table S3).40,41 These results confirm the surface-sensitivity of the

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FePPIX electronic states on Au surfaces, and reflect strong dispersion that also affects magnetic behavior, cf. Section 4 and drives E1/2 positively by at least 200 mV. 2.4 Interfacial electrochemical ET rate constants The cathodic and anodic peak potentials of both Potential 1 and 2 separate at scan rates > 1 V s-1. The interfacial ET rate constants could be calculated by the Laviron formalism42 (Figure S3), Table 2. The rate constants at the different electrode surfaces vary only two-to-five fold. If this variation is ascribed solely to activation energy differences, these amount to only 1.5~4 kJ mol-1. Such small differences are notable but cannot be modeled by DFT. Table 2. Standard Electrochemical Rate Constants, ks(s−1) of Fe(III/II)PPIX Adsorbed on Single−Crystal Au, Au(poly), BPG, EPG, and GC Electrodes at pH 11.7. −1

Electrodes

ks, s High−potential

Low−potential

Au(111)

110 ± 30

300 ± 30

Au(100)

110 ± 20

220 ± 40

Au(110)

160 ± 50

250 ± 10

Au(poly)

120 ± 20

120 ± 10

BPG

−

130 ± 10

EPG

−

55 ± 2

GCE

−

30 ± 9

2.5 DFT computations on free and adsorbed FePPIX Voltammetry and in situ STM do not directly disclose ligand and spin states of adsorbed FePPIX. To understand further carbon and gold electrochemistry of FePPIX, we analysed the electronic structures of free and adsorbed FePPIX species by DFT. 2.5.1 Dispersion forces and FePPIX spin states Dispersion, spin states, and zero point energies of FePPIX in free and adsorbed states were computed to analyze the electronic coupling between FePPIX and the electrode surfaces.43 D3 dispersion terms were included for all atoms in such a way that both the Au-heme dispersion interactions of the adsorbed state and the dispersion in Au-Au self-interactions that may affect gold’s perturbation of the redox potential of heme were accounted for. The surfaces were represented by a layer of 13 Au atoms with approximate (111)−structure and an aromatic layer of 28 C-atoms saturated at the periphery with hydrogen atoms. These models incorporate neither excess Ausurface charges44 nor functional groups on the C-surfaces, but enable studying local effects that mostly affect the heme redox potential, with dispersion and vibrational entropy included. This is not possible with larger surface models. Five- (OH−), and six-coordinate (*H2O)(OH−), (H2O)(*OH−), and (*OH−)(OH−) axial FePPIX ligations 4

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(*proximal from the electrode surface) were considered. Figure 3 shows some optimized structures.

version. However, secondary gold-gold interactions will modulate the gold-heme dispersion interaction. Using larger models still with the full heme system is beyond our resources, but we expect that they could affect the magnitude of the shifts observed by perhaps 50 %. Dispersion (van der Waals interactions not included in standard DFT) is the origin of the electronic couplings of Fe, C, N, O, H atoms to the surfaces and therefore of E½. п-п conjugation dominates interactions between FePPIX and basal-plane graphite, but couplings to Au include the full Au valence 5d and 4d shells along with Fe(III) 3d electrons. Dispersion is thus significantly stronger than on C-surfaces (Table S6-9). Table 3. DFT Free Energy Separations between HS and LS Free and Adsorbed Fe(III/II)PPIX, ∆E(HS-LS) (KJ mol−1). (Positive values mean LS states are favored). −1

∆E(HS-LS), KJ mol Va− − lence (*OH2) (*OH ) (*OH ) − (OH ) − − states (OH ) (OH2) (OH ) (III) 3 82 45 45 Free (II) -30 40 -19 -19 (III) 37 106 74 31 BPG (II) -34 -4 27 -3 Au (III) 17 54 34 51 (111) (II) 130 56 104 48 *Proximal axial ligand to the Au(111) or graphite surface.

Mod els

Figure 3. Proposed molecular LS states of free − − −Fe(III)(OH )(OH2) (A), −Fe(III)(OH ) on 28-atom C-surface (B), −Fe(III)(OH on 13-atom Au(111)-surface (C).

Since we were specifically interested in accurate spin states and redox states of the heme under the local influence of gold surface atoms, we required an accurate hybrid density functional (TPSSh; B3LYP* with 15% HF exchange could also have been used, cf.55). Since the physical effects (redox shift and spin state change) are local and depend strongly on details of the electronic structure and dispersion effects near iron, we needed to model a full heme system using a hybrid functional (TPSSh), zeropoint energies, dispersion, and free energy corrections, together with a large polarized basis sets to make these energetics accurate. TPSSh is one of very few functionals (consistently of the hybrid type) that can accurately model the energy difference between HS and LS and redox states in iron systems43,52. This would not be the case with a surface model, which is suitable for smaller molecule interactions and use smaller basis sets, GGA functionals, empirical scaling relations, or other assumptions to reach semiquantitative results. GGA functionals tend to artificially favor the LS state by typically 30-60 kJ/mol43,52. The shifts in potentials and spin states are dominated by the effects near the heme iron center, which is where the electronic structure changes during spin and redox con-

HS and LS FePPIX with the four ligations were combined with the Au(111)− and C−surface models, altogether 60 models, and structure optimized at the BP86/def2-SVP level45 including the Cosmo solvation model46 with static dielectric constant 80.47 Vertical ionization energies and electron affinities were computed for each ground state to obtain reorganization energies48-50, Section 2.5.4. The relative standard half-reduction potentials were calculated from fully relaxed geometries of both oxidation states. Vibrational frequency calculations of the thermochemical state functions were also incorporated, Tables S6-S9. 2.5.2 Spin states and spin interconversion of free heme Based on the computed HS and LS energies, we estimated the preferred FePPIX spin state in the different ligand and surface environments (Table 3). Electronic energies were computed using triple-zeta polarized basis sets with the meta hybrid functional of Tao, Perdew, Staroverov, and Scuseria (TPSSh),51 known to provide accurate spin state gaps for iron complexes.43,52,53 Dispersion changes the relative spin state energies by up to 29 KJ/mol (most for the 13-gold atom model with adsorbed −Fe(*OH-)(OH2)). Dispersion between Au- or C-surface atoms and FePPIX C, N, O, H, and Fe atoms are therefore crucial. This follows observations for Au-S surfaces.23,24 The HS/LS free energy separations of adsorbed FePPIX with the four ligations, ∆E(HS−LS) (KJ mol−1) are given in Tables S6−S9.53 ∆E(HS−LS) depends on the ligations and the 5

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interfaces, Table 3. Free Fe(III)(OH-) is close to spin crossover (∆E(HS−LS), ~3 KJ mol−1), while Fe(II)(OH-) favors high−spin by 30 KJ mol−1. When a second axial −OH2 ligand is bound, Fe(III) is entirely LS, while Fe(II) remains HS. With a second –OH- ligand bound, Fe(II) is converted to LS, consistent with a stronger ligand field. FePPIX thus crosses from LS to HS when Fe(III) is reduced to Fe(II) with the −(OH−) and −(OH-)(OH2) ligands, while the −(OH−)(OH-) spin state remains LS. Overall these observations accord with reported studies.19,43 2.5.3 FePPIX spin states on Au− and C−surface The HS/LS energy separation is significantly altered on interaction with the Au(111) surface due to strong dispersion forces. Coplanar FePPIX adsorption dominates. All Fe(III)PPIX species remain LS after adsorption, consistent with Fe(III) having tighter metal−ligand bonds and stronger ligand field than Fe(II).54,55 Interaction of FePPIX with Au atoms, however, turns all Fe(II) species into LS, in contrast to free and C-bound Fe(II)PPIX HS states. The C-lattice effects are small, and −Fe(II)(OH-) thus remains HS. −Fe(II)(*OH-)(OH-) and (*OH2)(OH-) are close to spin crossover also in the C-adsorbed state, with HS favored. Only −Fe(II)(*OH-)(OH2) is turned into LS. As indicated from low coverage and in situ STM, FePPIX adsorbs weakly on gold. The shift to the LS state on adsorption is therefore unexpected, but would explain why high−potential peaks appear for gold, but not for carbon. 2.5.4 DFT inner-sphere reorganization energies and E1/2 The reorganization energies are fairly similar for all the 6-coordinate models within each type of coordination, varying by 10-20 KJ/mol. The dihydroxo models exhibits the smallest reorganization energies, within the uncertainty of the method similar to those of the free heme, implying similar ET rates at this level of theory. However, a size effect is seen for the 6-coordinate systems probably due to the artifact of including more outer-sphere reorganization of the surface models. This affects more directly 5-coordinate heme with an open coordinate site to the redox active iron center. The Gibbs free energy change including ZPE and vibrational entropies, and E1/2 were computed using the assigned spin state energies, and the reorganization energy. The values for all the free and adsorbed FePPIX species are given in Table S7-S9 and in Table 4 The Gibbs free energy of HS −Fe(II)(OH-) and Fe(II)(*OH-)(OH2) is favored by up to 16 and 19 KJ/mol, respectively compared to the HS Fe(III) counterparts, (Table S11). This is due to the longer and weaker metal−ligand bonds of Fe(II), favoring larger vibrational entropy and lower ZPE. The absolute potentials are not meaningful due to the missing long−range components, but the potential shifts can be estimated by cancellation of this component. The calculated E½ values for the dominating species, −Fe(OH-)

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and Fe(*OH-)(OH-), reproduce the experimental observations in important respects. E1/2 of FePPIX on BPG is close to that of free FePPIX. A second –OH- ligand induces as expected a large negative potential shift (-1.04 V to -2.41 V). Secondly, the half-potentials of all FePPIX species on Au(111) are shifted significantly towards positive values compared to BPG as observed. Dispersion and innersphere reorganization are here the major driving factors. Table 4. DFT Computed Redox Potentials (E1/2, V) of Fe(III/II)PPIX with Different Ligands. E1/2, V vs. SHE -

−Fe (OH ) -

Carbon

Au 13−atom

−1.04

−1.09

−0.81

−2.41

−2.31

−1.10

−1.25

−1.83

−0.66

−1.25

−1.55

−0.19

-

−Fe(*OH )(OH ) -

−Fe(*OH2)(OH ) -

Free

−Fe(*OH )(OH2)

*The axial ligand proximal to the surface. Adsorbed FePPIX on carbon maintains only a distal −(OH-) ligand because of the strong л−л coupling,56 and a computed E1/2 of -1.09 V. The high−potential FePPIX species on Au(111) is most likely five−coordinate, −Fe(OH-) or six−coordinate −Fe(*OH2)(OH-) with computed E1/2 values of −0.81 and −0.66 V. Within computational uncertainty these shifts vs. free or C-bound five-coordinate FePPIX (−1.04, −1.09 V) of 0.23−0.43 V accord with the data. The shifts are much larger for all other FePPIX species. The low-potential peaks on Au(111) can then be attributed to residual, “loosely” adsorbed FePPIX on edge sites of the single-crystal Au surfaces, keeping electronic states that resemble those of free FePPIX (Table 4). As an accompanying note, both coordinated water ligands may not be deprotonated at high pH. We studied the possibilities that either a single or both water ligands are deprotonated, but the doubly deprotonated system does not concur with the data, probably because pKa of the second water is too high (> 11). As a second observation, it can be noted that OH- is slightly below water in the spectrochemical series. This series is, however, a series of ligand field parameters estimated from absorption maxima of coordination complexes with different ligands. For ligands close in the series this is not reliable, because real spin state preferences as of interest here (not spectroscopy) also depend on thermal vibrational and entropy corrections that favor the HS state but do so differently for different ligands. The impact of the spin pairing energy is not in the series either. As the two ligands are close in the series, we cannot expect the ∆0 effect not to be overruled by vibrational and entropy corrections, which will favor the longer bonds in water and the HS state. The effect in the standard series is thus subtle and not accu-

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rate enough for our purpose. The energies in Table 3 are free energies corrected for these effects. 3. Concluding remarks Monolayer voltammetry and electrochemical STM of FePPIX on carbon electrodes have been broadly studied.11,31 A single voltammetric peak corresponding to a single-PCET (proton coupled electron transfer) process is the most conspicuous feature.30,57 At pH 11-12 as mostly in the present work E1/2 ≈ -0.4 V vs. NHE. Little attention has, however, been given previously to electron spin or axial ligand changes in the electrochemical ET processes. In the present study FePPIX voltammetry on singlecrystal Au-electrodes was found to display a more complex pattern. We have addressed FePPIX voltammetry on all the three low−index single−crystal surfaces, Au(111), Au(100), and Au(110) as well as on polycrystalline Auelectrode surfaces. Two reversible voltammetric peaks were observed in all cases. The “low-potential peak” accords with the potential on carbon electrodes, i.e. E1/2 ≈ 0.4 V (NHE) at pH 11-12, but the physical nature of this peak on carbon and gold electrodes is different. A second and dominating “high-potential peak” is observed at a 200-400 mV higher potential and is not observed for carbon electrodes. The ratio between the high− and low−potential peak areas is lower the “rougher” the surface, i.e. ≈ 6 for Au(111) ≈ 17 for Au(100), but 5 for Au(110) and only 1.5 for Au(poly). The strikingly different FePPIX behavior on gold and carbon electrodes was explored further by DFT with focus on electronic interactions of different FePPIX spin and ligation species with two-dimensional assemblies of Au− and C−atoms. The objective was to identify the prevailing LS or HS states and six- or five-coordinate FePPIX species, and to illuminate the nature of the electronic interactions with the surfaces. The computations offer a rationale for the voltammetric behavior. All the free FePPIX species were HS Fe(II) and LS Fe(III). An exception is six−coordinated Fe(OH-)(OH-) which is LS in both oxidation states. Structure optimized FePPIX interaction with the Au(111) surface converts all the species to LS state. In contrast, LS Fe(III) and HS Fe(II) are largely retained on interaction with the carbon lattice. This difference is caused by strong dispersion forces on the gold surfaces. The following other outcomes and implications emerge: • The free and carbon bound LS Fe(II) structures are consistently less favored than Fe(III) (as expected55). However, when perturbed by Au atoms, this effect effectively disappears, so that LS is always favored, also for Fe(II). Resulting reduced LS Fe(II on Au, and therefore a higher midpotential is now more favored than the free and carbon-bound states because of the dispersion stabilization of the additional electron. Or expressed differently, the redox-active electron of Fe(II) is stabilized more, when gold polarizes heme because the additional electron

density is more strongly polarized and its energy relative to the Fe(III) state lowered. • The prevailing adsorbed FePPIX species on the carbon surface is five−coordinate Fe(OH-) with distal axial OH-Fe(III) in LS and Fe(II) in HS state. • FePPIX adsorbs in two modes on Au. Fe(OH-) with distal –OH- ligand in planar orientation on Au-terraces gives the new high−potential peak. Different midpoint potentials of the same species on two quite different electrode materials is notable and caused by different electron delocalization from FePPIX to the electrodes. • The low-potential peak on the Au-electrodes is rooted in electronic interactions which differ both from those at the gold terraces and from the C-surfaces. The peak ratios are smaller the “rougher” the gold electrodes, i.e. significantly smaller for Au(110) and Au(poly) than Au(111) and Au(100), but such observations are not covered by DFT. Specific surface binding of complex target molecules such as FePPIX thus control crucially the voltammetric patterns. • As noted, we propose that the multifarious binding modes may apply not only to direct target molecular adsorption but also to intercalation of FePPIX and related target molecules triggering long-range ET such as in our recent DNAzyme study9. The FePPIX voltammetry can finally be compared with recent studies of magnetic order in two-dimensional phthalocyanine arrays on Au(111)-surfaces in UHV at cryogenic temperatures.33,35 Ordering of these molecular lattices was shown to be controlled by exchange interactions via the Au-substrate, rooted in filled 5d and partially filled 6s bands of gold. If FePPIX adsorption on the Ausurfaces involves both such long-range interactions and “loosely” bound adsorption, the dual voltammetric FePPIX behavior on Au- but not on C-electrodes can be understood, with notions such as electrochemical Kondo interactions opening. 4. Methods 4.1 Chemicals and Preparations Chloroprotoporphyrin IX iron(III) (hemin, porcine, C34H32ClFeN4O4, ≥ 98.0 %), sodium hydroxide (NaOH, 99.99%), and sodium perchlorate (NaClO4, ≥ 99.0 %) were from Sigma−Aldrich and used as received. FePPIX solutions for further use were prepared by dissolving 1 mM FePPIX in 10 mM sodium hydroxide. Millipore water (Milli−Q, 18.2 MΩ cm) was used throughout. 4.2 Instruments Single-crystal Au(111), Au(100), and Au(110) bead electrodes (diameter, ca. 3.0 mm) were prepared as described and checked by cyclic voltammetry in 0.1 M H2SO4.58 Prior to use the electrodes were cleaned by H2 flame annealing and quenched in Millipore water saturated with H2. The hanging meniscus mode in a three-electrode electro7

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chemical setup and an Autolab potentiostat/galvanostat system (Eco Chemie, The Netherlands) controlled by the NOVA 2.0 software were used.27 A coiled platinum wire was used as counter electrode and a freshly prepared reversible hydrogen electrode (RHE) in the same supporting electrolyte, as the reference electrode. The electrolyte was deoxygenated by purified argon (Chrompack, 5 N) for one hour, and an argon stream maintained throughout the experiments. UV−visible absorption spectra were recorded using an Agilent G1103A instrument. Poly−crystalline Au and glassy carbon, basal, and edge plane graphite electrodes were used as references. The electrodes were polished with 0.3 and 0.05 µm Al2O3 slurry and sonicated in Milli−Q water. Details on the analysis of electrochemical data are given in the Supporting Information, Tables S1−S5 and Figure S3. A Pico SPM instrument (Molecular Imaging Co., U.S.A) was used for in situ STM. In−house STM Tips were prepared by etching tungsten or Pt/Ir (80/20) wire followed by coating with Apiezon wax. An in-house in situ STM PTFE cell (2.0 ~ 2.5 mL) was equipped with Pt wires as reference and counter electrodes. The Au(111)−electrode (D 12 mm) was the substrate. The potentials of the Au(111)−electrode and the Pt/Ir tips in the supporting electrolyte were controlled by a bipotentiostat.

D3). Computed energies of redox reactions and spin transitions depend almost linearly on the amount of HF exchange.63-65 TPSSh was used for its high accuracy for first−row transition metal systems52,66-68, including porphyrins43,69. The electronic energies are given in Tables S6-S9. The relative standard half reduction potentials were calculated from the fully relaxed geometries of the oxidized and reduced states. Harmonic frequencies were calculated for the free FePPIX models using the Cosmo solvent model for optimized solvent geometries, as implemented in Turbomole. Zero−point energies (ZPE) and thermochemical state functions (G, S, H) were computed for Fe(III) high−spin and low-spin, and for Fe(II) high−spin and low−spin states of all the three FePPIX models to estimate the vibrational and thermal corrections (Table S11). Energies of states where an electron was added or removed were computed to obtain vertical ionization energies and electron affinities used in calculation of self−exchange inner−sphere reorganization energies, by the procedure described by Ryde and associates.48,49,66. Only the inner−sphere values for FePPIX can be directly compared, but the variations in the long-range solvent reorganization are largely cancelled in the comparisons.

4.3 DFT Computations DFT calculations were performed using the Turbomole software59, version 7.0. The numbers of unpaired electrons were zer0 for Fe(II) LS and one for Fe(III) LS in the free FePPIX and FePPIX-C models. An unpaired 6s electron was left on gold on the FePPIX−gold models which included the full valence 5d shell and a relativistic effective core potential to model core electrons. This gives both a ferromagnetic (MS = 1) and an anti−ferromagnetic (MS = 0) Fe(III) state, both of which were geometry optimized. They have similar energies with a small preference for anti−ferromagnetic coupling, i.e. this coupling is well−behaved and does not produce artifacts. All geometries were optimized at the BP86/def2-SVP level45 using the Cosmo solvation model46 with a static dielectric constant of 80, as condensed phase screening is known to improve the accuracy of charged metal cluster geometries47. The solvent probe radii were 2.0 Å for C, 1.83 Å for N, 1.72 Å for O, 1.3 Å for H, and 2.0 Å for Fe, and 2.5 Å for Au. Electronic energies converged to 10−7 a.u., and the energy gradient in geometry optimization to 10−3 a.u. After convergence of all geometries, the energies of each state were computed with a larger, polarized basis set def2−TZVPP60 to ensure that polarization on all FePPIX and surface atoms are incorporated. Energies converged to 10−7 a.u. The FePPIX axial ligand hydrogen atoms do not include polarization in a TZVP basis set. All energies were computed with the TPSSh functional,51,61 including Grimme's D3 dispersion correction62 (TPSSh-

ASSOCIATED CONTENT Supporting Information. Tables of voltammetric half−widths, DFT energies, and calculations of electrochemical ET rate constants. This material is available free of charge at http://pubs.acs.org.

AUTHOR INFORMATION Corresponding Author * [email protected] * [email protected]

Author Contributions The manuscript was written by equal contributions of all authors.

ORCID: Ling Zhang: orcid.org/0000-0003-1124-3545 Kasper Kepp: orcid.org/0000-0002-6754-7348 Jingdong Zhang: orcid.org/0000-0002-0889-7057

Jens Ulstrup: orcid.org/0000-0002-2601-7906 Notes The authors declare no competing financial interest.

ACKNOWLEDGMENT LZ acknowledges the award of a H.C. Ørsted/Marie Curie Cofund grant. Financial support from The Danish Council for Independent Research for the YDUN project (DFF 40938

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00297) and the Lundbeck Foundation for project R141-201313273 to JZ is gratefully acknowledged.

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(68) Zhao, Y.; Truhlar, D. G. Comparative assessment of density functional methods for 3d transition-metal chemistry. J. Chem. Phys. 2006, 124, 224105-224110.

(69) Kepp, K. P.; Dasmeh, P. Effect of Distal Interactions on O2 Binding to Heme. J. Phys. Chem. B 2013, 117, 3755-3770.

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SYNOPSIS TOC Redox Potentials and Electronic States of Iron Porphyrin IX Adsorbed on Single Crystal Gold Electrode Surfaces Ling Zhang, Kasper P. Kepp, Jens Ulstrup*, Jingdong Zhang*

A previously unobserved redox state of iron porphyrin IX with distinct electrochemistry on single-crystal and polycrystalline gold electrodes is observed and found to arise from dispersion-controlled electronic structure changes upon adsorption.

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