Low-Spin Ferriheme Models of the Cytochromes: Correlation of Molecular Structure with EPR Spectral Type

Published on Web 11/26/2003

Low-Spin Ferriheme Models of the Cytochromes: Correlation

of Molecular Structure with EPR Spectral Type^†

Liliya A. Yatsunyk, Michael D. Carducci, and F. Ann Walker*

Contribution from the Department of Chemistry, UniVersity of Arizona,

Tucson, Arizona 85721-0041

Received May 28, 2003; E-mail: awalker@u.arizona.edu

Abstract: The preparation and characterization of the following bis-imidazole and bis-pyridine complexes

of octamethyltetraphenylporphyrinatoiron(III), Fe(III)OMTPP, octaethyltetraphenylporphyrinatoiron(III), Fe-

(III)OETPP, and tetra-â,â′-tetramethylenetetraphenylporphyrinatoiron(III), Fe(III)TC₆TPP, are reported: paral-

[FeOMTPP(1-MeIm)₂]Cl, perp-[FeOMTPP(1-MeIm)₂]Cl, [FeOETPP(1-MeIm)₂]Cl, [FeTC₆TPP(1-MeIm)₂]Cl,

[FeOMTPP(4-Me₂NPy)₂]Cl, and [FeOMTPP(2-MeHIm)₂]Cl. Crystal structure analysis shows that paral-

[FeOMTPP(1-MeIm)₂]Cl has its axial ligands in close to parallel orientation (the actual dihedral angle between

the planes of the imidazole ligands is 19.5°), while perp-[FeOMTPP(1-MeIm)₂]Cl has the axial imidazole

ligand planes oriented at 90° to each other and 29° away from the closest N_P-Fe-N_Paxis. [FeOETPP-

(1-MeIm)₂]Cl has its axial ligands close to perpendicular orientation (the actual dihedral angle between the

planes of the imidazole ligands is 73.1°). In all three cases the porphyrin core adopts relatively purely

saddled geometry. The [FeTC₆TPP(1-MeIm)₂]Cl complex is the most planar and has the highest contribution

of a ruffled component in the overall saddled structure compared to all other complexes in this study. The

estimated numerical contribution of saddled and ruffled components is 0.68:0.32, respectively. Axial ligand

planes are perpendicular to each other and 15.3° away from the closest N_P-Fe-N_Paxis. The Fe-N_P

bond is the longest in the series of octaalkyltetraphenylporphyrinatoiron(III) complexes due to [FeTC₆TPP-

(1-MeIm)₂]Cl having the least distorted porphyrin core. In addition to these three complexes, two crystalline

forms each of [FeOMTPP(4-Me₂NPy)₂]Cl and [FeOMTPP(2-MeHIm)₂]Cl were obtained. In all four of these

cases the axial planes are in nearly perpendicular planes in spite of quite different geometries of the porphyrin

cores (from purely saddled to saddled with 30% ruffling). The EPR spectral type correlates with the geometry

of the OMTPP, OETPP and TC₆TPP complexes. For the paral-[FeOMTPP(1-MeIm)₂]Cl, a rhombic signal

with g₁) 1.54, g₂) 2.51, and g₃) 2.71 is consistent with nearly parallel axial ligand orientation. For all

other complexes of this study, “large g_max” signals are observed (g_max) 3.61 - 3.27), as are observed for

nearly perpendicular ligand plane arrangement. On the basis of this and previous work, the change from

“large g_max” to normal rhombic EPR signal occurs between axial ligand plane dihedral angles of 70° and

30°.

Introduction

high enough resolution to obtain the precise structure of the

heme center with regard to the orientation of the axial ligands.

Bis-histidine-coordinated heme centers are involved in elec-

tron transfer in a number of cytochrome-containing systems

including complexes II, III, and IV of inner mitochondrial

membranes. Complex III, also called the cytochrome bc₁

complex or ubiquinol:cytochrome c oxidoreductase, plays an

important role in electron-transfer processes in mitochondria,

chloroplasts, and in many aerobic and photosynthetic bacteria.

It transfers electrons from ubiquinol to soluble cytochrome c;

this process is coupled to translocation of two protons across

the inner mitochondrial membrane. Several crystal structures

of this complex have been reported^1-4but they do not have

It is believed that the arrangement of the axial ligands plays an

important role in defining the spectroscopic properties, and

possibly also the reduction potentials of these heme centers.

One of the first and most useful spectroscopic tools that

provided much insight into the number, structure, properties,

and roles of heme centers in the cytochrome bc₁complex was

EPR spectroscopy. The unusual EPR spectra for the cytochromes

bc₁were first reported by Orme-Johnson, Hansen, and Beinert⁵

and later analyzed in detail by Salerno.⁶EPR data for the bc₁

complex show that both of the b hemes (as well as the c₁heme)

(1) Xia, D.; Yu, C.-A.; Kim, H.; Xia, J.-Z.; Kachurin, A. M.; Zhang, L.; Yu,

L.; Deisenhofer, J. Science 1997, 277, 60-66.

^†Abbreviations: OMTPP, octamethyltetraphenylporphyrin; OETPP,

octaethyltetraphenylporphyrin; TC₆TPP, tetra-â,â′-methylenetetraphenylpor-

phyrin; TPP, tetraphenylporphyrin; OEP, octaethylporphyrin; ProtoIX,

protoporphyrin IX.; TMP, tetramesitylporphyrin; 1-MeIm, 1-methylimida-

zole; 2-MeHIm, 2-methylimidazole; 1,2-Me₂Im, 1,2-dimethylimidazole;

5-MeHIm, 5-methylimidazole; 4-Me₂NPy, 4-(dimethylamino)pyridine; Py,

pyridine.

(2) Iwata, S.; Lee, J. W.; Okada, K.; Lee, J. K.; Iwata, M.; Rasmussen, B.;

Link, T. A.; Ramaswamy, S.; Jap, B. K. Science 1998, 281, 64-71.

(3) Hunte, C.; Koepke, J.; Lange, C.; Rossmanith, T.; Michel, H. Structure

2000, 8, 669-684.

(4) Zhang, Zh.; Huang, L.; Shulmeister, V. M.; Chi, Y.-I.; Kim, K. K.; Hung,

L.-W.; Crofts, A. R.; Berry, E. A.; Kim, S.-H. Nature 1998, 392, 677-

684.

9

15986

J. AM. CHEM. SOC. 2003, 125, 15986-16005

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

7

exhibit single feature EPR signals known as the “large g_max

”

Previous systems investigated as models of these bis-histidine-

coordinated cytochromes b have all utilized synthetic hemes

such as octaethylporphyrinatoiron(III)/(II) (OEPFe) or tetraphe-

nylporphyrinatoiron(III)/(II) (TPPFe), or other tetraarylporphy-

rin-type systems such as tetramesitylporphyrinatoiron(III)/(II)

(TMPFe).^20,24,25These systems often adopt nonplanar porphyrin

ring conformations due to steric interaction between the

peripheral substituents or between the porphyrin and the axial

ligands. In general, there are four major types of nonplanar

distortion: saddled, ruffled, domed, and waved,²¹with saddled

and ruffled distortions being the most commonly observed in

the model systems. In the saddled conformation, adjacent pyrrole

rings are tilted up and down with respect to the porphyrin mean

plane and the meso-carbons are in the plane, while in the ruffled

conformation the adjacent pyrrole rings are twisted clockwise

and counterclockwise, bringing the meso-carbons above and

below the porphyrin mean plane. Both ruffling and saddling

result in the formation of two mutually perpendicular cavities,

one above and one below the macrocycle plane;^22,23these

cavities are thus capable of orienting the planar aromatic axial

ligands perpendicular to each other. In the case of the saddled

conformation, the axial ligands are expected to be near the

porphyrin nitrogens or nearly eclipsed with the N_P-Fe-N_P

vectors. In the ruffled conformation the axial ligands are oriented

above the porphyrin meso-carbons or, in other words, form an

approximately 45° angle with the closest N_P-Fe-N_Pvector. It

has been found that for low-spin (LS) Fe(III) porphyrinates, all

of the TPP- and TMP-derived systems studied previously adopt

ruffled conformations when the axial ligands are in perpen-

dicular planes lying at ∼45° to the N_P-Fe-N_Pvectors, i.e.,

when the axial ligands are hindered imidazoles (2-MeHIm, 1,2-

Me₂Im) or pyridines.^20,24-26However, for the Fe(II) analogues

of these TPP/TMP complexes, no structure of a bis-hindered

imidazole complex has been reported, and all structures of bis-

pyridine complexes have the axial ligands in parallel planes lying

at about 45° to one of the N_P-Fe-N_Pvectors, with the

conformation of the porphyrin ring being planar.²⁷Hence, it

appears that pyridine ligands are capable of binding to iron(II)

porphyrinates without ruffling of the porphyrin ring. To sum-

marize, then, for meso-only substituted Fe(III) (LS d⁵) porphy-

rinates with bulky axial ligands and/or meso-substituents, the

preferred geometry is with axial ligands in perpendicular planes

and a ruffled porphyrin ring, while for Fe(II) (LS d⁶) porphy-

rinates, the preferred geometry of all bis-ligand complexes for

which structures have been reported is with axial ligands in

parallel planes and a planar porphyrin ring. The fact that

hindered (2-substituted) imidazoles cannot bind to Fe porphy-

rinates of either oxidation state unless they are placed in

or “HALS” (highly anisotropic low-spin)^8,9type. These signals

are observed at temperatures below about 10 K, and all have

the only resolved feature, the g_maxsignal, with the g-value g

3.2 and with the other two g-values undetectable. For the

cytochrome bc₁complex of mitochondria and the related

cytochrome b₆f complex of chloroplasts, these signals “relax”

to normal rhombic EPR signals when the cytochrome b protein

is extracted from the mitochondrial membrane and the other

proteins of the complex.^10,11At the highest resolution obtained

thus far (2.2 Å),¹²the cytochrome bc₁structure has been

modeled with the two b heme centers having axial histidine

imidazole plane dihedral angles of 84° and 38°. On the basis

of redox titration, the former heme center, called b_L, was

assigned the EPR signal with g_max) 3.75-3.78 and the latter

one, called b_H, the EPR signal with g_max) 3.41-3.44.^5,6Typical

reduction potentials for the b_Hand b_Lcenters of bovine heart

complex III are 105 and -5 mV, respectively.¹³

Model systems have been great aids in correlating the

structure of heme centers with their spectroscopic properties.

In the early 1980s it was shown that the “large g_max” signal can

be created for model ferrihemes by binding bulky imidazoles

(2-methylimidazole, 1,2-dimethylimidazole, etc.) or some py-

ridines (3,4-dimethylpyridine, pyridine itself, etc.) to iron(III)

tetraphenylporphyrin (TPPFe(III))¹⁴or ProtoIXFe(III).^8,9Later,

Walker, Scheidt, and their co-workers showed that the “large

g

_max” signal occurs for ferriheme complexes with (d_xy)²(d_xz,d_yz)³

electronic ground states when the axial ligands are in perpen-

dicular planes,^7,15and hence established the first correlation of

structure with EPR spectral type: “large g_max” f axial ligands

in perpendicular planes; normal rhombic f axial ligands in

parallel planes. “Large g_max” signals are observed for ferriheme

complexes in which the splitting between the d_xzand d_yzorbitals

is very small (less than the value of the spin-orbit coupling

constant, λ, or ,400 cm^-1),^7,19i.e., the case where axial ligands

are in perpendicular planes or where ligands without planes are

used (e.g., CN^-, phosphines or NH₃),^16-18whereas normal

rhombic EPR signals are observed when the splitting between

these two orbitals is larger, on the order of 2-3 times the spin-

orbit coupling constant, λ, or 600-1000 cm^{-1 7,19}

i.e., when

planar axial ligands coordinated to iron are oriented in parallel

planes. It is interesting to note that the smaller of the dihedral

angles of the b hemes of the cytochrome bc₁complex (38°)

,

does not appear to be consistent with the fact that a “large g_max

signal is observed for both b hemes.

”

(5) Orme-Johnson, N. R.; Hansen, R. E.; Beinert, H. Biochem. Biophys. Res.

Commun. 1971, 45, 871-878.

(6) Salerno, J. C. J. Biol. Chem. 1984, 259, 2331-2336.

(7) Walker, F. A.; Huynh, B. H.; Scheidt, W. R.; Osvath, S. R. J. Am. Chem.

Soc. 1986, 108, 5288-5297.

(8) Migita, C. T.; Iwaizumi, M. J. Am. Chem. Soc. 1981, 103, 4378.

(9) Carter, K. R.; T'sai, A.-L.; Palmer, G. FEBS Lett. 1981, 132, 243-246.

(10) T'sai, A.-L.; Palmer, G. Biochim. Biophys. Acta 1982, 681, 484-495.

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261.

(20) Munro, O. Q.; Serth-Guzzo, J. A.; Turowska-Tyrk, I.; Mohanrao, K.;

Shokhireva, T. Kh.; Walker, F. A.; Debrunner, P. G.; Scheidt, W. R. J.

Am. Chem. Soc. 1999, 121, 11144-11155.

(21) http://www.chem.ucdavis.edu/groups/smith/chime/structs/

ruf_structs.html.

(12) Iwata, S. Personal communication.

(22) Walker, F. A.; Simonis, U. J. Am. Chem. Soc. 1991, 113, 8652-8657.

Walker, F. A.; Simonis, U. J. Am. Chem. Soc. 1992, 114, 1929.

(23) Sparks, L. D.; Medforth, C. J.; Park, M. S.; Chamberlain, J. R.; Ondrias,

M. R.; Senge, M. O.; Smith, K. M.; Shelnutt, J. A. J. Am. Chem. Soc.

1993, 115, 581-592.

(13) Von Jagow, G.; Engel, W. D. Angew Chem., Int. Ed. Engl. 1980, 19, 659-

675.

(14) Walker, F. A.; Reis, D.; Balke, V. L. J. Am. Chem. Soc. 1984, 106, 6888-

6898.

(15) Scheidt, W. R.; Kirner, J. F.; Hoard, J. L.; Reed, Ch. A. J. Am. Chem. Soc.

1987, 109, 1963-1968.

(24) Safo, M. K.; Gupta, G. P.; Walker, F. A.; Scheidt, W. R.; J. Am. Chem.

Soc. 1991, 113, 5497-5510.

(16) Innis D.; Soltis, S. M.; Strouse, C. E. J. Am. Chem. Soc. 1988, 110, 5644-

5650.

(25) Safo, M. K.; Gupta, G. P.; Walker, F. A.; Watson, C. T.; Simonis, U.;

Scheidt, W. R. J. Am. Chem. Soc. 1992, 114, 7066-7075.

(26) Munro, O. Q.; Marques, H. M.; Debrunner, P. G.; Mohanrao, K.; Scheidt,

W. R. J. Am. Chem. Soc. 1995, 117, 935-954.

(17) Watson, C. T.; Walker, F. A., unpublished data.

(18) Ikeue, T.; Ohgo, Y.; Saitoh, T.; Yamaguchi, T.; Nakamura, M. Inorg. Chem.

2001, 40, 3423-3434.

(27) Safo, M. K.; Nesset, M. J. M.; Walker, F. A.; Debrunner, P. G.; Scheidt,

W. R. J. Am. Chem. Soc. 1997, 119, 9438-9448.

(19) Walker, F. A. Coord. Chem. ReV. 1999, 185-186, 471-534.

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15987

A R T I C L E S

Yatsunyk et al.

perpendicular planes (because of the bulky 2-substituent), along

with the fact that bis-hindered imidazole complexes of Fe(II)

porphyrinates are very unstable and can only be formed and

studied at extremely low temperatures,^28,29suggests that Fe(II)

porphyrinates having a ruffled core are thermodynamically

unstable. DFT calculations of Mo¨ssbauer parameters at 4.2 K

support a perpendicular ligand orientation with ruffled porphyrin

core for the bis-2-methylimidazole complex of TMPFe(II),³⁰

which only forms at very low temperatures.²⁹

both of these complexes had “large g_max” EPR signals.³²Thus,

it is clear that an axial ligand plane dihedral angle of 70° is

sufficiently large to yield a “large g_max” EPR signal. This is a

very important finding with respect to the membrane-bound

cytochromes b,^1-4for it indicates that the observed “large g_max

”

EPR signals⁶could be expected if the dihedral angles between

histidine ligand planes were as small as 70°. Determining how

much smaller than 70° this dihedral angle could be and yet give

rise to a “large g_max” EPR signal was one of the goals of this

work.

Cytochromes b are redox proteins, and thus both oxidation

states must be structurally stable, with little reorganizational

energy involved in the redox process. In this regard, it is

unreasonable to think that the ligands can change from

perpendicular (Fe(III)) to parallel (Fe(II)) upon redox. Hence,

to model the bis-histidine-coordinated heme centers of the bc₁

complex, in which it appears that at least one of the hemes has

the histidine ligands in perpendicular planes,^1-4TPP/TMP-

derived iron porphyrinates do not appear to reproduce the

structures and properties of both the Fe(III) and Fe(II) oxidation

states. Thus model hemes must be found that will support

perpendicular ligand planes for both oxidation states of iron.

Therefore, we have turned to an investigation of the octaalky-

ltetraphenylporphyrin complexes of iron as possible model

hemes that could support perpendicular ligand orientations not

only for Fe(III) but also for Fe(II). Since all of these complexes

adopt predominantly saddled conformations, it was expected

that the axial ligand planes would be perpendicular and oriented

above or nearly above the porphyrin nitrogens.

In this paper we describe the crystal structures and EPR

spectra of eight crystalline forms of octaalkyltetraphenylpor-

phyrinatoiron(III) with different axial ligands. All of the iron

porphyrinate molecules in this study adopt predominantly

saddled conformations, and we find that this class of synthetic

porphyrinates is exceptionally rich in stabilizing a variety of

axial ligand orientations, dihedral angles, and porphyrin core

conformations. The overall goal of this project is to determine

the limits on axial ligand plane dihedral angle for each type of

EPR and Mo¨ssbauer signal and to see if there is any correlation

between g-values or Mo¨ssbauer spectral parameters observed

and ligand plane dihedral angle. This is being done by

determining the molecular structures of a series of mainly

saddled Fe(III) and Fe(II) octaalkyltetraphenylporphyrinate

complexes, in the hope of finding nonruffled porphyrinate cores

that will stabilize the Fe(II) state with perpendicular axial ligand

planes. A related goal of this project is to measure the reduction

potentials of the complexes that are characterized structurally

and spectroscopically, to correlate the geometry of the active

site at the heme center in models and proteins with the reduction

potential of the heme, as well as with the EPR spectrum of the

Fe(III) state of the center and the Mo¨ssbauer spectra of both

oxidation states. The Mo¨ssbauer spectra of four of these LS

ferriheme complexes are presented elsewhere.³³

Along with the lack of structural data on Fe(II) porphyrinates

with perpendicular axial ligands and a ruffled porphyrinate core,

redox data strongly indicate that complexes with bulky ligands

that would have to bind in a perpendicular orientation over the

meso positions (i.e., just the right situation to encourage ruffling)

have very negative reduction potentials compared to those

having nonbulky ligands that can bind in parallel planes and

maintain a planar porphyrin ring (-212 mV as compared to

-130 mV vs SCE for 2-MeHIm and 1-MeIm, respectively, for

TMPFe).³¹The more negative reduction potential means that

the Fe(III) state is strongly stabilized over the Fe(II) state when

hindered imidazoles are bound to the metal. The derived binding

constants support this (log â₂^III) 7.4 and 7.9, respectively, while

Experimental Section

Synthesis of (OMTPP)FeCl. Octamethyltetraphenylporphyrin (H₂-

OMTPP) was prepared by first synthesizing 3,4-dimethylpyrrole.³⁴Next,

the porphyrinogen was synthesized by reaction of the pyrrole with

benzaldehyde and oxidized with 2,3-dichloro-5,6-dicyano-1,4-benzo-

quinone (DDQ), according to the literature procedure³⁵except that both

steps (condensation and oxidation) were done in one reaction flask.

The product was purified by column chromatography (3 × 30 cm³

Alumina, Brockman grade III). Elution first with 1:1 CH₂Cl₂:C₆H₆, next

with CH₂Cl₂, and finally with 2% methanol in CH₂Cl₂yielded the

desired porphyrin, which eluted as a very narrow dark green band

(probably in the form of H₄OMTPP²⁺) in the final step. Solvent was

removed under reduced pressure, and the resulting material was

redissolved in a small quantity of CH₂Cl₂and recrystallized from 0.2%

KOH in ethanol. Iron was inserted using anhydrous iron(II) chloride

(Aldrich) in DMF³⁶with subsequent recrystallization of the product

from CH₂Cl₂/ether solvent mixtures. A quantitative yield of (OMTPP)-

FeCl crystals was obtained.

II

log â₂) 5.5 and 7.3, respectively, for TMPFe complexes of

2-MeHIm and 1-MeIm).³¹

In our earlier publication on bis-axial ligand complexes of

octaethyltetraphenylporphyrinatoiron(III), Fe(III)OETPP,³²we

found that the bis-2-MeHIm complex had perpendicular axial

ligand planes, offset from the N_P-Fe-N_Paxes by 14°, a very

small angle as compared to TPP and TMP complexes of Fe-

(III) with hindered imidazoles,^15,20while the bis-4-Me₂NPy

complex had a 70° dihedral angle between axial ligand planes,

and the smallest angle yet observed for bis-pyridine complexes

between the ligand plane and the N_P-Fe-N_Paxis of 9°, yet

Synthesis of (OETPP)FeCl. Octaethyltetraphenylporphyrin (H₂-

OETPP) was prepared by first synthesizing 3,4-diethylpyrrole.^34-36The

(28) Polam, J. R.; Wright, J. L.; Christensen, K. A.; Walker, F. A.; Flint, H.;

Winkler, H.; Grodzicki, M.; Trautwein, A. X. J. Am. Chem. Soc. 1996,

118, 5272-5276.

(29) Polam, J. R.; Shokhireva, T. Kh.; Raffii, K.; Simonis, U.; Walker, F. A.

Inorg. Chim. Acta 1997, 263/1-2, 109-117.

(33) Teschner, T.; Yatsunyk, L.; Schu¨nemann, V.; Trautwein, A. X.; Walker,

F. A. Manuscript in preparation.

(34) Cheng, D. O.; Bowman, T. L.; LeGoff, E. Tetrahedron Lett. 1976, 13,

1145-1147.

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Smith, K. M. J. Am. Chem. Soc. 1990, 112, 8851-8857.

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M. R.; Senge, M. O.; Smith, K. M.; Shelnutt, J. A. J. Am. Chem. Soc.

1993, 115, 581-592.

(30) Grodzicki, M.; Flint, H.; Winkler, H.; Walker, F. A.; Trautwein, A. X. J.

Phys. Chem. A 1997, 101, 4202-4207.

(31) Nesset, M. J. M.; Shokhirev, N. V.; Enemark, P. D.; Jacobson, S. E.; Walker,

F. A. Inorg. Chem. 1996, 35, 5188-5200.

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6564-6578.

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Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

overall yield was 35% starting from the propionaldehyde. The por-

phyrinogen and porphyrin were then prepared as reported earlier³⁵

without the modification used for H₂OMTPP. Namely, the porphy-

rinogen was synthesized first, solvent was removed under reduced

pressure, and the residue was washed with methanol, yielding a white

precipitate which was filtered, redissolved in a small amount of CH₂-

Cl₂, and recrystallized from methanol again, yielding 48% of the pure

porphyrinogen. It was oxidized with 4 equiv of DDQ, and the crude

product was applied to a column of alumina (Brockman grade III, 2.5

× 15 cm³column) eluted first with CH₂Cl₂, next 2% methanol in CH₂-

Cl₂and finally 2:1 CH₂Cl₂: methanol) and recrystallized from 0.2%

KOH in ethanol. The resulting crystals were dried in a vacuum oven

for 4 h at 70 °C. Yield 67%. Iron insertion was carried out as described

above. An excellent method of purification of (OETPP)FeCl was

discovered. After removal of the solvent, the dry residue was washed

with pentane, yielding, after filtration, a dark brown powder of very

pure (OETPP)FeCl. It was washed repeatedly with cold pentane and

dried in the vacuum oven for 4 h at 70 °C.

cyclohexane. Usually deuturated methylene chloride and chloroform

were used due to their high purity and dryness. Other solvent systems

were tried as well, but these two were used most frequently and

successfully. EPR spectra were recorded on a Bruker ESP-300E EPR

spectrometer (operating at 9.4 GHz) equipped with Oxford Instruments

ESR 900 continuous flow helium cryostat. Spectra were obtained for

crystalline samples at 4 K. Microwave frequencies were measured using

a Systron-Donner frequency counter. Typical values for microwave

power, modulation frequency, and modulation amplitude were 0.2 mW,

100 kHz, and 1 G, respectively.

Computational Methods. Ab inito DFT calculations with the

unrestricted hybrid method B3LYP and relatively small 3-21G basis

set were applied to study the optimal ligand orientation in the nonplanar

porphyrin molecules. The calculations were carried out using the

commercial program package Gaussian 98,⁴³and models were generated

using Spartan 5.1. All coordinates were taken from the crystal structures

of [FeOETPP(4-Me₂NPy)₂]Cl³²and [FeOMTPP(4-Me₂NPy)₂]Cl (struc-

tures A and B) discussed below. No geometry optimization was

performed; single-point calculations were done in all cases. First,

porphyrin core models for all three complexes were generated from

the crystal structures by removing axial 4-Me₂NPy ligands and

substituting peripheral groups, Me, Et, and Ph with H. In each case we

obtained the following porphyrin core: FeN₄C₂₀H₁₂. Then two pyridine

ligands were added to each model (first they were oriented in the same

way as in the crystal structures (see Table 2 below) and then one of

them was constrained to be at 0° to the N_P-Fe-N_Pvector) and the

single-point energies were calculated again. For the B:[FeOMTPP(4-

Me₂NPy)₂]Cl complex, structures with different ligand orientation were

generated. The angle between two ligand planes was fixed to 88.5°,

and both ligands were rotated simultaneously in steps of 15°.

Structure Determination. General. Crystals of each complex were

mounted on glass fibers in random orientation and examined on a

Bruker SMART 1000 CCD detector X-ray diffractometer at 100(2) K

for paral- and perp-[FeOMTPP(1-MeIm)₂]Cl, at 170(2) K for [FeO-

ETPP(1-MeIm)₂]Cl, [FeTC₆TPP(1-MeIm)₂]Cl, [FeOMTPP(2-MeIm)₂]-

Cl (molecule C and D), and [FeOMTPP(4-Me₂NPy)₂]Cl (molecule B),

and at 200(2) K for [FeOMTPP(4-Me₂NPy)₂]Cl, molecule A. All

measurements utilized graphite-monochromated Mo KR radiation (λ

) 0.71073 Å) with a power setting of 50 kV, 40 mA. Final cell

constants and complete details of the intensity collection and least

squares refinement parameters for all complexes are summarized in

Table 1 and in the Supporting Information.

Synthesis of (TC₆TPP)FeCl. (TC₆TPP)FeCl was synthesized ac-

cording to literature procedures^37,38with some modifications. First ethyl

3,4-butanopyrrole-2-carboxylate was synthesized using the procedure

of Barton and Zard^39,40from 1-nitrocylohexane and ethyl isocyano-

acetate in the presence of guanidine base.^41,42Hydrolysis and decar-

boxylation of ethyl 3,4-tetramethylenepyrrole-2-carboxylate with so-

dium hydroxide in refluxing ethylene glycol afforded 3,4-tetrameth-

ylenepyrrole in 32% yield (from 1-nitrocyclohexane).³⁹Next, the

porphyrinogen was prepared and oxidized with DDQ, according to the

literature procedure³⁵with the modification used for the H₂OMTPP

synthesis. The solvent was evaporated to dryness, and the residue was

taken up in CH₂Cl₂. The free-base porphyrin solution was applied to a

column of alumina (3 × 30 cm², alumina Brockman Grade III, packed

by the wet method with 1:1 CH₂Cl₂/C₆H₆mixture) and eluted with 1:1

C₆H₆:CH₂Cl₂, then pure CH₂Cl₂, and finally 2% methanol in CH₂Cl₂.

The desired porphyrin eluted as a narrow dark brown-green band with

2% methanol in CH₂Cl₂. Solvent was removed and the resulting material

was dissolved in a small amount of hot CH₂Cl₂and recrystallized from

hot 0.2% KOH in ethanol. By cooling slowly and letting the solution

stand at 5 °C, large crystals formed. The product was collected by

filtration and dried in a vacuum oven for 4 h at 70 °C to afford 53 mg

of blue needlelike crystals (21% yield). Fe insertion was done as

described above. Large dark blue crystals suitable for X-ray structure

determination were formed in 63% yield (from the porphyrin) after

recrystallization from the CH₂Cl₂/ether. The optical spectrum of (TC₆-

TPP)FeCl shows a split Soret band: 397.3 nm (1.054), and 427.7 nm

(0.967) and several poorly resolved bands in the 500-650 nm region

of the spectrum, namely, 530.2 nm (0.177), 572.0 nm (0.135), and 707.5

nm (0.070). ¹H NMR (CD₂Cl₂, 600 MHz, 298 K, referenced to residual

solvent peak at 5.32 ppm): δ ppm, 55.20 and 53.55 (s, 8H each, CH₂-

(R)), 13.25 and 12.84 (s, 4H each, Ph-m), 9.40 and 6.85 (br, 4H each,

Ph-o), 7.56 (s, 4H, Ph-p), 7.04 and 5.61 (s, 8H each, CH₂(â)).

In most cases, a total of 3736 frames at 1 detector setting covering

0 < 2θ < 60° were collected, having an omega scan width of 0.2° and

an exposure time of 20 s per frame. In the case of A:[FeOMTPP(4-

Me₂NPy)₂]Cl, [FeOETPP(1-MeIm)₂]Cl, and [FeOMTPP(2-MeHIm)₂]-

Cl (C and D), the exposure time was 10, 10, 60, and 60 s, respectively.

The frames were integrated using the Bruker SAINT software package’s

narrow frame algorithm.⁴⁴Initial cell constants and an orientation matrix

for integration were determined from reflections obtained in three

orthogonal 5° wedges of reciprocal space.

1-Methylimidazole (1-MeIm), 4-(dimethylamino)pyridine (4-Me₂-

NPy), and 2-methylimidazole (2-MeHIm) complexes of (OMTPP)FeCl,

(OETPP)FeCl, and (TC₆TPP)FeCl were obtained by simply placing

3-6 equiv of the chosen axial ligand in a methylene chloride solution

of the chosen porphyrinatoiron(III) chloride. Crystals were grown by

liquid diffusion methods. In most cases two solvent systems were

used: (1) methylene chloride and dodecane; (2) chloroform and

All structures were solved using SHELXS in the Bruker SHELXTL

(Version 6.0) software package.⁴⁵Refinements were performed using

SHELXL, and illustrations were made using XP.⁴⁵Solution was

(43) Gaussian 98, Revision A.7, Frisch, M. J.; Trucks, G. W.; Schlegel, H. B.;

Scuseria, G. E.; Robb, M. A.; Cheeseman, J. R.; Zakrzewski, V. G.;

Montgomery, Jr., J. A.; Stratmann, R. E.; Burant, J. C.; Dapprich, S.;

Millam, J. M.; Daniels, A. D.; Kudin, K. N.; Strain, M. C.; Farkas, O.;

Tomasi, J.; Barone, V.; Cossi, M.; Cammi, R.; Mennucci, B.; Pomelli, C.;

Adamo, C.; Clifford, S.; Ochterski, J.; Petersson, G. A.; Ayala, P. Y.; Cui,

Q.; Morokuma, K.; Malick, D. K.; Rabuck, A. D.; Raghavachari, K.;

Foresman, J. B.; Cioslowski, J.; Ortiz, J. V.; Baboul, A. G.; Stefanov, B.

B.; Liu, G.; Liashenko, A.; Piskorz, P.; Komaromi, I.; Gomperts, R.; Martin,

R. L.; Fox, D. J.; Keith, D.; Al-Laham, M. A.; Peng, C. Y.; Nanayakkara,

A.; Gonzalez, C.; Challacombe, M.; Gill, P. M. W.; Johnson, B.; Chen,

W.; Wong, M. W.; Andres, J. L.; Gonzalez, C.; Head-Gordon, M.; Replogle,

E. S.; Pople, J. A. Gaussian, Inc., Pittsburgh, PA, 1998.

(37) Medforth, C. J.; Senge, M. O.; Smith, K. M.; Sparks, L. D.; Shelnutt, J. A.

J. Am. Chem. Soc. 1992, 114, 9859-9869.

(38) Medforth, C. J.; Berber, M. D.; Smith, K. M. Tetrahedron Lett. 1990, 31

(26), 3719-33722.

(39) Barton, D. H. R.; Kervagoret, J.; Zard, S. Z. Tetrahedron 1990, 26 (21),

7587-7598.

(40) Chen, Sh.; Lash, T. D. J. Heterocycl. Chem. 1997, 34 (1), 273-278.

(41) Barton, D. H. R.; Elliot, J. D.; Gero, S. D. J. Chem. Soc., Perkin Trans. I

1982, 2085-2090.

(42) Barton, D. H. R.; Elliot, J. D.; Gero, S. D. J. Chem. Soc., Chem. Commun.

1981, 1136-1137.

(44) Bruker (2002) SAINT Reference Manual Version 6.0, Bruker AXS Inc.,

Madison, WI.

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15989

A R T I C L E S

Yatsunyk et al.

Table 1. Summary of Crystal Data and Intensity Collection Parameters

paral-[FeOMTPP(1-

MeIm ]Cl‚CD Cl₂

perp-[FeOMTPP(1-

MeIm ]Cl‚2.43CDCl₃

[FeOETPP(1-

MeIm)₂]Cl‚2CDCl₃‚C H

[FeTC TPP(1-

6

molecule

emp form.

MeIm)₂]Cl‚2CD Cl₂

2

6

12

2

C

₆₁H₅₈Cl₃FeN₈

C_62.43H_58.43Cl_8.3FeN₈

C

₇₆H₈₆Cl₇FeN₈

C

₇₀H₆₈Cl₅FeN₈

form. wt

temp, K

1065.35

100(2)

1270.89

100(2)

1415.53

170(2)

1244.34

170(2)

crystal system

space group

a, Å

b, Å

c, Å

R, â, γ, deg

volume, Å³

Z

monoclinic

Pc

cubic

I-43d

monoclinic

P2₁

12.860(2)

22.101(3)

13.791(2)

90, 107.936(2), 90

3729.2(8)

2

tetragonal

I4₁/a

13.8856(10)

10.1279(7)

18.5327(13)

90, 95.925(2), 90

2592.4(3)

2

1.365

0.495

1114

26.153(2)

90, 90, 90

17887(3)

12

1.416

0.673

7874

19.8263(17)

15.230(3)

90, 90, 90

5986.8(13)

4

1.381

0.526

2580

density (calc), g/cm³

abs coeff., mm^-1

F(000)

1.261

0.500

1486

crystal dimension, mm

θ limits

0.46 × 0.25 × 0.06

2.01 to 33.26

-21 e h e 21,

-15 e k e 15,

-28 e l e 28

48078

18847 [R_int) 0.0367,

R_σ) 0.059]

2.55

0.49 × 0.48 × 0.37

1.91 to 24.93

-30 e h e 30,

-30 e k e 30,

-30 e l e 30

93819

2578 [R_int) 0.0725,

R_σ) 0.022]

36.4

0.49 × 0.33 × 0.20

1.55 to 27.55

-16 e h e 16,

-28 e k e 28,

-17 e l e 17

46562

17070 [R_int) 0.0446,

R_σ) 0.063]

2.73

0.26 × 0.20 × 0.12

1.69 to 25.07

-23 e h e 23,

-23 e k e 23,

-18 e l e 18

27945

2647 [R(int) ) 0.1287,

R_σ) 0.090]

10.6

limiting indices

reflcns utilized

indep reflcns

redundancy

reflcns with I > 2σ(I)

completeness, %

max and min.

15443 (81.9%)

96.6

0.9709, 0.8042

2544 (98.7%)

99.1

0.7889, 0.7340

13710 (80.3%)

99.6

0.9066, 0.7918

1389 (52.5%)

99.7

0.999, 0.808

transmission

data/restraints/params

18847/5/683

1.039

2578/106/182

1.281

17070/49/829

1.014

2647/201/253

0.924

GoF on F²

final R indices

[I > 2σ(I)]

R₁) 0.0481,

wR₂) 0.1109

R₁) 0.0666,

wR₂) 0.1229

0.764 and -0.731

R₁) 0.0926,

wR₂) 0.2256

R₁) 0.0935,

wR₂) 0.2261

0.250 and -0.204

R₁) 0.0563,

wR₂) 0.1338

R₁) 0.0754,

wR₂) 0.1445

0.676 and -0.410

R1 ) 0.0565,

wR₂) 0.1458

R₁) 0.1219,

wR₂) 0.1731

0.488 and -0.474

R indices (all data)

largest diff. peak

and hole, e/Å³

RMS diff

0.081

0.054

0.071

0.062

density, e/Å³

A: [FeOMTPP(4

B: [FeOMTPP(4

-Me₂NPy)₂]Cl‚4CDCl₃

C: [FeOMTPP(2-

MeHIm)₂]Cl‚2CDCl₃

D: [FeOMTPP(2-

molecule

-Me₂NPy)₂]Cl‚4CD Cl₂

MeHIm)₂]Cl‚3CD Cl₂

2

emp form.

form. wt

temp, K

crystal system

space group

a, Å

b, Å

c, Å

R, â, γ, deg

volume, Å³

Z

C

₇₀H₇₂Cl FeN₈

C

₇₀H₆₈Cl₁₃FeN₈

C

₆₈H₇₀Cl₇FeN₈

C₆₃H₆₂Cl₇FeN₈

1400.26

200(2)

monoclinic

C2/c

21.766(5)

22.069(5)

17.816(4)

90, 127.096(3), 90

6826(3)

1538.02

170(2) K

monoclinic

P2₁/c

15.9507(13)

23.2709(19)

19.5217(16)

90, 94.396(2), 90

7224.9(10)

4

1303.32

170(2)

monoclinic

P2₁/c

14.0780(14)

26.710(3)

17.2488(18)

90, 96.765(2), 90

6440.8(11)

4

1.344

0.573

1235.21

170(2)

triclinic

P1h

13.800(6)

15.151(7)

16.566(8)

66.513(14), 71.841(13), 88.719(12)

2998(2)

4

2

density (calc), g/cm³

abs coeff., mm^-1

F(000)

1.363

0.621

2908

1.414

0.737

3164

1.368

0.611

1282

2716

crystal dimension, mm

θ limits, deg

limiting indices

0.55 × 0.40 × 0.28

1.85 to 27.70°

-27 e h e 26,

-28 e k e 28,

-23 e l e 22

37026

7569 [R(int) ) 0.0214,

R_σ) 0.019]

4.96

0.55 × 0.25 × 0.25

1.55 to 27.80

-20 e h e 20,

-29 e k e 30

, -25 e l e 24

77824

15968 [R(int) ) 0.1010,

R_σ) 0.097]

4.87

0.28 × 0.06 × 0.02

1.41 to 25.77

-17 e h e 17,

-32 e k e 32,

-21 e l e 21

64028

12312 [R(int) ) 0.1866,

R_σ) 0.238]

5.20

0.20 × 0.08 × 0.08

1.42 to 20.80

-13 e h e 13,

-15 e k e 15,

-16 e l e 16

17070

6254 [R(int) ) 0.1192,

R_σ) 0.141]

2.73

reflctns utilized

indep reflctns

redundancy

reflectn with

5827 (77.0%)

8572 (53.4%)

4824 (39.2%)

3563 (57.0%)

I >2σ(I)

completeness, %

max and min.

transmission

data/restraints/params

GoF on F²

94.4

0.8429, 0.7271

93.5

0.8372, 0.6874

99.6

0.9886, 0.8561

99.8

0.9528, 0.8897

7569/3/455

1.031

15968/168/946

1.036

12312/0/785

0.930

6254/234/721

1.024

final R indices

R₁) 0.0535,

wR₂) 0.1404

R₁) 0.0725,

wR₂) 0.1606

0.682 and -0.412

R₁) 0.0739,

wR₂) 0.1882

R₁) 0.1504,

wR₂) 0.2456

0.674 and -0.766

R₁) 0.0759,

wR₂) 0.1558

R₁) 0.1997,

wR₂) 0.1895

0.582 and -0.567

R₁) 0.0806,

wR₂) 0.1621

R₁) 0.1555,

wR₂) 0.1897

0.749 and -0.664

[I > 2σ(I)]

R indices (all data)

largest diff. peak

and hole, e/Å³

RMS diff

0.075

0.097

0.085

0.075

density, e/Å³

9

15990 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

achieved utilizing direct (or in some cases Patterson) methods followed

by Fourier synthesis. Hydrogen atoms were added at idealized positions,

constrained to ride on the atom to which they are bonded, and were

given thermal parameters equal to 1.2 or 1.5 times U_isoof that bonded

atom. Empirical absorption and decay corrections were applied using

the program SADABS.⁴⁶Scattering factors and anomalous dispersion

were taken from International Tables (Volume C, Tables 4.2.6.8 and

6.1.1.4.).

[FeTC₆TPP(1-MeIm)₂]Cl. A dark blue block of FeN₄C₆₀H₅₂‚

2(N₂C₄H₆)‚(Cl)‚2(CD₂Cl₂) was crystallized from methylene chloride-

d₂/dodecane. The unit cell contains 4 porphyrin molecules that occupy

4h positions, 8 methylene chloride molecules that sit on general positions

around the 1h position, and 4 chloride counterions, which sit on general

positions around 4h. Due to the symmetry found in the molecule, the

ligands are 2-fold disordered. They were modeled in the same way as

in the case of perp-[FeOMTPP(1-MeIm)₂]Cl. The tetra-â,â′-tetra-

methylene substituents (namely, C8, C9, and C10) on â-carbons were

disordered between two sites due to thermal motion. The population

of each part was refined to 0.83:0.17. The methylene chloride molecule

is disordered between two sites. As was already mentioned, the CD₂-

Cl₂sits on a general position. In I4h₁/a there are 16 general positions.

However, in a given unit cell CD₂Cl₂molecules occupy only 8 of them

and in a different unit cell they occupy different 8 positions, giving on

average all 16 positions occupied with 0.5 occupancy. These two sites

are related by an inversion center. The chloride anion was disordered

paral-[FeOMTPP(1-MeIm)₂]Cl. A purple block of FeN₄C₅₂H₄₄‚

2(N₂C₄H₆)‚(Cl)‚(CD₂Cl₂) was crystallized from methylene chloride-

d₂/dodecane. The asymmetric unit contains one porphyrin molecule,

one solvent (CD₂Cl₂), and chloride as a counterion. All molecules are

on the general positions. Both solvent and chloride were refined by

splitting them into two pieces. The population of each part was refined

to 0.85:0.15 and 0.77:0.23 for CD₂Cl₂and chloride, respectively. Solvent

disorder is due to a solvent rocking motion.

perp-[FeOMTPP(1-MeIm)₂]Cl. A dark red tetrahedron of FeN₄-

C₅₂H₄₄‚2(N₂C₄H₆)‚(Cl)‚2.43(CDCl₃) was crystallized from chloroform-

d/cyclohexane. The unit cell of perp-[FeOMTPP(1-MeIm)₂]Cl contains

12 porphyrin molecules that occupy 4h positions. After completing the

initial structure solution, it was found that 25% of the cell volume was

filled with disordered solvent. First, solvent was modeled as discrete

molecules. There were 32 chloroform molecules that occupy two

different C₃positions, and 12 chloride ions, which sit on C₃positions.

1

between 4 sites with each having /₄occupancy.

A:[FeOMTPP(4-Me₂NPy)₂]Cl. A dark red irregular block of

FeN₄C₅₂H₄₄‚2(N₂C₇H₁₀)‚(Cl)‚4(CD₂Cl₂) was crystallized from methyl-

ene chloride-d₂/dodecane. The porphyrin molecule as well as the

chloride anion sits on the 2-fold axis, and solvent molecules (CD₂Cl₂)

are on general positions. That is why the asymmetric unit contains only

half of the porphyrin molecule, 2 solvent molecules, and half of the

chloride anion for charge balance. Both methylene chloride molecules

are disordered between two sites (relative population is 0.5) due to a

rocking motion.

3

There are 16 C₃special positions in the I4h3d group, but only /₄of

them are occupied with chloride anion, giving 12 chlorides, which

balances the charge of 12 porphyrins. Chloroform molecules and

chlorides occupy distinct channels in the crystal; therefore they were

highly disordered. Analysis of solvent voids using Platon⁴⁷gave a

volume of 4376.1 Å³/cell. From this point on, atoms in the solvent

region including counterion (Cl^-) were removed and the solvent region

was refined as a diffuse contribution without specific atom positions

using the Platon module SQUEEZE.⁴⁸Four voids with volume of

1085-1086 Å³were found in the unit cell. Each void contained 477-

479 electrons, giving a total of 1913 electrons/cell. The given electron

count and volume can be accounted for by 12 Cl^-and 29.2 CDCl₃per

unit cell. While not part of the atom list, these are included in the

formulas, F000, density, and absorption coefficient. An improvement

was observed in all refinement parameters and indices except GoF

which increased by 0.2.

B:[FeOMTPP(4-Me₂NPy)₂]Cl. A dark red distorted parallelepiped

of FeN₄C₅₂H₄₄‚2(N₂C₇H₁₀)‚(Cl)‚4(CDCl₃) was crystallized from chlo-

roform-d/cyclohexane. Many crystals were tried but all of them were

nonmerohedral twins. Data were still acquired. Only the major

component of the data was integrated, using GEMINI Twinning

Solution Program Suite.⁴⁹Overlaps were ignored. The asymmetric unit

contains one porphyrin molecule, 4 solvent molecules, and the chloride

anion. All molecules occupy general positions. Three of the CDCl₃

molecules form hydrogen bonds to the chloride anion. Three out of

four CDCl₃molecules are disordered between two sites with equal

population and the same coordinates and anisotropic parameters for

carbon atoms. This disorder is due to rotational motion of the CDCl₃

molecule. The fourth CDCl₃molecule is disordered between two sites

with equal population and the same coordinates and anisotropic

parameters for all Cl atoms. This disorder is due to an “umbrella-in-

the-wind” motion of the CDCl₃molecule.

As was already mentioned, the porphyrin molecules occupy 4h

1

positions. Therefore only

/ of the porphyrin is present in the

4

asymmetric unit. Due to the symmetry of the molecule, the 1-meth-

ylimidazole (1-MeIm) ligands are 2-fold disordered. Each of them was

modeled using two parts: one contained three nitrogens in positions

1, 3, 4 (numbering starts at the ligated nitrogen) and two methyl groups

attached to nitrogens in positions 3 and 4. The second molecule had

only one nitrogen in position 1 and no methyl group. Both parts of the

1-MeIm molecule were assigned half occupancy, giving on average

one “normal” 1-MeIm molecule. All distances in 1-MeIm molecules

were fixed with appropriate values for ordered 1-MeIm (data taken

from the structure for paral-[FeOMTPP(1-MeIm)₂]Cl) and the coor-

dinates and anisotropic parameters for N2 and N4 (nitrogens that are

coordinated to iron) of the axial ligand were forced to be the same.

C:[FeOMTPP(2-MeHIm)₂]Cl. A dark purple plate of FeN₄C₅₂H₄₄‚

2(N₂C₄H₆)‚(Cl)‚2(CDCl₃)‚(C₆H₁₂) was crystallized from chloroform-

d/cyclohexane. Empirical absorption and decay corrections were applied

using the program SADABS.⁴⁶Following parameters were obtained:

g ) 0.4739, and T_min/T_max) 0.883598. The g value does not seem

reasonable and indicates overcorrection of the data and the T_min/T_max

ratio does not agree well with the one predicted based upon crystal

dimension and absorption parameters of the atoms (see Table 1);

therefore uncorrected data were used for crystal refinement.

The asymmetric unit contains one porphyrin molecule, one chloride,

two chloroforms, and a cyclohexane molecule. All molecules occupy

general positions. One of the solvent molecules (C600) is disordered

between two sites due to rotational motion around its carbon. Therefore

the coordinates and anisotropic parameters of carbon atoms from the

two parts were fixed to be the same. The population was refined to

0.62:0.38 (C600:C700). All other solvent molecules are relatively well

ordered. There are hydrogen bonds between the chloride and N1 of

the axial ligands and carbon atoms of chloroform molecules.

[FeOETPP(1-MeIm)₂]Cl. A dark purple block of FeN₄C₆₀H₆₀‚

2(N₂C₄H₆)‚(Cl)‚2(CDCl₃)‚(C₆H₁₂) was crystallized from chloroform-

d/cyclohexane in the course of 10 days. The asymmetric unit contains

one porphyrin, one chloride, a cyclohexane, and two chloroform

molecules. All of them occupy general positions. Distances and angles

in cyclohexane were fixed to idealize values. There is no disorder

present.

D:[FeOMTPP(2-MeHIm)₂]Cl. A dark blue parallelepiped of

FeN₄C₅₂H₄₄‚2(N₂C₄H₆)‚(Cl)‚3(CD₂Cl₂) was crystallized from methylene

(45) Bruker (2002) SHELXTL Reference Manual Version 6.0, Bruker AXS Inc.,

Madison, WI.

(46) Sheldrick, G. SADABS 2.3, 2002.

(47) Spek, A. L. Acta Crystallogr. 1990, A46, C-34.

(48) Van der Sluis, P.; Spek, A. L. Acta Crystallogr. 1990, A46, 194-201.

(49) Bruker (1999) GEMINI Twinning Solution Program Suite Version 1.0,

Bruker AXS Inc., Madison, WI.

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15991

A R T I C L E S

Yatsunyk et al.

chloride-d₂/dodecane. The asymmetric unit contains one porphyrin

molecule, three solvent (CD₂Cl₂) molecules, and chloride as a coun-

terion. All molecules are on general positions. There is no disorder

present in this crystal. There are hydrogen bonds between the chloride

and the H atom attached to N1 of the axial ligands and the D atoms

attached to carbon atoms of methylene chloride molecules.

Results and Discussion

[FeOMTPP(L)₂]Cl with 1-methylimidazole, 4-(dimethylami-

no)pyridine, and 2-methylimidazole were each obtained in two

different crystalline forms, from methylene chloride/dodecane

and chloroform/cyclohexane solvent systems. In addition, [FeO-

ETPP(1-MeIm)₂]Cl and [FeTC₆TPP(1-MeIm)₂]Cl were each

obtained in one crystalline form from chloroform-d/cyclohexane

and methylene chloride-d₂/dodecane, respectively. Atomic

coordinates, complete bond length and angles table, anisotropic

thermal parameters, hydrogen coordinates and complete torsion

angles for all complexes in this study are listed in Tables S1-

S40 in the Supporting Information.

paral-[FeOMTPP(1-MeIm)₂]Cl. The molecular structure of

paral-[FeOMTPP(1-MeIm)₂]Cl together with the numbering

scheme for crystallographically unique atoms is displayed in

the ORTEP diagram of Figure 1. The molecule is nonplanar

and adopts an almost purely saddled conformation with axial

ligands in near parallel planes. This is evident from Figures 1

and 2 as well as from the linear display shown in Figure S1 of

the Supporting Information. Figure 2 displays the deviation of

all the atoms from the mean porphyrin plane together with the

arrangement of the axial ligands. The average deviations of the

pyrrole â-Cs (1.05 Å for two opposite pyrrole rings and 0.96 Å

for the other pair) as well as the average deviations of the meso-

Cs ((0.01 Å) from the 25-atom mean porphyrin plane are

consistent with the pure saddled conformation of the porphyrin

core.

The saddled porphyrin core together with the peripheral

substituents form two mutually perpendicular pockets, one above

and one below the porphyrin mean plane. They are expected to

orient two axial ligands perpendicular to each other. However,

the actual dihedral angle between the planes of the axial ligands

in paral-[FeOMTPP(1-MeIm)₂]Cl is 19.5°, far from being

perpendicular. This is the unique feature of this structure which

is, to our knowledge, the only example of a strongly saddled

porphyrin core with nearly parallel axial ligand arrangement.

Both axial ligands are oriented above the N1-Fe-N3 vector

(Figure 1) with ligand 1, L1, (having N5 and N6) being in

“correct” position (in the cavity formed by the porphyrin core

and peripheral substituents) and ligand 2, L2, (having N7 and

N8) in nonoptimal, “wrong” orientation (almost perpendicular

to the porphyrin cavity). Despite the “wrong” orientation, L2

is closer to the N1-Fe-N3 vector than is L1: the projections

of the two imidazole ligand planes onto the 25-atom mean

porphyrin plane makes angles of -6.9 and 12.6° to the same

N1-Fe-N3 vector for L2 and L1, respectively. Molecular

mechanics calculations on [CoOETPP(L)₂]⁺(where L is 1-MeIm

or 1-PhIm)⁵⁰have shown that constraining the plane of one axial

ligand to be 90° to the cavity formed by the porphyrin

macrocycle increased the energy of the molecule by 72-79 kJ/

mol compared to the energy minimized structure; this value

Figure 1. (a) ORTEP diagram of the porphyrin macrocycle of paral-

[FeOMTPP(1-MeIm)₂]Cl with the numbering scheme for the unique atoms

in the porphyrin core. Near-parallel orientation of the axial ligands can be

seen clearly. (b) ORTEP plot showing numbering scheme and arrangement

of axial ligands. Both methyl groups are above N3 of the porphyrin core.

Thermal ellipsoids are shown at 50% probability. Hydrogen atoms have

been omitted for clarity.

complexes that are not forced to have as large a saddled

distortion, as shown by some DFT calculations on [FeOMTPP-

(L)₂]⁺and [FeOETPP(L)₂]⁺complexes discussed below.

The question is, how, geometrically, does the purely saddled

structure accommodate axial ligands in near-parallel planes?

From Figure 2 one can see uneven deviations of the â-pyrrole

carbons. One pair of opposite pyrrole rings deviates more from

the mean porphyrin plane than does the other pair. The average

deviation of the â-C is 0.96 and 1.05 Å for the first and the

second pair, respectively, creating a difference of 0.09 Å. Both

axial ligands are oriented along the N1-Fe-N3 axis with those

two pyrrole rings (N1-C1-C2-C3-C4 and N3-C11-C12-

C13-C14) having smaller deviation from planarity. In addition,

N1, N3, and Fe are not in the mean porphyrin plane but slightly

out of it in the direction opposite to the side having the

nonoptimally oriented ligand, L2 (the deviation for the nitrogens

is -0.15 Å and for Fe is -0.07 Å). On the other hand, N2 and

N4 are almost in the porphyrin mean plane. These, together

+

should be considerably smaller for analogous OMTPPML₂

(50) Medforth, C. J.; Muzzi, C. M.; Shea, K. M.; Smith, K. M.; Abraham, R.

J.; Jia, S.; Shelnutt, J. A. J. Chem. Soc., Perkin Trans. 2 1997, 833-837.

9

15992 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

(1-MeIm)₂]Cl with a nonplanar, saddled porphyrin core and

nearly parallel axial ligands is the first of its kind to be described

in the literature.

The average Fe-N_Pdistance in paral-[FeOMTPP(1-MeIm)₂]-

Cl is 1.990(2) Å. It is slightly longer than the same distances

in other porphyrins in this study (Table 2). The interesting fact

is that two adjacent Fe-N_Pdistances, Fe-N1 and Fe-N2, are

similar to each other (1.9783(18) Å and 1.9788(17) Å) and

shorter than the other pair (1.9886(17) Å and 2.0016(17) Å),

Fe-N3 and Fe-N4, meaning that the Fe atom is not in the

center of the porphyrin. Such arrangement seems to be

inconsistent with the orientation of the axial ligands above and

below the N1-Fe-N3 vector: we would expect Fe-N1 and

Fe-N3 bonds that are almost eclipsed with the axial ligand

planes, not Fe-N3 and Fe-N4 bonds, to be longer. However,

similar situations, where the Fe(III) atom is not in the center of

the porphyrin core, have been found for other LS Fe(III)

porphyrinates.^26,51The average Fe-N_Pdistance in [FeTMP(1-

MeIm)₂]ClO₄of 1.995(3) Å is longer than the same distance in

any of the 1-methylimidazole complexes of this study. This is

due to the planarity of the porphyrin core in the TMP case.

Again, it is commonly observed that a planar porphyrin core

correlates with longer Fe-N_Pdistance.⁵⁰

Figure 2. Formal diagram of paral-[FeOMTPP(1-MeIm)₂]Cl showing the

displacement of the atoms in units of 0.01 Å from the mean plane of the

25-atom core. The orientations of the axial ligands with the closest Fe-N_P

vector and selected bond angles and lengths are also shown.

perp-[FeOMTPP(1-MeIm)₂]Cl. The molecular structure of

perp-[FeOMTPP(1-MeIm)₂]Cl is displayed in Figure 3. Both

the perpendicular orientation of the axial ligands and the saddled

conformation of the porphyrin core are obvious. The deviation

of each unique atom in the porphyrin core from the 25-atom

mean plane, together with the arrangement of axial ligands and

typical bond lengths and angles are shown in Figure 4. The

molecule adopts a saddled conformation with some ruffling

admixture. The ruffling component can be seen in the deviation

of both the meso-Cs and the â-Cs from the porphyrin mean

plane. The positions of two adjacent â-C are alternately

displaced by (0.95 and (0.99 Å from the 25-atom mean plane,

and the meso-Cs lie (0.10 Å out of this plane. An unexpectedly

large angle between the axial ligand plane and the closest N_P-

Fe-N_Paxis (29°) is observed in this structure, as shown in

Figure 4. This large angle is likely responsible for the ruffling

component of the core geometry.

with one longer Fe-N_axdistance (2.0155(19) Å for the

nonoptimally oriented ligand vs 1.9747(19) Å for the “correctly”

oriented ligand) provide the room for two axial ligands along

the N1-Fe-N3 vector and the “parallel” (19.5°) orientation to

be possible. The axial ligands are tilted with respect to the mean

porphyrin plane: the dihedral angles between each imidazole

ligand and the porphyrin mean plane are 80.9 and 86.8° for L1

and L2, respectively.

As commonly found in saddled octaalkyltetraphenylporphy-

rins,³²the phenyl rings rotate toward the porphyrin plane to

minimize unfavorable contacts with the â substituents on the

pyrrole rings. The average dihedral angles of the phenyl rings

with the macrocycle plane are 45.5°, 46.0°, 50.3°, and 46.3°.

This correlates with the degree of saddled distortion in the

molecule: the steeper saddles result in more acute dihedral

angles for the phenyl rings.³²The average bond length between

the meso-C and phenyl rings is 1.492(3) Å.

Because the Fe atom in the crystal of perp-[FeOMTPP(1-

Other examples of Fe(III) porphyrinates with parallel imi-

dazole ligands include [FeTMP(1-MeIm)₂]ClO₄²⁴and [FeTMP-

(5-MeHIm)₂]ClO₄.²⁰There are two independent molecules with

planar porphyrin cores and parallel ligand orientations in the

asymmetric units of each structure. In the structure of [FeTMP-

(1-MeIm)₂]ClO₄the parallel imidazole planes (∆æ ) 0°) form

dihedral angles of 23° and 41° to the closest N_P-Fe-N_Paxis

for molecules 1 and 2, respectively.²⁴The imidazole planes do

not lie strictly along the normal to the porphyrin core but form

angles of 83.7° and 88.8° to the mean porphyrin plane.²⁴In

comparison, in the molecular structure of [FeTMP(5-MeHIm)₂]-

ClO₄²⁰the axial ligand planes are not strictly parallel; dihedral

angles between the two axial ligands, ∆æ, are 26° and 30° for

molecules 1 and 2, respectively. The imidazole planes are tilted

somewhat with respect to the mean porphyrin plane forming

dihedral angles of 86.0° and 88.3° in molecule 1 and 83.2° and

86.6° in molecule 2. Near-parallel orientation of the imidazole

MeIm)₂]Cl occupies a 4h position, the asymmetric unit contains

1

only

/ of the porphyrin molecule, which requires 2-fold

4

disorder of the axial ligands and an exact 90° angle between

their planes. The axial ligands were modeled by splitting them

into two parts and constraining only the nitrogens coordinated

to Fe to have the same anisotropic parameters and coordinates

(Experimental Section). After final refinement, the angle

between the projection of the two parts of the axial ligand and

the closest N_P-Fe-N_Pvector is 21.6° and 36.9° for the N4-

C8-C9 and N2-C6-N3 parts, respectively. In other words,

the measured angle between the two parts of the two imidazole

ligands is 15.3°. This may mean that the barrier to axial ligand

rotation is low and the ligand adopts slightly different positions

in different molecules.

As was shown for saddled metalloporphyrins with five-

membered aromatic axial ligands using molecular mechanics

calculations with a force-field that has been applied with

considerable success to the prediction of crystal structure for

many highly nonplanar porphyrins,⁵⁰axial ligand planes are

24

ligands in the structures of [FeTMP(1-MeIm)₂]ClO₄and

20

[FeTMP(5-MeHIm)₂]ClO₄is accompanied by nearly planar

porphyrin cores. Therefore, the structure of paral-[FeOMTPP-

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15993

A R T I C L E S

Yatsunyk et al.

Table 2. Comparison of Structural Parameters for Complexes of This Study with Those from Related Complexes

angle æ

av dihedral

angles of

phenyls,

compound

Fe−Np, Å

Fe−N , Å

av∆|C_m|, Å

av∆|C |, Å

between Np−Fe−Np

axis and

dihedral

angle, ∆æ,

deg

ax

â

ligand planes, deg

deg

ref

1.975(2)

2.016(2)

-0.96

+1.05

pral-[FeOMTPP(1-MeIm)₂]Cl‚CD₂Cl₂

1.990(2)

(0.01

(0.10

(0.03

(0.26

(0.28

(0.42

(0.07

(0.13

(0.21

(0.09

(0.40

(0.51

(0.72

-12.6; 6.9

-29.3; 60.7

+9.6, +82.7

-15.3; 74.7

-9.0; 61.0

-0.8; 78.0

-1.0; 87.5

-11.2; 69.5

-13.1; 71.0

-14; 76

19.5

90.0

73.1

90.0

70.0

78.8

88.5

80.7

82.1

90

47.0

TW

(0.99

(0.95

perp-[FeOMTPP(1-MeIm)₂]Cl‚2.43CDCl₃1.969(7)

1.982(10)

46.3

40.0

71.8

37.4

57.5

55.8

49.5

53.9

42

TW

32

1.976(3)

1.978(3)

(1.22

(1.25

[FeOETPP(1-MeIm)₂]Cl‚2CDCl₃‚C₆H₁₂

[FeTC₆TPP(1-MeIm)₂]Cl‚CD₂Cl₂

[FeOETPP(4-Me₂NPy)₂]Cl‚CDCl₃

A: [FeOMTPP(4-Me₂NPy)₂]Cl‚4CD₂Cl₂

B: [FeOMTPP(4-Me₂NPy)₂]Cl‚4CDCl₃

D: [FeOMTPP(2-MeHIm)₂]Cl‚3CD₂Cl₂

C: [FeOMTPP(2-MeHIm)₂]Cl‚2CDCl₃

[FeOETPP(2-MeIm)₂]⁺(SbF₆^-, Cl^-)

[FeTPP(2-MeHIm)₂]ClO₄

1.970(7)

2.005(3)

1.951(5)

1.981(2)

1.983(3)

1.979(7)

1.977(4)

1.974(9)

1.971(4)

1.964(10)

1.937(12)

(0.35

(0.65

2.005(8)

1.984(5)

2.099(12)

(1.34

(1.11

2.018(3)

2.021(3)

(0.61

(0.90

TW

32

2.000(4)

2.003(4)

(0.93

(0.88

2.007(7)

2.010(7)

(0.97

(1.08

2.006(5)

2.032(5)

(0.86

(1.04

(1.20

(1.23

2.09(2)

2.015(4)

2.010(4)

(0.17

(0.20

-32; 57

89

76

15

1.989(4)

1.978(4)

[FeTMP(4-Me₂NPy)₂]ClO₄

-37; 42

79

24

2.004(5)

(0.23

(0.24

[FeTMP(1,2-Me₂Im)₂]ClO₄

-45; 45

90

87

26

1.985(6)

1.979(6)

1.988(6)

1.973(6)

perp-[FeTMP(5-MeHIm)₂]ClO₄

paral-[FeTMP(5-MeHIm)₂]ClO₄

1.957(6); 1.973(6)

(0.32

(0.13

-30; 46

76

82.9

20

1.983(4)

1.981(5)

1.978(6); 1.961(5)

1.980(5); 1.985(5)

(0.11

(0.05

(0.16

(0.07

-10; 20

-14; 12

30

26

83.2

85.2

20

24

[FeTMP(1-MeIm)₂]ClO₄1

[FeTMP(1-MeIm)₂]ClO₄2

1.988(20) 1.975(3)

1.987(1) 1.965(3)

(0.01

(0.08

(0.02

(0.07

23

41

0

81

expected to be almost eclipsed with the closest N_P-Fe-N_P

vector (the minimum energy angle is 2-3°). However, this does

not hold true in the case of perp-[FeOMTPP(1-MeIm)₂]Cl where

the dihedral angle between the averaged imidazole planes and

the closest N_P-Fe-N_Pvector is much larger (29.3°). Due to

the symmetry found in this crystal, both ligands lie along the

normal to the porphyrin mean plane (however, some off-axis

positioning could be possible if it is obscured by the disorder).

Both the average angle between the phenyl ring and the mean

porphyrin plane and the distance from the meso-C to the phenyl

ring are close to the corresponding values in paral-[FeOMTPP-

(1-MeIm)₂]Cl (46.3° vs 47.0°; and 1.470(8) vs 1.492(3) Å for

perp- and paral-[FeOMTPP(1-MeIm)₂]Cl, respectively).

crystallographically unique atoms is displayed in Figure 5. The

molecule is nonplanar and adopts an almost purely saddled

conformation with axial ligands in near perpendicular planes.

This is evident in Figures 5 and 6 as well as in the linear display

shown in Figure S1 of the Supporting Information. Figure 6

displays the deviation of all the atoms from the mean porphyrin

plane together with the arrangement of the axial ligands. The

average deviations of the adjacent â-Cs ((1.22 Å and (1.25

Å) as well as the average deviations of the meso-Cs ((0.03 Å)

from the 25-atom mean porphyrin plane are consistent with the

pure saddled conformation of the porphyrin core.

The actual dihedral angle between the planes of the axial

ligands in [FeOETPP(1-MeIm)₂]Cl is 73.1°, close to the

minimum angle of 70° observed thus far for iron(III) porphy-

rinates that have “large g_max” EPR spectra.³²The projection of

the two imidazole ligand planes onto the 25-atom mean

porphyrin plane makes angles of 9.6° and 82.7° to the same

N1-Fe-N3 vector. The nitrogens of the porphyrinate ring are

not in the mean plane, but rather N1, N3 are slightly above

(0.10 Å) while the other two are slightly below (-0.09 Å). The

axial ligands deviate insignificantly from the normal to the mean

plane of the porphyrin ring, with L1 (N5, N6) being at a dihedral

The linear deviation of each unique atom from the mean

porphyrin plane in both paral- and perp-[FeOMTPP(1-MeIm)₂]-

Cl structures is shown in Figure S1 in the Supporting Informa-

tion. It is important to note that the two complexes have

extremely similar geometry of the porphyrin cores, regardless

of the striking difference in the axial ligand orientations (close

to parallel vs perpendicular).

[FeOETPP(1-MeIm)₂]Cl. The molecular structure of [FeO-

ETPP(1-MeIm)₂]Cl together with the numbering scheme for

9

15994 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

Figure 3. (a) ORTEP diagram of the porphyrin macrocycle of perp-

[FeOMTPP(1-MeIm)₂]Cl with the numbering scheme for the crystallo-

graphically unique atoms. Thermal ellipsoids are shown at 30% probability.

Perpendicular orientation can be clearly seen. (b) ORTEP plot showing

saddled conformation of the porphyrin core. Hydrogen atoms have been

omitted for clarity.

Figure 5. (a) ORTEP diagram of the porphyrin macrocycle of [FeOETPP-

(1-MeIm)₂]Cl. Close to perpendicular orientation of the axial ligands can

be clearly seen. Methyl groups of 1-methylimidazole ligands are above N2

and N3. (b) ORTEP diagram, side view, of the porphyrin core together

with the numbering scheme for axial ligands. Saddled geometry is observed.

Thermal ellipsoids are shown at 50% probability. Hydrogen atoms have

been omitted for clarity.

The average dihedral angle of the phenyls in [FeOETPP(1-

MeIm)₂]Cl is 40.0° (the individual values are 41.7°, 38.8°, 37.1°,

and 42.3°) and is quite a bit smaller than the 46.3° and 47.0°

angles observed in perp- and paral-[FeOMTPP(1-MeIm)₂]Cl.

This is in accord with the higher saddled distortion of the former

complex. The average value of the bonds between the meso-Cs

and phenyl rings is 1.498(4) Å.

Figure 4. Formal diagram of perp-[FeOMTPP(1-MeIm)₂]Cl showing the

displacement of the atoms in units 0.01 Å, from the mean plane of the

25-atom core. The orientations of the axial ligands with the closest Fe-N_P

vector are also drawn.

angle of 86.68° and L2 (N7, N8) having a dihedral angle of

87.51° to the porphyrin mean plane. The average Fe-N_Pbond

length is 1.970(7) Å, very similar to that for perp-[FeOMTPP-

(1-MeIm)₂]Cl and [FeOETPP(2-MeHIm)₂]⁺but longer than that

for the other OETPP structure, [FeOETPP(4-Me₂NPy)₂]Cl.³²

The average Fe-N_axbond length is 1.977(3) Å, again similar

to that of perp-[FeOMTPP(1-MeIm)₂]Cl and shorter than that

of [FeOETPP(4-Me₂NPy)₂]Cl and [FeOETPP(2-MeHIm)₂]^{+ 32}

(Table 2).

[FeTC₆TPP(1-MeIm)₂]Cl. It should first be noted that this

is the only one of the [FeTC₆TPP(L)₂]Cl complexes that was

crystallized. It turned out that in all other crystallization attempts

the mixture did not produce any crystals but rather turned into

an oil, even though two successful attempts, the (TC₆TPP)FeCl⁵³

and [FeTC₆TPP(1-MeIm)₂]Cl, produced crystals of much better

quality that any other crystals of this research. The molecular

structure and numbering scheme for the crystallographically

unique atoms of [FeTC₆TPP(1-MeIm)₂]Cl are shown in the

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15995

A R T I C L E S

Yatsunyk et al.

Figure 8. Formal diagram of [FeTC₆TPP(1-MeIm)₂]Cl showing the

displacement of the atoms, in units 0.01 Å, from the mean plane of the

25-atom core. The orientations of the axial ligands with the closest Fe-N_P

vector are also drawn. The admixture of saddled and ruffled geometry is

clearly observed. Alternant pyrrole rings are still tipped above and below

the porphyrin mean plane (as expected for the pure saddled conformation)

but the meso-C are displaced above and below the porphyrin mean plane

as well (as expected for the ruffled conformation).

Figure 6. Formal diagram of [FeOETPP(1-MeIm)₂]Cl showing the

displacement of the atoms, in units 0.01 Å, from the mean plane of the

25-atom core. The orientations of the axial ligands with the closest Fe-N_P

vector are also drawn. The nearly pure saddled geometry is clearly observed.

is 11.3°. Again as in the case of perp-[FeOMTPP(1-MeIm)₂]-

Cl this may be due a slight random difference in the axial ligand

arrangement throughout the crystal. The projection of the planes

of the two imidazole parts on the porphyrin mean plane forms

angles of 9.6 and 20.9° to the same N_P-Fe-N_Pvector.

Therefore the average angle is 15.3°.

The deviations of all the porphyrin atoms from the mean

plane, as well as axial ligand orientations and selected bond

lengths and angles are shown in the formal diagram of Figure

8. From Figure 8 and the linear diagram of the porphyrin

deviation from planarity (Figure S1) one can clearly see that

the porphyrin adopts an admixture of ruffled and saddled

conformations. As in the purely saddled conformation, the

pyrrole rings are displaced above and below the porphyrin mean

plane. But as in the ruffled conformation the meso-Cs are no

longer in the porphyrin mean plane but rather are displaced by

(0.26 Å above and below it; the pyrrole rings are twisted

clockwise and counterclockwise, causing a noneven deviation

for adjacent pyrrole â-Cs ((0.42 and (0.65 Å). Using the

program of Shelnutt, available on the Web⁵²(Normal-Coordinate

Structural Decomposition (NSD) method), the nonplanarity of

the porphyrin core can be described in terms of displacements

along the lowest frequency normal coordinates of the porphyrin

macrocycle in order to quantify the contribution from different

types of distortion (saddled, ruffled, etc.). Moreover, the sum

of all the coefficients of the vibrational modes can be used to

compare the degree of nonplanarity between different porphy-

rins: A larger sum of the vibrational coefficients correlates with

a higher degree of nonplanar distortion. There are six out-of-

plane displacements along the lowest frequency vibrational

modes of the porphyrin macrocycle: B_2u(Saddle), B_1u(Ruffle),

A_2u(Dome), E_g(x) (Wave(x)), E_g(y) (Wave(y)), and A_1u-

(Propeller). For all the complexes of this study except paral-

Figure 7. ORTEP diagram of the porphyrin macrocycle of [FeTC₆TPP-

(1-MeIm)₂]Cl. Thermal ellipsoids are shown at 50% probability. Perpen-

dicular orientation of the axial ligands can be clearly seen. Hydrogen atoms

have been omitted for clarity.

ORTEP diagram of Figure 7. According to the symmetry of

the porphyrin molecule that sits on the 4h position, the planes of

the axial ligands are mutually perpendicular. For the same reason

they each lie along the normal to the porphyrin mean plane.

Since only ¹/₄of the molecule is present in the asymmetric unit,

the axial ligands are 2-fold disordered. They were modeled in

the same way as in the case of perp-[FeOMTPP(1-MeIm)₂]Cl

by using two different molecules with half occupancy. Both

parts of the imidazole model were allowed to rotate freely and

only the nitrogens coordinated to iron were constrained to have

the same anisotropic parameters and coordinates. In the final

model the dihedral angle between the two parts of the imidazole

(51) Scheidt, W. R.; Osvath, S. R.; Lee, Y. J. J. Am. Chem. Soc. 1987, 109,

1958-1963.

(52) http://jasheln.unm.edu/jasheln/content/nsd/NSDengine/.

9

15996 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

Table 3. Normal-Coordinate Structural Decomposition (NSD)⁵²of Distortion Modes of the Complexes of This Study

B ,

saddle

B ,

ruffle

A ,

dome

E (x),

wave(x)

E (y),

wave(y)

A ,

propeller

sum

av ∆|C_m|,

av ∆|C |,

ruf/sum %

2u

1u

2u

g

1u

â

compound

Å

-0.96

+1.05

paral-[FeOMTPP(1-MeIm)₂]Cl‚CD₂Cl₂

3.0449

0.0192

0.1793

0.0367

0.0393

0.0314

3.3508

3.2448

3.9949

2.3553

3.3981

3.0262

4.6564

3.6346

3.7717

(0.01

(0.10

(0.03

(0.26

(0.42

(0.07

(0.28

(0.21

(0.13

0.6

9.4

(0.99

(0.95

perp-[FeOMTPP(1-MeIm)₂]Cl‚CDCl₃

[FeOETPP(1-MeIm)₂]Cl‚2CDCl₃‚C₆H₁₂

[FeTC₆TPP(1-MeIm)₂]Cl‚CD₂Cl₂

2.9400

3.7320

1.6073

2.3007

2.7554

3.7289

2.8971

3.1513

0.3035

0.0792

0.7463

1.0067

0.1748

0.8024

0.5964

0.3786

0.0006

0.0360

0.001

0.0000

0.1054

0.0000

0.0593

0.0363

0.0682

0.1035

0.0000

0.0315

0.0000

0.0148

0.0367

0.0661

0.0697

0.0007

0.0108

0.0007

0.0094

0.0200

0.0027

0.0010

0.0245

(1.22

(1.25

2.0

(0.35

(0.65

31.7

29.6

5.8

(0.61

(0.90

A:[FeOMTPP(4-Me₂NPy)₂]Cl‚CD₂Cl₂

B:[FeOMTPP(4-Me₂NPy)₂]Cl‚CDCl₃

[FeOETPP(4-Me₂NPy)₂]Cl‚CDCl₃

C:[FeOMTPP(2-MeIm)₂]Cl‚2CDCl₃

D:[FeOMTPP(2-MeIm)₂]Cl‚3CD₂Cl₂

0.0813

0.0019

0.0494

0.0058

0.0441

(0.93

(0.88

(1.34

(1.11

17.2

16.4

10.0

(0.86

(1.04

(0.97

(1.08

[FeOMTPP(1-MeIm)₂]Cl only two of them are of major

importance: B_2u(Sad) and B_1u(Ruf). The contributions from the

other types of nonplanar distortion are either small or absent.

In the case of paral-[FeOMTPP(1-MeIm)₂]Cl the major con-

tribution to the geometry of the porphyrin core comes from B_2u-

(Saddle) and A_2u(Dome) (the coefficients are 3.0449 and 0.1793,

respectively, see Table 3). This might be due to the near parallel

ligand orientation in this complex. As for the [FeTC₆TPP(1-

MeIm)₂]Cl, the degree of saddling, B_2u, is equal to 1.6073 and

the amount of ruffling, B_1u, is equal to 0.7463. The contribution

from other vibration modes is negligible. From the numbers

obtained the conclusion can be drawn that molecular structure

of [FeTC₆TPP(1-MeIm)₂]Cl consists of saddled and ruffled

components in the approximate ratio 0.68:0.32. This is one of

the few examples of the dodecasubstituted metalloporphyrins

having a substantial degree of ruffling distortion in overall

saddled structure. The other cases are (TC₆TPP)FeCl (38%),⁵³

[FeOMTPP(4-Me₂NPy)₂]Cl (30%), [FeOETPP(4-Me₂NPy)₂]Cl

(17%),³²and [FeOMTPP(4-CNPy)₂]ClO₄(17%).⁵⁴Even though

the contribution from the ruffled component in the molecular

structure of [FeTC₆TPP(1-MeIm)₂]Cl is the largest among the

complexes in this study (Table 3), the angle between the

imidazole ligand planes and the nearest N_P-Fe-N_Paxis (æ )

15.3°) is not the largest. When the sum of NSD parameters for

[FeTC₆TPP(1-MeIm)₂]Cl is compared to the same numbers for

both the [FeOMTPP(1-MeIm)₂]Cl and [FeOETPP(1-MeIm)₂]-

Cl structures, one can clearly see that the former is the most

planar of the three (Table 3). The same is true for the five-

coordinate Fe(III) chlorides of (TC₆TPP)FeCl, (OMTPP)FeCl,

and (OETPP)FeCl.⁵³

angle is 15.3°, which is reasonably close to that calculated

(around 4° smaller) for the admixture of saddled and ruffled

conformation of the porphyrin core observed.

The Fe-N_Pdistance in [FeTC₆TPP(1-MeIM)₂]⁺is 2.005(3)

Å, the longest among Fe-N_Pdistances for nonplanar bis-

imidazole complexes with OMTPP and OETPP porphyrin cores

of this study (Table 2). For the two crystalline forms of

[FeOMTPP(1-MeIm)₂]Cl and for [FeOETPP(1-MeIm)₂]Cl the

average Fe-N_Pdistances are 1.969(7), 1.990(2), and 1.970(7)

Å, respectively. This is in accord with molecular mechanics

calculations involving [CoOETPP(L)₂]⁺and [CoT^tBuP(L)₂]⁺

with various axial ligands,⁵⁰where shorter Co(III)-N_Pdistances

are normally observed for more distorted porphyrins. The

average Fe-N_axbond is 1.984(4) Å and is similar to Fe-N_ax

distances in many other nonplanar porphyrins with the same

type of axial ligands (Table 2).

[FeOMTPP(4-Me₂NPy)₂]Cl. The molecular structures of the

two complexes are shown in the ORTEP diagrams for [FeOMT-

PP(4-Me₂NPy)₂]Cl, molecule A (Figure 9), and molecule B

(Figure S2) together with the numbering scheme for crystallo-

graphically unique atoms. Figure 10 shows the perpendicular

displacement of the crystallographically unique atoms from the

25-atom mean plane (in units of 0.01 Å) and the arrangement

of the axial ligands. Both porphyrin molecules are nonplanar

and adopt predominantly saddled conformations with a similar

degree of nonplanarity. The major difference in the core

geometry of A and B is the amount of ruffling present in their

molecular structures (29.6% in the case of A and 5.8% for B

molecules, estimated using the coefficients of the lowest

frequency vibrational modes⁵²(Table 3)). The average deviations

of adjacent â-C are (0.61, (0.90 Å for molecule A and (0.88,

(0.93 Å for B (Table 2). One can see that the pyrrole rings in

A are twisted, causing strongly uneven deviation of the adjacent

â-Cs, which is characteristic of a ruffled geometry. Another

indication of the presence of a ruffling component is the

deviation of the meso-carbons from the mean plane. While in

A the meso-C are (0.36 Å above and below the porphyrin mean

plane, B has its meso-C almost in the porphyrin mean plane

According to molecular mechanics calculations on [CoO-

ETPP(1-MeIm)₂]⁺,⁵⁰the angle of minimum energy between the

projection of the axial ligand plane and closest N_P-Fe-N_P

vector is 2-3° for the saddled and 45° for the ruffled

conformation for five-membered aromatic sterically nonhindered

axial ligands. In the structure of [FeTC₆TPP(1-MeIm)₂]Cl the

(53) Yatsunyk L. A., Ph.D. Dissertation. University of Arizona, 2003.

(54) Yatsunyk, L. A.; Walker, F. A. Inorg. Chem. 2003, 42. In press.

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15997

A R T I C L E S

Yatsunyk et al.

Figure 9. (a) ORTEP diagram for [FeOMTPP(4-Me₂NPy)₂]Cl, molecule

A. Close to perpendicular orientation of the axial ligands can be clearly

seen. (b) The ORTEP diagram, showing the numbering scheme and

arrangement of the axial ligands. An admixture of saddled and ruffled

geometry can be seen. Thermal ellipsoids are shown at 50% probability.

Hydrogen atoms have been omitted for clarity.

Figure 10. Formal diagram of the porphyrinate core in [FeOMTPP(4-

Me₂NPy)₂]Cl for molecules A and B showing the displacement of the atoms,

in units 0.01 Å, from the mean plane of the 25-atom core. The orientations

of the axial ligands with the closest Fe-N_Pvector are also drawn.

bis-pyridine complexes,²⁵as well as the complex with the

sterically hindered 1,2-dimethylimidazole ligand.²⁶In compari-

son, [FeOEP(4-Me₂NPy)₂]ClO₄is essentially planar. Again,

planar geometries of the FeOEP core are observed for complexes

with various axial ligands and may be a property of that

porphyrin core itself.⁵⁵

(the deviation is only (0.05 Å). Both the twisting of the pyrrole

rings and the alternation in the displacements of the meso-Cs

of the porphyrin ring are indications of significant ruffling

(29.6%) in the overall saddled structure of A. A similar

molecular structure is observed for [FeOETPP(4-Me₂NPy)₂]Cl

reported earlier: saddled with some ruffling component.³²The

average displacements of adjacent â-Cs are (1.13 Å and (1.34

Å and meso-Cs are (0.28 Å above and below the porphyrin

mean plane (Table 2).³²In general, the latter complex is more

distorted from planarity compared to both A and B [FeOMTPP-

(4-Me₂NPy)₂]Cl molecules due to the ethyl substituents on the

pyrrole â positions, but it has a smaller ruffling component than

A, yet larger than B.

The ORTEP diagrams show that the axial 4-Me₂NPy ligand

planes are nearly perpendicular to each other in both structures

of [FeOMTPP(4-Me₂NPy)₂]Cl (Figures 9 and S2). The actual

dihedral angles between the axial ligand planes are 78.8° for

molecule A and 88.5° for B. In the case of A, the dihedral angle

between the axial ligands differs significantly from the expected

90° value. For the saddled [FeOETPP(4-Me₂NPy)₂]Cl com-

plex,³²perpendicular orientation of the axial ligands was also

expected. However, the dihedral angle is 70°, the smallest among

the dihedral angles observed at that time for complexes with

“large g_max” EPR signals.³²Significant deviation of axial ligand

Different geometries of the porphyrin core are observed for

[FeTMP(4-Me₂NPy)₂]ClO₄and [FeOEP(4-Me₂NPy)₂]ClO₄.²⁴

The [FeTMP(4-Me₂NPy)₂]ClO₄complex is strongly ruffled with

an average displacement of the meso-C equal to (0.51(5) Å

and the axial ligands in perpendicular planes. The same

geometry of the FeTMP core is observed in the cases of other

(55) Geiger, D. K.; Lee, Y. J.; Scheidt, W. R. J. Am. Chem. Soc. 1984, 106,

6339-6343.

9

15998 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

planes from the predicted perpendicular orientation is also

observed in the structure of the ruffled complex [FeTMP(4-

Me₂NPy)₂]ClO₄(79°).²⁴In comparison, for the case of planar

[FeOEP(4-Me₂NPy)₂]ClO₄, parallel orientation of the axial

ligands is observed.²⁴

structures of the complexes that could be forcing the particular

dihedral angles observed.

The angles between the planes of the phenyl rings and the

mean porphyrin plane are 57.5°, 55.1°, and 57.3°, 54.4°, 54.8°,

56.6° for the A and B molecules, respectively. They are smaller

compared to the same angles in [FeTMP(4-Me₂NPy)₂]⁺(78.7°

average),²⁴and consistent with the predominantly saddled

geometry of the present complexes. On the other hand, in planar

or ruffled porphyrins the orientation of the phenyl rings is close

to perpendicular with respect to the porphyrin core.

According to molecular mechanics calculations involving

[CoOETPP(L)₂]⁺,⁵⁰the expected angle between the projection

of the six-membered aromatic axial ligands (i.e., pyridines) and

the closest N_P-Fe-N_Pvector of the saddled porphyrin core is

10° due to repulsion between the 2,6-H on the pyridine ligands

and the nitrogens of the porphyrin. In the complexes under study,

the projection of the two axial ligand planes onto the porphyrin

mean plane form 0.8°, 12.0° and 1.0°, 2.5° angles to the closest

N_P-Fe-N_Pvector for molecules A and B, respectively. In the

molecular structure of A, one of the axial ligands has close to

the predicted orientation (æ₁) 12°) and the second is essentially

eclipsed with the closest N_P-Fe-N_Pvector (æ₂) 0.8°).

However, the measured contact distances between the 2,6-H

on the pyridine and the closest nitrogens in A are similar for

both axial ligands (2.397 and 2.382 Å), as are the Fe-N_axbond

lengths (2.018(3) and 2.021(3) Å). Even though one ligand is

nearly eclipsed with the N_P-Fe-N_Paxis, the geometry of the

complex allows it to avoid repulsion by alternating the porphyrin

nitrogen atoms above and below the porphyrin mean plane by

(0.11 Å. In the case of B both axial ligand planes are essentially

eclipsed with the closest N_P-Fe-N_Pvector. This still results

in long enough distances between the 2,6-H of pyridine and

the nitrogen atoms of the porphyrin ring (2.386, 2.355, 2.341,

and 2.408 Å) to allow them to avoid steric repulsion. This is in

good agreement with the molecular mechanics calculation done

on [CoOETPP(Py)₂]⁺that showed only a very small increase

in the calculated energy of the complex when the structure was

energy-minimized with one ligand constrained to lie exactly

parallel to the Co-N_Pbond (∆E° ) 0.2 kJ/mol).⁵⁰

The average Fe-N_Pdistances in A and B are very similar to

each other (1.9813(19) Å and 1.983(3) Å) and to the distance

in [FeOEP(4-Me₂NPy)₂]⁺(1.986(2) Å)²⁴but are much longer

then the same distances in both [FeTMP(4-Me₂NPy)₂]⁺(1.964-

(10) Å)²⁴and [FeOETPP(4-Me₂NPy)₂]⁺(1.951(5) Å).³²This

agrees with the fact that both ruffled (TMP) and highly saddled

(OETPP) porphyrins have shorter Fe-N_Pdistances compared

to the more planar complexes. The average Fe-N_axdistances

in [FeOMTPP(4-Me₂NPy)₂]⁺(molecule A and B) differ sub-

stantially (2.020(3) Å and 2.002(4) Å, respectively). The same

distances in all other complexes studied are shorter: 1.984(5),

2.015(6) Å; 1.989(4), 1.978(4) Å; 1.995(3) Å for [FeOETPP-

(4-Me₂NPy)₂]⁺,³²[FeTMP(4-Me₂NPy)₂]⁺,²⁴and [FeOEP(4-Me₂-

NPy)₂]⁺,²⁴respectively.

In general, the structures of A and B have similar axial ligand

orientation (the dihedral angles between the axial ligand planes

are 78.8° and 88.5°, both close to perpendicular) but strikingly

different porphyrin core geometries (Table 2 and Figure S1).

This is opposite to what is observed in the structure of

[FeOMTPP(1-MeIm)₂]Cl complexes, where the porphyrin cores

have the same type of geometry but the orientation of the axial

ligands is substantially different.

[FeOMTPP(2-MeHIm)₂]Cl. The molecular structures of

[FeOMTPP(2-MeHIm)₂]Cl molecules C and D, together with

the numbering scheme for crystallographically unique atoms

are displayed in Figures S3 and 11, respectively. Figure 12

displays the value of the perpendicular displacements of the

unique atoms, in units of 0.01 Å from the mean plane of the

24-atom porphyrin core for both molecules, together with the

relative orientation of the axial ligands. In both cases (molecule

C and D) the porphyrin molecule is nonplanar and adopts a

strongly saddled conformation with a small admixture of

ruffling. The average deviations of the adjacent â-carbon atoms

from the mean plane are (0.86 Å and (1.04 Å for molecule C

and (0.97 Å and (1.08 Å for D (Table 2). The meso-carbons

are on average (0.21 Å and (0.14 Å above and below the

porphyrin mean plane, for C and D, respectively. The above

data, together with the parameters from NSD calculation (Table

3), indicate that both structures have saddled geometries, but

molecule D is more distorted overall (the sum of all the

coefficients of the vibrational modes is 3.7717, higher than that

for C, 3.6346), yet has a smaller ruffling component (10% vs

16%) in comparison to molecule C. Other complexes with

2-MeHIm and other sterically hindered ligands such as 1,2-

Me₂Im have been studied and reported in the literature.^15,26,32,55

All of them can be divided into three groups: those with

predominantly saddled, those with predominantly ruffled non-

planar core, and those with planar porphyrin core. [FeOETPP-

(2-MeHIm)₂]^{+ 32}and [FeOMTPP(2-MeHIm)₂]Cl (this work),

which each have a small ruffled component in an overall saddled

Different orientations of the axial ligands are observed in

[FeOETPP(4-Me₂NPy)₂]Cl: they form 9° and 29° angles with

respect to the closest N_P-Fe-N_Pvector.³²The fact that this

large angle of 29° occurs despite the presence of mutually

perpendicular pockets (this is true for both saddled and ruffled

geometries) confirms the observation of Medforth et al.⁵⁰that

the potential energy curve for axial ligand rotation is fairly flat.

The dihedral angles between the projection of axial ligand onto

porphyrin mean plane and N_P-Fe-N_Pvector of 37° and 42°

observed in [FeTMP(4-Me₂NPy)₂]ClO₄are typical for a pre-

dominantly ruffled geometry.²⁴

The axial ligand planes in [FeOMTPP(4-Me₂NPy)₂]Cl (mol-

24

ecule A) and [FeOEP(4-Me₂NPy)₂]ClO₄are not tilted but

rather lie along the normal to the porphyrin mean plane as

required by the symmetry present in the molecules (in A the

porphyrin occupies the C₂axis and in [FeOEP(4-Me₂NPy)₂]-

ClO₄the inversion center). In other structures the angles between

the pyridine planes and the core show substantial deviation from

perpendicular arrangement: 88.5 and 86.6°; 88.3 and 82.4°; 90

and 81.4° for [FeOMTPP(4-Me₂NPy)₂]Cl (molecule B), [FeTMP-

(4-Me₂NPy)₂]⁺,²⁴and [FeOETPP(4-Me₂NPy)₂]⁺,³²respectively.

These deviations from orthogonality may be due to crystal

packing forces as has been suggested in previous cases.²⁴

However, while off-axis tilting may in some cases occur because

of crystal packing forces, we find no close contacts in the

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 15999

A R T I C L E S

Yatsunyk et al.

Figure 11. (a) ORTEP diagram and numbering scheme for the macrocycle

of D:[FeOMTPP(2-MeHIm)₂]Cl. Methyl groups are above N2 and N3. (b)

Edge-on view of the complex, showing slight distortion of the porphyrin

core from pure saddled geometry. Thermal ellipsoids are shown at 50%

probability. Hydrogens are omitted for clarity.

structure, belong to the first group. The former complex is more

distorted from planarity overall but has a smaller degree of

ruffling present.³²The C_âof adjacent pyrrole rings in [FeO-

ETPP(2-MeHIm)₂]⁺are alternately displaced by (1.23 Å and

(1.20 Å from the 24-atom mean plane, and the meso-carbons

lie (0.09 Å out of the plane. On the other hand, the porphyrin

cores in the [FeTPP(2-MeHIm)₂]ClO₄¹⁵and [FeTMP(1,2-Me₂-

Figure 12. Formal diagrams of the porphyrinato core in [FeOMTPP(2-

MeHIm)₂]Cl, C and D. All displacements are given in units of 0.01 Å. The

orientations of the axial ligands with the closest Fe-N_Pvector and selected

bond lengths and angles are also shown.

The average dihedral angles of the phenyls of 54° and 50°

for C and D, respectively, are smaller compared to the same

values in [FeTPP(2-MeHIm)₂]ClO₄(76°) and [FeTMP(1,2-Me₂-

Im)₂]ClO₄(87°) and are in good agreement with the earlier

finding that the phenyl dihedral angles of saddled porphyrins

are all smaller than those for ruffled porphyrins.^23,35-38When

predominantly saddled complexes are compared ([FeOMTPP-

(2-MeHIm)₂]⁺(C and D) and [FeOETPP(2-MeHIm)₂]⁺³²), the

dihedral angles of the phenyls decrease in the order C (54°) >

D (50°) > [FeOETPP(2-MeHIm)₂]⁺(42°) and in the same order

the degree of nonplanarity and absolute value of saddled

distortion increases (judged by the B_2ucoefficient): C (2.8971)

< D (3.1513) < OETPP (3.7320). Therefore, the average value

of the dihedral angles of the phenyls can be used as an indication

of the degree of saddledness: the more acute dihedral angle of

the phenyls correlates with the higher degree of saddled

distortion.

26

Im)₂]ClO₄are S₄ruffled with the latter having the meso-C

(0.72 Å out of the porphyrin mean plane. This is the largest

deviation observed so far in an iron(III) porphyrinate complex.

55

And finally, the porphyrin core of [FeOEP(2-MeHIm)₂]ClO₄

is essentially planar. However, this complex contains high-spin

Fe(III), with an Fe-N_Pbond length of 2.275 Å. The ∼0.24-

0.27 Å increase in the axial bond distance compared to other

Fe(III) porphyrinates (Table 2) with hindered axial ligands is

due to the change in spin state from low spin (in [FeOMTPP-

(2-MeHIm)₂]Cl (this work), [FeOETPP(2-MeHIm)₂]⁺,³²[FeTPP-

(2-MeHIm)₂]ClO₄,¹⁵and [FeTMP(1,2-Me₂Im)₂]ClO₄²⁶) to high

spin in [FeOEP(2-MeHIm)₂]ClO_4.⁵⁵Therefore, the structure of

this complex is not comparable to those of the low-spin Fe(III)

complexes of this study, and it will not be considered further.

9

16000 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

Table 4. Hydrogen Bonds for C:[FeOMTPP(2-MeHIm)₂]Cl, [Å and

deg]

The average Fe-N_Pbond distances of 1.977(4) Å and 1.979-

(7) Å for molecules C and D, respectively, are typical for other

OMTPPFe(III) complexes with various axial ligands (Table 2),

close to the same distance in [FeOETPP(2-MeHIm)₂]⁺, 1.974-

(9) Å,³²and slightly longer than the same distance in [FeTPP-

(2-MeHIm)₂]ClO₄, 1.970(4) Å,¹⁵since the latter macrocycle is

less distorted from planarity. However, the average Fe-N_P

distance in [FeTMP(1,2-Me₂Im)₂]ClO₄, 1.937(12) Å,²⁶is much

shorter than the same distance in the OETPP and OMTPP

saddled and TPP ruffled analogues and is the shortest reported

for Fe(III) porphyrinates. This is due to the severe ruffling of

the TMP porphyrin core that is usually associated with shorter

Fe-N_pdistances.

D−H‚‚‚A

d(D−H)

d(H‚‚‚A)

d(D‚‚‚A)

(DHA)

N(6)-H(6A)‚‚‚Cl(1)

0.86

0.98

0.86

2.35

2.55

2.58

2.48

2.30

3.166(5)

3.459(8)

3.460(10)

3.145(5)

159.3

153.8

149.8

176.4

169.8

C(500)-H(50H)‚‚‚Cl(1)

C(600)-H(60A)‚‚‚Cl(1)

C(700)-H(70A)‚‚‚Cl(1)

N(8)-H(8A)‚‚‚Cl(1)^a

^aSymmetry transformations used to generate equivalent atoms: -x +

1, y - 1/2, -z + 3/2.

Table 5. Hydrogen Bonds for D:[FeOMTPP(2-MeHIm)₂]Cl, [Å and

deg]

D−H‚‚‚A

d(D−H)

d(H‚‚‚A)

d(D‚‚‚A)

(DHA)

N(8)-H(8A)‚‚‚Cl(1)

N(6)-H(6A)‚‚‚Cl(1)^a

C(500)-H(50B)‚‚‚Cl(1)

C(700)-H(70B)‚‚‚Cl(1)

0.88

0.99

2.30

2.21

2.61

2.59

3.142(8)

3.093(8)

3.555(14)

3.531(12)

160.0

179.3

158.7

158.4

The bond distances, angles, and displacements from the mean

porphyrin plane in [FeOMTPP(2-MeHIm)₂]Cl (molecules C and

D) are typical for six-coordinate OMTPP complexes, as well

as for other nonplanar six-coordinate porphyrin systems (OET-

PP, TMP, OEP). The axial Fe-N5 and Fe-N7 bond distances

are 2.006(5) and 2.032(5) Å for C and 2.007(7) and 2.010(7) Å

for D. These distances are very close to those in [FeTPP(2-

MeHIm)₂]ClO₄(2.015(4) and 2.010(4) Å)¹⁵and in [FeTMP-

(1,2-Me₂Im)₂]ClO₄(2.004(5) Å)²⁶but are shorter than 2.09(2)

Å in [FeOETPP(2-MeHIm)₂]⁺.³²

^aSymmetry transformations used to generate equivalent atoms: x - 1,

y, z.

32° and 45° to the closest N_P-Fe-N_Pvector in [FeTPP(2-

MeHIm)₂]ClO₄¹⁵and [FeTMP(1,2-Me₂Im)₂]ClO_4,²⁶respectively.

These are expected values for ruffled iron porphyrinates.

The N6 and N8 atoms of the two 2-MeHIm ligands in each

C and D structure, as well as C500, C600, and C700 of the

CHCl₃and C500 and C700 of CH₂Cl₂molecules in C and D,

respectively, are hydrogen bonded to Cl1 and another symmetry-

generated chloride. Hydrogen bond distances and angles are

presented in Tables 4 for molecule C and Table 5 for D.³²

H-bonds form an extended network through the entire crystal

along the a axis, shown in Figures S4. In both cases the

hydrogen bonds are shorter between the chloride and NH (2.30,

2.35 and 2.21, 2.30 Å, for C and D, respectively) and longer

between the chloride and C-H of the solvents (2.48, 2.55, 2.58

and 2.59, 2.61 Å for C and D, respectively).

Calculation of Energy Barriers. Utilizing ab initio DFT

calculations (B3LYP, 3-21G), the relative single-point energies

of the porphyrin cores of FeOETPP⁺and two FeOMTPP⁺

molecules were calculated to be 0.00, -61.57, and -40.84 kJ/

mol. Cores were generated from the crystal structure data for

[FeOETPP(4-Me₂NPy)₂]Cl³²and two structures of [FeOMTPP-

(4-Me₂NPy)₂]Cl, A and B, by substituting all the groups, Me,

Et, and Ph, with Hs and removing the axial ligands. No geometry

optimization was performed. It was found that the FeOMTPP⁺

cores have lower energy than their FeOETPP⁺counterpart and

between the two FeOMTPP⁺cores the one with admixture of

saddled and ruffled geometry (Table 2) is stabilized by more

than 20 kJ mol^-1. Electronic potential surfaces were calculated.

The main electron density is on the porphyrin nitrogens, while

the metal ion is electron deficient. Thus it reacts readily with

the electron pairs of donor ligands. From the electron potential

surface, the Fe atom in FeOETPP⁺is the least electron deficient;

therefore, the addition of the pyridines gives the structure with

the highest relative energy, 0.00 vs -123.45 and -118.57 kJ

mol^-1for [FeOETPP(Py)₂]⁺, [FeOMTPP(Py)₂]⁺A and B,

respectively. The orientation of the pyridine ligands was taken

to be the same as in the crystal structures (Table 2). Then the

positions of both pyridine ligands were constrained to be 0° to

the nearest N_P-Fe-N_Pvector. This caused the energy of the

molecules to increase by only 0.79 and 0.93 kJ mol^-1for

[FeOMTPP(Py)₂]⁺A and B, respectively. Similar results were

Not all axial ligand planes lie strictly along the normal to

the porphyrin mean plane. They form 81° and 85° dihedral

angles with the mean porphyrin plane in [FeOMTPP(2-Me-

HIm)₂]⁺, molecule C, and 86° and 90° in molecule D. With

this information in hand, and with the data from Figure 12, one

can see that the metal in the D molecule is in a symmetrical

tetragonal environment.

The orientation of the axial ligand planes in complexes with

highly hindered ligands is strongly influenced by the conforma-

tion of the porphyrin macrocycle. The planes of the axial ligands

in most OMTPP complexes are oriented nearly parallel to the

mutually perpendicular cavities formed by the nonplanar por-

phyrin macrocycle and the methyl groups on the pyrrole rings.

The dihedral angles between the axial ligand planes are 82.1°

and 80.5° for C and D, respectively. The same angles in

[FeOETPP(2-MeHIm)₂]⁺,³²[FeTPP(2-MeHIm)₂]ClO₄,¹⁵and

[FeTMP(1,2-Me₂Im)₂]ClO₄²⁶are 90°, 89.3°, and 89.4°, respec-

tively.

In the case of sterically hindered axial ligands (2-MeHIm,

and 1,2-Me₂Im) the orientation of the axial ligands is determined

not only by the geometry of the pockets but also by the steric

interaction between the ligands and the pyrrole N atoms. In

[FeOMTPP(2-MeHIm)₂]Cl and [FeOETPP(2-MeHIm)₂]⁺(both

mainly saddled with some ruffling) the ligands are rotated away

from the N_P-Fe-N_Pbond by 13.1, 19.0°; 11.2, 20.5°; and 14°

for C, D, and [FeOETPP(2-MeHIm)₂]⁺,³²respectively. The

observed angles can be explained mainly by steric repulsion

between the methyl group of the axial ligand and the Ns of the

porphyrin core and also to some extent by the presence of the

ruffling component in the crystal structures of the complexes

discussed. Nevertheless, the perp-[FeOMTPP(1-MeIm)₂]Cl

complex has a much larger æ angle of 29° than do the 2-MeHIm

complexes of either OMTPP or OETPP, supporting the sug-

gestion that the energy profile for orientation of unhindered five-

membered axial ligands is fairly flat in these saddled porphy-

rinates.⁵⁰In the ruffled porphyrins the projections of the

imidazole planes onto the porphyrinato core make angles of

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 16001

A R T I C L E S

Yatsunyk et al.

obtained using molecular mechanics calculations⁵⁰involving

[CoOETPP(Py)₂]⁺: the increase in the energy of the molecule,

where one ligand was constrained to lie exactly parallel to the

Co(III)-N_Pbonds was only 0.2 kJ mol^-1higher relative to the

energy of minimized structure.⁵⁰The increase in energy is due

to the close contact between the ligand protons (H2 and H6 in

the case of pyridine) and the porphyrin nitrogens.

Finally, a detailed analysis was performed on the core of

B:[FeOMTPP(Py)₂]⁺in order to find the potential energy of

axial ligand rotation. It was proposed from the molecular

mechanics calculations for [CoOETPP(L)₂]⁺that this energy

surface is fairly flat.⁵⁰In our DFT calculations the ligands were

constrained to having a dihedral angle of 88.5 ( 0.2° (the same

as in the crystal structure, Table 2) and were rotated simulta-

neously in steps of 15°. The result of a series of calculations is

shown in Figure S5. The highest energy (107.83 kJ mol^-1) was

observed when both ligands were rotated by 90° from their

crystal structure position, i.e., to positions opposing the shape

of the saddled porphyrinate ring. The energy increased by 63.30

and 142.57 kJ mol^-1for A:[FeOMTPP(Py)₂]⁺and [FeOETPP-

(Py)₂]⁺, respectively, when both pyridine ligands were rotated

by 90° from their original positions. It is reasonable to expect

that in the case of five-membered aromatic nonhindered ligands

(for example, 1-MeIm) and the OMTPP porphyrin core the

increase in potential energy upon rotation of one or both of the

axial ligands would be much smaller than for any OETPP case

or the case of FeOMTPP⁺with hindered axial ligands (Py,

2-MeHIm). These small increases in energy can be readily offset

by the stabilization expected from the Jahn-Teller effect for

these low-spin d⁵complexes when axial ligands are not in

perpendicular planes.²⁰This energy offset justifies the fact that

in the crystal structures reported herein so many different angles

between the axial ligands are obtained and that in many cases

the ligands are not in the optimized positions.

Figure 13. X-band EPR spectrum at 4.2 K for (a) perp-[FeOMTPP(1-

MeIm)₂]Cl crystals grown from chloroform/cyclohexane mixture run at 0.2

mW microwave power and 1 G modulation amplitude. This spectrum is of

the “large g_max” type with g ) 3.61. As usual, the other two g values are

not resolved. The relatively high noise level is due to the low power setting

used in order to prevent saturation of the signal. (b) paral-[FeOMTPP(1-

MeIm)₂]Cl crystals grown from methylene chloride/dodecane mixture. This

spectrum is clearly rhombic with three g values 2.71, 2.51, and 1.54; Σg²

) 16.02. (c) Solution of [FeOMTPP(1-MeIm)₂]Cl in CD₂Cl₂. Two types

of EPR signals are observed: a “large g_max” signal with g ) 3.12, and a

normal rhombic signal with g ) 2.84, 2.32, and approximately 1.6.

rhombicity have been reported,^57-61two of which involved Fe-

(III) porphyrinate complexes with pyrazoles,^60,61which are

significantly weaker σ-donors than imidazoles. Hence, it is

tempting to suggest that such large values of V/∆ may occur

when the axial ligands are weak σ-donors eVen though the

largest g value remains aligned along the heme normal.^60,61

The rhombic splitting, V/λ ) 2.44, for paral-[FeOMTPP(1-

MeIm)₂]⁺is of the order of 700-1000 cm^-1, depending on the

value taken for the spin-orbit coupling constant λ (300-400

cm^-1) for low-spin Fe(III),¹⁹or about 8.4-12 kJ mol^-1. While

these values are much smaller in magnitude than the energy

destabilization of axial pyridine ligands when rotated by 90°

against the saddled macrocycle, found in the DFT calculations

discussed above, the fact that 1-MeIm is a much less sterically

demanding ligand may still suggest that these energies can offset

each other.

EPR Studies of Polycrystalline and Frozen Solution

Samples of the Complexes of This Study. The X-band EPR

spectra for the polycrystalline and solution samples of both perp-

[FeOMTPP(1-MeIm)₂]Cl and paral-[FeOMTPP(1-MeIm)₂]Cl

were recorded at 4.2 K and very low power settings (0.2 mW)

to avoid saturation of these easily saturated signals and are

shown in Figure 13. The sample with near-parallel ligand planes

shows a rhombic EPR spectrum with the following g values:

2.71, 2.51, and 1.54; Σg²) 16.02. The rhombic signal is

indicative of the low spin (LS) iron(III) heme center having

“parallel” ligand orientation. It was found previously²⁰that even

for an axial ligand plane dihedral angle as large as 30° a rhombic

EPR signal is still observed. For the paral-[FeOMTPP(1-

MeIm)₂]Cl complex, the small tetragonal splitting ∆/λ⁵⁶(1.82,

compared to 2.79 for the analogous OETPP complex and

especially compared to values of 3-3.5 usually observed for

bis(imidazole) complexes of hemins¹⁹) may be a result of a

longer Fe-N_axbond, since one ligand occupies a nonoptimal

position. The rhombic splitting, V/λ, is 2.44, yielding the value

of the rhombicity, V/∆, of 1.34. The latter is twice as large as

the limiting value of 0.67 for the ideal case,⁵⁶where magnetic

axes are permuted to achieve this limiting value. We have

maintained the common assignment, where g_zzis the largest g

value and is aligned along the normal to the average porphyrin

core, as has been shown for [FeTPP(HIm)₂]⁺and a large number

of related complexes.^57-59Other similarly large values of the

The EPR spectrum of the polycrystalline sample of perp-

[FeOMTPP(1-MeIm)₂]Cl displays a single-feature signal with

g_max) 3.61. The “large g_max” signal is consistent with near-

degeneracy of the d_xzand d_yzorbitals (near-axial electronic

symmetry) and perpendicular orientation of the axial ligands.^24,25,62

In the polycrystalline sample of perp-[FeOMTPP(1-MeIm)₂]Cl

several minor impurity signals are also present near the g values

3.0 and 2.1. Such additional signals are often observed for “large

g

_max” spectra,^7,8,14and although they appear significant in the

derivative mode spectra, they reflect only very small integrated

signal areas relative to those of the large g_maxspecies, and thus,

there is only a small percentage of the sample with this

“impurity” EPR signal. From the fits of the magnetic Mo¨ssbauer

spectra reported elsewhere,³³the values of g_xxand g_yywere

estimated (0.63 and 1.53, respectively) and the crystal field

parameters calculated. They show that the splitting between the

9

16002 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

be calculated (1.30), assuming Σg²) 16.⁵⁶These values lead

to calculated crystal field parameters of V/λ ) 1.22, ∆/λ ) 5.09,

V/∆ ) 0.24. However, fits of the magnetic Mo¨ssbauer spectra³³

led to a smaller value of g_yy) 2.00, yielding g_xx) 1.14,

indicating that the second g value measured from the spectrum

of Figure 14a probably results from a nonrandom orientation

of crystallites; unfortunately the sample tube was not rotated to

check this possibility. The new g values give V/λ ) 1.16, ∆/λ

) 3.44, V/∆ ) 0.34; the value of the tetragonality, ∆/λ, obtained

from these g values is much more reasonable for a complex in

which the axial ligand bond lengths are equal and typical of

these low-spin ferriheme complexes. It thus appears that only

the largest g value can be reliably measured from the EPR

spectra of these “large g_max” complexes and that the other two

g values must be estimated from single-crystal EPR spectroscopy

or the fits of magnetic Mo¨ssbauer spectra.

Figure 14. X-band EPR spectrum at 4.2 K of (a) [FeOETPP(1-MeIm)₂]-

Cl crystallites immediately after isolation from the mother liquor; (b) of

the same sample after 1 week at ambient temperature without the mother

liquor.

If the polycrystalline sample of [FeOETPP(1-MeIm)₂]Cl from

which the EPR spectrum of Figure 14a was obtained was

allowed to sit in air at room temperature for an extended period

of time (allowing the loss of solvent molecules), the appearance

changed from crystallites through oil to powder, and a second

d_xzand d_yzorbitals, V, is indeed small (0.67λ, where λ is the

spin-orbit coupling constant).

recording of the EPR spectrum showed that the “large g_max

”

The solution sample of [FeOMTPP(1-MeIm)₂]Cl in CD₂Cl₂

(Figure 13c) has rhombic (g ) 2.83, 2.32, and ∼1.59, Σg²)

15.92) and “large g_max” (g ∼ 3.12) signals present in the EPR

spectrum, as observed previously for the solution sample of

[FeOETPP(1-MeIm)₂]Cl.³²In the case of the rhombic signal

the tetragonal splitting, ∆/λ, is 3.10 and the rhombic splitting,

V/λ, is 2.18, yielding the value of the rhombicity, V/∆, of 0.70,

which is close to the ideal value of 0.67.⁵⁶The EPR g values

are not the same as for the polycrystalline samples, probably

because the angles in the crystal are not the same as the average

angles in solution. Apparently, in the solution, both parallel and

perpendicular orientations of the axial ligands are possible,

which is reflected in the presence of both signals in the EPR

spectrum. “Large g_max” signals usually appear to be weak in

the derivative mode because of weak transition probabilities

compared to those of rhombic low-spin Fe(III) species, because

these transition probabilities are proportional to the sum of the

squares of the other two g values.⁶³These two much smaller g

values are not resolved in the EPR spectra of “large g_max” EPR

signals because of a combination of g strain and a spread in the

values of these two g values due to sample microheterogeneity.

This fact makes it difficult to quantify the relative amounts of

species with parallel (rhombic EPR signal) and perpendicular

(“large g_max” EPR signal) ligand arrangement present in the

frozen solution sample of [FeOMTPP(1-MeIm)₂]Cl.

signal had decreased in intensity and shifted to g ) 3.14 and a

new rhombic signal had appeared (g ) 2.75, 2.36, 1.62; V/λ )

2.41, ∆/λ ) 2.82, V/∆ ) 0.85), Figure 14b. The EPR spectrum

of the powdered material is very similar to that of the frozen

solution of [FeOETPP(1-MeIm)₂]Cl,³²and most probably has

the same origin. It is thus due to the presence of some complex

ions with axial ligand plane orientations that are close to

perpendicular and others that are close to parallel. We have

obtained crystals of [FeOETPP(1-MeIm)₂]Cl with an apparent

50° dihedral angle between the axial ligand planes that give

rise to a very similar rhombic signal (g ) 2.75, 2.34, 1.54),⁵³

but unfortunately there is a serious problem with this crystal

structure (the crystals are probably merohedral triplets) and we

have not as yet been able to solve the structure of this “parallel”

form.

The EPR spectrum of the frozen solution of [FeTC₆TPP(1-

MeIm)₂]Cl in CD₂Cl₂is very similar to that of [FeOMTPP(1-

MeIm)₂]Cl. It contains both “large g_max” (g_max) 3.14) and

rhombic (g ) 2.86, 2.39, and 1.45; the third feature is unresolved

and was calculated from the sum of g²) 16⁵⁶) types. From the

rhombic signal g values, the tetragonal splitting, ∆/λ, was

calculated to be 2.33 and the rhombic splitting, V/λ, 1.97, yields

the value of the rhombicity, V/∆, of 0.85, that is slightly higher

than the ideal value of 0.67.⁵⁶

The EPR spectra of frozen solutions of [FeOMTPP(4-Me₂-

NPy)₂]Cl and [FeOMTPP(2-MeHIm)₂]Cl in CD₂Cl₂have “large

Crystals of [FeOETPP(1-MeIm)₂]Cl exhibited a clean “large

g_max” EPR signal immediately following isolation from the

g

_max” signals with g ) 3.29 and 3.27, respectively. For the bis-

(4-Me₂NPy) complex this signal is observed in the polycrys-

talline samples of A and B as well (g ) 3.29). The “large g_max

signal is also observed for the bis(4-Me₂NPy) and bis(2-MeHIm)

complexes of Fe(III)OETPP.³²The difference in the “large g_max

mother liquor, but with two resolved g values (3.27, 1.90), as

shown in Figure 14a. From these two, the third g value could

”

(56) Taylor, C. P. S. Biochim. Biophys. Acta 1977, 491, 137-148.

(57) Quinn, R.; Valentine, J. S.; Byrn, M. P.; Strouse, C. E. J. Am. Chem. Soc.

1987, 109, 3301.

”

g values of the bis(4-Me₂NPy) and bis(2-MeHIm) complexes

of both OMTPP and OETPP is less than experimental error,

while the difference between these g values and those of the

frozen solutions of the bis(1-MeIm) complexes of OMTPP and

TC₆TPP is considerable. Thus, it appears that while solution

EPR spectra of the more sterically demanding axial ligand

complexes of the octaalkyltetraphenylporphyrinato-iron(III)

(58) Soltis, S. M.; Strouse, C. E. J. Am. Chem. Soc. 1988, 110, 2824.

(59) Astashkin, A. V.; Raitsimring, A. M.; Walker, F. A. J. Am. Chem. Soc.

2001, 123, 1905-1913.

(60) Raitsimring, A. M.; Borbat, P.; Shokhireva, T. Kh.; Walker, F. A. J. Phys.

Chem. 1996, 100, 5235-5244.

(61) Schu¨nemann, V.; Raitsimring, A. M.; Benda, R.; Trautwein, A. X.;

Shokhireva, T. Kh.; Walker, F. A. J. Biol. Inorg. Chem. 1999, 4, 708-

716.

(62) Palmer G. Biochem. Soc. Trans. 1985, 13, 548-560

(63) Aasa, R.; Va¨nngård, J. Magn. Reson. 1975, 19, 308-315.

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 16003

A R T I C L E S

Yatsunyk et al.

systems may reflect the same g values as observed in the solid

state, less sterically demanding axial ligand complexes produce

somewhat different g values in frozen solution than in the solid

state. This likely means that solid-state EPR data are more

reliable for understanding the relationship between g values and

molecular structure and suggests that the EPR parameters of

the polycrystalline sample of paral-[FeTMP(5-MeHIm)₂]ClO₄

may be more characteristic of that particular structure than are

the parameters obtained from the frozen solution of the

complex.²⁰

rhombic signal can be observed when the dihedral angle between

planar axial ligands is as large as 30° ²⁰has narrowed the range

of angles over which the type of EPR signal must switch from

normal rhombic to “large g_max” and has modified our under-

standing of what “perpendicular” may actually mean in the

structures of the bis-histidine-coordinated cytochromes of mi-

tochondrial complexes II and III. However, we cannot be

completely certain that the switch from normal rhombic to “large

g

_max” signal type occurs at the same axial ligand plane dihedral

angle for all porphyrin ring conformations; hence it is possible

that this angle may be somewhat porphyrin specific. Neverthe-

less, the complexes of the present study add significantly to

our understanding of the flexibility of the porphyrin ring and

the multiple ways in which particular axial ligand dihedral angles

can be accommodated. Although we have looked carefully at

the EPR data for the complexes of this study, we can find no

correlation between structural features (bond lengths, axial

ligand plane dihedral angles, out-of-plane distortions of por-

phyrin nitrogens) and the “large g_max” value. However, it is clear

that for complexes that have a wide range of dihedral axial

ligand plane angles possible the frozen solution EPR spectrum

has a smaller “large g_max” value than that observed for the

polycrystalline sample. Hence, it is as yet unclear how “large

Conclusions. As a result of the present research, the crystal

structures of five new complexes of dodecasubstituted (OMTPP,

OETPP, and TC₆TPP) iron(III) porphyrinates with imidazole

and pyridine axial ligands have been obtained. These structures

provide excellent models for the cytochrome b heme centers.

From the point of view of structural diversity, the most

interesting complex is [FeOMTPP(1-MeIm)₂]Cl, which has been

obtained in two crystalline forms with distinctly different axial

ligand orientation, yet strikingly similar porphyrin core geom-

etry. One form, perp-[FeOMTPP(1-MeIm)₂]Cl, has axial ligands

in strictly perpendicular planes; the second form, paral-

[FeOMTPP(1-MeIm)₂]Cl, has the particularly unusual (for a

saddled porphyrinate) axial ligand dihedral angle of 19.5° and

may demonstrate the energy stabilization available due to Jahn-

Teller distortion of these low-spin d⁵complexes. The molecular

structures of both [FeOMTPP(1-MeIm)₂]Cl complexes correlate

nicely with the type of EPR spectra observed. Ab initio DFT

calculations indicate that both perpendicular and “parallel”

orientation of the axial ligands are possible.

g

_max” values as large as 3.76-3.78⁶arise for heme b_Lof

mitochondrial complex III, or values of 3.41-3.44⁶arise from

heme b_H, when the current structural model for that heme has

the imidazole plane dihedral angle of 38°,^2,12and model heme

complexes having sugh g-values^7,24have axial ligand dihedral

angles of 89° ¹⁵amd 79°.²⁴

FeOMTPP⁺complexes with sterically demanding axial

ligands, 4-Me₂NPy and 2-MeHIm, have each been obtained in

two crystalline forms with slightly different axial ligand

orientations and porphyrin core geometries. In all four cases,

the orientation of the axial ligands is very close to perpendicular

and corresponds to the original expectation for these porphy-

rinate complexes. Quite different geometries of the porphyrin

cores (from purely saddled to saddled with 30% ruffling) are

observed, reflecting high flexibility of these systems. In all cases

the expected “large g_max” signal (g ) 3.29, 3.27), previously

shown to be indicative of perpendicular ligand orientation,^7,15,24

is observed.

It should be emphasized that although we have utilized

saddled Fe(III) porphyrinates for the present attempts to model

the bis-histidine-ligated cytochromes, we are not proposing that

the membrane-bound proteins have highly saddled hemes.

Rather, we have used these Fe(III) octaalkyltetraphenylporphy-

rinates because they allow the possibility, in model heme

complexes that are unconstrained with respect to their surround-

ings (in contrast to the heme centers in membrane-bound

proteins), for axial ligands to be trapped lying close to the N_P-

Fe-N_Paxes in perpendicular planes, which may stabilize Fe-

(II) complexes with this axial ligand arrangement. It remains

to be found whether this will in fact be the case; attempts to

prepare samples of the Fe(II) analogues of several of the Fe(III)

complexes of the present study are underway. In the present

work, we have found that Fe(III) octaalkyltetraphenylporphy-

rinatoiron(III) complexes provide a rich variety of axial ligand

orientations and porphyrin core conformations, among which

are several that lead to important insights into the possibilities

for axial ligand orientations in the membrane-bound heme

proteins. In fact, it can certainly be said that we have learned

something important from each of the 8 structures of this study.

[FeTC₆TPP(1-MeIm)₂]Cl is the only bis-ligated complex of

[FeTC₆TPP(L)₂]Cl that could be crystallized. It has a much more

planar porphyrin core than in the case of either OETPP or

OMTPP with 0.68:0.32 admixture of saddled and ruffled

components. Axial ligands are in perpendicular orientation, as

required by the symmetry of the crystal, but probably other

orientations are possible as well (as is indicated by the presence

of both normal rhombic and “large g_max” EPR signals in the

frozen solution sample). On the other hand, this system is found

to be too flexible for the purposes of the present research.

Acknowledgment. We thank the National Institutes of Health,

Grant DK-31038 (F.A.W.), National Science Foundation, Grant

CHE9610374, and the University of Arizona Molecular Struc-

ture Laboratory for support of this research. This paper was

revised while F.A.W. was on Sabbatical leave at the Institute

of Physics of the University of Lu¨beck with support of an

Alexander von Humboldt Senior Research Award. We thank

Asha Rajapakshe for her help in collecting the data and solving

the structure of [FeTC₆TPP(1-MeIm)₂]Cl. This paper is dedi-

cated to Helmut Beinert, who, with co-workers, published the

[FeOETPP(1-MeIm)₂]Cl was obtained in two crystalline

forms, only one of which has, thus far, given rise to a solved

crystal structure. In this case the axial ligand dihedral angle is

found to be 73.1°, and the porphyrinate core is essentially purely

saddled. A “large g_max” EPR signal (g ) 3.27) is also observed

for this complex.

In previous work we showed that a “large g_max” EPR signal

is obtained when the dihedral angle between axial ligand planes

is as small as 70°.³²This, coupled with the finding that a normal

9

16004 J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003

Low-Spin Ferriheme Models of the Cytochromes

A R T I C L E S

first EPR study of the ferrihemes of the bc₁complex, including

assignment of the spectral features observed to the three heme

centers present, in 1971 (ref 5), on the occasion of his 90th

birthday.

(4-Me₂NPy)₂]Cl, C:[FeOMTPP(2-MeHIm)₂]Cl, and D:[FeOMT-

PP(2-MeHIm)₂]Cl, and [FeOETPP(1-MeIm)₂]Cl, respectively.

Figure S1: linear deviation of each unique atom from the

porphyrin mean plane for all the structures in this study. Figures

S2 and S3: ORTEP diagram for B:[FeOMTPP(4-Me₂NPy)₂]-

Cl and C:[FeOMTPP(2-MeHIm)₂]Cl, respectively; Figure S4:

hydrogen bonding network for C:[FeOMTPP(2-MeHIm)₂]Cl and

D:[FeOMTPP(2-MeHIm)₂]Cl. Figure S5: calculated energy of

the structure of the [FeOMTPP(Py)₂]⁺depending upon the

orientation of the ligands. This material is available free of

charge via the Internet at http://pubs.acs.org.

Supporting Information Available: Table S1-S5, atomic

coordinates and equivalent isotropic displacement parameters;

bond lengths and angles; anisotropic displacement parameters;

hydrogen coordinates and isotropic displacement parameters;

torsion angles for paral-[FeOMTPP(1-MeIm)₂]Cl. Tables S6-

S10, S11-S15, S16-S20, S21-S25, S26-S30, S31-S35, and

S36-S40: the same for perp-[FeOMTPP(1-MeIm)₂]Cl, [FeTC₆-

TPP(1-MeIm)₂]Cl, A:[FeOMTPP(4-Me₂NPy)₂]Cl, B:[FeOMTPP-

JA036398R

9

J. AM. CHEM. SOC. VOL. 125, NO. 51, 2003 16005

Article Doi

Low-Spin Ferriheme Models of the Cytochromes: Correlation of Molecular Structure with EPR Spectral Type

DOI: 10.1021/ja036398r

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Article abstract of DOI:10.1021/ja036398r

Full text of DOI:10.1021/ja036398r

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