CaMn3IVO4 Cubane Models of the Oxygen Evolving Complex: Spin Ground States S < 9/2 and the Effect of Oxo Protonation

CaMn

Cubane Models of the Oxygen Evolving Complex:

Spin Ground States

< 9/2 and the Effect of Oxo Protonation

Heui Beom Lee

[a]

Angela A. Shiau

[a]

David A. Marchiori

[b]

Paul H. Oyala

[a]

Byung-Kuk

Yoo

[a]

Jens T. Kaiser

[a]

Douglas C. Rees

[a]

R. David Britt

[b]

Theodor Agapie

[a]

Department of Chemistry and Chemical Engineering, California Institute of Technology, 1200 E

California Blvd MC 127-72, Pasadena, CA 91125, United States

[b]

Department of Chemistry, University of California, Davis, One Shields Ave, Davis, California

95616, United States

Abstract

We report single crystal XRD and MicroED structure, magnetic susceptibility, and EPR data of a

series of CaMn

and YMn

complexes as structural and spectroscopic models of the

cuboidal subunit of the OEC. The effect of changes in heterometal identity, cluster geometry, and

bridging oxo protonation on spin state structure was investigated. In contrast to previous

computational models, we show that the spin ground state of CaMn

complexes and variants

with protonated oxo moieties need not be

= 9/2. Desymmetrization of the

pseudo

symmetric

Ca(Y)Mn

core leads to a lower

= 5/2 spin ground state. The magnitude of the magnetic

exchange coupling is attenuated upon oxo protonation, and an

= 3/2 spin ground state is

observed in CaMn

(OH). Our studies complement the observation that the interconversion

between the low spin and high spin forms of the S

state is

H dependent, suggesting that

(de)protonation of bridging or terminal oxygen atoms in the OEC may be connected to spin state

changes.

Graphical Abstract

agapie@caltech.edu.

Supporting information for this article is given via a link at the end of the document.

HHS Public Access

Author manuscript

Angew Chem Int Ed Engl

. Author manuscript; available in PMC 2022 August 02.

Published in final edited form as:

Angew Chem Int Ed Engl

. 2021 August 02; 60(32): 17671–17679. doi:10.1002/anie.202105303.

Author Manuscript

To better describe the electronic structure of the S

state intermediates of Photosystem II, a

ferromagnetically coupled CaMn

subunit with an

= 9/2 ground state has been proposed.

This assignment has played a key role in the mechanism of water oxidation, but structure–

electronic structure studies of CaMn

complexes remain rare. Through cluster

desymmetrization or oxo protonation, lower spin ground states are found to be accessible,

challenging prior models.

Keywords

oxygen evolving complex; model complex; electronic structure; magnetic susceptibility; spin state

Introduction

Biological water oxidation is catalyzed at the oxygen evolving complex (OEC) of

Photosystem II.

[

]

The OEC has been characterized by crystallography, revealing a

heterometallic CaMn

cubane motif binding to a fourth Mn center via bridging (hydr)oxo

moieties.

[

]

Mechanistic studies have been performed within the context of the Joliot-Kok

cycle of S

(

= 0~4) states.

[

]

Starting from the dark-stable S

state (Mn

III

), light-

induced one e

−

oxidation leads to the formation of the S

state, and numerous studies have

been performed to better understand the (electronic) structure of the S

state and the

requirements needed to advance to the higher S

states.

[

]

In the absence of unambiguous

and direct structural data concerning the O

─

O bond forming S

intermediate, structural and

spectroscopic characterization of lower S

state intermediates influence mechanistic

proposals for O

─

O bond formation.

[

]

Lee et al.

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Connected to Mn oxidation state and structural changes, each of the S

state intermediates

adopts a unique electronic structure with a characteristic spin ground state

[

]

) =

1/2,

[

]

) = 0

[

]

or higher

[

]

) = 1/2 or 5/2,

[

]

) = 3.

[

]

The

interconversion between the

= 1/2 and

= 5/2 forms of the S

state is notable.

[

]

One

interpretation invokes structural changes in the CaMn

core centered around the location of a

particular O(5) oxo moiety, with concomitant changes in the magnetic coupling interactions

resulting in a different

[

]

In the so-called “closed-cubane” structure with

= 5/2,

ferromagnetic coupling between Mn(1), Mn(2), and Mn(3) is proposed to lead to an

= 9/2

spin state for the CaMn

cuboidal subunit; antiferromagnetic coupling to the dangling

Mn(4) would lead to the observed

= 5/2 (Figure 1). In the “open-cubane” structure where

O(5) bridges Mn(3) and Mn(4) instead, an internal valence redistribution is proposed, with

the CaMn

III

subsite now proposed to have an

= 1 spin state; antiferromagnetic

coupling to the dangling Mn(4) would lead to the observed

= 1/2.

[

]

The above

structural isomerism model helps explain the high- and low-spin forms of the S

state.

Importantly, however, the model depends on the closed-cubane motif (region within the red

box, Figure 1) having a ferromagnetically coupled

= 9/2 spin state. At room temperature,

under turnover conditions, only the open-cubane form has been observed

crystallographically thus far.

[

]

While experimental data remains very limited, two

synthetic CaMn

model complexes have been reported with

= 9/2 (Figure 2),

[

]

supporting the coupling scheme for the closed-cubane structure and the possible structural

flexibility of the OEC core as an explanation for the spin state interconversion observed in

the S

state. Subsequent XFEL structural studies show the incorporation of a sixth oxygen

O(6) in the cleft between Mn(1) and Mn(4), a possible site for O

─

O bond formation (Figure

1).

[

]

A similar magnetic coupling scheme has been advanced for the S

state (Mn

featuring a ferromagnetically coupled CaMn

subunit with an

= 9/2 spin state;

antiferromagnetic coupling to Mn(4) would lead to the observed

= 3 (Figure 1).

[

]

Similar to the S

state, a structural interpretation for the observed spectral heterogeneity in

the S

state is the subject of ongoing investigation.

[

]

An alternative interpretation for the

spin state interconversion in the S

state is based on the observation that this process is

dependent, with a higher

H favoring the high-spin ground state.

[

]

Notably, other

effects such as low temperature irradiation of the S

state and the introduction of F

−

favor

formation of the high-spin state.

[

]

Insofar as the

H effect, the aquo moiety bound to

Mn(4) was hypothesized to be the site that is deprotonated following the observation that no

H dependent behavior is observed when NH

is bound to this aquo site.

[

]

Structural

changes to the OEC through either oxo exchange or (de)protonation would be accompanied

by concomitant changes in the nature and magnitude of the magnetic exchange coupling

which in turn affect not only the

of the cluster but also other spectroscopic properties

such as the sign and magnitude of the projected

Mn hyperfine coupling constants.

[

]

In a related computational study, protonation of the bridging oxo O(4) (Figure 1) in the S

state is proposed to lead to a high spin state, while maintaining the open-cubane structure.

[

]

XAS studies performed on the high-spin form of the S

state indeed show structural

differences to the low-spin form, but extracted Mn-Mn distances do not appear consistent

with the closed-cubane structure.

[

]

Such computational and experimental discrepancies

highlight the need for data on model compounds in which mechanistic hypotheses can be

Lee et al.

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Author Manuscript

tested and the effects of structural changes on the electronic structure of the OEC can be

evaluated.

Despite significant synthetic efforts to prepare heterometallic complexes that mimic the

OEC in terms of structure and redox state,

[

]

the effect of structural distortions or

protonation state on the electronic structure of multimetallic Mn complexes is not well

understood, and can be summarized as follows.

[

]

In a series of dinuclear complexes

featuring Mn

, Mn

O(OH), and Mn

(OH)

cores, the antiferromagnetic coupling is

strongest in the fully deprotonated form, with successive oxo protonations resulting in

weaker antiferromagnetic coupling.

[

]

A complete shift from ferromagnetic to

antiferromagnetic coupling is observed upon a single protonation of the adamantane-shaped

[Mn

]

core.

[

]

While representing incomplete models of the OEC, CaMn

complexes offer an opportunity to better understand the magnetic properties of the OEC, as

it relates to current discussions on the geometry and the spin state of the S

state. Any

changes to the spin state of the cubane portion would result in a different total spin of the

cofactor when magnetically coupled to the dangler Mn(4). The ground state of both the

pseudo

symmetric and the Ca-bound asymmetric Ca

model complexes has

been assigned to

= 9/2 on the basis of magnetic, spectroscopic, and computational data

(Figure 2).

[

]

Subsequent computational studies concluded that the spin ground

state of cuboidal CaMn

complexes and all possible protonated analogues

CaMn

(OH)

(4–

)

(

= 0~4) is

= 9/2.

[

]

Studies that probe the effect of distinct

structural changes or oxo protonation on the electronic structure of CaMn

complexes

have not been reported.

Herein, we report single crystal XRD and MicroED structure, magnetic susceptibility, and

EPR data of a series of cuboidal complexes featuring CaMn

, YMn

, and

CaMn

(OH) cores. Our results show that the electronic structure of CaMn

complexes is highly sensitive to changes promoted by the nature of the supporting ligands

(reminiscent to studies of Mn

III

complexes)

[

]

and the protonation state. We show

that ground states such as

= 5/2 and

= 3/2 are possible in CaMn

complexes,

which challenge the proposed model that a closed cubane such as that in the S

state of the

OEC must be

= 9/2.

Results and Discussion

Synthesis and crystal structure.

The acetate-bridged complex

1-Ca

was used as a precursor for other complexes (Scheme 1).

[

]

Magnetic susceptibility and computational studies on

1-Ca

indicate an

= 9/2 ground

state.

[

]

Treatment of

1-Ca

with Y(OTf)

leads to the analogous complex

1-Y

[

]

Magnetic studies show that

1-Y

has a similar

= 9/2.

[

]

Desymmetrization of the

pseudo

symmetric complexes

1-Ca

and

1-Y

was achieved via substitution of two acetate

moieties with a chelating bis-oxime proligand (H

). Treatment of

1-Ca

with H

results in the formation of

2-Ca

via a protonolysis reaction.

[

]

Similarly, treatment of

1-Y

with H

results in the formation of the analogous complex

2-Y

[

]

Due to its limited

solubility, suitable samples of

2-Ca

for single crystal X-ray diffraction studies could not be

obtained. The structure of

2-Ca

was determined using MicroED.

[

]

A powder sample of

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was judiciously treated with MeCN to obtain a TEM grid with non-aggregated particles

2-Ca

without loss of crystallinity. Complex

2-Ca

dissolves in MeCN only sparingly,

which is critical in obtaining a TEM grid with dispersed but intact microcrystals. The

resolution and refinement parameters of

2-Ca

were similar to those obtained for other

MicroED organometallic structures (Table S4).

[

]

Importantly, the MicroED structure of

shows that the CaMn

core is preserved, with a coordination sphere that is analogous

to that of

2-Y

[

]

The CaMn

core of

2-Ca

can be further desymmetrized via

treatment with 2,6-lutidinium triflate, which results in the protonation of a unique oxo in

between the oximate moieties to afford a complex with a CaMn

(OH) core (

3-Ca

Toward expanding the series of CaMn

complexes with chelating ligands of similar

basicity to the oximate moieties, an amidate-bridged complex was targeted. Treatment of

with a triethylene glycol derived bis-amide (H

diam) in the presence of NaO

Bu leads to

the formation of

4-Ca

. The crystal structure of

4-Ca

is consistent with the LCaMn

(diam)

(OAc) formulation in which two acetate moieties of

1-Ca

are replaced by the chelating bis-

amidate moiety (Figure 3). Overall,

1-Ca(Y)

2-Ca(Y)

3-Ca

, and

4-Ca

represent a unique

series of complexes mimicking the cuboidal substructure of the OEC in which cluster

symmetry, heterometal identity, bridging ligand, and oxo protonation state is systematically

varied.

Metal-oxo distances were compared across the series to understand the effect of chelating

ligands and oxo protonation on structure (Table S1). Within each complex

1-Ca

4-Ca

Ca-oxo, Mn-Mn, and M-O(4) distances are all similar to each other; the other six Mn-oxo

distances alternate between 1.83 and 1.87 Å along the

pseudo

axis of symmetry parallel

to the Ca-O(4) vector. A similar

pseudo

symmetry is observed in

1-Y

and in other known

analogues such as

1-Gd

[

]

The high symmetry of the metal-oxo core is broken with the

oximate-bridged complexes. Because precise structural metrics could not be obtained from

the MicroED structure of

2-Ca

, the structure of

2-Y

was used as a surrogate for the structure

2-Ca

for structural comparisons. Notably, the structure of

2-Y

and the Gd analogue

2-Gd

are very similar to each other, with Mn-oxo distances within 0.01 Å, indicating that general

structural trends are observable. In

2-Y

, the Y-O(1) distance is significantly shorter by 0.1 Å

than the other two Y-oxo distances. O(1) is the unique oxo that is located between the two

oximate donors, suggesting that the metal-oxo core has been structurally and electronically

desymmetrized. While the difference is smaller, the Mn-oxo distances trans to the Mn-

oximate bonds are slightly elongated compared to the corresponding Mn-oxo distance trans

to the Mn-acetate/amidate bond. Similarly, Mn-Mn distances in

2-Y

also distort in a manner

that is consistent with a

pseudo

symmetry with the mirror plane containing the Y(1)–

O(1) vector and bisecting the Mn(1)–Mn(2) vector. On the basis that the three-fold

symmetry of

1-Y

(

) is broken upon substitution of two acetates with the bridging oxime

, a similar structural distortion is expected in

2-Ca

, away from the

pseudo

symmetry of

1-Ca

. The structure of

3-Ca

is also consistent with a

pseudo

symmetry,

with Mn-(μ

-OH) distances that are slightly elongated by roughly 0.1 Å in comparison to the

corresponding Mn-(μ

-O) distances in

1-Ca

. Overall, distinct structural changes are

observed depending on the nature of the bridging ligands and the protonation state of

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Author Manuscript

bridging oxos; these relatively small structural changes across the series have a significant

influence in the electronic structure of the CaMn

core.

Magnetometry.

To obtain insight into the electronic structure of the series of CaMn

complexes, magnetic

susceptibility studies were performed (Figure 4). For a

pseudo

symmetric Mn

core, an

isotropic spin exchange Hamiltonian (eq 1) with two distinct magnetic interactions can be

employed, with a unique

and

(subscripts follow the Mn numbering

scheme in Figure 3).

[

]

For Mn

systems with local spin

= 3/2, application of the

vector coupling model

gives rise to twelve

∣

⟩

states, in which

varies in integer increments from 0 to 2

(i.e.

= 0, 1, 2, 3); for each value of

varies in integer increments from

∣

−

∣

(i.e. for

= 3,

= 3/2, 5/2, 7/2, 9/2).

The energies of the individual

∣

⟩

states can be expressed as shown in eq 2. By

incorporating the energies of the twelve

∣

⟩

states into the Van Vleck equation, an

analytical solution for the magnetic susceptibility X can be obtained. Qualitatively, one can

regard X to be derived from the sum of the individual

∣

⟩

states weighed by their

Boltzmann populations. At sufficiently low temperatures where only the ground state is

significantly populated, reduced magnetization studies can be performed to obtain

information about zero field splitting. Finally, while the relative energies of the individual

states depend on the sign and magnitude of

and

, the ground state is more easily

determined from the ratio of

(Figure 5).

[

]

= − 2

(

) − 2

′

(1)

∣

′〉 = −

(

+ 1) − (

′ −

)

′(

′ + 1)

(2)

Structurally most similar to

1-Ca

4-Ca

was studied by magnetometry (Figure 4a). The XT

value (units of emu K mol

−1

) of 5.60 at 300 K increases with cooling to reach a maximum

XT value of 11.98 at 2 K. This maximum value is in good agreement with the expected

value of 12.375 for

= 9/2 (

= 2). Previous magnetic studies on

1-Ca

show that while the

structure is more consistent with a

pseudo

symmetry, the data is better fit with two values

= 3.5 cm

−1

and

= −1.8 cm

−1

[

]

The data for

4-Ca

was similarly fit with two values

5.0 cm

−1

= −1.6 cm

−1

, and

= 1.97. Using the fitted

values, the relative energies of the

individual electronic states can be calculated. The

∣

9/2, 3

⟩

ground state is separated from the

∣

7/2, 2

⟩

first excited state by 5.5 cm

−1

and from the

∣

5/2, 1

⟩

second excited state by 8.8 cm

−1

The small separation between the ground and excites states is evident in the fact that XT

decreases sharply from the maximum value upon warming. The

ratio of −3.125 is fully

consistent with

= 9/2 and comparable to the value of −3.75 obtained for the asymmetric

complex.

[

]

The reduced magnetization data for

4-Ca

(Figure 4d) shows little

deviation from the ideal Brillouin function for

= 9/2, indicating the presence of a small

zero-field splitting estimated at

= −0.1 cm

−1

by EPR. Magnetic studies on

4-Ca

show that

changing the bridging ligands from acetates to amidates does not result in significant

changes to the electronic structure of the complex in the absence of notable structural

distortions to the metal-oxo core.

Lee et al.

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Featuring a lower symmetry, distorted metal-oxo core compared to

1-Ca

and

4-Ca

2-Ca

was studied by magnetometry (Figure 4a). The XT value of 4.526 at 300 K decreases slowly

to a local minimum XT value of 4.313 at 150 K. Upon further cooling, the XT value

increases slowly to reach a value of 4.405 at 15 K, in good agreement with the expected

value of 4.375 for

= 5/2 (

= 2). Further decrease in XT with temperature can be

attributed to intermolecular antiferromagnetic interactions and/or zero-field splitting. The

temperature dependence of XT observed in

2-Ca

is indicative of an irregular spin state

structure where the first excited state is

≤ 3/2 and the second excited state is

≥ 5/2.

Similar magnetic behavior has been observed in other trinuclear systems.

[

]

On the basis

of the small curvature of the XT vs. T curve, the expected separation between the spin

ground state and the first excited state is in the order of hundreds of wavenumbers. To

simulate the susceptibility data, the following parameters were used:

= 1.99,

= 250 ± 50

−1

= −280 ± 50 cm

−1

. Due to the small curvature of the XT vs. T curve, a relatively

large variance is reported for the

values, which should not be treated as exact values but as

estimates. However, the range in the

ratio is narrower, between −0.90 and −0.93, and

falls within the predicted region for

= 5/2 (Figure 5).

[

]

The

∣

5/2, 1

⟩

ground state is

separated from the

∣

3/2, 0

⟩

first excited state by 210 ± 50 cm

−1

and from the

∣

7/2, 2

⟩

second

excited state by 350 ± 50 cm

−1

. Thermally well-isolated spin ground states have been

observed in multinuclear complexes, with values of

∣

in the range of 160~900 cm

−1

[

]

Such systems behave as Curie paramagnets, with no temperature dependence of XT. In the

absence of double exchange or close metal-metal contacts, the physical nature of the large

increase of

2-Ca

remains unclear, but we provide the following hypothesis. In

1-Ca

and

4-Ca

where each Mn(IV) ion is coordinated by mostly

-only ligands, the principal

symmetry axis for each Mn center is ill-defined, and thus several competing exchange

pathways can be envisioned between d

, d

, and d

, resulting in the overall weak coupling

observed. In

2-Ca

and

2-Y

, in contrast, Mn(1) and Mn(2) are coordinated by oximates

which may act as p

-donors (also more basic

-donors than carboxylates). This defines the

Mn-O(oxime) vector as the z axis for Mn(1) and Mn(2). Because d

and d

may be

involved in d

-p

bonding with the oximates, contributions from exchange pathways such

as (d

)

∣

)

that weaken the overall magnitude of the antiferromagnetic coupling may

be reduced. The exchange pathway through the geometrically “aligned” d

orbitals on

Mn(1) and Mn(2) may explain the larger

. For

2-Ca

, the reduced magnetization isofield at 7

T reaches a value of 4.71

at 1.8 K, consistent with

= 5/2 (Figure 4b). Reduced

magnetization isofields were simulated assuming a single value of

= +1.46 cm

−1

or −1.17

−1

. In many cases, powder susceptibility data is insensitive to the sign of

[

]

This value

is inconsistent with the value obtained from EPR, at 0.3 cm

−1

(Figure 6a). Using this

value instead and incorporating the mean field model of intermolecular antiferromagnetic

interaction z

, a satisfactory fit can be obtained (Figure S7). The magnetic data on

2-Y

, for

which a high resolution crystal structure has been obtained, is also consistent with

= 5/2,

showing that the change in the spin ground state from

= 9/2 to

= 5/2 is also observed

going from

1-Y

2-Y

(Figure S8). The data on

2-Y

was simulated with the following

parameters:

= 2.0,

= 280 ± 50 cm

−1

= −315 ± 55 cm

−1

= −0.89. Importantly,

magnetic studies on

2-Ca

show that an intact CaMn

cubane moiety need not

necessarily have an

= 9/2 ground state.

Lee et al.

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Featuring a bridging hydroxo moiety,

3-Ca

was studied by magnetometry (Figure 4). The

XT value of 3.856 at 300 K decreases monotonically with temperature to reach a value of

1.886 at 10 K, in good agreement with the expected value of 1.875 for

= 3/2 (

= 2). To

simulate the susceptibility data, the following parameters were used:

= 2.0,

= +11 cm

−1

= −55 cm

−1

. The

ratio of −0.2 falls within the predicted region for

= 3/2 (Figure 5).

[

]

The

∣

3/2, 0

⟩

ground state is separated from the

∣

5/2, 1

⟩

first excited state by 77 cm

−1

and

from the

∣

3/2, 1

⟩

second excited state by 132 cm

−1

. Similar to

4-Ca

, magnetization studies

show little deviation from the ideal Brillouin function for

= 3/2, indicating the presence of

a small zero-field splitting (Figure 4c). Importantly, magnetic studies on

3-Ca

show that

protonation of a single bridging oxo moiety has a strong influence in attenuating the

magnitude of the magnetic coupling interactions.

[

]

While protonation of

2-Ca

does not

change the nature (sign) of the magnetic coupling interactions in

3-Ca

, the relative

magnitudes of

and

result in a change of spin ground state, from

= 5/2 in

2-Ca

3/2 in

3-Ca

. In a tetranuclear Mn

system, a complete reversal from ferromagnetic to

antiferromagnetic interactions has been reported.

[

]

With a structure that closely resembles

the closed-cubane subunit of the OEC, the spin state of

3-Ca

differs from the predicted

9/2, and an

= 3/2 is observed.

[

]

To obtain magnetostructural insight for the observed

changes in spin ground state, the geometry of the Mn(1)-O(1/4)-Mn(2) subsite was closely

examined. Mn(1)-O-Mn(2) angles increase slightly going from the

pseudo

symmetric

complex

1-Ca

to the desymmetrized complex

2-Y

(Table S2). A comparably more dramatic

increase in the Mn-O-Mn angles is observed in the protonated complex

3-Ca

. The observed

trend of increasing Mn-O-Mn angles is consistent with the decrease in spin ground state

within the series, and can be explained in the context of an increased antiferromagnetic

exchange for a more linear Mn-O-Mn linkage. Complex

3-Ca

with the widest Mn-O-Mn

angles therefore has the smallest

ratio and the lowest spin state. Most importantly,

magnetic studies show that spin states such as

= 5/2 and 3/2 are possible for a closed-

cubane structure.

EPR spectroscopy.

To obtain further insight into the electronic structure of complexes

2-Ca

3-Ca

, and

4-Ca

, X-

band EPR studies were conducted (Figure 6). Qualitatively, the spectrum of

2-Ca

suggests

that the weak field regime is operative, (

≫

≈

0.3 cm

−1

at X-band), where

is the axial

component of the zero-field splitting (ZFS) parameter. In such cases, as illustrated in the

rhombograms for half-integer spin states

> 1/2, peak positions are primarily determined by

the

ratio where

is the transverse component of the ZFS parameter. The spectrum of

features three transitions at

= 6.3 (108 mT),

= 4.3 (160 mT), and

= 2 (340 mT) that

can be assigned to the

∣

±1/2

⟩

Kramers doublet of an axial (

≈

= 5/2. The spectrum

2-Ca

can be approximated using parameters that are consistent with this qualitative

analysis (Figure 6a). The broad spectrum of

2-Ca

was simulated with a Gaussian

distribution of

centered at 0.06 with a full width at half-maximum of 0.03 (Figure S9).

The spectrum of

2-Y

is similar to that of

2-Ca

, consistent with the magnetic data showing

that both have an

= 5/2 ground state (Figure S10). The spectrum of

3-Ca

features two

main transitions at

= 5.1 (133 mT) and

= 2.1 (330 mT) that can be assigned to the

∣

±1/2

⟩

Kramers doublet of a rhombic (

≈

0.3)

= 3/2 (Figure 6b). While not amenable for a

simple qualitative analysis, the spectrum of

4-Ca

suggests a higher

= 9/2 with multiple

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overlapping transitions from the five Kramers doublets and is reminiscent of the spectrum of

the Ca

complex with an

= 9/2 ground state (Figure 6c).

[

]

The ZFS parameters

4-Ca

were obtained by simultaneously fitting spectra obtained at X- and D-band (130

GHz). At higher microwave frequencies, the electron Zeeman term that splits the energy

levels of a spin system in an applied magnetic field may be appreciably larger than that of

the ZFS parameter. This is the case for

4-Ca

at 130 GHz, where hv >>

. In such cases, the

resulting EPR spectrum is centered around the

value that defines the total spin system. The

width of the spectrum is determined by

, while the spacing of the EPR transitions is

determined by

E/D

. The D-band electron-spin echo EPR spectrum of

4-Ca

(Figure S11)

displays approximately nine transitions centered about

= 1.99 and spans approximately 1.5

T. The transitions that appear at magnetic fields lower than 4.67 T (

= 1.99) are evenly

spaced by approximately 200 mT, while those at fields higher than 4.67 T are unevenly

spaced. This is consistent with a small, negative ZFS parameter (

= −0.1 cm

−1

) that is axial

(

E/D

= 0.11). Overall, EPR spectroscopic studies of

2-Ca

4-Ca

are consistent with the

electronic structure and spin ground state description obtained from magnetic susceptibility

studies.

Conclusion

In summary, a series of CaMn

cuboidal complexes has been synthesized and

characterized by XRD/MicroED, magnetometry and EPR spectroscopy. To our knowledge

this is the first set of experimental studies that directly addresses the effect of systematic

changes in cluster geometry and bridging oxo protonation on the spin state structure of

CaMn

cubane models of the OEC. With implications in the interpretation of OEC

spectroscopic properties, our benchmarking results show that the electronic structure of the

CaMn

core is highly sensitive to small geometric changes, nature of the bridging ligands,

and protonation state of the bridging oxo moieties. Even in the absence of large oxo

movements proposed to account for the high spin and low spin signals of the S

state of the

OEC, we find that spin ground states such as

= 3/2, 5/2, or 9/2 are accessible for the

CaMn

subsite (Figure 4). Importantly, desymmetrization of

pseudo

symmetric

complexes

1-Ca

(

1-Y

) and

4-Ca

with

= 9/2 lead to a lower,

= 5/2 in

2-Ca

(

2-Y

Protonation of a single bridging oxo moiety in

2-Ca

has a strong influence in attenuating the

magnitude of the magnetic exchange coupling interactions, and

= 3/2 is observed in

. The nature of the magnetic exchange interactions does not need to change to result in a

different spin ground state; differences in the relative ratio of

values can lead to different

ground states (Figure 5). Our results strongly argue against the idea that the ground state of

CaMn

(OH)

(4−

)

(

= 0~4) complexes must necessarily be

= 9/2 as previously

reported; the protonation of a single bridging oxo may result in spin ground state changes in

tetranuclear complexes.

[

]

Nevertheless, while the present results demonstrate that closed

CaMn

(OH)

(4−

)

cubane motifs can have spin states different from

= 9/2, they do

not rule out such an interpretation for the CaMn

subunit of the OEC. However, they do

add support to mechanistic proposals that do not require structural distortions of the overall

cluster for the observation of additional spin states. For example, recent

H dependence

studies show that the

= 1/2 form of the S

state converts to the

= 5/2 form at high

[

]

On the basis of the results presented in this study, we support an interpretation based

Lee et al.

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on spin state changes following deprotonation of a bridging hydroxo or terminal aquo. Most

importantly, our results indicate that interpretation of EPR signals and subsequent structural

assignments should not be limited to an

= 9/2 spin state for the CaMn

subsite of the

OEC.

Supplementary Material

Refer to Web version on PubMed Central for supplementary material.

Acknowledgements

This research was supported by the NIH (R01-GM102687B to T.A.), Dow Next Generation Educator

(instrumentation), NSF-1531940 (Caltech EPR facility), the Division of Chemical Sciences, Geosciences, and

Biosciences (R.D.B. grant DE-SC0007203) of the Office of Basic Energy Sciences of the U.S. Department of

Energy. We thank Dr. Michael K. Takase and Mr. Lawrence M. Henling at Caltech for assistance with XRD; Dr.

Ignacio B. Martini at UCLA for assistance with magnetometry (NSF, MRI-1625776).

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