Highly
Activated
Terminal
Carbon
Monoxide
Ligand
in
an
Iron
−
Sulfur
Cluster
Model
of
FeMco
with
Intermediate
Local
Spin
State
at
Fe
Linh
N. V. Le, Justin
P. Joyce,
Paul H. Oyala,
Serena
DeBeer,
*
and Theodor
Agapie
*
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This:
J. Am. Chem.
Soc.
2024,
146, 5045−5050
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Supporting
Information
ABSTRACT:
Nitrogenases,
the enzymes
that convert
N
2
to NH
3
, also catalyze
the reductive
coupling
of CO to yield hydrocarbons.
CO-coordinated
species
of nitrogenase
clusters
have been
isolated
and used to infer mechanistic
information.
However,
synthetic
FeS clusters
displaying
CO ligands
remain
rare, which
limits
benchmarking.
Starting
from
a synthetic
cluster
that models
a cubane
portion
of the FeMo
cofactor
(FeMoco),
including
a bridging
carbyne
ligand,
we report
a heterometallic
tungsten
−
iron
−
sulfur
cluster
with a single
terminal
CO coordination
in two oxidation
states
with a high level of CO activation
(
ν
CO
= 1851
and 1751
cm
−
1
). The local
Fe coordination
environment
(2S, 1C, 1CO)
is identical
to that in the protein
making
this system
a suitable
benchmark.
Computational
studies
find an unusual
intermediate
spin electronic
configuration
at the Fe sites promoted
by the
presence
the carbyne
ligand.
This electronic
feature
is partly
responsible
for the high degree
of CO activation
in the reduced
cluster.
S
ubstrate
activation
at complex
inorganic
cofactors
in
enzyme
active
sites
has raised
fundamental
questions
about
the role of the cluster
structure
on reactivity.
For
example,
the challenging
conversion
of N
2
to NH
3
by
nitrogenase
enzymes
occurs
at FeMo
cofactor
(FeMoco)
(M
= Mo, V, or Fe), which
comprises
complex
double
cubane
clusters
with the MFe
7
S
9
C composition.
1,2
Nitrogenases
also
catalyze
the reductive
coupling
of CO to form
hydrocarbons
for M = Mo and V.
3,4
Despite
interest
in these
transformations,
the characterization
of substrate-bound
clusters
is very rare,
which
limits
insight
into the site of small
molecule
activation
and reaction
mechanism.
5
−
11
Only
two CO-bound
species
of
FeMoco
and
FeVco
have
been
characterized
structur-
ally.
9,10,12,13
Structural
characterization
of N
2
-derived
species
remains
debated.
14
−
16
Synthetic
models
promise
to facilitate
a better
understanding
of the impact
of cluster
structure
on substrate
binding
and level
of activation.
17
−
22
However,
few examples
of synthetic
iron
−
sulfur
clusters
with terminal
or bridging
N
2
or CO ligands
have
been reported,
many
of which
possess
multiple
CO ligands
that
drastically
alter
the electronic
structure
of the cluster
and
complicate
comparisons
to FeMoco
(Figure
1).
23
−
29
Only
one
type of FeS cluster
with a single
terminal
CO ligand
has been
characterized,
ligated
by three
carbene
ligands.
30,31
Having
accessed
a partial
synthetic
analogue
1
of the cluster
core
of FeMoco
displaying
a
μ
3
-carbyne
ligand
with
the
WFe
3
S
3
CR composition,
where
W is the isoelectronic
analogue
of Mo,
32
we targeted
the coordination
of nitrogenase
substrates
(Scheme
1).
33
Herein,
we report
the reactivity
of
1
with isocyanides
and CO, which
affords
an FeS cubane
with
a single
terminal
CO.
We characterize
this cluster
in two
oxidation
states,
which
show
a high level of CO activation,
as
observed
in the low CO stretching
frequency
(1751
−
1851
cm
−
1
) by IR spectroscopy.
Received:
October
27, 2023
Revised:
January
29, 2024
Accepted:
January
30, 2024
Published:
February
15,
2024
Figure
1.
Structures
of FeS clusters
with CO coordination:
(a) CO-
bound
FeMoco
(PDB:
4TKV);
(b) synthetic
cluster
with
carbide
ligand;
26,27
(c) Fe
4
S
4
cluster
with a single
terminal
CO;
30
(d) present
report.
Local
coordination
sphere
of Fe
−
CO
moiety
highlighted
in
(a), (c), and (d).
Communication
pubs.acs.org/JACS
© 2024
The Authors.
Published
by
American
Chemical
Society
5045
https://doi.org/10.1021/jacs.3c12025
J. Am. Chem.
Soc.
2024,
146, 5045
−
5050
This article is licensed under CC-BY 4.0
We employed
isocyanides
as isoelectronic
analogues
of CO
and substrates
of nitrogenase
34
that also allow
for a more
controlled
reactivity.
Treating
1
with
t
BuNC
or XylNC
(Xyl =
2,6-dimethylphenyl)
gives
2-
t
Bu
or
2-Xyl
(Scheme
1),
respectively,
through
the insertion
of isocyanide
into the Fe
−
C(vinyl)
bond,
which
demonstrates
rare examples
of C
−
C
bond
formation
at an FeS cluster.
35
−
38
Heating
2-
t
Bu
in THF
at 70
°
C for 16 h leads
to the formation
of
3
, where
XRD
and
NMR
studies
are consistent
with
the loss of a
t
Bu radical
(leaving
an
η
2
-nitrile
ligand).
39
While
determining
the
protonation
state
of the N atom
solely
on the basis
of XRD
is inconclusive,
the short
C
−
N
bond
length
of 1.205(6)
Å
Scheme
1. Syntheses
of Clusters
Figure
2.
Crystal
structures
of
2-
t
Bu
,
3
,
4
, and
4-K(18-crown-6)
.
Ellipsoids
are shown
at 50% probability
level.
Hydrogen
atoms,
solvent
molecules,
and the BAC
ligand,
except
for the carbene
C, are omitted
for clarity.
Journal
of
the
American
Chemical
Society
pubs.acs.org/JACS
Communication
https://doi.org/10.1021/jacs.3c12025
J. Am. Chem.
Soc.
2024,
146, 5045
−
5050
5046
compared
with
∼
1.25
Å for
η
2
-iminoacyl
(see the Supporting
Information
for additional
literature
comparison
and support
by ATR
IR spectroscopy)
is indicative
of an
η
2
-nitrile
motif.
40
Loss of the
t
Bu radical
suggests
a propensity
for side-on
nitrile
binding,
which
is an intriguing
observation
in the context
of
the nitrogenase
substrates
displaying
triple
bonds,
including
N
2
, acetylene,
and isocyanides.
41
The conversion
from
2-
t
Bu
to
3
, which
involves
the loss of a
t
Bu radical,
formally
represents
one-electron
oxidation
of the WFe
3
metal
core.
In contrast
to
2-
t
Bu
,
2-Xyl
is stable
under
the same
conditions,
which
is
consistent
with a lower
tendency
to lose the more
reactive
aryl
radical.
42
With
3
in hand,
we explored
reactions
with CO. Cluster
3
reacts
with 1 atm CO to form
4
within
5 min, which
shows
substitution
of one bis(diisopropylamino)cyclopropenylidene
(BAC)
ligand
with
CO (83%
yield,
Scheme
1) in an
uncommon
instance
of carbene
lability.
43
The average
Fe
−
C(
μ
3
) distance
remains
similar
to
2-
t
Bu
and
3
at 1.95 Å, but
the range
for the individual
bond
lengths
increases
to 1.88
−
2.00 Å (compared
with 1.92
−
1.95
Å in
2-
t
Bu
and 1.95
−
1.96
Å
in
3
), which
suggests
that the carbyne
ligand,
and potentially
the carbide
in FeMoco,
has the ability
to accommodate
distinct
electronic
demands
of different
Fe centers
through
structural
changes.
44
This
is in contrast
to spectroscopic
studies
suggesting
that the central
carbide
serves
to maintain
the
rigid core structure.
8,45
To the best
of our knowledge,
4
is the only
well-
characterized
example
of a heterometallic
MFe
3
S
3
(CR)
cubane
cluster
bearing
a single
terminal
CO ligand.
This provides
an
opportunity
for benchmarking
the impact
of structure
and
coordination
environment
relative
to FeMoco.
The
THF
solution
IR spectrum
of
4
displays
a prominent
peak at 1851
cm
−
1
, assigned
as the C
−
O
stretch
(Figure
3) and confirmed
by
13
CO labeling
(
ν
13CO
exp
= 1807
cm
−
1
,
ν
13CO
calc
= 1810
cm
−
1
), thereby
suggesting
highly
activated
CO.
To study
the effects
of cluster
oxidation
state on the level of
CO activation,
we reduced
4
with one equivalent
of KC
8
or
potassium
naphthalenide
to yield
4-K
(S = 3/2,
see the
Supporting
Information)
(Scheme
1). As expected,
the CO
bond
length
increases
upon
reduction
from
1.15(1)
to
1.198(3)
Å. The solution
IR spectrum
of
4-K
shows
two C
−
O bands
at 1794
and 1751
cm
−
1
(Figure
3), which
is
consistent
with the crystal
structure
of
4-K
displaying
CO
−
K
+
interactions
disordered
over
two positions:
terminal
(36%
occupancy)
(assigned
as
4-K
terminal
) and
η
2
(64%
occupancy)
(assigned
as
4-K
η
2
). These
isomers
are collectively
referred
to
as
4-K
.
Chelation
of K
+
with
18-crown-6
results
in the
formation
of
4-K(18-crown-6)
.
XRD
shows
that the K
+
ion is
present
in only one location
and interacts
end-on
with the O
atom
of CO (Figure
2). In agreement,
the IR spectrum
shows
a
single
band
at 1782
cm
−
1
(Figure
3;
ν
13CO
exp
= 1740
cm
−
1
;
ν
13CO
calc
= 1742
cm
−
1
). The same
band
is observed
upon
treatment
with [2.2.2]cryptand,
thereby
suggesting
that the K
+
ion in
4-K(18-crown-6)
does
not impact
CO activation
substantially.
46
Both
4-K
and
4-K(18-crown-6)
exhibit
highly
activated
CO
ligands
coordinated
to Fe in a terminal
fashion.
The interaction
with K
+
in different
binding
modes
affects
the level
of CO
activation
in the 1794
and 1751
cm
−
1
range.
Previous
computational
work
describes
a semibridging
CO ligand
at
Fe2 in FeMoco
with a frequency
of 1718
cm
−
1
,
47
very close
to
that assigned
to the bridging
CO in lo-CO
at 1715
cm
−
1
.
48
This is slightly
lower
than the typical
values
observed
for
μ
2
-
CO ligands,
which
lie in the 1720
−
1850
cm
−
1
range.
49
Hydrogen
bonding
between
the carbonyl
oxygen
and the
nearby
His195
residue
is proposed
to further
activate
CO.
47
Similarly,
in
4-K
, the K
+
cation
can play the same
role as the
hydrogen
bonding
network
and lower
the C
−
O
stretching
frequency.
Nevertheless,
ν
CO
values
below
1800
cm
−
1
are
unprecedented
for FeS clusters.
For comparison,
the CO
adducts
of
N
-heterocyclic
carbene
(NHC)-supported
Fe
4
S
4
clusters
reported
by Suess
and co-workers
display
C
−
O
stretching
frequencies
of 1832
cm
−
1
for the [Fe
4
S
4
]
0
and 1902
cm
−
1
for the [Fe
4
S
4
]
+
states.
30
The
local
coordination
environment
at each
Fe (FeS
2
C in
4
and
4-K
and FeS
3
in
[Fe
4
S
4
]
+,0
) and oxidation
state
distribution
between
different
metal
sites
can
contribute
to the level
of diatomic
activation.
30,50,51
In order
to understand
the electronic
structure
origin
of the
profound
CO activation
in these
clusters,
we employed
computational
methods
using
broken
symmetry
density
functional
theory
(BS-DFT).
Our computational
procedure
detailed
in the Supporting
Information
accurately
assigns
the
geometric,
Mo
̈
ssbauer,
and vibrational
properties
of
4
and
4-K
.
Here,
we highlight
the impact
of the carbyne,
W
3+
center,
and a
K
+
countercation
with respect
to the strong
CO activation
in
4-
K
.
The carbyne
has three
anionic
lone pairs oriented
along
the
Fe-bonding
axes in its
μ
3
-binding
mode.
The localized
orbitals
characterize
the carbyne
lone pairs
as
σ
-donors
that stabilize
the intermediate
spin (IS) state of the three
formal
Fe
2+
(
S
=
1) centers.
Observing
the IS state at the Fe sites that do not
bind
CO suggests
that it is an innate
property
of the
μ
3
-
carbyne
ligand.
The IS state in Fe
2+
centers
give full occupation
of its
π
-backbonding
orbitals,
consistent
with the increased
CO
activation
in
4-K
. In agreement,
hyperfine
sublevel
correlation
(HYSCORE)
spectra
of
4-K(
13
CO)
show
small
hyperfine
coupling
to the
13
C center
of CO {
A
(
13
C) = [
−
0.5,
1.0,
−
0.5]
MHz;
see the Supporting
Information}.
A partially
occupied
Fe
−
CO
backbonding
orbital
is expected
to result
in larger
coupling.
5,52,53
In comparison,
Fe centers
in FeS clusters
are
Figure
3.
IR spectra
of
4
,
4-K
, and
4-K(18-crown-6)
(THF
solution)
with
ν
CO
values
shown.
Dashed
spectra
correspond
to
13
CO-labeled
species
with
ν
13CO
in gray. The feature
at 1830
cm
−
1
unchanged
upon
13
CO labeling
is assigned
to BAC.
Journal
of
the
American
Chemical
Society
pubs.acs.org/JACS
Communication
https://doi.org/10.1021/jacs.3c12025
J. Am. Chem.
Soc.
2024,
146, 5045
−
5050
5047
routinely
assigned
as high-spin
because
of their
weak
ligand
field environment,
such as the
S
= 3/2 state
assigned
to the
CO-bound
Fe
1+
by Suess
and co-workers.
30
Furthermore,
the Fe centers
are preferentially
ferromagneti-
cally coupled,
which
results
in the equal
delocalization
of two
electrons
among
the three
Fe atoms
(Figure
4). This formally
lowers
the oxidation
state
of the CO-bound
Fe site from
its
formal
2+ to 1.33+
charge
and proportionately
increases
the
other
Fe centers
to 2.33+;
their resonance
states
are illustrated
in the Supporting
Information.
This
is analogous
to the net
Fe
2.5+
oxidation
state resulting
from the equal
delocalization
of
one electron
between
two Fe sites
in formal
Fe
2+
−
Fe
3+
dimers.
54
This
pairwise
delocalization
supports
a reduced
state
at the CO-bound
center
that is otherwise
inaccessible
under
biological
conditions.
Similarly,
redox
disproportiona-
tion
has been
proposed
in previously
reported
[Fe
6
(
μ
6
-
C)(CO)
18
] and Fe
4
S
4
(CO)(IMes)
3
clusters,
where
Fe sites
of different
oxidation
states
are within
close
proximity.
30,55
The
anionic
charge
of
4
−
supports
strong
noncovalent
interactions
with its countercation.
The geometry
optimization
of
4-K
preferentially
binds
K
+
in an
η
2
-conformation
with
respect
to the CO bond.
The
calculated
CO stretching
frequency
decreases
from 1800
cm
−
1
without
K
+
to 1756
cm
−
1
,
which
is consistent
with
the distinct
vibrational
modes
observed
in the IR spectrum
of
4-K
. The electronic
structure
of the cluster
is not impacted
by K coordination,
thereby
suggesting
that it is a purely
ionic
interaction
that stabilizes
the
π
-bonding
of the CO ligand.
The CO lone pair can overlap
with orbitals
arising
from the
Fe
−
W
interaction
assigned
as purely
covalent
in
4
−
on the
basis
of the localized
orbitals
(see Figure
S34 for a graphical
representation).
The Fe
−
W
covalent
interaction
redistributes
electron
density
between
the metal
centers
promoting
the
electrostatic
attraction
with the CO lone pair and consequently
also enhances
the
π
*
-backbonding
discussed
above.
56,57
The
other
Fe centers
exhibit
bonding
characters
that
are
intermediate
of a covalent
and magnetic
interaction,
analogous
to bonding
properties
detailed
in the Mo
3+
heteroatom
of
FeMoco.
58,59
In contrast,
this is not observed
for the cluster
reported
by Suess
and
co-workers
30
because
of the
comparatively
weak
bonding
interactions
between
Fe sites.
Overall,
these
factors
contribute
to the stronger
CO activation
in
4
−
compared
with these
reported
clusters
with an average
metal
oxidation
state of 2+, despite
the higher
average
metal
oxidation
state of 2.25+
in
4
−
.
30
In summary,
we have
reported
a series
of heterometallic
WFe
3
S
3
CR cubanes
and
demonstrated
several
types
of
organometallic
transformations
and binding
modes
that are
rare for iron
−
sulfur
clusters.
These
compounds
show
C
−
C
coupling,
along
with
side-on
binding
of an organic
nitrile
moiety
at one Fe site. Furthermore,
we characterized
the first
example
of a heterometallic
iron
−
sulfur
cluster
with a single
terminally
bound,
highly
activated
CO ligand
in two oxidation
states.
Computation
suggests
an unusual
carbyne-promoted
intermediate
spin electronic
configuration
at all Fe sites,
along
with a low oxidation
state
of 1.33+
for Fe(CO)
in
4
−
. This
electron
configuration
affords
full occupancy
of the two
π
-
back-bonding
orbitals
to CO, which
are responsible
for the
high
level
of CO activation
in the reduced
clusters.
The
negative
charge
of the cluster
and the metal
−
metal
covalency
were
found
computationally
to also impact
CO activation.
These
findings
provide
a set of parameters
to evaluate
in future
studies
for the conversion
of substrates
in nitrogenase.
■
ASSOCIATED
CONTENT
*
sı
Supporting
Information
The Supporting
Information
is available
free of charge
at
https://pubs.acs.org/doi/10.1021/jacs.3c12025.
General
methods,
synthetic
procedures,
product
iso-
lation
and characterization,
NMR
spectra,
structural
information,
and computational
methods
(PDF)
Accession
Codes
CCDC
2130433
−
2130434,
2130436,
2233067
−
2233070,
and
2233072
contain
the supplementary
crystallographic
data for
this paper.
These
data can be obtained
free of charge
via
www.ccdc.cam.ac.uk/data_request/cif,
or by emailing
data_
request@ccdc.cam.ac.uk,
or by contacting
The
Cambridge
Crystallographic
Data
Centre,
12 Union
Road,
Cambridge
CB2 1EZ,
UK; fax: +44 1223
336033.
■
AUTHOR
INFORMATION
Corresponding
Authors
Serena
DeBeer
−
Max
Planck
Institute
for Chemical
Energy
Conversion,
45470
Mu
̈
lheim
an der Ruhr,
Germany;
orcid.org/0000-0002-5196-3400;
Email:
serena.debeer@cec.mpg.de
Theodor
Agapie
−
Division
of Chemistry
and Chemical
Engineering,
California
Institute
of Technology,
Pasadena,
California
91125,
United
States;
orcid.org/0000-0002-
9692-7614;
Email:
agapie@caltech.edu
Authors
Linh
N. V. Le
−
Division
of Chemistry
and Chemical
Engineering,
California
Institute
of Technology,
Pasadena,
California
91125,
United
States
Justin
P. Joyce
−
Max
Planck
Institute
for Chemical
Energy
Conversion,
45470
Mu
̈
lheim
an der Ruhr,
Germany
Paul
H. Oyala
−
Division
of Chemistry
and Chemical
Engineering,
California
Institute
of Technology,
Pasadena,
California
91125,
United
States;
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Figure
4.
Local
oxidation
and spin states
of the metal
centers
of
4
−
(
S
= 3/2)
with respect
to the Mulliken
spin population
of their
PM-
localized
orbitals
(Figures
S34
−
36).The
curved
green
arrow
denotes
a
pair of electrons
that are equally
delocalized
among
the Fe centers
(illustrated
in the inset)
with respect
to its localized
spin density.
The
degenerate
Fe
−
CO
π
-bonding
interactions
are shown
at the bottom
with respect
to their localized
orbitals.
Journal
of
the
American
Chemical
Society
pubs.acs.org/JACS
Communication
https://doi.org/10.1021/jacs.3c12025
J. Am. Chem.
Soc.
2024,
146, 5045
−
5050
5048
https://pubs.acs.org/10.1021/jacs.3c12025
Notes
The authors
declare
no competing
financial
interest.
■
ACKNOWLEDGMENTS
We are grateful
to the National
Institutes
of Health
(R01-
GM102687B
to T.A.)
and the Humboldt
Foundation
for
funding
for T.A.
(a Bessel
Research
Award)
and J.P.J.
We
thank
the Beckman
Institute
and the Dow
Next
Generation
Grant
for instrumentation
support.
Michael
Takase
and
Lawrence
Henling
are thanked
for assistance
with crystallog-
raphy.
J.P.J. and S.D. acknowledge
the Max Planck
Society
for
funding.
■
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