Hexanickel enediolate cluster generated in an acireductone dioxygenase model reaction

Article abstract of DOI:10.1021/ic100775m

A nickel(II) enediolate cluster (2) forms upon treatment of [(6-Ph ₂TPA)Ni(PhC(O)C(OH)C(O)Ph)]ClO₄ (1) with Me₄NOH 5H₂O in CH₃CN. Crystallographic studies of 2 revealed a hexanuclear structure of S₆ symmetry with a formula of {[Ni(PhC(O)C(O)C(O)Ph)(CH₃OH)] 1.33CH₃OH}₆. Because isolation of bulk amounts of 2 from the reaction involving 1 proved impossible, a solvation analogue of 2 (labeled 5) was generated from admixture of Ni(ClO₄)₂ 6H₂O, 2-hydroxy-1,3- diphenylpropane-1,3-dione, and Me₄NOH 5H₂O in CH ₃OH/CH₃CN. Complex 5 is formulated as {[Ni(PhC(O)C(O)C(O) Ph)(H₂O)] H₂O 0.25CH₃CN}₆ based on elemental analysis, a molecular weight determination, UV-vis, and a magnetic moment measurement. Treatment of 5 with O₂ and 6-Ph₂TPA (6 equiv) results in the formation of CO and [(6-Ph₂TPA)Ni(O ₂CPh)₂(H₂O)] (3), the latter of which was isolated in 69% yield. The level of ¹⁸O incorporation in this reaction matches that for a reaction wherein 2 is generated from 1. These results provide evidence that a nickel(II) enediolate cluster is the O ₂ reactive species in a previously reported model reaction for nickel(II)-containing acireductone dioxygenase.

Full text of DOI:10.1021/ic100775m

Inorg. Chem. 2010, 49, 7623–7625 7623
DOI: 10.1021/ic100775m
Hexanickel Enediolate Cluster Generated in an Acireductone Dioxygenase
Model Reaction
Katarzyna Rudzka,† Katarzyna Grubel,† Atta M. Arif,‡ and Lisa M. Berreau*,†
†Department of Chemistry and Biochemistry, Utah State University, Logan, Utah 84322-0300, and
‡Department of Chemistry, University of Utah, Salt Lake City, Utah 84112
Received April 21, 2010
Scheme 1
A nickel(II) enediolate cluster (2) forms upon treatment of [(6-Ph2-
TPA)Ni(PhC(O)C(OH)C(O)Ph)]ClO4 (1) with Me4NOH 5H2O in
3
CH3CN. Crystallographic studies of 2 revealed a hexanuclear struc-
ture of S6 symmetry with a formula of {[Ni(PhC(O)C(O)C(O)Ph)-
(CH3OH)] 1.33CH3OH}6. Because isolation of bulk amounts of 2
3
from the reaction involving 1 proved impossible, a solvation analogue of
2 (labeled 5) was generated from admixture of Ni(ClO4)2 6H2O,
3
2-hydroxy-1,3-diphenylpropane-1,3-dione, and Me4NOH 5H2O in
CH3OH/CH3CN. Complex 5 is formulated as {[Ni(PhC(O)C(O)C(O)-
Ph)(H2O)] H2O 0.25CH3CN}6 based on elemental analysis, a mole-
3
ina shift inthe absorption maximumofthe complex from399
to ∼420 nm (Scheme 2).3 We proposed that this spectral shift
was associated with the formation of a complex (2) contain-
ing a coordinated enediolate form of the 2-hydroxy-1,3-
diphenylpropane-1,3-dione ligand. The addition of O2 to this
proposed enediolate species resulted in the formation of CO
and a nickel(II) dibenzoate complex, [(6-Ph2TPA)Ni(O2CPh)2-
(H2O)] (3). Because examples of coordination complexes hav-
ing enediolate ligation of relevance to NiIIARD are rare, in the
research described herein we have further investigated the pro-
perties of the proposed enediolate species 2.
3
3
cular weight determination, UV-vis, and a magnetic moment mea-
surement. Treatment of 5with O2 and 6-Ph2TPA (6 equiv) results in the
formation of CO and [(6-Ph2TPA)Ni(O2CPh)2(H2O)] (3), the latter of
which was isolated in 69% yield. The level of 18O incorporation in this
reaction matches that for a reaction wherein 2 is generated from 1.
These results provide evidence that a nickel(II) enediolate cluster is the
O2 reactive species in a previously reported model reaction for
nickel(II)-containing acireductone dioxygenase.
A reexamination of the reaction mixture produced upon
treatment of 1 with Me4NOH 5H2O in CH3CN using thin-
3
layer chromatography revealed the presence of free 6-Ph2-
TPA in the solution. This suggested that 2 (λmax = 420 nm)
contained some mixture of nickel(II) and the enediolate form
of 2-hydroxy-1,3-diphenylpropane-1,3-dione. After exhaus-
tive attempts toward crystallizing this species (2), one dark
orange-brown platelike crystal suitable for single-crystal
X-ray diffraction was obtained from CH3OH/CH3CN/
Et2O.4 The crystal lattice of 2 contains hexanickel clusters
packed in layers parallel to the [110] direction. Each hex-
anickel cluster (Figure 1) is comprised of two layers of NiII
centers, with each layer having three pseudo-octahedral NiII
centers. The deprotonated central oxygen of the enediolate
ligand forms the linkage between the layers. Each NiII is
coordinated by five oxygenatoms from the enediolate ligands
and is capped with an oxygen atom from a coordinated
methanol. The Ni-O distances within each layer are in the
Metal-coordinated enediolate species are proposed to form in
the reaction pathways of several enzyme-catalyzed reactions.1 In
nickel(II)-containing acireductone dioxygenase (NiIIARD), an
enediolate form of the substrate is proposed to coordinate to the
metal center via a six-membered chelate ring structure (Scheme
1).2 The reaction of this enzyme/substrate complex with O2
results in aliphatic C-C bond cleavage and the release of CO.
Of relevance to NiIIARD, we have previously reported
that treatment of the mononuclear nickel(II) enolate complex
[(6-Ph2TPA)Ni(PhC(O)C(OH)C(O)Ph)]ClO4 (1) with Me4-
NOH 5H2O in CH3CN under anaerobic conditions results
3
*To whom correspondence should be addressed. E-mail: lisa.berreau@
usu.edu.
(1) (a) Yew, W. S.; Fedorov, A. A.; Fedorov, E. V.; Wood, B. M.; Almo,
S. C.; Gerlt, J. A. Biochemistry 2006, 45, 14598–14608. (b) Kim, K.; Kim, H. J.;
Oh, D. K.; Cha, S. S.; Rhee, S. J. Mol. Biol. 2006, 361, 920–931. (c) Akana, J.;
Fedorov, A. A.; Fedorov, E.; Novak, W. R.; Babbitt, P. C.; Almo, S. C.; Gerlt, J. A.
Biochemistry 2006, 45, 2493–2503. (d) Jelakovic, S.; Kopriva, S.; S€uss, K. H.;
Schulz, G. E. J. Mol. Biol. 2003, 326, 127–135. (e) Creighton, D. J.; Hamilton,
D. S. Arch. Biochem. Biophys. 2001, 387, 1–10.
(2) Pochapsky, T. C.; Ju, T.; Dang, R.; Beaulieu, R.; Pagani, G. M.
OuYang, B. In Metal Ions in Life Sciences; Sigel, A., Sigel, H., Sigel, R. K. O.,
Eds.; Wiley-VCH: Weinheim, Germany, 2007; pp 473-500.
(3) Szajna, E.; Arif, A. M.; Berreau, L. M. J. Am. Chem. Soc. 2005, 127,
17186–17187.
(4) 2: C104H116Ni6O32, M = 2230.23, trigonal, R3, orange-brown plates,
a = 17.2952(3) A, b = 17.2952(3) A, c = 30.7825(10) A, V = 7974.2(3) A ,
Z = 3, T = 150(1) K, 6503 total reflections, 3461 independent reflections
{R1 [I >2σ(I)] = 0.0501, wR2 (all data) = 0.1241}.
3
˚
˚
˚
˚
r
2010 American Chemical Society
Published on Web 08/06/2010
pubs.acs.org/IC

7624 Inorganic Chemistry, Vol. 49, No. 17, 2010
Rudzka et al.
Figure 2. Thermal ellipsoid drawings of one layer of 2 (top) and the core
of the trinuclear 4 (bottom). Ellipsoids are drawn at the 50% probability
level. Hydrogen atoms and the tetradentate 6-NA-6-Ph2TPA supporting
chelate ligand of the Ni(1) center in 4 have been omitted for clarity. Color
coding for atoms: carbon, gray; oxygen, red; nickel, green. Selected bond
distances (A) for 2: Ni(1)-O(1) 2.023(2), Ni(1)-O(2) 2.041(2), Ni(1)-O-
(3) 2.045(2), Ni(1)-O(4) 2.082(3) (methanol).
Figure 1. Thermal ellipsoid drawings of the nickel(II) enediolate cluster.
Ellipsoids are drawn at the 50% probability level. Color coding for atoms:
carbon, gray; oxygen, red; nickel, green. Hydrogen atoms have been omitted
for clarity. In the bottom structure, the phenyl appendages have been
truncated at the ipso carbon to aid visualization of the cluster connectivity.
˚
C-O distances of the enediolate coordination in these com-
Scheme 2
plexes are generally similar. However, there are slight differe-
˚
nces in the backbone C-C distances [2, C(1)-C(2) 1.404(5) A
˚
˚
and C(2)-C(3) 1.403(5) A; 4, C(36)-C(37) 1.419(5) A and
˚
C(37)-C(38) 1.387(5) A]. This could be a consequence of the
enediolate bridge being between pseudo-octahedral NiII centers
in 2 and square-planar and pseudo-octahedral NiII centers in 4.
Isolation of a bulk amount of 2 from the reaction mixture
proved impossible because of the extreme O2 sensitivity of
this compound and the difficulty of isolating the cluster
compound away from the other reaction products (6-Ph2-
TPA and Me4NClO4). For this reason, we pursued the
independent synthesis of an analogue of 2 via treatment of
Ni(ClO4)2 6H2O with an equimolar amount of 2-hydroxy-
3
1,3-diphenylpropane-1,3-dione in the presence of 2 equiv of
Me4NOH 5H2O in CH3CN/CH3OH. Following workup, an
3
orange-brown precipitate was isolated from CH2Cl2/Et2O
and was subsequently dried extensively under vacuum. Ele-
mental analysis of this solid revealed an empirical formula of
[Ni(C15H10O3) 2H2O 0.25CH3CN] (5). This formulation is
˚
range of 2.02-2.05 A. The Ni-O distance between the layers
˚
is 2.133(3) A. The capping methanol ligand has a Ni-
O(methanol) distance of 2.082(3) A. Positioned between the
˚
3
3
very similar to that found per NiII center in the X-ray
phenyl appendages of different dianionic 2-hydroxy-1,3-di-
phenylpropane-1,3-dione ligands within each layer is a mo-
lecule of methanol (total of three per layer). An additional
one-third occupied methanol molecule per NiII center is posi-
tioned between the clusters in the lattice.
Each layer of 2 (Figure 2a) has some similarity to the
Ni3(enediolate)2 core found in a trinuclear nickel(II) complex
4 (Figure 2b).5 In both complexes, the enediolate coordinates
as a bridging ligand between two NiII centers. The Ni-O and
structure of 2, [Ni(C15H10O3) 2.33CH3OH]. Specifically,
3
one enediolate and ∼2.3 molecules of solvent are present
per NiII center in both 2 and 5. Unfortunately, efforts to
crystallize 5, even under the same conditions as those used to
produce the X-ray crystal of 2, were unsuccessful. Therefore, to
determine whether 5 is a hexanickel cluster, a molecular weight
determination in naphthalene was performed using the Rast
method and 6-Ph2TPA as a standard.6 On the basis of a series
(5) Rudzka, K.; Arif, A. M.; Berreau, L. M. Inorg. Chem. 2008, 47, 10832–
(6) Pasto, D. J.; Johnson, C. R. Laboratory Text for Organic Chemistry;
10840.
Prentice-Hall: Englewood Cliffs, NJ, 1979; pp 101 and 102.

Communication
Inorganic Chemistry, Vol. 49, No. 17, 2010 7625
of measurements (see the Supporting Information), the mole-
cular weight of 5was determined to be 2100(350) g/mol. Within
the limitations of the experiment, this is consistent with the
formulation of 5 as a hexanickel cluster. Thus, we propose
that both 2 and 5 are hexanickel clusters, albeit they differ in
the nature of the solvate molecules that are present. For the
magnetic and spectroscopic studies outlined below, on the basis
of the elemental analysis data, we have formulated 5 as {[Ni-
(PhC(O)C(O)C(O)Ph)(H2O)] H2O 0.25CH3CN}6, which has
5-11 ppm region.11 A resonance for H2O could not be
identified in the1H NMR spectrum of 5.
To test the viability of a hexanickel nickel cluster as the O2
reactive species generated in the reaction of 1 with Me4-
NOH 5H2O (Scheme 2), we have combined 5 with 6 equiv of
3
6-Ph2TPA in CH3CN and exposed the solution to O2. This
results in the formation of CO and 3 (Scheme 2), the latter of
which was isolated in 69% yield from the reaction mixture
(see the Supporting Information). This yield matches well
with that previously reported (75%) starting from treatment
3
3
a molecular weight of 2059 g/mol.
Complex 5 has been characterized by a magnetic moment
measurement. With formulation as a hexanickel cluster, a
magnetic moment of 8.7(4) μB was determined using the Evans
method at ambient temperature.7 Because the magnetic proper-
ties of a hexanickel cluster are of current interest,8 the magnetic
properties of 5 remain under investigation.
of 1 with Me4NOH 5H2O in CH3CN followed by exposure
3
to O2.3 Performing the reaction involving 5 in the presence
of 18O2 resulted in a level of isotope incorporation for one
oxygen atom of each benzoate ligand (83-86%) that
matches with that found starting from 1 (86%).12 This level
of 18O incorporation is the same as that found for the reaction
of [(6-NA-6-Ph2TPANi)2(μ-PhC(O)C(O)C(O)Ph)2Ni](ClO4)2
(4). These combined results demonstrate that a similarity in the
coordination modes for the enediolate ligand leads to similar
levels of 18O incorporation. It should be noted that the reactions
involving enediolate complexes (2/5 and 4) exhibit higher levels
of 18O incorporation than is reported for the NiIIARD enzy-
matic reaction (77.5%).13
The UV-vis absorption spectrum of 5 [λmax = 420 nm
(ε ∼ 2400 M-1 cm-1)] is identical with that produced upon
treatment of 1 with Me4NOH 5H2O in CH3CN, which are
3
the conditions under which 2 is generated. This absorption
feature is tentatively assigned as a π f π* transition involving
the coordinated enediolate unit. This absorption is red-
shifted from that found in 1 (λmax = 399 nm).9 The FTIR
spectrum of 5 [Figure S1(top) in the Supporting Information]
has been measured in the solid state (KBr). The vibrations of
the enediolate ligand are broadened relative to the vibrations
in the starting neutral 2-hydroxy-1,3-diphenylpropane-1,3-
dione [Figure S1(bottom) in the Supporting Information].
A broad vibration at ∼3420 cm-1 in the spectrum of 5 is
consistent with the presence of water in the sample. Vibra-
tions in the region of ∼1640-1550 cm-1 are associated with
the enolate C-C and C-O units, as well as aromatic CdC
In summary, this study has provided evidence that the
reactive species in the NiIIARD model reaction shown in
Scheme 2 is a novel hexanuclear nickel(II) enediolate cluster.
Because little is currently known about the coordination
chemistry of acireductone-type enediolate ligands, this study
provides important insight that can be used in the design of
new complexes. Specifically, in future efforts toward model-
ing of the NiIIARD ES complex, it will be important to
employ a supporting chelateligand that is not easily displaced
upon metal enediolate ligation.
1
bonds. The H NMR spectrum of 5 was collected under
paramagnetic conditions with a spectral window of >220
ppm.10 Two broad phenyl proton resonances were identifed
in the spectra and located at ∼7.8 and 3.1 ppm (Figure S2 in
the Supporting Information). Decomposition of 5 upon
exposure to O2 results in only minor changes in the spectrum,
primarily in the region of 7-9 ppm. We note that paramag-
netic mononuclear nickel(II) benzoate compounds have been
previously shown to exhibit aryl 1H NMR resonances in the
Acknowledgment. Funding for this research was pro-
vided by the National Science Foundation (Grant CHE-
0848858).
Supporting Information Available: Synthetic and character-
ization details for 5 including FTIR and 1H NMR spectra and
experimental details of molecular weight determination of 5 and
18O-labeling experiments. This material is available free of
charge via the Internet at http://pubs.acs.org.
(7) Evans, D. F. J. Chem. Soc. 1959, 2003–2005.
(8) (a) Reddy, B. V.; Nayak, S.; Khanna, S. N.; Rao, B. K.; Jena, P.
J. Phys. Chem. A 1998, 102, 1748–1759. (b) Biswas, B.; Pieper, U.; Weyherm€uller,
T.; Chaudhuri, P. Inorg. Chem. 2009, 48, 6781-6793 and references cited
therein.
ꢀ
(11) Santana, M. D.; Garcia, G.; Lopez, G.; Lozano, A.; Vicente, C.;
ꢀ
Garcia, L.; Perez, J. Polyhedron 2007, 26, 1029–1036.
(12) We have previously reported that the level of 18O incorporation for
(9) Szajna-Fuller, E.; Rudzka, K.; Arif, A. M.; Berreau, L. M. Inorg.
Chem. 2007, 46, 5499–5507.
(10) Szajna, E.; Dobrowolski, P.; Fuller, A. L.; Arif, A. M.; Berreau,
L. M. Inorg. Chem. 2004, 43, 3988–3997.
the reaction involving 1 in the presence of Me4NOH 5H2O was ∼67%.
3
Repeating this experiment under more careful conditions resulted in a higher
level (86%) of 18O incorporation.
(13) Wray, J. W.; Abeles, R. H. J. Biol. Chem. 1995, 270, 3147–3153.