A Homoleptic Thioether Coordination Sphere That Supports Nickel(I)

Full text of DOI:10.1021/ic960515k

5408
Inorg. Chem. 1996, 35, 5408-5409
A Homoleptic Thioether Coordination Sphere That Supports Nickel(I)
Pinghua Ge,† Charles G. Riordan,*,† Glenn P. A. Yap,‡ and Arnold L. Rheingold‡
Departments of Chemistry, Kansas State University, Manhattan, Kansas 66506, and University of Delaware, Newark, Delaware 19716
ReceiVed May 9, 1996
Certain hydrogenases ([NiFe]H2ase) and carbon monoxide
dehydrogenase (CODH) are nickel-containing enzymes found
in methanogenic, sulfate-reducing, and acetogenic bacteria that
catalyze the oxidation of H2, reduction of H+ and CO oxidation,
acetyl-CoA synthesis, respectively.1 While the designed role
for each is distinct, the primary coordination sphere about Ni
in each is predominantly (or solely) sulfur ligation. The
structure of the [NiFe]H2ase from DesulfoVibrio gigas, recently
determined by X-ray methods, revealed the Ni to be coordinated
to four cysteines in a distorted geometry.2 In CODH, there are
two catalytically distinct, yet structurally similar, Ni sites,
clusters A and C, in which the average Ni environment as
deduced from Ni EXAFS is S4 or N(O)2-3S2.3 Our current
mechanistic understanding of these enzymes suggests that during
catalysis the Ni cycles through the Ni(I) oxidation state.1 The
reduction from Ni(II) occurs at E1/2 ) -235 mV for [NiFe]H2-
ase (Ni-C) and at E1/2 ) -541 mV for CODH (NiFeC).4
While low molecular weight complexes have modeled the Ni-
(II/III) redox couple in an S-only environment, to our knowledge
there is no example of a homoleptic NiIISx system that yields a
stable NiISx homologue upon chemical reduction.5,6 Our
understanding of these nickel-containing metalloenzymes would
be greatly enhanced by the synthesis and characterization of
model complexes that stabilize the +1 oxidation state in a sulfur-
only ligation sphere. This account details our successful efforts
toward stabilizing Ni(I) in such a coordination environment
using poly((methylthio)methyl)borates as monoanionic chelates.7
Reaction of 2 equiv of [Bu4N]Ph2Bt8 with Ni(BF4)2‚6H2O
in acetone resulted in precipitation of a deep red solid, [Ph2-
Bt]2Ni, 1, in 55% yield, eq 1. Electronic and 1H NMR
2[Bu4N][Ph2Bt] + Ni(BF4)2‚6H2O f
+ 2[Bu N][BF ] (1)
[Ph2Bt]2Ni
4
4
1
spectroscopies9 were consistent with a square planar structure
(S ) 0), which was confirmed by X-ray diffraction.10 The
molecular structure of 1 is depicted in Figure 1. The Ni ion
resides on a crystallographic inversion center which renders
trans thioethers metrically equivalent and ensures a planar
ligation sphere. The Ni-S distances of 2.200(1) and 2.240(1)
Å are similar to the Ni-Seq distance observed in the D. gigas
[NiFe]H2ase structure (average of 3 Ni-Seq ) 2.25 Å, Ni-Sax
) 2.6 Å)2 and in one of the Ni EXAFS studies on CODH (2.23
Å).3 The bond lengths are also consistent with other Ni(II)-
S(thioether) distances in square planar geometries and are ca.
0.1 Å longer than Ni(II)-S(thiolate) bond lengths.11 The bite
angle of the borate chelate is slightly less than ideal: S(1)-
Ni-S(2) ) 86.31(4)°. The six-membered chelate ring resides
in a twisted-boat conformation which orients one of the CH3
groups (C(15)) essentially perpendicular to the S4 plane
(displacement from S4 plane 1.66 Å) while the other (C(16))
lies nearly in the S4 plane (displacement from S4 plane 0.11
Å). This disposition of the chelate places the phenyl substituents
in distinct positions. One (Pheq) is directed away from the Ni,
while the other (Phax) is located directly above the NiS4 plane.
This latter orientation results in phenyl canopies protecting the
open axial coordination sites with the Phax centroid-Ni distance
equal to 3.79 Å. A similar placement of pseudoaxial Ph groups
* To whom correspondence should be addressed. E-mail:
Riordan@ksu.ksu.edu.
† Kansas State University.
‡ University of Delaware.
(1) (a) Ragsdale, S. W. Crit. ReV. Biochem. Mol. Biol. 1991, 26, 261-
300. (b) Lancaster, J. R., Ed. The Bioinorganic Chemistry of Nickel;
VCH Publishers: New York, 1988; Chapters 8-10.
(2) Volbeda, A.; Charon, M.-H.; Piras, C.; Hatchikian, E. C.; Frey, M.;
Fontecilla-Camps, J. C. Nature 1995, 373, 580-587. The authors
describe the Ni coordination sphere as neither square planar nor
tetrahedral.
(3) (a) Cramer, S. P.; Pan, W.-H.; Eidness, M. K.; Morton, T.; Ragsdale,
S. W.; Der Vartanian, D. V.; Ljungdahl, L. G.; Scott, R. A. Inorg.
Chem. 1987, 26, 2477-2479. (b) Bastian, N. R.; Diekert, G.;
Niederhoffer, E. C.; Teo, B.-K.; Walsh, C. T.; Orme-Johnson, W. H.
J. Am. Chem. Soc. 1988, 110, 5581-5582. (c) Xia, J.; Dong, J.; Wang,
S.; Scott, R. A.; Lindahl, P. A. J. Am. Chem. Soc. 1995, 117, 7065-
7070.
(7) (a) Ge, P.; Haggerty, B.; Rheingold, A. L.; Riordan, C. G. J. Am.
Chem. Soc. 1994, 116, 8406-8407. (b) Ohrenberg, C.; Ge, P.;
Schebler, P.; Riordan, C. G.; Yap, G. P. A.; Rheingold, A. L. Inorg.
Chem. 1996, 35, 749-754. (c) Ohrenberg, C.; Saleem, M. M.; Riordan,
C. G.; Yap, G. P. A.; Verma, A. K.; Rheingold, A. L. J. Chem. Soc.,
Chem. Commun. 1996, 1081-1082.
(4) For potentials vs NHE, see for example: (a) Coremans, J. M. C. C.;
van der Zwaan, J. W.; Albracht, S. P. J. Biochim. Biophys. Acta 1989,
997, 256-267. (b) Gorst, C. M.; Ragsdale, S. W. J. Biol. Chem. 1991,
266, 20687-20693.
(8) Abbreviations: Ph2Bt-, diphenylbis((methylthio)methyl)borate; [14]-
aneS4, 1,4,8,11-tetrathiacyclotetradecane; tmc, 1,4,8,11-tetramethyl-
1,4,8,11-tetraazacyclotetradecane.
(5) For an example of a NiIIS4 complex which is stable to electrochemical
reduction, see: Yamamura, T.; Sakurai, S.; Arai, H.; Miyamae, H. J.
Chem. Soc., Chem. Commun. 1993, 1656-1658.
(9) 1H NMR (CDCl3, 27 °C): δ 7.26 (br, o-H, 8 H), 7.20 (t, m-H, 8 H),
7.06 (t, p-H, 4 H), 1.82 (s, CH3SCH2, 20 H). UV-vis (CH2Cl2), λmax
(ꢀ, M-1 s-1): 354 (7300), 412 (7800), 510 (sh) nm. Anal. Calcd for
1 (C32H40B2NiS4): C, 60.70; H, 6.37; S, 20.25. Found: C, 60.49; H,
6.17; S, 19.85.
(6) For examples of Ni(I) complexes with other chromophores see the
following. NiIN4: (a) Ram, M. S.; Riordan, C. G.; Ostrander, R.;
Rheingold, A. L. Inorg. Chem. 1995, 34, 5884-5892. (b) Szalda, D.
J.; Fujita, E.; Sanzenbacher, R.; Paulus, H.; Elias, H. Inorg. Chem.
1994, 33, 5855-5863. (c) Suh, M. P.; Kang, S.; Goedken, V. L.; Park,
S. Inorg. Chem. 1991, 30, 360-365. (d) Lahiri, G. K.; Schussel, L.
J.; Stolzenberg, A. M. Inorg. Chem. 1992, 31, 4991-5000. NiIS3N2:
(e) Marganian, C. A.; Vazir, H.; Baidya, N.; Olmstead, M. M.;
Mascharak, P. K. J. Am. Chem. Soc. 1995, 117, 1584-1594. (f)
Baidya, N.; Olmstead, M. M.; Mascharak, P. K. Inorg. Chem. 1991,
30, 929-937. NiIN2S2: (g) Farmer, P. J.; Reibenspies, J. H.; Lindahl,
P. A.; Darensbourg, M. Y. J. Am. Chem. Soc. 1993, 115, 4665-4674.
NiINS3C: (h) Stavropoulos, P.; Muetterties, M. C.; Carrie´, M.; Holm,
R. H. J. Am. Chem. Soc. 1991, 113, 8485-8492. NiIN5: (i) Suh, M.
P.; Oh, K. Y.; Lee, J. W.; Bae, Y. Y. J. Am. Chem. Soc. 1996, 118,
777-783.
(10) Crystal data for 1: C32H40B2NiS4; red block, monoclinic, P21/n, a )
10.3144(9) Å, b ) 9.365(2) Å, c ) 16.7929(12) Å, â ) 107.624(9)°,
V ) 7242(3) Å3, Z ) 2. The structure was solved using direct methods,
completed by subsequent difference Fourier syntheses, and refined
by full-matrix least-squares procedures. Semiempirical absorption
corrections were not required because of the <10% variation in the
integrated ψ-scan intensities. All non-hydrogen atoms were refined
with anisotropic displacement coefficients. Hydrogen atoms were
treated as idealized contributions. The final residuals for 178 variables
refined against 2006 unique reflections were R(F) ) 4.04% and Rw-
(F2) ) 8.53%.
(11) Halcrow, M. A.; Christou, G. Chem. ReV. 1994, 94, 2421-2481.
S0020-1669(96)00515-0 CCC: $12.00 © 1996 American Chemical Society

Communications
Inorganic Chemistry, Vol. 35, No. 19, 1996 5409
Figure 1. Thermal ellipsoid plot of 1 at the 35% probability level
with hydrogen atoms removed for clarity. Selected bond distances (Å)
and bond angles (deg): Ni-S(1), 2.244(1); Ni-S(2), 2.200(1); S(1)-
Ni-S(1A), 180.0; S(2)-Ni-S(2A), 180.0; S(2)-Ni-S(1), 86.31(4);
S(2)-Ni-S(1), 93.69(4).
Figure 2. X-band EPR spectrum of Na[(Ph2Bt)2Ni] in THF at 77 K.
consistent with a NiIS4 species which is structurally distinct from
its square planar Ni(II) derivative.
The present system demonstrates that thioethers are competent
ligands for modeling the Ni(II/I) potential for enzyme active
sites that contain thiolates in the primary coordination sphere.
We set forth several rationales that may explain this finding.
First, if the cysteines are involved in H-bonding, their donor
ability would be greatly diminished and the redox properties
significantly altered.6g,17 Under these conditions, thioethers may
serve as more accurate ligand models in aprotic solvents.
Second, the monoanionic borate chelates employed in this study
allow the preparation of neutral complexes of divalent metal
ions. The overall complex charge is a significant factor in
determining redox potentials.7 Finally, in the [NiFe]H2ases and
CODH the Ni ions are coupled to redox-active Fe centers.1,2
The extent to which the Fe serves to modulate the Ni(II/I)
potential, while not known, is certainly substantial.18 Current
efforts are directed toward the synthesis of Ni-Fe4S4 systems
with the aim of evaluating the latter.
has been noted in the structure of [Ph2B(pz)2]2Ni, in which the
Phax centroid-Ni distance equals 3.45 Å.12
While the orientation of the Phax groups suggests a measure
1
of kinetic protection from exogenous substrates, the H NMR
spectrum at 27 °C reveals that in solution the Ph groups are
magnetically equivalent. Cooling the solution to -50 °C results
in a slow-exchange spectrum with two sets of Ph resonances.13
These spectra are consistent with a fluxional process in which
the twist-boat rings are inverting to a second twist-boat
configuration, thus exchanging the Pheq and Phax positions.
The cyclic voltammogram of 1 displayed a single, quasi-
reversible wave at -421 mV (vs NHE)14 assigned to the Ni-
(II/I) couple. This potential is intermediate between those of
[NiFe]H2ase and CODH and is significantly positive of that of
Ni(tpttd), the only other NiS4 chromophore that exhibits an
electrochemically reversible Ni(II/I) couple (E1/2 ) -1180
mV).5 While thiolate ligation favors higher oxidation states (Ni-
(III)), thioethers stabilize lower oxidation states (Ni(I), Ni(0)).
In general however, Ni(I) ions are unstable with respect to
disproportionation to Ni(II) and Ni(0). For example, the more
rigid square planar [Ni([14]aneS4)]2+ decomposes upon at-
tempted reduction.15 Remarkably, 1 may be chemically reduced
with Na/Hg amalgam, resulting in a color change from red to
yellow. Frozen THF solutions of the reduced species exhibited
a rhombic EPR spectrum, Figure 2, with g1 ) 2.27, g2 ) 2.11,
and g3 ) 2.03, consistent with metal-centered reduction.16 The
quasi-reversible reduction and the rhombic EPR signal are
Acknowledgment. We gratefully acknowledge financial
support from the donors of the Petroleum Research Fund, admin-
istered by the American Chemical Society (27076-G3), the NSF
(OSR-9255223), the Exxon Educational Fund, and DuPont
Central Research and Development. C.G.R. thanks the NSF
for a National Young Investigator Award (1994-1999).
Supporting Information Available: Tables giving structure de-
termination summary, atomic coordinates, bond lengths and bond
angles, anisotropic thermal parameters, and hydrogen atom parameters
for 1 (5 pages). Ordering information is given on any current masthead
page.
IC960515K
(12) Cotton, F. A.; Murillo, C. A. Inorg. Chim. Acta 1976, 17, 121-124.
(13) 1H NMR (acetone-d6, -50 °C): δ 7.54, 7.31, 7.17, 7.10, 7.00, 1.97,
1.84, 1.71, 1.59.
(16) 1 was stirred in THF over Na/Hg for 30 min. The solution was
transferred to an EPR tube, and the spectrum was recorded at 77 K.
An identical spectrum was obtained in DME.
(17) (a) Huang, J.; Ostrander, R. L.; Rheingold, A. L.; Leung, Y.; Walters,
M. A. J. Am. Chem. Soc. 1994, 116, 6769-6776. (b) Kru¨ger, H.-J.;
Peng, G.; Holm, R. H. Inorg. Chem. 1991, 30, 734-742.
(18) Mills, D. K.; Hsiao, Y. M.; Farmer, P. J.; Atnip, E. V.; Reibenspies,
J. H.; Darensbourg, M. Y. J. Am. Chem. Soc. 1991, 113, 1421-1423.
-1
(14) ∆E ) 150 mV, ipcipa ) 0.9. All experiments were recorded in a
cell consisting of a glassy carbon working electrode (1 mm), a Pt wire
counter electrode, and an Ag/AgCl reference electrode. CH2Cl2
solutions contained 0.1 M electrolyte ([Bu4N][PF6]) and 10 mM
sample. Potentials were referenced to internal Fc/Fc+ (+630 mV vs
-1
NHE, ∆E ) 108 mV, ipcipa ≈ 1.0).
(15) Rosen, W.; Busch, D. H. J. Am. Chem. Soc. 1969, 91, 4694-4697.