J. Am. Chem. Soc. 1999, 121, 10035-10046

10035

Ligand K-Edge and Metal L-Edge X-ray Absorption Spectroscopy
and Density Functional Calculations of Oxomolybdenum Complexes
with Thiolate and Related Ligands: Implications for Sulfite Oxidase
Yasuo Izumi,†,§ Thorsten Glaser,† Kendra Rose,† Jonathan McMaster,⊥ Partha Basu,⊥
John H. Enemark,*,⊥ Britt Hedman,*,†,‡ Keith O. Hodgson,*,†,‡ and Edward I. Solomon*,†Contribution from the Department of Chemistry and Stanford Synchrotron Radiation Laboratory,
Stanford UniVersity, Stanford, California 94305, and Department of Chemistry, UniVersity of Arizona,
Tucson, Arizona 85721
ReceiVed February 5, 1999

Abstract: X-ray absorption spectra have been measured at the S K-, Cl K-, and Mo L3- and L2-edges for thed0 dioxomolybdenum(VI) complexes LMoO2(SCH2Ph), LMoO2Cl, and LMoO2(OPh) (L ) hydrotris(3,5dimethyl-1-pyrazolyl)borate) to investigate ligand-metal covalency and its effects on oxo transfer reactivity.
Two dominant peaks are observed at the S K-edge (2470.5 and 2472.5 eV) for LMoO2(SCH2Ph) and at the
Cl K-edge (2821.9 and 2824.2 eV) for LMoO2Cl, demonstrating two major covalent contributions from S and
Cl to the Mo d orbitals. Density functional calculations were performed on models of the three Mo complexes,
and the energies and characters of the Mo 4d orbitals were interpreted in terms of the effects of two strong
cis-oxo bonds and additional perturbations due to the thiolate, chloride, or alkoxide ligand. The major perturbation
effects are for thiolate and Cl- π mixed with the dxz orbital and σ mixed with the dz2 orbital. The calculated
4d orbital energy splittings for models of these two major contributions to the bonding of thiolate and Cl
ligands (2.47 and 2.71 eV, respectively) correspond to the splittings observed experimentally for the twodominant ligand K-edge peaks for LMoO2(SCH2Ph) and LMoO2Cl (2.0 and 2.3 eV, respectively) after
consideration of final state electronic relaxation. Quantification of the S and Cl covalencies in the d orbital
manifold from the pre-edge intensity yields, ∼42% and ∼17% for LMoO2(SCH2Ph) and LMoO2Cl, respectively.
The Mo L2-edge spectra provide a direct probe of metal 4d character for the three Mo complexes. The spectra
contain a strong, broad peak and two additional sharp peaks at higher energy, which are assigned to 2p transitions
to the overlapping t2g set and to the dz2 and dxy levels, respectively. The total peak intensities of the Mo L2edges for LMoO2(OPh) and LMoO2Cl are similar to and larger than those for LMoO2(SCH2Ph), which agrees
with the calculated trend in ligand-metal covalency. The theoretical and experimental description of bonding
developed from these studies provides insight into the relationship of electronic structure to the oxo transfer
chemistry observed for the LMoO2X complexes. These results imply that anisotropic covalency of the MoScys bond in sulfite oxidase may promote preferential transfer of one of the oxo groups during catalysis.

1. Introduction
Mo-containing enzymes are essential for all forms of life.
With the exception of nitrogenase, most of these enzymes
catalyze reactions in which there is a net transfer of an oxygen
atom between substrate and water, as shown in eq 1.1

X + H2O h XO + 2H+ + 2e-(1)

Prior to 1995, structural information about the Mo centers inthese enzymes was deduced principally from EXAFS at the Mo
K-edge and EPR spectroscopy of their transient Mo(V) states.1
Since then, several protein crystal structures have beenreported.2-11 These protein structures confirm that there are three
distinct structural families for the Mo centers: the xanthineoxidase, DMSO reductase, and sulfite oxidase families.1 In all* To whom correspondence should be addressed.
† Stanford University.
‡ Stanford Synchrotron Radiation Laboratory, SLAC.
⊥ The University of Arizona.
§ On leave from Interdisciplinary Graduate School of Science andEngineering, Tokyo Institute of Technology, Yokohama, Japan.
(1) Hille, R. Chem. ReV. 1996, 96, 2757-2816.

three structural families, the Mo center is coordinated by S
donors from the cis-ene-1,2-dithiolate (dithiolene) of one (ortwo) novel pyranopterin (molybdopterin) units.1,12 This ligand
system is unique to Mo and W in metalloproteins, and it appears
that coordination by this ligand (and in some cases an additional
S ligand) is essential for the catalytic function of these enzymes.
(2) Romão, M. J.; Archer, M.; Moura, I.; Moura, J. J. G.; LeGall, J.;
Engh, R.; Schneider, M.; Hof, P.; Huber, R. Science 1995, 270, 11701176.
(3) Huber, R.; Hof, P.; Duarter, R. O.; Moura, J. J. G.; Moura, I.; Liu,
M. Y.; Legall, J.; Hille, R.; Archer, M.; Romão, M. Proc. Natl. Acad. Sci.
U.S.A 1996, 93, 8846-8851.
(4) Schindelin, H.; Kisker, C.; Hilton, J.; Rajagopalan, K. V.; Rees, D.
C. Science 1996, 272, 1615-1621.
(5) Schneider, F.; Löwe, J.; Huber, R.; Schindelin, H.; Kisker, C.;
Knäblein, J. J. Mol. Biol. 1996, 263, 53-59.
(6) McAlpine, A. S.; McEwan, A. G.; Shaw, A. L.; Bailey, S. J. Biol.
Inorg. Chem. 1997, 2, 690-701.
(7) McAlpine, A. S.; McEwan, A. G.; Bailey, S. J. Mol. Biol. 1998,
275, 613-623.
(8) Boyington, J. C.; Gladyshev, V. N.; Khangulov, S. V.; Stadtman, T.
C.; Sun, P. D. Science 1997, 275, 1305-1308.
(9) Kisker, C.; Schindelin, H.; Pacheco, A.; Wehbi, W. A.; Garrett, R.
M.; Rajagopalan, K. V.; Enemark, J. H.; Rees, D. C. Cell 1997, 91, 973983.

10.1021/ja9903678 CCC: $18.00 © 1999 American Chemical Society
Published on Web 10/13/1999

10036 J. Am. Chem. Soc., Vol. 121, No. 43, 1999
Scheme 1. (Top) Coordination of the Mo Site of Sulfite
Oxidase, Showing the Novel Pyranopterin That Contributes
the Ene-1,2-dithiolate Group, and (Bottom) Proposed
Reaction Cycle for Sulfite Oxidaseaa Sulfite (X) is oxidized by oxygen atom transfer (OAT) from[MoVIO2]2+, water coordinates to the reduced [MoIVO(H2O)]2+ center,and two successive coupled electron-proton transfers reoxidize theMo site back to [MoVIO2]2+.

The coordination about the Mo atom from the X-ray crystal
structure of chicken liver sulfite oxidase at 1.9 Å resolution isshown in Scheme 1.9 The Mo atom is five-coordinate andexhibits approximate square pyramidal coordination geometry,with oxygen atoms in the axial and equatorial positions. BothEXAFS13-16 and resonance Raman spectroscopy17 indicate thatthe oxidized enzyme possesses two oxo groups coordinated toa Mo(VI) center. The remaining equatorial positions areoccupied by the two S atoms from one ene-1,2-dithiolate ligand
and the S atom from the side chain of a cysteine that isconserved throughout all sulfite oxidases. Site-directed mutagenesis of this cysteine to serine in the human or rat enzymes
results in an inactive enzyme.18
The proposed reaction cycle for the Mo center of sulfite
oxidase (Scheme 1) involves the transfer of an O atom from a
dioxo-Mo(VI) center of the enzyme to sulfite to generate an
oxo-Mo(IV) center and sulfate.19 The active site is regenerated
by two consecutive one-electron processes involving the heme
prosthetic groups in the protein and ultimately cytochrome c.
The first electron-transfer reaction generates a paramagnetic Mo(V) state that can be detected by EPR spectroscopy.15,20-23(10) Czjzek, M.; Dos Santos, J.-P.; Pommier, J.; Giordano, G.; Méjean,V.; Haser, R. J. Mol. Biol. 1998, 284, 435-437.
(11) Dias, J. M.; Than, M. E.; Humm, A.; Huber, R.; Bourenkov, G. P.;
Bartunik, H. D.; Bursakov, S.; Calvete, J.; Caldeira, J.; Carneiro, C.; Moura,
J. J. G.; Moura, I.; Romão, M. J. Structure 1999, 7, 65-79.
(12) Rajagopalan, K. V. AdV. Enzymol. Relat. Areas Mol. Biol. 1991,
64, 215-289.
(13) Cramer, S. P.; Wahl, R.; Rajagopalan, K. V. J. Am. Chem. Soc.
1981, 103, 7721-7727.
(14) George, G. N.; Garrett, R. M.; Prince, R. C.; Rajagopalan, K. V. J.
Am. Chem. Soc. 1996, 118, 8588-8592.
(15) George, G. N.; Kipke, C. A.; Prince, R. C.; Sunde, R. A.; Enemark,J. H.; Cramer, S. P. Biochemistry 1989, 28, 5075-5080.
(16) George, G. N.; Pickering, I. J.; Kisker, C. Inorg. Chem. 1999, 38,2539-2540.
(17) Garton, S. D.; Garrett, R. M.; Rajagopalan, K. V.; Johnson, M. K.
J. Am. Chem. Soc. 1997, 119, 2590-2591.
(18) Garrett, R. M.; Rajagopalan, K. V. J. Biol. Chem. 1996, 271, 73877391.
(19) Enemark, J. H.; Young, C. G. AdV. Inorg. Chem. 1993, 40, 1-88.

Izumi et al.
Single turnover experiments on DMSO reductase from Rhodobacter sphaeroides24 and on xanthine oxidase25 are consistent
with oxygen atom transfer (OAT) at the Mo center in these
enzymes and provide support for Scheme 1, proposed for sulfite
oxidase.
Extensive investigations into the chemistry of oxomolybdenum(IV), -(V), and -(VI) have accompanied the studies on thenative sulfite oxidases.19,26-28 Analogues incorporating thefacially coordinating hydrotris(3,5-dimethyl-1-pyrazolyl)borate(L) ligand have been particularly successful as functional mimics
for enzymes with [MoVIO2]2+ centers. The reaction of LMoVIO2X(X ) Cl, Br, OPh, SPh, SCH2Ph, SCH(CH3)2) with PPh3
generates an unsaturated “LMoIVOX” center that can be trappedwith pyridine to form LMoIVOX(pyridine). In wet, oxygenatedsolvents, “LMoIVOX” undergoes two successive one-electron
reactions through a paramagnetic LMoVOX(OH) intermediate
to regenerate the catalytic LMoVIO2X complex.29-31 Isotopic
oxygen atom tracer studies on this system demonstrate that theO atom transferred to PPh3 derives from the [MoO2]2+ centerand that H2O, not dioxygen, is the ultimate source of the O
atoms.32 This is the only synthetic system that incorporates the
key features of Scheme 1, proposed for the catalytic cycle ofsulfite oxidase. A theoretical study on the energetics of thiscatalytic cycle reveals that the direction of approach of thesubstrate to the [MoVIO2]2+ center in the OAT step is criticalto maximizing the stability of the “LMoIVOX(OPPh3)” adduct.33
The calculations also indicate that the displacement of theoxidized substrate from the “LMoIVOX(OPPh3)” center by H2O
occurs through a concerted associative mechanism. The Mo(IV), Mo(V), and Mo(VI) intermediates in the catalytic cycle
have been trapped and examined structurally and spectroscopically.29-32 LMoVOY2 (Y ) SR, OR; R ) alkyl, aryl) havebeen subjected to extensive EPR, PES (photoelectron spectroscopy), and MCD (magnetic circular dichroism) studies, and anelectronic structure model for these complexes has beendeveloped.34-37 These studies reveal considerable S ligand
contribution to the singly occupied dxy orbital of these complexes. The relative rates of OAT catalysis by LMoVIO2X
depend on X (X ) Cl > SR > OR) (Table 1).30,32(20) Lamy, M. T.; Gutteridge, S.; Bray, R. C. Biochem. J. 1980, 185,397-403.
(21) Bray, R. C.; Gutteridge, S.; Lamy, M. T.; Wilkinson, T. Biochem.
J. 1983, 211, 227-236.
(22) George, G. N.; Prince, R. C.; Kipke, C. A.; Sunde, R. A.; Enemark,J. H. Biochem. J. 1988, 256, 307-309.
(23) Gutteridge, S.; Lamy, M. T.; Bray, R. C. Biochem. J. 1980, 191,
285-288.
(24) Schultz, B. E.; Hille, R.; Holm, R. H. J. Am. Chem. Soc. 1995,
117, 827-828.
(25) Hille, R.; Sprecher, H. J. Biol. Chem. 1987, 262, 10914-10917.
(26) Holm, R. H. Chem. ReV. 1987, 87, 1401-1449.
(27) Holm, R. H. Coord. Chem. ReV. 1990, 100, 183-221.
(28) Schultz, B. E.; Holm, R. H. Inorg. Chem. 1993, 32, 4244-4248.
(29) Xiao, Z.; Bruck, M. A.; Doyle, C.; Enemark, J. H.; Grittini, C.;
Gable, R. W.; Wedd, A. G.; Young, C. G. Inorg. Chem. 1995, 34, 59505962.
(30) Roberts, S. A.; Young, C. G.; Kipke, C. A.; Cleland, W. E.;
Yamanouchi, K.; Carducci, M. D.; Enemark, J. H. Inorg. Chem. 1990, 29,
3650-3656.
(31) Xiao, Z.; Young, C. G.; Enemark, J. H.; Wedd, A. G. J. Am. Chem.
Soc. 1992, 114, 9194-9195.
(32) Xiao, Z.; Bruck, M. A.; Enemark, J. H.; Young, C. G.; Wedd, A.
G. Inorg. Chem. 1996, 35, 7508-7515.
(33) Pietsch, M. A.; Hall, M. B. Inorg. Chem. 1996, 35, 1273-1278.
(34) Dhawan, I. K.; Enemark, J. H. Inorg. Chem. 1996, 35, 4873-4882.
(35) Carducci, M. D.; Brown, C.; Solomon, E. I.; Enemark, J. H. J. Am.
Chem. Soc. 1994, 116, 11856-11868.
(36) Holm, R. H.; Berg, J. M. Acc. Chem. Res. 1986, 19, 363-370.
(37) Inscore, F. E.; McNaughton, R.; Westcott, B. L.; Helton, M. E.;
Jones, R.; Dhawan, I. K.; Enemark, J. H.; Kirk, M. L. Inorg. Chem. 1999,
38, 1401-1410.

Oxomolybdenum Complexes with Thiolate and Related Ligands

J. Am. Chem. Soc., Vol. 121, No. 43, 1999 10037

Table 1. Rate Constants for Reaction of Oxomolybdenum
Complexes with PPh3 at 298 K and Reduction Potentials
versus SCE
complexk (M-1 s-1)

E1/2 (V)b

LMoO2Cl
LMoO2(SPh)LMoO2(SCH2Ph)
LMoO2(OPh)LMoO2(OCH3)

very fast (J10-2)a,c
6 ×10-4 a

-0.62
-0.76
-0.84
-0.88
-1.13

2 ×10-6 a∼0aaReference 30. b Reference 29. c Reaction was too fast to bequantitatively measured.

The analysis of pre-edge X-ray absorption spectra (XAS) isestablished as an effective probe of the electronic structure ofan absorbing atom. Metal K-38-43 and L-edge44-47 XAS provides
a direct measure of the metal contribution to the half orunoccupied valence antibonding molecular orbitals. Ligand
K-edge XAS48-59 provides an experimental estimate of ligand
character in these valence orbitals due to covalent bonding,which is similar to information obtained from an analysis of
the ligand superhyperfine splittings obtained from EPR. How(38) Heald, S. M.; Tranquanda, J. M. In Physical Methods of Chemistry;
Rossiter, B. W., Hamilton, J. F., Eds.; Wiley: New York, 1990; Vol. 5, pp
189-272.
(39) Bianconi, A. In X-ray Absorption; Koningsbeiger, D. C., Prins, R.,
Eds.; Wiley: New York, 1988; pp 573-662.
(40) Kau, L. S.; Spira-Solomon, D. J.; Penner-Hahn, J. E.; Hodgson, K.
O.; Solomon, E. I. J. Am. Chem. Soc. 1987, 109, 6433-6442.
(41) Roe, A. L.; Schneider, D. J.; Mayer, R. J.; Pyrz, J. W.; Widom, J.;
Que, L., Jr. J. Am. Chem. Soc. 1984, 106, 1676-1681.
(42) Eidsness, M. K.; Sullivan, R. J.; Scott, R. A. In Bioinorganic
Chemistry of Nickel; Lancaster, J. R., Ed.; VCH: Deerfield Beach, FL,
1988; pp 73-92.
(43) Conradson, S. D.; Burgess, B. K.; Newton, W. E.; McDonald, J.
W.; Rubinson, J. R.; Gheller, S. F.; Mortenson, L. W.; Adams, M. W. W.;
Mascharack, P. K.; Armstrong, W. A.; Holm, R. H.; Hodgson, K. O. J.
Am. Chem. Soc. 1985, 107, 7935-7940.
(44) George, S. J.; Lowery, M. D.; Solomon, E. I.; Cramer, S. P. J. Am.
Chem. Soc. 1993, 115, 2968-2969.
(45) George, G. N.; Cleland, W. E., Jr.; Enemark, J. H.; Smith, B. E.;
Kipke, C. A.; Roberts, S. A.; Cramer, S. P. J. Am. Chem. Soc. 1990, 112,2541-2548.
(46) Mansour, A. N.; Cook, J., J W.; Sayers, D. E. J. Phys. Chem. 1984,
88, 2330-2334.
(47) Wang, H.; Ge, P.; Riordan, C. G.; Brooker, S.; Woomer, C. G.;
Collins, T.; Melendres, C. A.; Graudejus, O.; Bartlett, N.; Cramer, S. P. J.
Phys. Chem. B 1998, 102, 8343-8346.
(48) Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc.
1990, 112, 1643-1645.
(49) Hedman, B.; Frank, P.; Gheller, S. F.; Roe, A. L.; Newton, W. E.;
Hodgson, K. O. J. Am. Chem. Soc. 1988, 110, 3798-3805.
(50) Shadle, S. E.; Penner-Hahn, J. E.; Schugar, H. J.; Hedman, B.;
Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc. 1993, 115, 767-776.
(51) Shadle, S. E.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. Inorg.
Chem. 1994, 33, 4235-4244.
(52) (a) Shadle, S. E.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J.
Am. Chem. Soc. 1995, 117, 2259-2272. (b) Note that the R2 term in Table
6 of ref 52a is not appropriate for a core-to-valence CT transition: Neese,F.; Hedman, B.; Hodgson, K.; Solomon, E. I. Inorg. Chem., in press.
(53) Rose Williams, K.; Gamelin, D. R.; LaCroix, L. B.; Houser, R. P.;
Tolman, W. B.; Mulder, T. C.; de Vries, S.; Hedman, B.; Hodgson, K. O.;
Solomon, E. I. J. Am. Chem. Soc. 1997, 119, 613-614.
(54) Rose Williams, K.; Hedman, B.; Hodgson, K. O.; Solomon, E. I.
Inorg. Chim. Acta 1997, 263, 315-321.
(55) Rompel, A.; Andrews, J. C.; Cinco, R. M.; Wemple, M. W.;
Christou, G.; Law, N. A.; Pecoraro, V. L.; Sauer, K.; Yachandra, V. K.;
Klein, M. P. J. Am. Chem. Soc. 1997, 119, 4465-4470.
(56) Rose, K.; Shadle, S. E.; Eidsness, M. K.; Kurtz, D. M., Jr.; Scott,
R. A.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem. Soc.
1998, 120, 10743-10747.
(57) Jollet, F.; Petit, T.; Gota, S.; Thromat, N.; Gautiersoyer, M.; Pasturel,
A. J. Phys. Condens. Matter 1997, 43, 9393-9401.
(58) Wu, Z. Y.; Gota, S.; Jollet, F.; Pollak, M.; Gautiersoyer, M.; Natoli,
C. R. Phys. ReV. B 1997, 55, 2570-2577.
(59) Rose, K.; Shadle, S. E.; Glaser, T.; de Vries, S.; Cherepanov, A.;
Canters, G. W.; Hedman, B.; Hodgson, K. O.; Solomon, E. I. J. Am. Chem.
Soc. 1999, 121, 2353-2363.

Figure 1. Schematic representation of the contributions to the energyof the ligand K-edge and metal L-edge pre-edge features. The ligand
K-edge observes the transition from the ligand 1s to the antibonding
orbital(s) of metal md with ligand np. Metal L3- and L2-edges are thetransitions from 2P3/2 and 2P1/2 terms, respectively, to metal md, splitby the spin-orbit interaction due to the final state spin-orbit coupling.

ever, ligand K-edge XAS has the advantage of being applicable
to complexes without an EPR signal and to ligands without anuclear spin.
Ligand K-edge XAS probes the electronic transition from aligand 1s orbital (Figure 1). The pre-edge feature involves thetransition to the antibonding molecular orbital Ψ* ) (1 R′ 2)1/2ψM - R′ψL, where ψM and ψL are metal and ligand wave
functions, respectively, and R′ is the ligand coefficient in the
antibonding molecular orbital Ψ*.48,50-52 The transition intensityof the pre-edge feature is proportional to that of the dipoleallowed ligand-based 1s f 3p transition, weighted by its
antibonding character in Ψ* (R′2, eq 2).

I(ligand 1s f Ψ*) ) R′ 2I(ligand 1s f 3p)(2)

Thus, the pre-edge intensity provides a direct probe of the ligand(S or Cl) covalency in the unoccupied metal d orbitals. The
pre-edge energy of the ligand K-edge is dependent on therelative orbital energies of the Mo 4d and ligand 1s levels. Thesevary with the effective nuclear charges and the ligand field
splittings (Figure 1) within the complex.
Metal L-edge spectroscopy probes the electronic transition
from the metal 2p orbital to Ψ*. Spin-orbit coupling splits theMo 2p into the 2P3/2 (L3-edge) and the 2P1/2 (L2-edge) states,
separated by ∼105 eV (Figure 1). The intensity of thesetransitions is proportional to the dipole-allowed 2p f 4dtransition intensity (eq 3), where (1 - R′ 2) represents the metal
4d contribution to the Ψ* orbital.44

I(metal 2p f Ψ*) ) (1 - R′ 2)I(metal 2p f 4d)(3)

The pre-edge intensity of the metal L-edge complements theligand K-edge data and provides a direct probe of the metal
contribution (1 - R′ 2) to the unoccupied orbitals in the ligand
field manifold. The 2p and 4d spin-orbit and 2p core-hole4d multiplet interactions may affect the peak intensities of thesetransitions and must be considered in the analysis of the L3and L2-edge spectra.60(60) de Groot, F. M. F.; Hu, Z. W.; Lopez, M. F.; Kaindl, G.; Guillot,
F.; Tronc, M. J. Chem. Phys. 1994, 101, 6570-6576.

10038 J. Am. Chem. Soc., Vol. 121, No. 43, 1999
Herein, the ligand K- and metal L-edge spectra are reported
and analyzed for the diamagnetic Mo(VI) chromophores
LMoVIO2X (X ) Cl, SCH2Ph, OPh). The series includes the
benzyl thiolate complex to mimic the Mo-S interaction ofcysteine with the Mo center in the sulfite oxidases. The
experimental estimates of covalency are compared to density
functional calculations for analogues of each complex. These
results are used to obtain electronic structure insight into theoxo transfer reactivity for the LMoVIO2X complexes and toevaluate the role of the cysteine S in the function of the active
site of the sulfite oxidase family of oxomolybdoenzymes.
2. Experimental Section
2.1. Synthesis. All reactions were carried out under an argon
atmosphere using standard Schlenk line techniques. Tetrahydrofuran(THF) was dried and distilled from sodium and benzophenone. Toluene
was dried and distilled from sodium. The compounds LMoVIO2X(X ) Cl, SCH2Ph, OPh) were prepared according to publishedmethods.29,30 Sodium benzyl thiolate was prepared as follows. Sodium
sand was prepared by rapid stirring of molten sodium (0.250 g, 11mmol) in toluene (10 mL). After the mixture cooled, the toluene wasdecanted and the sodium washed with three portions of THF (10 mL).
The sodium sand was suspended in THF (20 mL), and benzyl mercaptan(1.76 mL, 15 mmol) was added rapidly. The reaction mixture was stirred
for 12 h. The white precipitate was removed by filtration and washedwith three portions of THF (25 mL) and then with three portions ofdiethyl ether (25 mL) and dried under vacuum. Yield was 1.35 g (84%).
2.2. Sample Preparation. LMoO2Cl, LMoO2(SCH2Ph), and LMoO2(OPh) were ground into a fine powder, which was dispersed as thinly
as possible on Mylar tape to minimize the possibility of saturation.
The procedure has been verified to minimize saturation effects in thedata by systematically testing progressively thinner samples until theobserved intensity no longer varies with the thickness of the sample.
The Mylar tape contained an acrylic adhesive which was determined
to have a level of S, Cl, and Mo contaminants below that which isdetectable under the conditions of the XAS measurements. The powder
on tape was mounted across the window of an aluminum plate. The
samples were prepared in dry, anaerobic atmospheres. A 6.35-µm
polypropylene window protected the samples from exposure to air
during sample transfer from the glovebox to the experimental He-filled
sample chamber.
2.3. X-ray Absorption Measurements. XAS data were measured
at the Stanford Synchrotron Radiation Laboratory using the 54-pole
wiggler beamline 6-2 in a high magnetic field mode of 10 kG with a
Ni-coated harmonic rejection mirror and a fully tuned Si(111) double
crystal monochromator under ring conditions of 3.0 GeV and 50-100
mA. The entire path of the beam was in a He atmosphere. Details of
the optimization of this setup for low-energy studies have been described
previously.50,52
All XAS measurements were made at room temperature in fluorescence excitation mode.61,62 For reproducibility, two or three scans were
measured for each sample. The maximum of the first pre-edge featurein the S K-edge spectrum of Na2S2O3‚5H2O was assigned to 2472.02
eV and was used for energy calibration of the S K- and Mo L-edges.
The energy of the Cl K-edge data was calibrated by using the energyof the first edge-region feature of Cs2CuCl4. The maximum of this peak
was assigned to 2820.20 eV. The scans ranges were 2420-2740 eV
for the S K- and Mo L3-, 2560-2880 eV for the L2-, and 2810-2850
eV for Cl K-edges, with a step size of 0.08 eV in the edge region. The
spectrometer energy resolution was ∼0.5 eV.48,50 Comparison of thefirst and second derivatives of the spectra of model compounds
measured repeatedly during different experimental sessions indicatesa reproducibility in edge position of ∼0.1 eV.
2.4. Data Analysis. A smooth background was removed from all
spectra by fitting a polynomial to the pre-edge regions and subtracting(61) Lytle, F. W.; Greegor, R. B.; Sandstrom, D. R.; Marques, E. C.;
Wong, J.; Spiro, C. L.; Huffman, G. P.; Huggins, F. E. Nucl. Instrum.
Methods 1984, 226, 542-548.
(62) Stern, E. A.; Heald, S. M. ReV. Sci. Instrum. 1979, 50, 1579-1582.

Izumi et al.
this polynomial from the entire spectrum. Normalizations of the S K-,
Cl K-, Mo L3-, and Mo L2-edge data were accomplished by fitting aflat polynomial or straight line to the post-edge region and normalizing
the edge jump to 1.0 at 2490, 2840, 2545, and 2655 eV, respectively.
The splining and normalization procedure for the Cl K-edge spectrumof LMoO2Cl is complicated by the presence of the Mo L1-edge at∼2866 eV. Utilizing the whole energy range to 3150 eV, i.e., ignoring
the intensity of the Mo L1-edge, yielded a normalization, which gave
the absolutely lowest limit for the pre-edge intensity, which was lower
than the true value by the total edge jump contribution of the Mo L1edge. A maximum pre-edge intensity was obtained by manuallyrescaling an estimated Cl K-edge-only edge jump from the spectrum,as the narrow Cl K-edge-only data range was too short to enable anaccurate spline fit.
Peak fittings of S or Cl K-edge spectra were performed on thenormalized data of LMoO2(SCH2Ph) with Na(SCH2Ph) as referenceand LMoO2Cl. The fitting program EDG_FIT,63 which utilizes the
public domain MINPAK fitting library,64 was used. Pre-edge features
were modeled by pseudo-Voigt line shapes (simple sums of Lorentzianand Gaussian functions). This line shape is appropriate, as theexperimental features are expected to be a convolution of the Lorentziantransition envelope48 and the Gaussian line shape imposed by thespectrometer optics.50,61 A fixed 1:1 ratio of Lorentzian to Gaussian
contributions for the pre-edge feature successfully reproduced the S
and Cl K-edge spectral features. For the peak fitting of Mo L3- andL2-edge spectra, the Lorentzian-to-Gaussian ratio was varied. Best fitswere obtained when the Lorentzian component was more than 70%.
The rising edge is an arctangent function obtained from fits to the Mo
L3- and L2-edge spectra of Mo foil (L3 ) 2521.01 and L2 ) 2626.20
eV).
Fits used in the calculation of pre-edge peak intensity were optimized
to reproduce both the data and their second derivatives. The peakintensity was approximated by peak area, calculated as the height ×full width at half-maximum (fwhm). The standard deviation of theaverage of the areas was calculated to quantitate the uncertainty of thefit for each sample. Our fit criterion is that Rf ) ∑[y(data) - y(fit)]2/∑[y(data)]2 should be less than 5%.
There are several possible sources of systematic error in the analysisof these spectra. Normalization procedures can introduce a 1-3%
difference in pre-edge peak intensity. This maximum of ∼3% error
and the error resulting from the fit procedure discussed above weretaken into account in the calculation of pre-edge intensities.
2.5. DFT Calculations. Spin-restricted calculations were performed
using ADF version 2.0.1 employing the local density approximation
formulated by Vosko, Wilk, and Nusair.65 Nonlocal gradient corrections
were included for exchange (Becke66) and for correlation (Perdew67)
effects. Basis functions, core expansion functions, core coefficients,and fit functions for Mo, P, S, Cl, C, N, and O were used as provided
from database IV of the ADF suite. This includes Slater type orbital(STO) triple-ζ basis sets for Mo, P, S, Cl, C, N, and O and a single-ζ
polarization function for P, S, Cl, C, N, and O. The functions used for
H were from database I, which includes a single-ζ STO basis without
polarization functions. All core levels (up to 4p for Mo, up to 2p for
P, S, Cl, and the 1s for C, N, O) were treated as frozen orbitals andorthogonalized to the valence orbitals with core expansion functions.
The DFT calculations were performed on models in which thenitrogen atoms of the ligand L were replaced by three ammonia
molecules and the thiolate and alkoxide ligands were represented by
SCH3 and OCH3, respectively (Chart 1). The geometry of the [(NH3)3MoO2(SCH3)]+ model was based on the crystal structure of LMoO2(SPh)29 and was idealized to Cs symmetry. The structure of LMoO2Cl
was assumed to be that of LMoO2(SCH3) with substitution of chloride
for thiolate. The Mo-Cl distance was obtained by geometry optimiza(63) Written by G. N. George at Stanford Synchrotron Radiation
Laboratory.
(64) Garbow, B. S.; Hillstrom, K. E.; More, J. J. MINPAK; Argonne
National Laboratory: Argonne, IL, 1980.
(65) Vosko, S. H.; Wilk, L.; Nusair, M. Can. J. Phys. 1980, 58, 12001211.
(66) Becke, A. D. Phys. ReV. A 1988, 38, 3098-3100.
(67) Perdew, J. P. Phys. ReV. B 1986, 33, 8822-8824.

Oxomolybdenum Complexes with Thiolate and Related Ligands

J. Am. Chem. Soc., Vol. 121, No. 43, 1999 10039

Chart 1. Coordinate Systems of [(NH3)3MoO2(SCH3)]+ (a),[(NH3)3MoO2Cl]+ (b), and [(NH3)3MoO2(OCH3)]+ (c) for
DFT CalculationsaaMolecular parameters appear in Table S1 (Supporting Information).

Scheme 2. Molecular Structures I, II, and III along theReaction Coordinate for Oxygen Atom Transfer (OAT) from[(NH3)3MoO2(SCH3)]+ to P(CH3)333 a

a Bond distances and angles for each structure are given in Table
S1 (Supporting Information).

tion using a quasi Newton approach.68 The resultant distance of 2.358
Å is in the range of Mo-Cl distances of 2.35-2.40 Å obtained froma search in the Cambridge Structural Database (CSD)69 for the cisMoVIO2Cl fragment. The Cl-ModO angles are in the range from 95°
to 97°. The calculations for [(NH3)3MoO2(OCH3)]+ were based on the
crystal structure of L′MoO2(OCH3) (L′ ) hydrotris(3-isopropyl)pyrazol1-yl)borate)29 and employed N-H and C-H distances and H-N-H
and H-C-H angles identical to those of [(NH3)3MoO2(SCH3)]+. The
coordinate system is rotated by 45° around the z-axis from the usual
coordinate system for Oh complexes. The yz-plane is the mirror planeand contains the S-C, Cl, Oal-C (Oal ) oxygen atom of alkoxide),and N1 (axial) atoms. The O1 and O2 atoms lie in the xy-plane, and they-axis bisects the O1dModO2 angle (Chart 1).
The reactivity of LMoO2X complexes with phosphines was investigated by DFT calculations of the interactions of the [(NH3)3MoO2X]+(X ) SCH3, Cl, OCH3) models with P(CH3)3 70 under three sets ofconditions: structure I, in which the geometry of the Mo complex was
not perturbed, and intermediate structures II and III, which involved
perturbation of the metal center upon interaction of one oxo group withthe phosphine (Scheme 2). The parameters for structures I, II, and III
were based on the calculations of Pietsch and Hall.33 The Mo-N
distances trans to O1 and O2 in structures I, II, and III were estimatedfrom the crystal structures of L′MoO2(OCH3)29 and LMoO(SPh)(pyridine).32 Detailed geometric parameters for the MO calculations
are given in Table S1 (Supporting Information).

3. Results
3.1. X-ray Absorption Spectroscopy. A. S K-Edge Data.
The normalized S K-edge spectra of LMoO2(SCH2Ph) and Na(SCH2Ph) are shown in Figure 2a. A strong pre-edge featureappears at 2470.5 eV in the spectrum of LMoO2(SCH2Ph) which
is not present in the spectrum of the Na(SCH2Ph). Further, the(68) Fan, L.; Ziegler, T. J. Chem. Phys. 1991, 95, 7401-7408.
(69) Allen, F. H.; Kennard, O. 3D Search and reference using theCambridge Structural Database. Chem. Des. Autom. News 1993, 8, 31.
(70) McKean, D. C.; McQuillan, G. P.; Murphy, W. F.; Zerbetto, F. J.
Phys. Chem. 1990, 94, 4820-4831.

Figure 2. (a) Normalized S K-edge spectra of LMoO2(SCH2Ph) (solidline) and Na(SCH2Ph) (dashed line). (b) Relationship between risingedge inflection point of the S K-edge data and the charge (q) on the S
atom determined by Mulliken population analysis of the DFT calculations for Na(SCH2Ph), Na2(mnt), and Na(Et2dtc) (q ) -1176.3 +0.47551x, R ) 0.99864). (c) Difference spectrum (bold solid line) of
normalized data for LMoO2(SCH2Ph) with an energy shift of +1.3 eVfrom the Na(SCH2Ph) data. Representative peak fit (solid lines) andtheir sum (dotted line).

S K-edge peak at 2473.1 eV of LMoO2(SCH2Ph) is more intensethan the corresponding feature of Na(SCH2Ph), suggesting thatsome of the intensity in this region of the spectrum results fromthe overlap of an additional pre-edge feature. The S K-edge
spectrum of LMoO2(SCH2Ph) contrasts with that of the Cu(II)(d9)-containing plastocyanin,50,71,72 which exhibits only one
peak at 2469.0 eV. This is consistent with transitions to morethan one unoccupied d orbital in the Mo(VI) complexes.
The S K-edge of Na(SCH2Ph) (2471.6 eV) is shifted to lower
energy relative to that of LMoO2(SCH2Ph), which is indicativeof a greater effective nuclear charge on the S atom in(71) Penfield, K. W.; Gewirth, A. A.; Solomon, E. I. J. Am. Chem. Soc.
1985, 107, 4519-4529.
(72) Gewirth, A. A.; Solomon, E. I. J. Am. Chem. Soc. 1988, 110, 38113819.

10040 J. Am. Chem. Soc., Vol. 121, No. 43, 1999

Izumi et al.

Figure 4. Normalized Mo L2-edge spectra of LMoO2(SCH2Ph) (solidline), LMoO2Cl (dashed line), LMoO2(OPh) (dotted line), and Mo foil
(dash-dotted line).

Figure 3. (a) Normalized Cl K-edge spectra of LMoO2Cl. The
spectrum was normalized utilizing the whole energy range to 3150 eV,
ignoring the intensity of the Mo L1 edge at ∼2866 eV. The dashedline is a graphical representation of the manual rescaling of an estimatedCl K-edge jump for a maximal pre-edge intensity (see Data Analysis).
(b) Representative peak fit (solid lines) and their sum (dotted line).

LMoO2(SCH2Ph). Prior to background subtraction, the absorption edge of Na(SCH2Ph) must be shifted to the absorption edgeof LMoO2(SCH2Ph). An estimate of edge energy can be madethrough a correlation between the charge on the S atom andthe edge position of essentially ionic thiolate salts: Na(SCH2Ph), Na2(mnt) and Na(Et2dtc). A plot of edge energies against
the charge on the S atom, estimated from a Mulliken population
analysis obtained from DFT calculations, is shown in Figure
2b. DFT calculations on [(NH3)3MoO2(SCH3)]+ give a chargeof -0.388 for the S atom. Thus, the absorption edge position
for LMoO2(SCH2Ph) is estimated to be 2472.9 eV, +1.3 eV tohigher energy than that for Na(SCH2Ph). The difference
spectrum of the +1.3 eV-shifted Na(SCH2Ph) and LMoO2(SCH2Ph) spectra is given in Figure 2c and has two major features at
2470.5 and 2472.5 eV, which are assigned as Mo-S pre-edge
features. The low-energy feature is substantially broader thanthe S pre-edge peak of plastocyanin (fwhm ∼ 1.7 vs 0.9 eV),
indicating that more than one transition contributes to this peak.
The total integrated intensity of the pre-edge feature is 2.28.
B. Cl K-Edge Data. The Cl K-edge spectrum of LMoO2Cl(normalized for the lowest limit of the pre-edge intensity) isshown in Figure 3a. The dashed line gives the estimate for thenormalization which yields the highest limit of the pre-edge
intensity (see Data Analysis). In contrast to the corresponding
S K-edge of LMoO2(SCH2Ph), the two main pre-edge featuresat 2821.9 and 2824.2 eV are well separated from the rising edge
region. Thus, a background subtraction procedure, as describedabove, is not necessary. The lower peak is broader than thatfor [CuCl4]2- (fwhm ∼ 1.6 vs 1.1 eV),50 indicating that morethan one transition contributes to this feature in LMoO2Cl. The
integrated intensity of the pre-edge features lies between 2.10
and 2.63.

C. Mo L-Edge Data. The Mo L2-edge spectra of LMoO2(SCH2Ph), LMoO2Cl, LMoO2(OPh), and Mo foil are shown in
Figure 4. Compared to the featureless spectrum of the Mo foil,
the L2-edge spectrum of LMoO2(SCH2Ph) is shifted towardhigher energy and exhibits three peaks at 2630.1, 2632.2, and2633.9 eV. The relatively flat spectrum of the Mo foil may be
due to saturation effects associated with the fluorescence
detection. The L2-edge features of LMoO2Cl are at 2630.4,
2632.4, and 2634.1 eV, while those for LMoO2(OPh) are at
2630.4, 2632.9, and 2633.9 eV. The splitting between the twohigher energy peaks is smaller for LMoO2(OPh) than for theother two complexes. The energy splittings within the L3-edge
spectra of LMoO2(SCH2Ph), LMoO2Cl, and LMoO2(OPh)(Supporting Information) are almost identical with those of theirrespective L2-edge spectra. However, the intensities of the lower
energy peaks in the L2-edge spectra are greater and those of
the middle and higher energy peaks are lower compared to thecorresponding features in the L3-edge spectra. Similar differences in intensity between Mo L2/L3-edge spectra have also been
observed for a variety of inorganic Mo complexes49,73 and havebeen associated with the effects of multiplet splitting.60 Therefore, our analysis focuses on the L2-edge features, where theseeffects are estimated to be small. The total peak intensities of
L2-edge spectra are in the order LMoO2(OPh) > LMoO2Cl >LMoO2(SCH2Ph) (Figure 4).
3.2. DFT Calculations. The calculated ligand field splittingsfor [(NH3)3MoO2X]+ (X ) SCH3, Cl, OCH3) are shown in
Figure 5, and the S 3p, Cl 3p, Oal 2p, and Mo 4d characters ofthe valence orbitals are listed in Table 2. The valence orbitalsof the two oxo groups are classified as σ+, σ-, πIP,+, πIP,-, πOP,+,and πOP,-. The subscripts IP/OP designate in/out of the xy-plane,
and the subscripts +/- designate the in-phase and out-of-phasecombinations of the 2p orbitals on each oxo group. The σ+,σ-, πIP,+, πOP,+, and πOP,- orbitals interact with the Mo dz2,
dxy, dx2-y2, dyz, and dxz orbitals, respectively. The πIP,- orbital
does not interact with the Mo d orbitals. The bonding is
dominated by the interactions of the [MoO2]2+ core, and all
three complexes show the same ordering of the Mo 4d orbitals.
The dxy and dz2 orbitals, derived from the eg set in Oh symmetry,are most destablized, with the energy of dxy > dz2. The dxy orbital
has a strong antibonding interaction with the oxo σ-* orbital,
and the dz2 orbital has a small contribution from oxo σ+*. The
orbitals derived from the t2g set in Oh symmetry have the energy
order dx2-y2 > dxz > dyz. This order results from a strong(73) Hedman, B.; Penner-Hahn, J. E.; Hodgson, R. O. In EXAFS andNear Edge Structure III, Proceedings of an International Conference,
Stanford, CA, July 16-20, 1984; Hedman, B., Penner-Hahn, J. E., Hodgson,
K. O., Eds.; Springer-Verlag: Berlin, 1984; pp 64-66.

Oxomolybdenum Complexes with Thiolate and Related Ligands

J. Am. Chem. Soc., Vol. 121, No. 43, 1999 10041

Figure 5. Energy diagram of the Mo 4d orbitals and the character for the ground state of [(NH3)3MoO2(SCH3)]+, [(NH3)3MoO2Cl]+, and [(NH3)3MoO2(OCH3)]+ obtained by DFT calculations using the geometries of Chart 1. The energy separations between the orbitals are given in electronvolts.
Table 2. Comparison of the Mo 4d Orbital Character and Relative Energies for [(NH3)3MoO2(SCH3)]+ (A), [(NH3)3MoO2Cl]+ (B), and[(NH3)3MoO2(OCH3)]+ (C) by DFT Calculations(A) [(NH3)3MoO2(SCH3)]+ a
orbitalcharacter

17a′dyz-O π*12a′′dxz-O π*-S π*

18a′dx2-y2-O π*

20a′dz2-S pseudo-σ*-O σ*

13a′′dxy-O σ*S 3p character (%)
Mo 4d character (%)
relative energy (eV)

2.90
58.74
0

11.69
54.89
0.606

3.44
54.83
1.198

17.50
31.99
3.072

0.74
50.15
4.838

(B) [(NH3)3MoO2Cl]+ b
orbitalcharacter

15a′dyz-O π*-Cl π*

11a′′dxz-O π*16a′dx2-y2-O π*

17a′dz2-O σ*-Cl σ*-N1 σ*

12a′′dxy-O σ*Cl 3p character (%)
Mo 4d character (%)
relative energy (eV)

10.03
58.76
0

4.89
57.65
0.316

2.26
56.24
1.085

12.05
48.94
2.706

0.20
51.48
4.839

(C) [(NH3)3MoO2(OCH3)]+ c
orbitalcharacter

17a′dyz-O π*-Oal pseudo-σ*

12a′′dxz-O π*-Oal π*18a′dx2-y2-O π*

20a′dz2-O σ*13a′′
dxy-O σ*Oal 2p character (%)
Mo 4d character (%)
relative energy (eV)

10.68
58.44
0

8.21
57.22
0.427

0.20
55.86
0.729

3.35
50.47
3.005

0
48.92
4.194

a The summation of S 3p character across five orbitals is 36.27% (total S 3p character). b The summation of Cl 3p character across five orbitals
is 29.43% (total Cl 3p character). c The summation of O 2p character across five orbitals is 22.44% (total Oal 2p character).

interaction between the dx2-y2 and oxo πIP,+* orbitals and froma greater overlap of dxz with oxo πOP,-* compared to dyz with
πOP,+*, due to the OdModO angle (∼103°).
The splittings of the Mo 4d orbitals are further modulatedby anisotropic bonding interactions with the X ligand, as shownin Figure 5 and the representative contour plots of Figure 6.
The 16° tilt of the Mo-X bond from the z-axis introduces
bonding anisotropy that is common to all X ligands (Figure 7).
For X ) Cl, the three 3p orbitals of Cl can form one σ and two
π bonds to Mo, and the only perturbing factor is the tilt of the
Mo-Cl bond. The Cl σ is antibonding to the dz2 orbital. The Cl
π* overlap with the dyz orbital (Figure 6d, Table 2B) is morethan twice the Cl π* contribution that destabilizes the dxz orbital(Figure 6e). For X ) SCH3, one of the three 3p orbitals of the
S atom of the thiolate ligand is used for S-C bonding, and theremaining two are available for π and pseudo-σ bonding to the
Mo. The term pseudo-σ is associated with the deviation of the
C-S-Mo angle (105.8°) from 90°.74 The S pseudo-σ* orbital
interacts primarily with the dz2 orbital (Figure 6c), but there arealso small contributions of the S pseudo-σ* to the dyz (Figure6a) and the dx2-y2 orbitals. The thiolate π* orbital overlaps
principally with dxz (Figure 6b), in contrast to X ) Cl, andthereby increases the splitting between the dyz and dxz orbitals
already induced by the overlap difference with πOP,+* andπOP,-*, respectively. The anisotropy of the thiolate π* interaction
with dxz and dyz also varies with the Mo-S-CH3 torsional angle(Figure 8). For X ) OCH3, the bonding is similar to that for
SCH3; the three 2p orbitals of the Oal are used in Oal-C bonding(74) Gebhard, M. S.; Deaton, J. C.; Koch, S. A.; Millar, M.; Solomon,
E. I. J. Am. Chem. Soc. 1990, 112, 2217-2231.

10042 J. Am. Chem. Soc., Vol. 121, No. 43, 1999

Figure 6. ADF contour plots of 17a′ (dyz) (a), 12a′′ (dxz) (b), 20a′ (dz2)(c) for [(NH3)3MoO2(SCH3)]+; 15a′ (dyz) (d), 11a′′ (dxz) (e), 17a′ (dz2)(f) for [(NH3)3MoO2Cl]+; 17a′ (dyz) (g), 12a′′ (dxz) (h), 20a′ (dz2) (i) for[(NH3)3MoO2(OCH3)]+.

Izumi et al.

Figure 8. (a) Calculated Mo dyz and dxz orbital energy changes and(b) calculated O1 and O2 pz character when the methyl group of thethiolate is rotated around the Mo-S bond for [(NH3)3MoO2(SCH3)]+.
This torsional angle is measured relative to the yz plane and is in an
anticlockwise sense.

Oal pseudo-σ* orbital with the dyz orbital that shifts it to highest
energy. The energy splitting of the dyz and dxz orbitals isdetermined by anisotropic contributions from S, Cl, or Oal in
addition to the strong πIP/OP bonds from the two oxo groups.
The splitting is largest (0.606 eV) for X ) SCH3, where the dxz
orbital is further destabilized by a S π* interaction; intermediate(0.427 eV) for X ) OCH3, where both the dxz and dyz orbitals
are destabilized by Oal pseudo-σ* and π* contributions; andsmallest (0.316 eV) for X ) Cl, where the dyz orbital isdestabilized by a Cl π* interaction (Figure 7).
4. Analysis: Peak Fit and Spectral Assignments

Figure 7. Energies and pictorial representations of the principal
interactions of the dyz and dxz orbitals with the oxo πOP,- and πOP,+ sets
and the Cl, S, Oal ligands.

and in σ and π bonding to Mo. The alkoxide π* interacts withthe dxz orbital (Figure 6h). The C-Oal-Mo angle of 139.7° 29
leads to overlap of the Oal pseudo-σ* orbital with the dyz orbital(Figure 6g, Table 2C) that is more than 3 times larger than theoverlap with the dz2 orbital (Figure 6i). This orbital composition
contrasts with that for X ) SCH3, where the dominant S pseudoσ* overlap is with the dz2 orbital (Figure 6c).
The calculated total covalency of the Mo-X bond for thethree [(NH3)3MoO2X]+ complexes increases in the order MoOCH3 < Mo-Cl < Mo-SCH3 (Table 2). The energy of theredox-active orbital depends on X [Cl (-8.326) < SCH3(-7.724) < OCH3 (-7.229 eV)], but the Mo 4dyz character ofthe orbital is similar for all three complexes. The estimatedcharge on the Mo ion from a Mulliken population analysis for
X ) Cl (+2.242) and X ) SCH3 (+2.207) is consistent withthe energy order.75 However, the estimated higher charge on
Mo for X ) OCH3 (+2.432) does not lower the energy of theredox-active orbital. Rather, it is the significant overlap of the(75) Cimino, A.; de Angelis, B. A. J. Catal. 1975, 36, 11-22.

A. S K-Edge. The two strong peaks in the difference
spectrum of LMoO2(SCH2Ph) (Figure 2c) were first modeledwith only two peaks. The fwhm were fixed in the range of 0.91.1 eV, values that have been observed for the pre-edge ofplastocyanin.50,53 The difference of the spectrum and this twopeak model gives rise to three additional features, a stronger
one in the center and two weaker ones at the sides. A reasonable
simulation with this five-peak model is shown in Figure 2c,and the peak areas and energies are listed in Table 3A. Due tothe subtraction procedure described in the Results section, theenergies and intensities can only be analyzed in a qualitative
manner, but the total intensity is reasonable.
Using the DFT calculations as a guide, the two strong peaks
at 2470.7 and 2472.5 eV can be assigned as transitions to thedxz-S π* (12a′′) and dz2-S pseudo-σ* (20a′) orbitals, respectively (Figure 5). The splitting is found to be 1.8 eV, supportingthe calculated orbital splitting of dxz and dz2 (2.47 eV), assuming
a final state reduction of ∼0.7. The other three weaker peaks,
at 2470.2, 2471.5, and 2472.5 eV, are assigned to S pseudo-σ*
contributions to dyz (17a′), dx2-y2 (18a′), and dxy (13a′′) respectively, based on their energies and low peak intensities incomparison to the coefficients in Table 2A. The peak areas andenergies (Table 3A) are in qualitative agreement with the S 3p
character in the five Mo 4d orbitals obtained from the DFT
calculations (Table 2A). The differences are due to final state
relaxation effects; e.g., the electron-electron repulsion contribution in the final state relaxation varies for different transitions
due to differences in delocalization over the ligands. Addition-

Oxomolybdenum Complexes with Thiolate and Related Ligands

J. Am. Chem. Soc., Vol. 121, No. 43, 1999 10043

Table 3. Average Deconvoluted Peak Area and Energy from S K- and Cl K-Edges for Oxomolybdenum Complexes
peak
edge

sampleLMoO2(SCH2Ph)a area
energy (eV)relative to peak 1(B) Cl K LMoO2Clb
area
energy (eV)relative to peak 1(A) S K

1

2

3

0.24 ( 0.01
2470.20 ( 0.06
00.65 ( 0.02
2821.81 ( 0.01
00.70 ( 0.08
2470.68 ( 0.06
0.48
0.31 ( 0.07
2822.56 ( 0.09
0.75

0.32 ( 0.05
2471.51 ( 0.04
1.31
0.34 ( 0.03
2823.36 ( 0.15
1.55

4

5

total

0.86 ( 0.04
0.16 ( 0.04
2.28
2472.49 ( 0.02 2472.95 ( 0.02
2.29
2.75
0.79 ( 0.04
2.10
2824.27 ( 0.04
2.46

a
The errors given for the S K-edge fitting are for the fitting procedure to the difference spectrum obtained from the correlation described in the
Results section. b The areas of the Cl pre-edge peaks are given for the lowest intensity limit for pre-edge intensity (see text). The highest intensity
limit is obtained by multiplying by 1.25.

ally, the subtraction procedure yields large uncertainties,
especially for the higher energy part of the pre-edge.
To quantify the covalency, an equation relating the experimentally observed pre-edge intensity (D0) to ligand covalency
for the d0 system, based on the dipole strength expressions of
ref 52, is given in eq 4. This dipole strength expression for theintensity of a ligand K-edge transition for metal ions with only
one parent excited state is52

D0 )

(

)

ht2
he
c2 + c2 〈s|r|p〉2
3 t2 3 e(4)where ht2 and he are the number of holes in the t2 and e orbitals,
respectively, ct22 and c2e are the ligand characters in the t2 and eorbitals, respectively, and 〈s|r|p〉 is the transition moment
integral. The simple form of eq 4 derives from the weakcoupling of the ligand 1s core hole with the metal ion final
states. For a d0 system ht2 ) 6 and he ) 4. Note that while, in
ref 52a, only tetrahedral complexes were analyzed, octahedral
complexes may also be treated with this methodology. Thus,
ct22g and ce2g become the ligand π- and σ-covalencies in the t2g
and eg orbitals, respectively.
Application of eq 4 to the total S K pre-edge intensity of
LMoO2(SCH2Ph), using plastocyanin (renormalized intensity
1.02; 38% thiolate covalency)50,76 as the reference, yields a total
covalency, i.e., the total contribution of the thiolate ligand to
the five Mo d orbitals, of ∼42%. This value is 1.2 times greaterthan the total covalency obtained from the molecular orbital
calculation (36%, Table 2A).
In summary, the two main S K-edge peaks are assigned as S
1s transitions to the dxz-S π* and dz2-S pseudo-σ* molecularorbitals. The additional weak features are assigned to the dyz,
dx2-y2, and dxy orbitals, which have some limited overlap with
the S pseudo-σ* orbital.
B. Cl K-Edge. The spectrum of LMoO2Cl (Figure 3) showsat least three features in the pre-edge region, two strong peaks
2821.8 and 2824.3 eV and some intensity in the region between
these peaks. Fits with only three pre-edge peaks do not well
reproduce the region between the two strong peaks. Four peakmodels fit the absorption data and their second derivative. The
average peak areas and energies are listed in Table 3B, and a
representative fit is shown in Figure 3b. These values are morereliable than the corresponding S K-edge values because no
subtraction procedure was necessary for the Cl K-edge.
The two distinct peaks at 2821.8 and 2824.3 eV are assigned
as Cl 1s transitions to the dyz-Cl π* (15a′) and dz2-Cl σ* (17a′)levels, respectively, using the DFT calculations as a benchmark(Figure 5). The splitting is 2.5 eV, which is consistent with the(76) Note that the renormalization intensities used for the chloride andthiolate pre-edge involve normalization of the edge jump for each ligand
and thus can be compared for the same ligand type but not between different
ligand types.

orbital splitting of 2.71 eV from the ground-state calculations,assuming a final state relaxation factor of ∼0.9. The two weakerpeaks at 2822.6 and 2823.4 eV are assigned as transitions to
the Cl π* component of dxz and the Cl σ* component of thedx2-y2 levels, respectively, on the basis of their energies relative
to two main peaks and their reduced peak intensities. The ratiosof peak areas (Table 3B) are in reasonable agreement with therelative Cl 3p character in four Mo 4d orbitals from the DFT
calculations (Table 2B). The Cl 3p character in the dxy orbitalis negligible, supporting the four-peak fit.
The measured intensity of the pre-edge feature of the Cl
K-edge (2.1-2.6) yields [using eq 4 and D2d-[CuCl4]2(normalized intensity 0.526, 30% Cl covalency48,50)76 as thereference for calculation of the transition moment integral] a
total covalency over the five d orbitals of 15-19%. The
covalency obtained from the DFT calculation is ∼29%. Because
the structure of [LMoO2Cl] is not known, DFT calculations werealso performed on structures with varying Mo-Cl distances (upto 2.6 Å) and changes in the tilt angle of the Mo-Cl vector(from 0 to 16°). The calculated covalency varied by only a few
percent. DFT calculations using the ADF program suite on
mono- and binuclear iron chloride and thiolate complexes also
give an overestimation of the covalency for chloride and anunderestimation for sulfur ligation relative to experimental
values.77
C. Mo L2-Edge. The peak fits and spectral assignments for
the Mo L2-edge data are given in the Supporting Information.
5. Discussion
5.1. Description of the Bonding in [(NH3)3MoO2X]+ (X )SCH3, Cl, and OCH3) and Relation to Spectroscopic Data.
The DFT calculations for the model dioxomolybdenum complexes [(NH3)3MoO2X]+ (X ) SCH3, Cl, and OCH3) show thesame calculated energy order of the five Mo 4d orbitals for all
three complexes (dyz < dxz < dx2-y2 < dz2< dxy), consistent withthe two cis-oxo groups dominating the ligand field (Figure 5,
section 3.2). The energies are further perturbed by additional
covalent contributions from the X ligand. The splitting of thedxz and dyz orbitals increases in the order Cl < Oal < S, and the
major perturbing factor is the presence of the CH3 group in thethiolate and alkoxide ligands, which essentially eliminates oneof the valence π orbitals from bonding to the Mo d orbitals.
The Mo-X-CH3 torsional angle and the Mo-X-CH3 bondangles further modulate the overlap of the remaining pseudo-σ
and π orbitals with the Mo 4d orbitals (Figures 6 and 8). The
key orbital interactions with X are the following: Cl π* to dyz
and Cl σ* to dz2 for X ) Cl; S π* to dxz and S pseudo-σ* to dz2
for X ) SCH3; Oal π* to dxz and Oal pseudo-σ* to dxz for X )OCH3. The Cl and S K-edge spectra provide experimental proofof the two dominant (pseudo-σ* and π*) contributions to metal(77) Glaser, T.; Kennepohl, P.; Solomon, E. I. Unpublished results.

10044 J. Am. Chem. Soc., Vol. 121, No. 43, 1999

Izumi et al.

ligand covalency in LMoO2X compounds. The Mo L2-edge
spectra reflect the trend of total covalency of Cl, S, and Oal
with Mo: LMoO2(SCH2Ph) J LMoO2Cl > LMoO2(OPh).
5.2. Correlation to Reactivity. A. Reduction Potential. The
data in Table 1 show that the nature of X influences the
one-electron reduction potential of LMoO2X complexes(MoVI f MoV) as well as the rates of the two-electron reduction(MoVI f MoIV) that occurs during the OAT reaction of thesecomplexes with PPh3. The following sections consider each ofthese properties in light of the spectroscopic and theoreticalinvestigations of these systems described above.
There are several factors that influence redox potentials insolution. These include the effective nuclear charge on the metal
ion, the energy of the redox-active orbital, and electronic
relaxation.78 With increasing charge at the metal center, reduction should be easier; i.e., the reduction potential should increase.
The effective nuclear charge on the Mo in the [(NH3)3MoO2X]+
analogues was estimated from a Mulliken population analysisof the DFT results and the application of Slater’s rules (+4.67
for X ) SCH3, +4.68 for X ) Cl, and +4.75 for X ) OCH3).
There is no correlation between these calculated effective nuclear
charges and the experimental reduction potentials of Table 1.
However, the calculated energies of the redox active orbital (dyz,Figure 5: -8.326 for X ) Cl, -7.724 for X ) SCH3, and-7.229 eV for X ) OCH3) correlate well with the experimental
reduction potentials. The significant interaction with the Oal
pseudo-σ* destabilizes the dyz orbital and makes the dominant
contribution to the low reduction potential of X ) OCH3.
Geometric and electronic structural changes on reduction canalso contribute to the reduction potential of a metal complex.
For the [LMoO2(SPh)]0/- pair, the reduced MoV species has
longer MdO and Mo-S distances and a larger OdModO
angle.79 DFT calculations on a [(NH3)3MoVO2(SCH3)]0 model
idealized to Cs symmetry showed that interactions between theoxo groups and the Mo 4d orbitals dominate the ligand fieldsuch that the 4d orbital energy order of the MoVI complex(Figure 5, left-hand side) is conserved in the MoV complex.
The major contributions from S are π* (6.18%) to the dxz orbital
and pseudo-σ* (17.16%) to the dz2 orbital. Although thecalculated Mo-S covalency for the MoV complex is less thanthat for the MoVI thiolate complex (Table 2A), the generalbonding description is the same. Thus, it is reasonable to inferthat the experimental order of the reduction potentials (Cl >SCH2Ph > OCH3) reflects the differences in the anisotropic
covalent bonding interactions of the axial chloride, thiolate, andalkoxide ligands upon the energy of the redox-active orbital.
B. Oxo Transfer Reactivity. Oxygen atom transfer (OAT)
from the cis-[MoVIO2]2+ fragment to sulfite is proposed for the
first step in the catalytic cycle of sulfite oxidase (Scheme 1).19
Reactions of LMoVIO2X (X ) Cl, SPh, OPh, OCH3) with PPh3
mimic this OAT functionality, with the observed rate order being
Cl > SPh > OPh > OCH3 (Table 1) for the reduction of
LMoVIO2X to “LMoIVOX” and oxidation of PPh3 to OPPh3.
A theoretical model, employing Hartree-Fock and MøllerPlesset perturbation theory, has been used to propose intermediates for both the oxo transfer step and the subsequent displacement of the OPPh3 product by water.33 The energetics of thereaction pathway were probed using P(CH3)3 and cis-[(NH3)2MoO2(SH)2]0 as the model complex and by consideration of

one possible reaction mechanism for oxo transfer.36,80 The
geometries of the intermediates were optimized at the restricted
Hartree-Fock level and reveal that P(CH3)3 approaches one O
atom of cis-[(NH3)2MoO2(SH)2]0 at a OdModOsP dihedral
angle of approximately 90° and at a ModOsP angle of 130.7°.
A weak P-O interaction develops (P‚‚‚O ) 2.43 Å) at the topof an activation barrier of 14 kcal mol-1. Rotation of the P(CH3)3
group about the Mo-O bond to a OdModOsP dihedral angleof 0° generates a Mo(IV) intermediate that is approximately 69
kcal mol-1 lower in energy due to the formation of a PdO bond.
Displacement of OP(CH3)3 by water in an associative step
completes the OAT process.33
The bonding changes that occur in LMoVIO2X (X ) Cl,
SCH2Ph, OPh) along a reaction coordinate for OAT to PPh3
have been explored by DFT calculations. The geometries of
the reaction intermediates are based upon the estimates of
Pietsch and Hall,33 and frontier orbital theory is used torationalize the relative rates of the OAT reaction of LMoVIO2X
with PPh3. Scheme 2 illustrates structures I-III along acoordinate for the reaction of the [(NH3)3MoO2(SCH3)]+ modelwith P(CH3)3. Structure I corresponds to the reactants before
significant reaction, structure II to the transition state, andstructure III to the MoIVO(OP(CH3)3) intermediate in thescheme of Pietsch and Hall.33
The energies of the HOMO (the lone pair of the attacking Patom) and the LUMO (Mo dyz - OπOP,+*) for structures I andII and the HOMO for structure III are illustrated in Figure 9.
Before reaction with P(CH3)3, the major contribution of X to
the dyz and dxz orbitals is Cl π* to dyz (X ) Cl), S π* to dxz(X ) S), and Oal pseudo-σ* to dyz and Oal π* to dxz (X ) O)
(Figure 7). In the frontier orbital theory model, the energychange (∆E) when the HOMO of a nucleophile interacts with
the LUMO of an electrophile is formulated as follows:(78) Holm, R. H.; Kennepohl, P.; Solomon, E. I. Chem. ReV. 1996, 96,
2239-2314.
(79) Xiao, Z.; Gable, R. W.; Wedd, A. G.; Young, C. G. J. Am. Chem.
Soc. 1996, 118, 2912-2921.

(80) Tucci, G. C.; Donahue, J. P.; Holm, R. H. Inorg. Chem. 1998, 37,
1602-1608.
(81) Fleming, I. Frontier Orbitals and Organic Chemical Reactions; John
Wiley & Sons: Chichester, 1976.

∆E ) -

QnucleophileQelectrophile+R
2(cnucleophilecelectrophileβ)2(5)
EHOMO(nucleophile) - ELUMO(electrophile)where Q is the charge of reacting atom,  is the local dielectric
constant, R is the distance between the two reacting atoms, c isthe coefficient of the atomic orbital of the reacting atom in themolecular orbital, and β is the resonance integral for the two
wave functions corresponding to the cnucleophile and celectrophilecoefficients.81 This perturbation theory approach cannot be used
to estimate the activation energy of the first step of the OAT
reaction. Nevertheless, it does provide an estimate of the change
in energy (∆E) over the early part of the reaction coordinate.
The first term in eq 5 represents the Coulombic attraction
between the two reactants, and the second describes the partial
charge transfer that occurs as the frontier orbitals of theelectrophile and nucleophile interact. The contribution of eachterm to (∆E) depends primarily on |EHOMO - ELUMO|. When
this is large (|EHOMO - ELUMO| . 4β2), the Coulombic
interaction dominates, and the reaction is charge controlled. If
Qnucleophile and Qelectrophile are both small and EHOMO and ELUMO
are close in energy (|EHOMO - ELUMO| ≈ 0), then the second
term in eq 5 dominates, and the reaction is orbitally controlled.
The DFT calculations on [(NH3)3MoO2X]+ (X ) Cl, SCH3,
OCH3), before reaction, reveal estimated charges on the oxo

Oxomolybdenum Complexes with Thiolate and Related Ligands

J. Am. Chem. Soc., Vol. 121, No. 43, 1999 10045

Figure 9. Energy change of the HOMO of P(CH3)3 and the LUMO of [(NH3)3MoO2X]+ (X ) Cl, SCH3, OCH3) over the OAT reaction coordinate.
Structure I is before the reaction, II is with P-O ) 2.43 Å, and III is with P-O ) 1.53 Å (see Scheme 2).

groups of -0.53 (X ) Cl), -0.57 (X ) SCH3), and -0.58(X ) OCH3) and |EHOMO - ELUMO| values of 0.248 (X ) Cl),
0.310 (X ) SCH3), and 0.450 (X ) OCH3). Both trends predicta reactivity order Cl > SCH3 > OCH3, which parallels thereactivity order in Table 1. However, the small values of|EHOMO - ELUMO| and the larger variation of |EHOMO - ELUMO|
relative to Qnucleophile for X ) Cl, SCH3, and OCH3 indicate thatOAT from [(NH3)3MoO2X]+ to P(CH3)3 is orbitally controlled
and that |EHOMO - ELUMO| is the prime determinant of ∆E acrossthe series. The calculated values for celectrophile2 (the total orbital
character of the oxo group in the LUMO) are 25.84, 28.90, and22.26% for X ) Cl, X ) SCH3, and X ) OCH3, respectively,
and do not follow the trend in reactivities. Presumably, this isrelated to the overestimation in calculated Mo 4d-Cl covalency(section 4B) that would tend to lower celectrophile2 for X ) Cl.
At structure II, the two electrons that will be donated to[(NH3)3MoO2X]+ during OAT are still localized in a lone pairorbital on the P atom (HOMO of P(CH3)3 molecule), and the
Mo atom is in the formal VI oxidation state. As anticipatedfrom eq 5, the additional HOMO stabilization at structure II isin the order X ) Cl (0.247 eV) > X ) SCH3 (0.208 eV) >X ) OCH3 (0.117 eV) (Figure 9). Transfer of the two electrons
from P to Mo gives geometry III, in which the dyz and dxz
orbitals transform into a filled dyz+xz orbital (directed toward
O1) and an empty dyz-xz orbital (directed toward O2). The Cl
π*, S π*, and Oal π* contribute significantly to the dyz+xz orbital(Figure 9). The relative energy of the HOMO (dyz+xz - X π*)
at structure III compared to that of the LUMO at structure I isin the order X ) Cl (0.879) < X ) S (1.100) < X ) Oal (1.465
eV) (Figure 9). These values are in accord with the OAT
reactivity order (Table 1); however, the approximations used
to derive eq 5 may not remain valid when the reaction coordinate
has progressed to structure III.
For X ) SCH3 and OCH3 in structures I, II, and III, theC-S(Oal)-Mo torsional angle (relative to the yz-plane) was held
constant at 0° at all points along the reaction coordinate, as in
the previous calculations.33 The Walsh diagram in Figure 8
shows the dependence of the energies of the Mo dyz(LUMO)

and dxz orbitals, and the O1 and O2 pz character for the LUMO
with torsional angle. For angles between 0° and 180°, there isa large variation in O1 and O2 pz character (0.1-26.9%) and,
consequently, in the antibonding character for each oxo groupin the LUMO. Thus, in addition to LUMO energy modulation,
the variation of the Mo-S-C torsional angle also serves as amechanism for O atom selection. The oxo group with thegreatest antibonding character in the LUMO will be transferred
to PPh3 preferentially. For X ) Cl, no such selection mechanism
exists, and the oxo groups remain equivalent. This statisticaleffect may represent an additional factor in determining the ratesof oxo atom transfer by LMoO2X and the elevated reaction ratefor X ) Cl.
Besides anisotropic effects of the Cl, SCH3, and OCH3 ligands
and the energetic effects of the axial ligand on the O atomtransfer reactivity,82 steric factors may also play a role in theobserved reactivity (Table 1). Both LMoO2(SPh) and LMoO2(OPh) are more sterically hindered than LMoO2Cl, which reacts
rapidly with PPh3. However, the importance of electronic factors
in reactivity, especially |EHOMO - ELUMO|, is supported by acomparison of the reactivities of LMoO2(SPh) and LMoO2(OPh), which are of similar size. The SPh compound is 300
times more reactive, consistent with the DFT calculations andanalyses presented above.
C. Implications for Sulfite Oxidase. Site-directed mutagenesis on human sulfite oxidase has shown that the coordinationof a cysteine residue in addition to the ene-1,2-dithiolate derived
from molybdopterin is essential for enzyme activity,18 and Scys
coordination of the Mo center in the wild-type enzyme has been
corroborated by the recent X-ray crystal structure of chicken
liver sulfite oxidase (Scheme 1).9 The differences between the
Mo centers of the active wild-type and the inactive cysteine toserine mutant (C207S)18 forms of human sulfite oxidase havebeen probed by EXAFS,14 resonance Raman spectroscopy,17 andS K-edge spectroscopy.14 Particularly germane to the present
work are the S K-edge difference spectra of the wild-type and(82) Albright, T. A.; Burdett, J. K.; Whangbo, M. H. Orbital Interactionsin Chemistry; John Wiley & Sons: New York, 1985.

10046 J. Am. Chem. Soc., Vol. 121, No. 43, 1999
the C207S mutant forms of oxidized human sulfite oxidase,showing a distinct pre-edge feature at 2468.0 eV.14 Assumingthat the covalency of the Mo-S bonds involving the ene-1,2dithiolate is comparable for both the wild-type and mutant forms,
the pre-edge feature in the difference spectrum is strong evidence
for significant Mo-Scys covalency in the wild-type enzyme.14
The inactivity of the C207S mutant human enzyme showsthat the coordinated cysteine residue, and presumably thecovalency associated with its Mo-S bond, are essential for the
biological function of sulfite oxidase.18 Our analysis of therelative rates of reaction of LMoVIO2X (X ) Cl, SPh, OCH3)
with respect to OAT to PPh3 has stressed the importance of thecovalent anisotropic contributions of X in modulating the
reduction potential and reactivity of [MoVIO2X] cores. The X-ray
crystal structure of sulfite oxidase shows a Scys donor cis to the
O ligands (Scheme 1), permitting the full participation of the S
lone pairs in determining the energy of the redox-active dyz or
dxz orbital. This Scys ligation at the active site may determine
the energy of the metal-based frontier orbital that is critical for
determining the rate of sulfite oxidation by sulfite oxidase. The
anisotropic covalency associated with the Mo-Scys bond may
also serve as a switching mechanism during enzyme turnoverto promote preferential transfer of one of the oxo groups (Figure8). This idea is supported by the geometry at the active site ofsulfite oxidase, where the methylene C atom of the cysteine
residue is opposite the oxygen ligand that undergoes oxo transfer(the OdMosSsC dihedral angle ) 179.1°); a similar geometry
is observed for LMoIVO(pyridine)(SPh) (Npyridine-Mo-S-C )161.2°). In addition, our rationalization of the relative Mo(VI)/
Mo(V) reduction potentials of LMoO2X suggests that the Scys
ligation may also fine-tune the Mo(VI)/Mo(V) reduction
potential of the active site in sulfite oxidase that is essential indetermining the rate of regeneration of the Mo(VI) active site
during enzyme turnover (Scheme 1).
The ene-1,2-dithiolate ligation provided by molybdopterin
should also be critical in determining the reduction potential
and reactivity of the Mo center. This coordination has been
implicated in enhancing the ability of the active site to catalyze
OAT reactions by weakening the ModO bond through πelectron donation to the metal,35 by buffering the drastic changes
in electron density at the Mo center that would be expected toaccompany OAT,83 and by providing a σ-electron-transfer
pathway for regeneration of the active site during turnover.37
6. Summary
This study demonstrates for the first time that analyses ofpre-edge X-ray absorption intensity can be extended to ligand
S and Cl K-edge and Mo L-edge spectra of d0 dioxo MoVI
complexes. A detailed electronic structure description of
LMoO2X (X ) Cl, SCH2Ph, OPh) has emerged from ourspectroscopic results and DFT calculations on [(NH3)3MoO2X]+(X ) Cl, SCH3, OCH3) analogues. The metal-ligand bonding
is dominated by the two strong cis ModO bonds that control
the splittings of the d orbitals, such that the LUMO is dyz inour coordinate frame (Figures 5 and 7). Covalent contributions
from X, which perturb the energies of the d orbitals within theligand field manifold, are superimposed on this orbital scheme(Figure 7). The principal perturbations due to X are Cl π* todyz and Cl σ* to dz2 for X ) Cl, S π* to dxz, and S pseudo-σ*(83) Westcott, B. L.; Gruhn, N. E.; Enemark, J. H. J. Am. Chem. Soc.
1998, 120, 3382-3386.

Izumi et al.
to dz2 for X ) SCH3, and Oal pseudo-σ* to dyz and Oal π* to dxz
for X ) OCH3. The theoretical orbital splittings and key
covalent interactions due to X are directly reflected in thedominant experimental peak splitting and intensity variations
within the Cl and S K-edge (Figures 2 and 3) and the Mo L2edge spectra (Figure 4) for the complexes. However, thequantitative analysis of the Cl and S K-pre-edges reveals thatthe DFT calculations strongly overestimate Cl covalency,
whereas there is a small underestimation of S covalency.
Anisotropic covalent interactions with X modulate the energyof the redox-active dyz orbital and thereby influence the relative
Mo(VI)/Mo(V) reduction potentials and the relative rates ofreaction of LMoO2X with PPh3 (Table 1). The donor propertiesof X affect the LUMO (dyz)-HOMO (PPh3 lone pair) energy
gap, the charge on the oxo groups, and provide a mechanism
for “oxygen atom selection”. The principal factors in determining the anisotropy of the covalent contributions of X to Mo are
the OdMo-S(O)-C dihedral and OdMo-S(O) bond anglesof the thiolate and alkoxide ligands. These angles restrict oneof the ligand valence π orbitals from interacting with Mo andcontrol the bonding participation of the remaining ligand valenceorbitals within the metal d manifold.
Comparisons of sulfite oxidase with LMoVIO2X suggest that
the Scys ligation at the active site of sulfite oxidase may beplaying a similar role in determining the reactivity of the[MoVIO2]2+ center. The anisotropic covalency associated with
the Scys-Mo bond may facilitate OAT through a modulationof the energies of the Mo 4d orbitals and the preferential
selection of the O atom to be transferred during enzyme
turnover. However, a more complete understanding of the roleof cysteinyl ligation at the active site of sulfite oxidase must
await a better definition of the role(s) of the novel ene-1,2dithiolate coordination that is common to the active sites of all
oxomolybdoenzymes. This study has demonstrated that the
combined analyses of the of S and Cl K pre-edge and the Mo
L-edge XAS can provide details of the bonding framework of
LMoVIO2X complexes, a basis for understanding their chemical
properties, and insights into the role of Scys ligation at the active
site of sulfite oxidase.
Acknowledgment. This work was supported by grants from
NSF (CHE-9528250, E.I.S., and CHE-9423181, K.O.H.) andNIH (GM-37773, J.H.E and RR-01209, K.O.H.). SSRL operations are funded by the Department of Energy, Office of Basic
Energy Sciences. The Biotechnology Program is supported by
the National Institutes of Health, National Center for Research
Resources, Biomedical Technology Program. Further support
is provided by the DOE, Office of Biological and Environmental
Research. Y.I. was supported at Stanford University by a Foreign
Research Scientist Fellowship funded by the Ministry of
Education, Science, Sports, and Culture (Monbusho) of Japan.
T.G. thanks the Deutsche Forschungsgemeinschaft for a postdoctoral fellowship. We thank Dr. C. G. Young for advice on
the synthesis of the Mo complexes.
Supporting Information Available: Peak fits and spectral
assignments for the Mo L2-edge data, and tables of detailed
geometric parameters for the MO calculations and the energy
splittings within the L3-edge spectra of LMoO2(SCH2Ph),
LMoO2Cl, and LMoO2(OPh) (PDF). This material is available
free of charge via the Internet at http://pubs.acs.org.
JA9903678