A bioinspired oxoiron(iv) motif supported on a N2S2macrocyclic ligand

Article abstract of DOI:10.1039/d1cc00250c

A mononuclear oxoiron(iv) complex1-transbearing two equatorial sulfur ligations is synthesized and characterized as an active-site model of the elusive sulfur-ligated Fe^IVO intermediates in non-heme iron oxygenases. The introduction of sulfur ligands weakens the Fe-O bond and enhances the oxidative reactivity of the Fe^IVO unit with a diminished deuterium kinetic isotope effect, thereby providing a compelling rationale for nature's use of thecis-thiolate ligated oxoiron(iv) motif in key metabolic transformations.

Full text of DOI:10.1039/d1cc00250c

ChemComm
View Article Online
View Journal | View Issue
COMMUNICATION
A bioinspired oxoiron(IV) motif supported on a
N2S2 macrocyclic ligand†
Cite this: Chem. Commun., 2021,
57, 2947
a
a
Jennifer Deutscher,
Philipp Gerschel,b Katrin Warm,
Uwe Kuhlmann,c
d
d
d
c
Received 14th January 2021,
Accepted 17th February 2021
Stefan Mebs,
Michael Haumann,
Holger Dau,
Peter Hildebrandt,
be
a
Ulf-Peter Apfel
*
and Kallol Ray
*
DOI: 10.1039/d1cc00250c
rsc.li/chemcomm
A mononuclear oxoiron(IV) complex 1-trans bearing two equatorial hydrogen-atom abstraction, and C–S bond formation reactions
sulfur ligations is synthesized and characterized as an active-site in non-heme enzymes.
model of the elusive sulfur-ligated FeIV O intermediates in non-
For over 40 years, small-molecule complexes synthesized as
Q
heme iron oxygenases. The introduction of sulfur ligands weakens active-site models of the high-valent intermediates in heme and
Q
the Fe O bond and enhances the oxidative reactivity of the non-heme oxygenases have advanced our understanding of the
FeIV O unit with a diminished deuterium kinetic isotope effect, catalytic cycles.3,11–20 Despite these efforts, the synthesis of an
Q
thereby providing a compelling rationale for nature’s use of the oxoiron(IV) porphyrin complex with a thiolate ligand has not
cis-thiolate ligated oxoiron(IV) motif in key metabolic transformations. yet been achieved. Furthermore, [(TMCS)FeIV(O)]+ (TMCS =
1-mercaptoethyl-4,8,11-trimethyl-1,4,8,11-tetraazacyclotetra-decane;
Sulfur-ligated oxoiron(IV) centers are proposed as key oxidants (Scheme 1)), represents the only synthetic complex21 thus far to
in the catalytic cycles of various heme and non-heme iron model the RS-FeIVQO unit associated with the active oxidants of
oxygenases (Scheme 1).1–3 Iron(IV)–oxo porphyrin p-cation radical cytochrome P4502,6 and chloroperoxidase.4,5,10 Similarly,
a
(Cpd I) intermediates containing a thiolate ligand trans to the recently reported [(Me3TACN)FeIV(O)(S2Si(CH3)2)] (Me3TACN =
oxo group have been isolated and spectroscopically characterized 1,4,7-trimethyl-1,4,7-triazacyclononane)13 complex represents the
in a number of heme enzymes.4–6 The increased basicity of the only model complex for the postulated oxoiron(IV) core containing
oxoiron(IV) core caused by the strong electron donation from the a sulfur ligation cis to the oxo group in non-heme oxygenases.22,23
trans-sulfur ligand, is discussed as a strategy to perform hydro- However, the thermal instability of the compound has prevented any
gen atom abstraction by Cpd I at a lower redox potential without reactivity studies. Herein we report the synthesis and characteriza-
performing oxidative destruction of the surrounding enzyme tion of the S = 1 FeIVQO complex [(dithiacyclam)FeIV(O)(CH3CN)]2+
environment.5,7–10 However, similar knowledge on the effect of (1-trans, dithiacyclam24,25 = 1,8-dithia-4,11-diazacyclotetra-
cis-sulfur ligands on the reactivity of oxoiron(IV) cores in non- decane), which contains two thioether sulfur coordination sites
heme enzymes is lacking. Notably, identification of cis thiolate- poised cis to the oxo group. A comparative study between 1-trans,
ligated oxoiron(IV) species remained elusive in biology, although
they are suggested to be reactive intermediates for a wide range
of chemical transformations, including sulfur-oxygenation,
a
¨
¨
Institut fur Chemie Humboldt-Universitat zu Berlin, Brook-Taylor-Str. 2, 12489,
Berlin, Germany. E-mail: kallol.ray@hu-berlin.de
b
c
¨
¨
Anorganische Chemie 1 Ruhr-Universitat Bochum, Universitatsstraße 150, 44780,
Bochum, Germany
¨
¨
¨
Institut fur Chemie Technische, Universitat Berlin, Fakultat II Straße des 17,
Juni 135, 10623, Berlin, Germany
d
¨
¨
Institut fur Physik Freie, Universitat Berlin, Arnimallee 14, 14195 Berlin, Germany
e Department of Electrosynthesis, Fraunhofer UMSICHT, Osterfelder Str. 3,
46047 Oberhausen, Germany
Scheme 1 Top: Proposed structures of the thiolate-ligated oxoiron(IV)
reactive intermediates in biology; bottom: structures of [(TMCS)FeIV(O)]+,
1-trans and 2-trans.
† Electronic supplementary information (ESI) available. CCDC 2054129 and
2054130. For ESI and crystallographic data in CIF or other electronic format
see DOI: 10.1039/d1cc00250c
This journal is The Royal Society of Chemistry 2021
Chem. Commun., 2021, 57, 2947ꢀ2950 | 2947

View Article Online
Communication
ChemComm
containing a N2S2 macrocyclic ligand, and [FeIV(O)(cyclam)(CH3CN)]2+ DEQ = 0.26 mm sꢀ1 corresponds to the low-spin S = 0 FeII center
(2-trans; cyclam = 1,4,8,11-tetraazacyclotetradecane; (Scheme 1)),26 in 1a-trans (27%). Thus, CH3CN-binding favours the trans
based on the popular N4-donor cyclam ligand, provides some configuration and the coordination of both CH3CN is necessary
insight how cis-sulfur coordination influences the reactivity and for stabilizing the low-spin FeII state in 1a.
spectroscopic properties of the oxoiron(IV) unit.
A solution of 1a-trans in a CH2Cl2/CH3CN solvent mixture (95 : 5)
Combining the tetradentate dithiacyclam ligand with at ꢀ85 1C with 4 equiv. of 2-(tert-butylsulfonyl)iodosylbenzene
s
Fe(OTf)2(CH3CN)2 in acetonitrile yielded the iron(II) complex (tBuSO2C6H4IO, PhIO)27 led to the formation of a pale green
in two isomeric forms [FeII(dithiacyclam)(CH3CN)2](OTf)2 intermediate 1-trans (t1/2 = 10000 s at ꢀ65 1C) with absorption
(1a-trans) and [FeII(dithiacyclam)(OTf)2] (1a-cis). Crystals suitable maxima at 596 nm (emax = 226 Mꢀ1 cmꢀ1) and 815 nm (emax
=
for X-ray diffraction analysis were grown by vapour diffusion of 549 Mꢀ1 cmꢀ1), which are typical of S = 1 oxoiron(IV) cores (Fig. 2;
diethyl ether into an acetonitrile solution of the iron(II) complex left).11 The characteristic near-infrared band in 1-trans @
at ꢀ15 1C for 1a-cis or at ꢀ40 1C for 1a-trans. The X-ray structure 815 nm is significantly red-shifted relative to that in 2-trans,26
of 1a-trans displays a six-coordinate geometry with axially bound which is consistent with a weakened equatorial field in 1-trans.
CH3CN ligands (Fig. 1; Table S2, ESI†). The N2S2 donor atoms of Notably, in the absence of CH3CN, 1-trans was not generated.28
dithiacyclam occupy the equatorial coordination sites and show An electron spray ionization mass spectrum (Fig. S5, ESI†) of
average Fe–S and Fe–N distances of 2.252(6) Å and 1.985(18) Å, 1-trans exhibited a signal at m/z = 794.96, consistent with its
respectively. In contrast, in 1a-cis the sulfur donor atoms occupy formulation as {[(dithiacyclam)FeIV(O)(OTf)](SPhIO)}+ (m/z calc =
the axial coordination sites and show average Fe–S distances of 794.97), which is shifted by 4 units to m/z = 798.97, when sPhI18O
2.466(14) Å (Table S1, ESI†); the nitrogen atoms of the dithiacyclam was used to generate 1-trans. 19F-NMR (at ꢀ85 1C in a 95:5 mixture
and the oxygen atoms of the triflate (OTf) anions occupy equatorial of CD2Cl2 and CD3CN) shows a singlet at ꢀ77.0 ppm corres-
positions with average Fe–N and Fe–O distances of 2.2085(4) Å ponding to the free OTf anions in 1-trans (Fig. S6, ESI†). The
¨
¨
and 2.143(3) Å, respectively. The zero-field Moßbauer spectrum of zero-field Moßbauer spectrum of 1-trans in frozen acetone/
1a-cis in acetone (Fig. S1, ESI†) at 15 K reveals a single quadrupole CH2Cl2/CH3CN solution and recorded at 15 K exhibits a doublet
doublet with an isomer shift of d = 1.10 mm sꢀ1 and a large representing about 84% of the iron with DEQ = 1.21 mm sꢀ1 and
quadrupole splitting of (DEQ) = 3.26 mm sꢀ1, demonstrating that d = 0.13 mm sꢀ1 corresponding to the presence of an FeIV center
the iron(II) center remains in the high-spin configuration (S = 2). (Fig. 2; right); the remaining 16% of the signals with DEQ
=
In addition, the 1H- and 19F-NMR spectra (Fig. S2, ESI†) of 1a-cis in 1.57 mm sꢀ1 and d = 0.55 mm sꢀ1 correspond to a high-spin FeIII
d6-acetone at ꢀ85 1C display paramagnetically shifted peaks, product, arising from the decay of 1-trans.
indicative of the coordination of both OTf anions and further
The Fe K-edge X-ray absorption (Fig. S7 and Table S4, ESI†)
supporting the high-spin iron(II) assignment. In CH2Cl2/CH3CN spectrum of 1-trans reveals a K-edge energy of 7122.7 eV, which
solution, CH3CN gradually replaces the bound triflates of 1a-cis is lower relative to 2-trans (7123.9 eV). Furthermore, the pre-edge
to form 1a-trans with an S = 0 FeII ground-state, as evident from transition in 1-trans is less intense, which may reflect a less
1H-NMR (at ꢀ85 1C), which reveals peaks between 0 and 4 ppm covalent FeQO bond in 1-trans relative to 2-trans. The resonance
(Fig. S3, ESI,† left), and 19F-NMR (at ꢀ85 1C; Fig. S3, ESI,† right), Raman (rR) spectrum of 1-trans exhibits a n(FeQO) stretching
which shows a singlet at ꢀ79.0 ppm corresponding to free OTf mode at 793 cmꢀ1 (Fig. 2, inset), which is red-shifted by 49 cmꢀ1
anions. Freezing the solution leads to the partial re-binding of OTf relative to that in 2-trans (n(FeQO) = 842 cmꢀ1),26 thereby
II
¨
anion to Fe ; zero-field Moßbauer measurement (Fig. S4, ESI†) at demonstrating an elongation of the FeQO bond by B0.02 Å in
15 K shows a major quadrupole doublet with a new high-spin 1-trans relative to 2-trans.29 However, within the error of the
FeII signal (d = 1.15 mm sꢀ1 and DEQ = 2.31 mm sꢀ1; 73%) with
a significantly reduced DEQ relative to 1a-cis, presumably
corresponding to the trans-[(dithiacyclam)FeII(OTf)(CH3CN)]+
complex. An additional doublet with d = 0.52 mm sꢀ1 and
Fig. 2 Left: UV-Vis-spectrum of 1a-trans (black) and 1-trans (blue) in a
95 : 5 mixture of CH2Cl2 and CH3CN at ꢀ90 1C; the inset shows the
resonance Raman spectra of 16O- (black) and 18O-labelled (red) 1-trans
(4 mM) upon 413 nm irradiation at ꢀ90 1C. Solvent signal is indicated by an
asterisk. Right: Zero-field Moßbauer spectrum (black) of a frozen sample of
¨
Fig. 1 Molecular structures of 1a-cis and 1a-trans obtained by XRD.
Atoms are displayed as thermal ellipsoids at 50% probability level; triflate
counter ions for 1a-trans are omitted for clarity. Atom types: Fe: orange;
N: blue; C: grey; O: red; S: yellow; F: green; H: white.
1-trans in a solvent mixture of acetone/CH2Cl2/CH3CN (10 : 0.95 : 0.05)
and simulation (red) with d = 0.13 mm sꢀ1 and DEQ = 1.21 mm sꢀ1 for the
main species (blue, 84%). The minor species with d = 0.55 mm sꢀ1 and
DEQ = 1.57 mm sꢀ1 corresponds to the decay of 1-trans (brown, 16%).
2948 | Chem. Commun., 2021, 57, 2947ꢀ2950
This journal is The Royal Society of Chemistry 2021

View Article Online
ChemComm
Communication
842 cmꢀ1 for 2-trans. In summary, a 49 cmꢀ1 red-shift in the
n(Fe–O) of 1-trans relative to 2-trans, translates to an FeQO
elongation of only 0.02 Å (based on both constrained DFT
optimization and Badger’s rule29), which is not clearly discernible
within the error of the EXAFS analysis, but is reflected in a less-
intense pre-edge transition at the Fe K-edge.
The introduction of the equatorial sulfur ligands also exhibits
a significant effect on the reactivity of the oxoiron(IV) unit (Fig. 3
and Fig.s S8–S12, ESI†). In reactions with substrates containing
C-H bonds like xanthene, 1,4-cyclohexadiene (CHD), dihydroan-
thracene (DHA), fluorene and indene, 1-trans reacts at least 3–4
orders of magnitude faster than 2-trans (Table 1). Furthermore,
low kinetic isotope effects (KIEs) of 1.47 and 2.82 were deter-
mined in the reaction of 1-trans with xanthene (Fig. 3, top right)
and DHA (Fig. 3, bottom left), respectively, which are in contrast
to the previously reported value of 20.0 for reaction of xanthene
with 2-trans.26 Nevertheless, when the logarithms of the second
Fig. 3 Top left: Changes in the UV-Vis-spectra of a 1 mM solution of
1-trans in CH2Cl2/CH3CN (95 : 5) at ꢀ80 1C upon addition of 100 eq
xanthene; the inset shows the time trace for the decay of the 815 nm band
and its pseudo-first order fit; top right: plots of the pseudo-first order rate
constants kobs vs. the substrate concentrations for xanthene and
d2-xanthene in order to determine the kinetic isotopic effect (KIE) for
the reaction of 1-trans with xanthene; bottom left: plots of the pseudo-
first order rate constants kobs vs. the substrate concentrations for 9,10-
dihydroanthracene (DHA) and d4-DHA in order to determine the kinetic
isotopic effect (KIE) for the reaction of 1-trans with DHA; bottom right:
0
order rate constants (k2 ) were plotted vs. the BDE C–H values
of the substrates, the linear correlation previously reported for
2-trans were found to be also valid for 1-trans (Fig. 3, bottom
right). Thus, although proton-transfer is involved in the rate-
determining step of the oxidation of C-H bonds by 1-trans, the
large tunneling contribution in hydrogen atom abstraction
(HAA), which is observed in 2-trans and in most high-valent
metal-oxo mediated HAA reactions,11,12,30 is not applicable for
1-trans. In particular, in a previous study the axial thiolate ligand
of [FeIV(O)(TMCS)]+ has been suggested to play a unique role in
facilitating tunnelling, thereby resulting in a large KIE of 80 for
DHA oxidation.31 A contrasting effect is now demonstrated for
the equatorial sulphur ligation, which reduces the tunnelling
contribution to a minimum. The effect of N versus S donors in an
otherwise identical ligand environment is also reflected in the
higher oxygen atom transfer (OAT) ability of 1-trans relative to
2-trans (Table 1).
In summary, a minor 0.02 Å elongation of the FeQO bond
upon introduction of the equatorial sulfur ligands is shown to
have a dramatic influence on the spectroscopic (Table S7, ESI†)
and oxidative reactivity properties of the FeIVQO unit. Notably,
1-trans, similar to the previously reported13 [(Me3TACN)-
FeIV(O)(S2Si(CH3)2)] complex features a very low n(Fe–O), which
establishes a general trend of the activation of the Fe–O bond
in oxoiron(IV) complexes involving cis-sulphur ligands. The
enhanced reactivity of 1-trans relative to 2-trans, can presumably
0
plot of the logarithms of the second-order rate constants k2 vs. the C-H
BDEs of the substrates with 1-trans in CH2Cl2/CH3CN (95 : 5).
extended X-ray absorption fine structure (EXAFS) analysis, the
FeQO distances in 1-trans and 2-trans are not discernible; in
both cases a distance of 1.67 ꢁ 0.02 Å has been obtained.26 The
DFT optimized geometry of 1-trans in the S = 1 state slightly
underestimates the Fe–O bond (calculated @ 1.655 Å) from the
EXAFS data (Tables S5 and S6, ESI†), and as a result the calculated
n(Fe–O) is overestimated. This is a common problem that is
encountered in the oxoiron(IV) chemistry.8,13 However, a geometry
scan of the Fe–O bond length (Table S6, ESI†) reveals a relatively
flat surface potential, with the structures exhibiting Fe–O bond
lengths of 1.66–1.70 Å being within 1 kcal molꢀ1 in energy from
the lowest energy structure. In particular, a constrained optimiza-
tion with a fixed Fe–O distance @ 1.68 Å for 1-trans gives a
calculated n(Fe–O) of 794 cmꢀ1, in good agreement with the
experiment. Similarly, a constrained geometry with an Fe–O
distance of 1.66 Å can account for the experimental n(Fe–O) of
Table 1 Reactivity comparison of 1-trans and 2-trans
Substrate
BDEa [kcal molꢀ1
]
k2 [Mꢀ1sꢀ1] 1-trans
k2[Mꢀ1sꢀ1] 2-trans
Product (yield)d
Xanthone (36%)
Xanthene
1,4-CHD
DHA
Fluorene
Indene
Thioanisol
PPh3
75.2
76
76.3
82.2
83
—
—
205b
370b
355b
18.2c
17.6c
87c
1.1 ꢂ 10ꢀ1
9.7 ꢂ 10ꢀ2
4.9 ꢂ 10ꢀ2
7.1 ꢂ 10ꢀ3
5.8 ꢂ 10ꢀ3
—
Anthracene (48%)
Fluorenone (11%)
Indenone
n.d
5.9
OPPh3 (28%)
a
b
c
Values taken from ref. 32. Values calculated for 20 1C from experimental values determined at ꢀ80 1C using van’t Hoff equation. Values
d
calculated for 15 1C from experimental values determined at ꢀ65 1C using van’t Hoff equation. Specified yields correspond to the reactivity of
1-trans. n.d: the reaction was too fast for kinetic studies.
This journal is The Royal Society of Chemistry 2021
Chem. Commun., 2021, 57, 2947ꢀ2950 | 2949

View Article Online
Communication
ChemComm
9 R. K. Behan, L. M. Hoffart, K. L. Stone, C. Krebs and M. T. Green,
J. Am. Chem. Soc., 2006, 128, 11471–11474.
10 K. L. Stone, R. K. Behan and M. T. Green, Proc. Natl. Acad. Sci. U. S. A.,
2006, 103, 12307–12310.
be attributed to the positive shift in the redox potential upon
sulphur ligation, as evident from cyclic voltammetry experi-
ments, which shows a 170 mV positive shift in the Fe2+/3+
´
potential (Fig. S13, ESI†) in 1a-trans relative to 2a-trans. In 11 X. Engelmann, I. Monte-Perez and K. Ray, Angew. Chem., Int. Ed.,
2016, 55, 7632–7649.
12 R. A. Baglia, J. P. T. Zaragoza and D. P. Goldberg, Chem. Rev., 2017,
addition, a change in mechanism in the C–H bond oxidation
reactions from HAA to proton coupled electron transfer (PCET)33
117, 13320–13352.
is evident from the reduction of KIE from a value of 20 in 2-trans
to 1.47 in 1-trans (using xanthene as a substrate). This drastic
downshift in KIE is unique for sulfur substitution and is not
observed in the oxygen substituted oxoiron(IV) center.34 Under-
standing this lowering of KIE will require further experimental
and computational work. However the significant effect of the
equatorial sulfur ligation on the physical and chemical properties
of oxoiron(IV) cores may provide a compelling rationale for
nature’s use of the cis-thiolate ligated oxoiron(IV) motif in key
metabolic transformations that involve the activation of strong
C–H bonds.
This work was funded by the Deutsche Forschungsge-
meinschaft (DFG, German Research Foundation) under Germany’s
Excellence Strategy – EXC 2008 – 390540038 – UniSysCat to K. R.,
P. H., and H. D., Excellence Strategy – EXC-2033 – Project number
390677874 to U.-P. A. and P. G., AP242/5-1 to U.-P. A. and the
Heisenberg-Professorship and RA/2409/8-1 to K. R. We also thank
the Fraunhofer Internal Programs under Grant No. Attract 097-
602175 (U.-P. A.) and the Bundesministerium fu¨r Bildung und
Forschung (BMBF, Operando-XAS project, 05K19KE1). The
Helmholtz-Zentrum Berlin (HZB) is thanked for enabling the
XAS experiments at KMC-3 of the BESSY synchrotron.
13 J. B. Gordon, A. C. Vilbert, I. M. DiMucci, S. N. MacMillan,
¨
K. M. Lancaster, P. Moenne-Loccoz and D. P. Goldberg, J. Am. Chem.
Soc., 2019, 141, 17533–17547.
14 L. Vicens, G. Olivo and M. Costas, ACS Catal., 2020, 10, 8611–8631.
15 J. Chen, Z. Jiang, S. Fukuzumi, W. Nam and B. Wang, Coord. Chem.
Rev., 2020, 421, 213443.
16 T. Devi, Y.-M. Lee, W. Nam and S. Fukuzumi, Coord. Chem. Rev.,
2020, 410, 213219.
17 S. Fukuzumi, K.-B. Cho, Y.-M. Lee, S. Hong and W. Nam, Chem. Soc.
Rev., 2020, 49, 8988–9027.
18 S. Hong, Y.-M. Lee, K. Ray and W. Nam, Coord. Chem. Rev., 2017,
334, 25–42.
19 W. Nam, Y.-M. Lee and S. Fukuzumi, Acc. Chem. Res., 2018, 51,
2014–2022.
20 M. Sankaralingam, Y.-M. Lee, W. Nam and S. Fukuzumi, Coord.
Chem. Rev., 2018, 365, 41–59.
21 M. R. Bukowski, K. D. Koehntop, A. Stubna, E. L. Bominaar, J. A. Halfen,
E. Mu¨nck, W. Nam and L. Que, Science, 2005, 310, 1000–1002.
22 D. Kumar, W. Thiel and S. P. de Visser, J. Am. Chem. Soc., 2011, 133,
3869–3882.
23 S. Aluri and S. P. de Visser, J. Am. Chem. Soc., 2007, 129, 14846–14847.
24 P. Gerschel, B. Battistella, D. Siegmund, K. Ray and U.-P. Apfel,
Organometallics, 2020, 39, 1497–1510.
25 P. Gerschel, K. Warm, E. Farquhar, U. Englert, M. Reback,
D. Siegmund, K. Ray and U.-P. Apfel, Dalton Trans., 2019, 48,
5923–5932.
26 D. Kass, T. Corona, K. Warm, B. Braun-Cula, U. Kuhlmann, E. Bill,
S. Mebs, M. Swart, H. Dau and M. Haumann, J. Am. Chem. Soc., 2020,
142, 5924–5928.
27 D. Macikenas, E. Skrzypczak-Jankun and J. D. Protasiewicz, J. Am.
Chem. Soc., 1999, 121, 7164–7165.
28 Since we start with a pure solution of 1a-trans, the sole product that
is formed is 1-trans (see also ref. 33). Oxidation of a solution of 1a-cis
leads to only iron(III)products; so we presume that 1-cis is too
unstable to be trapped in high-yields.
Conflicts of interest
There are no conflicts to declare.
29 Acoording to Badger’s rule (R. M. Badger, J. Chem. Phys., 1935, 3,
710–714), which is previously shown to be valid for oxoiron(IV)
complexes (see ref. 8).
30 (a) D. Mandal and S. Shaik, J. Am. Chem. Soc., 2016, 138, 2094–2097;
(b) D. Mandal, D. Mallick and S. Shaik, Acc. Chem. Res., 2018, 51,
107–117; (c) E. J. Klinker, S. Shaik, H. Hirao and L. Que Jr., Angew.
Chem., Int. Ed., 2009, 48, 1291–1295.
31 J. E. M. N. Klein, D. Mandal, W.-M. Ching, D. Mallick, L. Que, Jr. and
S. Shaik, J. Am. Chem. Soc., 2017, 139, 18705–18713.
32 Y.-R. Luo, Comprehensive Handbook of Chemical Bond Energies,
CRC Press, 2007, DOI: 10.1201/9781420007282.
Notes and references
1 M. Costas, M. P. Mehn, M. P. Jensen and L. Que, Chem. Rev., 2004,
104, 939–986.
2 B. Meunier, S. P. de Visser and S. Shaik, Chem. Rev., 2004, 104,
3947–3980.
3 J. B. Gordon and D. P. Goldberg, Reference Module in Chemistry,
Molecular Sciences and Chemical Engineering, Elsevier, 2020, DOI:
10.1016/B978-0-12-409547-2.14906-6.
4 M. T. Green, J. H. Dawson and H. B. Gray, Science, 2004, 304, 1653–1656.
5 K. L. Stone, R. K. Behan and M. T. Green, Proc. Natl. Acad. Sci. U. S. A.,
2005, 102, 16563–16565.
6 J. Rittle and M. T. Green, Science, 2010, 330, 933–937.
7 F. Ogliaro, S. P. de Visser and S. Shaik, J. Inorg. Biochem., 2002, 91, 554–567.
8 M. T. Green, J. Am. Chem. Soc., 2006, 128, 1902–1906.
33 J. M. Meyer, Acc. Chem. Res., 2010, 44, 36–46.
´
34 I. Monte-Perez, X. Engelmann, Y.-M. Lee, M. Yoo, E. Kumaran,
E. R. Farquhar, E. Bill, J. England, W. Nam, M. Swart and K. Ray,
Angew. Chem., Int. Ed., 2017, 56, 14384–14388.
2950 | Chem. Commun., 2021, 57, 2947ꢀ2950
This journal is The Royal Society of Chemistry 2021