Vanadium speciation by XANES spectroscopy: A three-dimensional approach

Article abstract of DOI:10.1002/chem.201403993

A library of X-ray absorption near-edge structure (XANES) spectroscopic data for V^V, V^IV and V^III complexes with a broad range of biologically relevant ligand has been used to demonstrate that three-dimensional plots of key XANES parameters (pre-edge and edge energies; pre-edge and white line intensities) can be used for the prediction of V oxidation states and coordination numbers in biological or environmental matrices. The reliability of the technique has been demonstrated by re-analysis of the published XANES data for a V^V-dependent bromoperoxidase.

Full text of DOI:10.1002/chem.201403993

DOI: 10.1002/chem.201403993
Communication
&
Bioinorganic Chemistry
Vanadium Speciation by XANES Spectroscopy: A Three-
Dimensional Approach**
Aviva Levina, Andrew I. McLeod, and Peter A. Lay*[a]
VV/IV complexes, on the other, was recognised in earlier stud-
ies,[10] but no definitive correlations have emerged. More re-
cently, plots of normalised pre-edge peak intensities (or peak
areas) versus peak positions were used to separate samples of
VV, VIV and VIII oxides according to their oxidation states and co-
ordination numbers (four, five or six).[4,5] However, there is no
robust empirical method for distinguishing all of these differ-
ent classes of V complexes. Despite the recent developments
in theoretical XANES calculations for V and other transition-
metal species[3a,11] determination of average coordination envi-
ronments of metal ions in complex biological or environmental
matrices still relies on empirical techniques, such as principal
component analyses or multiple linear regression fitting.[1,12]
Our group has previously applied empirical analyses of
XANES spectra, based on the use of libraries of model com-
pounds, to a variety of problems related to the reactivity of
toxic and medicinal metal ions in biological media.[1b,13] In this
work, we developed a library of VV, VIV and VIII complexes with
biological or biomimetic ligands (1–18 in Figure 1), primarily
for biotransformation studies of V-based anti-diabetic drugs.[8]
Contrary to common conventions, V–oxido binding in VV/IV
complexes (except for 1, see Figure 1) is correctly represented
with triple, rather than double bonds (2.5<nꢀ3, in which n is
the bond order), due to the presence of one s and two p
bonds.[14]
Complexes 1 (Na3VVO4), 2 (VIVOSO4·5H2O) and 9 were from
commercial sources (purity, >99%). The synthesis and crystal
structure of 14 were reported previously.[15] Published XANES
spectra of 16a–f (electrochemically generated VV/IV/III catechola-
to complexes in MeCN)[16] were re-normalised by using the
method of Penner-Hahn and co-workers[17] (using the same
procedures as for 1–15; see Supporting Information for details
of XANES data processing). In addition, XANES spectra of two
VIII complexes, 17 (isolated solid) and 18 (0.10m solution of
VIIICl3 in 1.0m HCl), were taken from the literature.[18] All the
other complexes listed in Figure 1 were synthesised by modi-
fied literature procedures,[19] and characterised by elemental
analyses, infrared spectroscopy and electrospray mass spec-
trometry (see Supporting Information for details).
Abstract: A library of X-ray absorption near-edge structure
(XANES) spectroscopic data for VV, VIV and VIII complexes
with a broad range of biologically relevant ligand has
been used to demonstrate that three-dimensional plots of
key XANES parameters (pre-edge and edge energies; pre-
edge and white line intensities) can be used for the pre-
diction of V oxidation states and coordination numbers in
biological or environmental matrices. The reliability of the
technique has been demonstrated by re-analysis of the
published XANES data for a VV-dependent bromoperoxi-
dase.
During the last two decades, X-ray absorption near-edge struc-
ture (XANES) spectroscopy has become the leading tool for
speciation of transition-metal ions at low concentrations in
complex matrices. Its elemental specificity and sensitivity make
it particularly apt for the study of biological, environmental
and industrial samples.[1] Because of the importance of V
XANES to these diverse applications, it has been used for vana-
dium speciation in V-doped catalysts[2] or nanomaterials,[3] in
industrial by-products[4] or mineral samples,[5] as well as in V-
containing enzymes,[6] in V-accumulating sea organisms (tuni-
cates)[7] and in biotransformation products of V-based anti-dia-
betic drugs.[1b,8]
The high sensitivity of XANES spectroscopy to the oxidation
state and coordination geometry of metal ions[1] makes this
technique particularly attractive for the speciation of V, which
occurs in nature in a redox equilibrium of three oxidation
states (VV, VIV and VIII), and in a variety of coordination environ-
ments.[9] Most VIV and VV complexes contain between one and
four oxido ligands, which give rise to intense sharp pre-edge
features in XANES spectra, due to the symmetry-forbidden
1s!3d transition. This pre-edge feature gains intensity from
the mixing of p and d orbitals due to a change in coordination
geometry from octahedral to a five-coordinate or a tetrahedral
geometry, and/or metal–ligand p bonding.[1c,10] A link between
the intensity and position of the pre-edge peak, on the one
hand, and the oxidation states and coordination numbers of
Vanadium K-edge XANES spectra of 1–15 (solid mixtures
with BN, ca. 295 K) and those of 16a–f[15] were recorded with
fluorescence detection at the Australian National Beamline Fa-
cility (ANBF; beamline 20B at Photon Factory, KEK, Tsukuba,
Japan). In addition, the spectra of independent samples of 1,
2, 3 and 6 were collected at the X-ray absorption spectroscopy
beamline at the Australian Synchrotron, Melbourne.[20] Experi-
mental details of XANES spectroscopy are given in the Sup-
[a] Dr. A. Levina, A. I. McLeod, Prof. Dr. P. A. Lay
School of Chemistry, The University of Sydney
Sydney, NSW 2006 (Australia)
E-mail: peter.lay@sydney.edu.au
[**] XANES spectroscopy=X-ray absorption near-edge structure spectroscopy
Supporting information for this article is available on the WWW under
http://dx.doi.org/10.1002/chem.201403993.
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Figure 2. A comparison of typical XANES spectra of model VV, VIV and VIII
complexes (designations correspond to Figure 1). Spectra of 16a,c,f were re-
splines of the previously published data.[16] All the spectra were collected in
fluorescence detection mode at about 295 K (see text and Supporting Infor-
mation for details).
inset in Figure 2a shows changes in pre-edge positions for VV
and VIV oxido complexes. XANES from octahedral non-oxido VV,
VIV and VIII complexes (16–18 in Figure 1) were distinguished
by weak pre-edge absorbances (Figure 2b). Increases in V oxi-
dation state in these complexes resulted in increases in edge
energy of their XANES, as well as in slight changes in pre-edge
peak positions and intensities (Figure 2b).[16] Notably, for both
oxido and non-oxido V complexes, an increase in oxidation
state was accompanied by a decrease in white line (post-edge
absorbance) intensity (Figure 2a,b).[1c] All these changes in fea-
tures were diagnostic of the particular oxidation state and co-
ordination environment of V in complex biological, environ-
mental or material samples.[1b,4a,5,10]
As reported in the literature,[5] a plot of normalised pre-edge
peak height against pre-edge peak position (Figure 3a) gave
a good separation of VV and VIV oxido species (1–15, Figure 1)
according to their oxidation state and coordination number
(Figure 3a). Further processing of the pre-edge data to include
centroid peak positions and peak areas (Figure S2c,d, Support-
ing Information)[4a,21] gave inferior separation of groups of VV
and VIV complexes (Figure S4a, Supporting Information). This
was consistent with the reported lack of a good separation[4a]
for six-coordinate VV and VIV complexes. Principal component
analysis[12a,13a] of whole XANES spectra (5460–5520 eV), or pre-
edge and edge regions only (5460–5487 eV), gave inferior
XANES separation of 1–15 compared with a simple plot of pre-
Figure 1. Structures of model VV/IV/III complexes (1–18; see Supporting Infor-
mation for synthesis and characterisation) and of the active centre of VV-de-
pendent bromoperoxidase (BPO) from Ascophyllum nodosum.[6d,9,22]
porting Information, and parameters from both beamlines are
compared in Table S1. All the XANES spectra used in the data
analyses are shown in Figure S1 in the Supporting Information.
The determination of pre-edge and edge parameters is illus-
trated in Figure S2, and their numerical values are listed in
Table S2 (Supporting Information). Comparable XANES spectra
were obtained at both beamlines (Figure S1), but the numeri-
cal values differed slightly (Table S2), probably due to differen-
ces in the monochromator resolutions.[4a]
Selected XANES spectra of model VV, VIV and VIII complexes
are compared in Figure 2. Typical VV oxido complexes (5 and
1 in Figure 2a) were distinguished from VIV oxido complexes (3
and 4 in Figure 2a) by higher pre-edge absorbance intensities
and edge energies. When V compounds in the same oxidation
state and coordination geometry were considered, lower edge
energies were generally observed in the XANES from com-
plexes with O/N-donors, compared with those with O-donors
only (e.g, 8 vs. 5; 10 vs. 9; or 12 vs. 2; see Figure S3 in Sup-
porting Information). Increases in coordination number in
either VV or VIV oxido complexes led to decreases in pre-edge
peak XANES intensity (5 vs. 1 and 4 vs. 3 in Figure 2a). The
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Figure 3. Separation of model VV, VIV and VIII complexes (1–18 in Figure 1,
black dots and blue numbers) according to the oxidation state and coordi-
nation number of V, based on the pre-edge and edge parameters of their
XANES spectra (see Table S2 and Figures S1 and S2 in Supporting Informa-
tion for details). Designations of the areas (red): four-coordinate (tetraoxido)
VV complexes (A); five-coordinate (dioxido) VV complexes (B); six-coordinate
(dioxido) VV complexes (C); five-coordinate (monooxido) VIV complexes (D);
six-coordinate (monooxido) VIV complexes (E); six-coordinate (non-oxido) VV
complexes (F); six-coordinate (non-oxido) VIV complexes (G); and six-coordi-
nate (non-oxido) VIII complexes (H). The green dots and numbers represent
the published XANES data (Figure S6 in Supporting Information)[6b–d] for the
native (N1,[6b] N2[6c] and N3[6d]) and reduced (R1)[6b] forms of BPO from Asco-
phyllum nodosum (Figure 1).[9,22]
jump, see Figure S2b),[4a,5] as a third coordinate. This used the
distinct difference in edge energies between VV and VIV com-
plexes (Figure 2a). Furthermore, this approach allowed XANES
from non-oxido VV, VIV and VIII complexes to be included, for
which changes in pre-edge parameters were small and often
obscured by experimental noise (inset, Figure 2b). The resul-
tant three-dimensional clustering of XANES of model com-
plexes 1–18 was based on their pre-edge and edge parameters
(Figure 3b). The use of derivative-based XANES edge energies
(Table S2) gave an inferior separation (Figure S4b in Supporting
Information), probably because derivative spectra maxima
were often ill-defined (Figure S2b). By contrast, the use of nor-
malised white line heights instead of edge energies also result-
ed in a good clustering of 1–18 (Figure 3c).
These correlations (Figure 3) enabled a reanalysis of pub-
lished XANES by three independent groups on the algal V-con-
taining protein,[9] bromoperoxidase (BPO from Ascophyllum no-
dosum).[6b–d] Its crystal structure (2.0 ꢁ resolution)[22] and those
of other haloperoxidases,[6d,9,23] revealed five-coordinate VV at
the active centre (BPO Figure 1). The published XANES of
BPO[6b–d] are compared, together with those of model com-
plexes in Figure S6, and key XANES parameters are listed in
Table S2, Supporting Information. Early XANES data[6b,c] for the
native form of BPO (designated as N1[6b] and N2[6c]) were con-
sistent with each other and with a five-coordinate VV centre in
BPO (Figure 3).[22] By contrast, more recent XANES from a similar
enzyme preparation[6d] indicated the presence of a five-coordi-
nate VIV (N3 in Figure 3), in agreement with the conclusions of
the original study that used VIV Schiff base complexes as BPO
models.[6d] This clearly showed photo-reduction[24] of the VV
centre by a stronger photon flux used in the later work[6d] to
a five-coordinate VIV, which retained the geometry of the VV
parent, unlike the six-coordinate VIV centre in chemically re-
duced BPO[6b] (R1 in Figure 3).
In summary, three-dimensional XANES parameter plots deliv-
ered superior separation of VV, VIV and VIII species according to
both their oxidation state and coordination number, using
a much wider range of model species than those used previ-
ously,[5] including non-oxido catecholato VV, VIV and VIII com-
plexes (16a–f and 17, Figure 1). Non-oxido VIV complexes are
known to occur in nature (e.g., amavadin, a low-molecular-
mass VIV complex accumulated in some fungi).[9,25] Binding of
VV/IV by catecholato ligands is likely to be involved in environ-
mental harvesting of V by bacterial siderophores,[9,26] which is
edge peak intensities vs. peak positions (Figure S5 in Support-
ing Information).
An improvement in separation of VV and VIV oxido XANES ac-
cording to oxidation state and coordination number was ach-
ieved by adding the edge energy (determined at half-edge
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an essential step in nitrogen fixation.[9,27] Other models include
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ministration of V-based anti-diabetic drugs.[8,9,29] The new
methodology (Figure 3b,c) can be used to solve controversies
in V oxidation states and coordination geometries in biological,
environmental or material samples, as illustrated by BPO (N1-
N3 and R1 in Figure 3).[6b–d] Further examples of its applications
in elucidating the biotransformations of V drugs in biological
systems will be reported in the near future,[30] as will broad ap-
plications to speciation of other metals.
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Experimental Section
Detailed synthesis and characterisation of model complexes, and
XANES data collection and processing are given in the Supporting
Information.
Acknowledgements
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Keywords: bioinorganic chemistry · environmental chemistry ·
enzymes · vanadium · X-ray absorption spectroscopy
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Received: June 17, 2014
Published online on August 1, 2014
Chem. Eur. J. 2014, 20, 12056 – 12060
www.chemeurj.org
12060
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