Bis(hydroxylamino)triazines: High Selectivity and Hydrolytic Stability of Hydroxylamine-Based Ligands for Uranyl Compared to Vanadium(V) and Iron(III)

Article abstract of DOI:10.1021/acs.inorgchem.8b00582

The development of ligands with high selectivity and affinity for uranium is critical in the extraction of uranium from human body, radioactive waste, and seawater. A scientific challenge is the improvement of the selectivity of chelators for uranium over other heavy metals, including iron and vanadium. Flat ligands with hard donor atoms that satisfy the geometric and electronic requirements of the U^VIO₂²⁺ exhibit high selectivity for the uranyl moiety. The bis(hydroxylamino)(triazine) ligand, 2,6-bis[hydroxy(methyl)amino]-4-morpholino-1,3,5-triazine (H₂bihyat), a strong binder for hard metal ions (Fe^III, Ti^IV, V^V, and Mo^VI), reacted with [U^VIO₂(NO₃)₂(H₂O)₂]·4H₂O in aqueous solution and resulted in the isolation of the complexes [U^VIO₂(bihyat)(H₂O)], [U^VIO₂(bihyat)₂]^2-, and {[U^VIO₂(bihyat)(μ-OH)]}₂^2-. These three species are in equilibrium in aqueous solution, and their abundance varies with the concentration of H₂bihyat and the pH. Reaction of H₂bihyat with [U^VIO₂(NO₃)₂(H₂O)₂]·4H₂O in CH₃CN gave the trinuclear complex [U^VI₃O₆(bihyat)₂(μ-bihyat)₂]^2-, which is the major species in organic solvents. The dynamics between the U^VIO₂²⁺ and the free ligand H₂bihyat in aqueous and dimethyl sulfoxide solutions; the metal binding ability of the H₂bihyat over pyridine-2,6-dicarboxylic acid (H₂dipic) or glutarimidedioxime for U^VIO₂²⁺, and the selectivity of the H₂bihyat to bind U^VIO₂²⁺ in comparison to V^VO₄^3- and Fe^III in either U^VIO₂²⁺/V^VO₄^3- or U^VIO₂²⁺/Fe^III solutions were examined by NMR and UV-vis spectroscopies. The results revealed that H₂bihyat is a superior ligand for U^VIO₂²⁺ with high selectivity compared to Fe^III and V^VO₄^3-, which increases at higher pHs. Thus, this type of ligand might find applications in the extraction of uranium from the sea and its removal from the environment and the human body.

Full text of DOI:10.1021/acs.inorgchem.8b00582

Article
pubs.acs.org/IC
Cite This: Inorg. Chem. XXXX, XXX, XXX−XXX
Bis(hydroxylamino)triazines: High Selectivity and Hydrolytic Stability
of Hydroxylamine-Based Ligands for Uranyl Compared to
Vanadium(V) and Iron(III)
Sofia Hadjithoma,§ Michael G. Papanikolaou,‡ Epameinondas Leontidis,§ Themistoklis A. Kabanos,*,‡
and Anastasios D. Keramidas*,§
§Department of Chemistry, University of Cyprus, 2109 Nicosia, Cyprus
‡Department of Chemistry, Section of Inorganic and Analytical Chemistry, University of Ioannina, 45110 Ioannina, Greece
S
* Supporting Information
ABSTRACT: The development of ligands with high selectivity and affinity for uranium is critical in the extraction of uranium
from human body, radioactive waste, and seawater. A scientific challenge is the improvement of the selectivity of chelators for
uranium over other heavy metals, including iron and vanadium. Flat ligands with hard donor atoms that satisfy the geometric and
electronic requirements of the UVIO2 exhibit high selectivity for the uranyl moiety. The bis(hydroxylamino)(triazine) ligand,
2+
2,6-bis[hydroxy(methyl)amino]-4-morpholino-1,3,5-triazine (H2bihyat), a strong binder for hard metal ions (FeIII, TiIV, VV, and
MoVI), reacted with [UVIO2(NO3)2(H2O)2]·4H2O in aqueous solution and resulted in the isolation of the complexes
[UVIO2(bihyat)(H2O)], [UVIO2(bihyat)2]2−, and {[UVIO2(bihyat)(μ-OH)]}22−. These three species are in equilibrium in
aqueous solution, and their abundance varies with the concentration of H2bihyat and the pH. Reaction of H2bihyat with
[UVIO2(NO3)2(H2O)2]·4H2O in CH3CN gave the trinuclear complex [UVI3O6(bihyat)2(μ-bihyat)2]2−, which is the major species
in organic solvents. The dynamics between the UVIO22+ and the free ligand H2bihyat in aqueous and dimethyl sulfoxide solutions;
the metal binding ability of the H2bihyat over pyridine-2,6-dicarboxylic acid (H2dipic) or glutarimidedioxime for UVIO22+, and the
selectivity of the H2bihyat to bind UVIO2 in comparison to VVO4 and FeIII in either UVIO22+/VVO4 or UVIO22+/FeIII
2+
3−
3−
solutions were examined by NMR and UV−vis spectroscopies. The results revealed that H2bihyat is a superior ligand for UVIO2
2+
with high selectivity compared to FeIII and VVO43−, which increases at higher pHs. Thus, this type of ligand might find
applications in the extraction of uranium from the sea and its removal from the environment and the human body.
used successfully for separation of uranyl from mixed wastes and
chemicals.21−24
INTRODUCTION
■
Over the past few years, an intense scientific effort has taken place
to develop specific chelators for metal ions, including actinides,
to combat environmental contamination caused by heavy metals,
which is considered a serious and widespread health problem due
to their high toxicity.1−5 Uranium has been the primary target for
separation from the radioactive waste produced by nuclear
industries and chelation therapy to be removed from human
body.6 In the last few decades, multidentate complexing agents
with oxygen donor atoms, based on phosphonic ligands7−9 or
siderophore-based units10,11 and polysulfides,12−16 have been
identified as effective uranium chelators. Several of these ligands
reduce UVIO22+ in both kidneys and skeleton17−20 and have been
In addition, uranium is the principal fuel used in nuclear energy
generation. However, because of the limited amounts of uranium
in ground deposits, new technology is being developed for the
extraction of uranyl from the sludge of the desalination plants
due to its high abundance in the sea.25−28 This oceanic reserve
would supply sufficient quantities of uranium for sustained zero-
emission power production over 1000 years, if successfully
harvested.29
Received: March 6, 2018
© XXXX American Chemical Society
A
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
At present, amidoxime-based adsorbents are considered to be
the most promising materials for extraction of uranium from
seawater.30−38 However, amidoximes, such as glutarimidediox-
ime (Scheme 1), lack selectivity for uranyl binding in the
with hard acids is due to the coordination of the metal ions to the
two hard deprotonated hydroxylamine oxygens and a negatively
charged heterocyclic nitrogen donor atoms. In addition, BHT
ligands are planar, and thus, one or two ligands fit perfectly in the
equatorial plane of UVIO22+. Apparently, the strong ligation of
BHT ligands to the equatorial plane of UVIO2 makes them
2+
Scheme 1
strong candidates for the selective binding of uranyl in
comparison to other hard metal ions.
Herein, we report the syntheses and structural and solution
characterizations of four novel uranyl complexes coordinated
with the ligand 2,6-bis[hydroxy(methyl)amino]-4-morpholino-
1,3,5-triazine (H2bihyat; Scheme 1). To the best of our
knowledge, the ligand H2bihyat exhibits the strongest and
most selective binding of UVIO22+ moiety in either UVIO22+/FeIII
or UVIO22+/VVO43− solutions at alkaline pHs.
presence of high concentrations of transition metals, especially
iron and vanadium,36,39 which strongly compete with uranium in
the sequestration process.39−41 Several structural as well as
speciation studies have been employed to better understand the
ligand−uranyl binding process and design of strong selective
ligands and polymer sorbents for uranium.36,37,42−45
EXPERIMENTAL SECTION
■
Caution! Uranium (primary isotope 238U) is a weak α-emitter (4.197 MeV)
with a half-life of 4.47 × 109 years. All complexes were synthesized in
monitored fume hoods, in a laboratory equipped with α- and β-counting
equipment.
Materials and Methods. All chemicals and solvents were
purchased from Merck. Microanalyses for C, H, and N were performed
using a Euro-Vector EA3000 CHN elemental analyzer. Fourier
transform infrared (FT-IR) transmission spectra of the compounds, in
KBr pellets, were acquired using a JASCO-460 model spectropho-
tometer. The kinetic UV−vis measurements were recorded on a
Photonics UV−vis spectrophotometer model 400, equipped with a
CCD array, operating in the range from 250 to 1000 nm. The ligand
H2bihyat was synthesized with a modified procedure of the synthesis
reported in ref 48 and is described in the Supporting Information. The
ligand glutarimidedioxime was synthesized according to the procedure
in ref 54, and the product was recrystallized from ethanol.
Currently, the design of sorbents for selectivity is dictated by
the soft−hard acid−base properties of the metal ions and their
geometric preferences. For example, the available coordination
sites of UVIO2 are in the equatorial plane, and thus, planar
2+
ligands with hard donor atoms that fulfill the ligation
requirements of the UVIO22+ bind selectively the UVIO22+ moiety.
The binding occurs through the equatorial pentacoordination or
hexacoordination generally resulting in five- and six-membered
chelate rings with multidentate ligands (Scheme 1).10,11,44−47
A new family of compact nontoxic tridentate chelators, based
on an N,N′-disubstituted bis(hydroxyamino)-1,3,5-triazine
(BHT) motif, were reported to form hydrolytically stable
complexes with hard acids, such as FeIII and TiIV.48−50 Moreover,
our group reported that these ligands also possess high affinity
and hydrolytic stability for VV and MoVI over a wide pH range of
3−11.51−53 The large thermodynamic stability of BHT ligands
Synthesis of trans-[UVIO2(bihyat)(H2O)2]·H2O (1). To a stirred
aqueous solution (20 mL) of H2bihyat (13 mg, 0.051 mmol) was added
one portion (26 mg, 0.051 mmol) of [UVIO2(NO3)2(H2O)2]·4H2O
(pH ≈ 4). Upon addition of the uranyl salt, the reaction mixture became
brown, indicating complex formation. Brown crystals deposited upon
the partial slow evaporation of the mother liquor. The crystalline solid
Scheme 2. Synthetic Routes for the Complexes 1−4
B
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
a
Table 1. Selected Bond Lengths (Å) for Compounds 1−4
1
2
3
4
U(1)−O(1)
U(1)−O(2)
U(1)−O(4)
U(1)−O(3)
U(1)−N(3)
U(1)−O(7)
U(1)−O(6)
1.788(3)
1.774 (3)
2.359(3)
2.412(3)
2.436(4)
2.367(4)
2.380(3)
1.805(6)
1.809(6)
2.415(4)
2.447(4)
2.518(5)
1.785(4)
1.790(5)
2.354(5)
2.376(4)
2.418(5)
1.796(5)
1.786(6)
2.315(5)
2.405(6)
2.440(7)
1.798(5)
2.461(6)
2.450(5)
2.502(7)
b
b
2.354(4)
c
c
U(2)−O(3′)
U(2)−N(1′)
2.391(5)
2.880(6)
a
b
c
The two columns under 4 are referred to U(1) and U(2) atoms, respectively. Terminal H2O molecules for 1, μ-OH for 2. Bonds of U(1) atoms
with side-on −N(CH3)O coordination.
a
Table 2. Selected Bond Angles (deg) for Compounds 1−4
1
2
3
4
O(2)−U(1)−O(1)
O(2)−U(1)−N(3)
O(1)−U(1)−N(3)
O(4)−U(1)−N(3)
O(3)−U(1)−N(3)
O(4)−U(1)−O(6)
O(7)−U(1)−O(6)
O(7)−U(1)−O(3)
175.5(1)
91.1(1)
93.0(1)
63.5(1)
63.3(1)
74.8(1)
86.0(1)
72.4(1)
177.6(3)
88.1(1)
91.8(1)
61.1(1)
60.7(1)
178.0(2)
95.9(2)
86.2(2)
63.6(2)
63.2(2)
84.5(1)
74.0(1)
75.3(1)
177.4(3)
83.6(2)
96.7(2)
64.3(2)
62.4(2)
97.0(2)
83.0(2)
61.5(2)
60.8(2)
b
b
b
c
O(x)−U(1)−O(y)
58.9(1)
60.4(2)
75.0(2)
29.5(2)
98.9(2)
59.7(2)
O(3)−U(2)−O(4′)
O(3′)−U(2)−N(1′)
O(4)−U(2)−O(3′)
a
b
The two columns under 4 are referred to as U(1) and U(2) atoms, respectively. Angles between terminal H2O molecules for 1, μ-OH for 2.
c
Angles between neighboring bihyat2− ligands.
was recovered by filtration, washed with a minimum amount of cold
water, and dried under vacuum. Yield: 15 mg (51%, based on H2bihyat).
IR (ATR, cm−1): 1531 [ν(-CN-), s] 904 [νas(UO), s], 855 [νs(U
O), w]. Anal. Calcd for C9H20N6O8U (Mr = 578.3): C, 18.69; H, 3.49; N,
14.53; Anal. Found C, 18.69; H, 3.41; N, 14.54%.
in a clear brown solution. The solution was left undisturbed at ambient
temperature (25 °C) for 2 d, and brown crystals suitable for X-ray
diffraction analysis were obtained. The crystals were recovered by
filtration and dried under vacuum. Yield: 32 mg (85%) based on
H2bihyat. IR (ATR, cm−1):1535 [ν(-CN-), s] 902 [νas(UO), s],
855 [νs(UO), w]. Anal. Calcd for C56H100N30O18U3 (Mr = 2195.7):
C, 30.63; H, 4.59; N, 19.14; Anal. Found C, 30.56; H, 4.60; N, 19.18%.
Synthesis of trans-Na2[UVIO2(bihyat)2]·2H2O (2). To a stirred
aqueous solution (2 mL) of H2bihyat (20 mg, 0.078 mmol) was added
one portion (20 mg, 0.039 mmol) of [UVIO2(NO3)2(H2O)2]·4H2O.
The reaction mixture became brown, and the pH was adjusted to 11 with
ca. 130 μL of a 10% w/v NaOH solution. The solution was layered with
methyl alcohol, and brown crystals of compound 2 suitable for X-ray
diffraction analysis were formed after 5 d. The crystalline solid was
recovered by filtration, washed with a minimum amount of methyl
alcohol, and dried under vacuum. Yield: 15 mg (45%) based on
H2bihyat. IR (ATR, cm−1): 1535 [ν(-CN-), s] 846 [νas(UO), s],
761 [νs(UO), w]. Anal. Calcd for C18H32Na2N12O10U (Mr = 860.6):
C, 25.12; H,3.75; N, 19.53; Anal. Found C, 25.16; H, 3.69; N, 19.48%.
Synthesis of K2[UVI2O4(μ2-OH)2(bihyat)2]·3H2O (3). To a stirred
aqueous solution (4 mL) of H2bihyat (20 mg, 0.078 mmol) was added
one portion (39 mg, 0.078 mmol) of [UVIO2(NO3)2(H2O)2]·4H2O.
The reaction mixture became brown, and the pH was adjusted to 9 with
ca. 175 μL of a 10% w/v KOH solution. The solution was layered with
methyl alcohol, and brown crystals of compound 3 suitable for X-ray
diffraction analysis were formed after 8 d. The crystalline solid was
recovered by filtration, washed with a minimum amount of methyl
alcohol, and dried under vacuum. Yield: 18 mg (38%) based on
H2bihyat. IR (ATR, cm−1): 1554 [ν(-CN-), s] 887 [νas(UO), s],
RESULTS AND DISCUSSION
■
Synthesis of the Compounds 1−4. The uranyl complexes
1−4 were synthesized according to Scheme 2. The complexes 1−
3 were obtained in a one-pot reaction, in which
[UVIO2(NO3)2(H2O)2]·4H2O reacted with H2bihyat in aqueous
solution at a molar ratio of UVIO22+/H2bihyat 1:1 for 1 and 3 (eq
1) and 1:2 for 2.
2[UVIO2(NO3)2(H2O)2]·4H2O + 2H2bihyat + 6KOH
→ K2[(UVIO2)2(μ‐OH)2(bihyat)2] + 4KNO3 + 12H2O
(1)
The synthesis of the trinuclear compound 4 was accomplished
by reacting [UVIO2(NO3)2(H2O)2]·4H2O with the ligand
H2bihyat in CH3CN at a molar ratio of UVIO22+/H2bihyat 3:4
in the presence of Et3N (8 equiv) to deprotonate the ligand (eq
2).
825 [νs(UO), w]. Anal. Calcd for C18H36K2N12O15U2 (Mr
=
1214.58): C, 17.78; H, 2.98; N, 13.83; Anal. Found C, 17.70; H, 2.93;
N, 13.89%.
3[UVIO2(NO3)2(H2O)2]·4H2O + 4H2bihyat + 8Et3N
→ (Et3NH)2[(UVIO2)3(μ‐bihyat)2(bihyat)2]
Synthesis of (Et3N)2[UVI3O6(bihyat)4]·4CH3CN (4). Sequential
addition of [UVIO2(NO3)2(H2O)2]·4H2O (26 mg, 0.052 mmol) and
triethylamine (14 mg, 0.138 mmol,19 μL) into a stirred hot (70 °C)
acetonitrile (2 mL) solution of H2bihyat (18 mg, 0.069 mmol) resulted
+ 6Et3NHNO3 + 18H2O
(2)
C
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
The mononuclear complex 1 is slightly soluble in water at pH
= 7 and above. Compounds 1−4 are insoluble in CH3CN but
very soluble in dimethyl sulfoxide (DMSO) and H2O at pH ≥ 6.
At pH < 6 all UVIO22+ precipitates out as 1 and is insoluble. Thus,
all solution studies were performed at pH values above 6.0.
At this point, it is worth noting that the uranyl complexes 1, 2,
and 4 in DMSO and 1, 2, and 3 in H2O solution at pH ≥ 6 are in a
dynamic equilibrium, as it was found by NMR spectroscopy (vide
infra).
Scheme 3
X-ray Crystallographic Results. A summary of the
crystallographic data and the final refinement details for
compounds 1−4 are given in Table S1. Interatomic distances
and bond angles relevant to the uranium coordination sphere are
listed in Tables 1 and 2.
The crystal structure of 1 is shown in Figure 1A. The
uranium(VI) atom adopts the classical pentagonal bipyramidal
Therefore, a strong electron donation from the ring nitrogen
atom to uranium takes place, and this results in a very strong
UVI−N bond. The same trend for the UVI−Ntr bond distances is
observed in the structures of compounds 2, 3, and 4 (see Table
1).
The anion of the mononuclear complex 2 (Figure 1B) has a
hexagonal bipyramidal structure with the six donor atoms of two
tridentate bihyat2− ligands and the uranium(VI) atom [rms
deviation 0.082 Å] to occupy the equatorial plane, which is
perpendicular to the linear trans-[UVIO2]2+ moiety [(OU
O) = 177.6(3)°]. Uranyl oxido bond lengths for the eight-
coordinated ion of 2 [dmean(UO) = 1.807(6) Å]54,61,62 are
slightly longer than those in the seven-coordinate complex 1
[dmean(UO) = 1.781(3) Å] and the UVI−Ntr [2.518(5) Å] and
U−Oh [mean value = 2.431(4) Å] bonds are also longer for the
anion of 2 cf. 2.436(4) and 2.386(3) Å for 1. This bond
lengthening in the anion of 2 might be attributed to the higher
coordination number (eight) of it in comparison to seven for 1.
However, in two compounds [UVIO2(dipic)(H2O)2] and
[UVIO2(dipic)2]2−, which are the analogues of 1 and the anion
of 2, respectively, the uranyl oxido bond lengths are almost
identical [∼1.77 Å],46,47 and thus, the lengthening of UVIO
bonds in the anion of 2 in comparison to 1 was attributed to the
strong binding of the two bihyat2− ligands to the equatorial plane
of the anion of 2. The longer UO bond lengths for 2 in relation
to 1, 3, and 4 (see Table 1) are nicely reflected in the νas(UO),
which is 846 cm−1for 1 and ∼900 cm−1for 1, 3, and 4 (vide
supra).
Figure 1. ORTEP diagram of the mononuclear complexes 1 (A) and 2
(B) with 50% probability ellipsoids (hydrogen atoms and solvent
molecules were omitted for clarity).
configuration and is bonded to a tridentate bihyat2− ligand
through the pyridine-like nitrogen atom N(3), [d(U−Ntr) =
2.436(4) Å] and the two deprotonated hydroxylamine hydroxyls
O(3), O(4) [dmean(U−Oh)= 2.374(4) Å] as well as two oxygen
atoms O(6) and O(7) [dmean(U−Ow)= 2.386 Å] of two water
molecules and two trans oxido groups O(1) and O(2),
[dmean(UO) = 1.781(3) Å].55,56 The equatorial plane defined
by the U, O(3), N(3),O(4), O(6), and O(7) atoms [root-mean-
square (rms) deviation 0.060 Å] is perpendicular to the linear
trans-[UVIO2]2+ moiety [(OUO) = 175.5(1)°]. At this
point, it is worth noting that the UVI−Ntr bond distance of
2.436(4) Å is indicative of a very strong bond of the pyridine-like
triazine nitrogen to uranium(VI). The dipicolinate analogue of 1,
trans-[UVIO2(dipic)(H2O)2] (H2dipic = pyridine-2,6-dicarbox-
ylic acid), has a UVI−Npy bond length of 2.520(6) Å,47 and in
The structure of the anion of 3 (Figure 2) consists of two
distorted pentagonal bipyramidal uranyl units each bridged by
Figure 2. ORTEP diagram of dinuclear complex 3 with 50% probability
ellipsoids (hydrogen atoms and solvent molecules were omitted for
clarity).
2+
general, the UVIO2 complexes with tridentate ligands
containing pyridine nitrogens ligated to uranium(VI) have
UVI−Npy bond length in the range of 2.52−2.64 Å.46,47,57−60 The
ligand bihyat2− exhibits two resonance structures A and B
(Scheme 3).52,53 The flat sp2 hybridized hydroxylamine nitrogen
atoms are in agreement with a large contribution of the structure
“B”. The structure B presented in Scheme 3, according to which
all out-of-ring nitrogen atoms are of approximately sp2
configuration, and thus, the inner ring nitrogen atoms, including
the one ligated to uranium, possess high electron densities.
two hydroxido groups in a centrosymmetric dimer. Each uranyl
group is bonded to a tridentate bihyat2− ligand through two
hydroxylamino oxygen donor atoms and the central triazine
nitrogen atom. The structural features of the anion of 3 are very
similar to those of 1.
The structure of the anion of 4 (Figure 3) consists of three
distorted hexagonal bipyramidal uranyl units bridged by two
bihyat2− ligands in a centrosymmetric trimer [U(1) is the center
D
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
{1H} EXSY NMR spectra were acquired in both organic and
aqueous solutions.
In addition, the hydrolytic stability of UVIO22+-bihyat2−
complexes was studied in the presence of the competing for
2+
UVIO2 ligand dipicolinic acid (H2dipic). Moreover, the
2+
3−
selectivity of bihyat2− to bind UVIO2 in UVIO22+/VVO4 and
UVIO22+/FeIII solutions was also investigated with H NMR
1
spectroscopy. The drawings of all species that are formed in these
experiments were depicted in Scheme 4.
NMR in Organic Solvents. The 1H NMR spectrum of the
free ligand H2bihyat in DMSO-d6 solution gave peaks at 3.28,
3.63, and 3.74, which were assigned to the methyl hydroxylamino
(Hf), -N(CH2)- morpholino, and -(CH2)- morpholino protons,
respectively (Scheme 2).
Figure 3. ORTEP diagram of the trinuclear anion of 4 with 50%
probability ellipsoids (hydrogen atoms and solvent molecules were
omitted for clarity).
In the solution (CD3CN/DMSO-d6) the species 2, 4, and 5 are
formed, as it is evident by 1H NMR spectroscopy (Scheme 4). In
particular, the uranyl complex 4, in a mixed-solvent system of
1
CD3CN/DMSO-d6 (4:1), gave peaks in H and 2D {1H, 13C}
HMQC NMR spectra, which were assigned to complex 4 (96%),
to the mononuclear complex [(UVIO2)(bihyat)2(DMSO-d6)2]
(5) (3%) and to the free H2bihyat (1%) (Figure S1). The NMR
spectra show for complex 4 two different chemical shifts for the
hydroxylamine methyl protons and carbons at 3.636 (38.21) and
3.598 (37.50) ppm, which were assigned to the hydroxylamines
with sp3 (Ha) and sp2 (Hc,b) hybridized N atom, respectively (in
parentheses the chemical shifts of 13C nuclei). A solution of
2+
of symmetry]. The uranyl group U(2)O2 and its symmetry
related U(2A)O2 are bonded to a tridentate bihyat2− ligand
through two deprotonated hydroxylamine hydroxyls and the
central triazine nitrogen atom and are bridged with U(1)O2
2+
2+
group with two bihyat2−ligands. One hydroxylamino group of the
bridging bihyat2− bridges the two uranyl groups through its
oxygen atom, while the other hydroxylamino group of the same
ligand bridges the two uranyl groups in a side-on fashion. This
mode of bridging action of bihyat2− is the first example to be
reported. The N atom of the hydroxylamines in all complexes is
sp2 hybridized, and thus, it has a flat trigonal geometry. However,
the N atom of the hydroxylamine ligated to the uranium atom
with a side-on mode has a trigonal pyramidal geometry, and thus,
in 4, are sp3 hybridized, as expected, so that the unpaired
electrons of the N atom are available for donation to UVI ion.
The three uranium(VI) atoms are arranged in a linear fashion
[U(2A)−U(1)−U(2) = 180°].
1
compound 4 in DMSO-d6 gave H NMR peaks from 4, 5, and
free H2bihyat. Free H2bihyat is produced from 4 according to eq
3.
[UVI3O6(bihyat) + ]2− + 2H+ + 6DMSO‐d6
4
→ 3[(UVIO2)(bihyat)2(DMSO‐d6)2] + H2bihyat
(3)
1
The H NMR spectra of DMSO-d6 solutions containing
H2bihyat (5−30 mM) and [UVIO2(NO3)2(H2O)2]·4H2O (10
mM) gave peaks assigned to the complexes 3, 4, and 5 (Figure
4A). The hydroxylamino methyl protons for each of the species 3
(Hg), 4 (Hb, Hc), and 5 (He), gave a peak at 3.60 ppm. The 1H
NMR triplets of morpholino methylene protons of the three
complexes are overlapping at 3.67 and 3.80 ppm. Moreover,
complex 4 gave a peak at 3.64 ppm, which was assigned to the
hydroxylamino methyl protons attached to the two sp3
hydroxylamine N atoms. Addition of H2bihyat (10.0 mM) to a
DMSO-d6 solution of [UVIO2(NO3)2(H2O)2]·4H2O(10.0 mM)
mainly leads to the formation of 5 (90%) and of a minor quantity
of 4 (10%) (Figure 4A). The concentration of the trinuclear
complex 4 increases at higher concentrations (up to 17.5 mM) of
H2bihyat, whereas the quantity of 5 decreases. At H2bihyat
concentrations greater than 17.5 mM the quantity of complex 4
decreases, whereas the integral of the peak at 3.60 ppm increases
(Figure 4). The increment of the intensity of the peak at 3.60
Speciation, Dynamic, and Stability-Selectivity Studies
of Complexes 1−4 by NMR Spectroscopy. Complexes 1−4
were characterized by 1H NMR spectroscopy in DMSO-d6 and
D2O solutions. However, irrespective of the uranyl complex 1−4
dissolved in either DMSO-d6 or D2O the uranyl complexes 1, 2, 4
and 1−3 were formed in DMSO-d6 and D2O, respectively, and
their concentration was dependent on the initial concentration of
the uranyl complexes and the pHs of the aqueous solutions. The
1H NMR signals of the uranyl complexes were broad and
overlapping, and thus, two-dimensional (2D) {1H, 13C} HMQC
NMR (Figures S1 and S2) spectroscopy was used to resolve and
assign the signals. The 1H and 13C chemical shifts of the uranyl
complexes 1−4 are reported in Table 3.
The broad peaks reveal the existence of dynamic processes
between the UVIO22+-bihyat2− species and between the uranyl
species and the free ligand. To study this dynamic behavior 2D
a
Table 3. 1H(13C) Chemical Shifts (ppm) of Complexes 1−4 and H2bihyat
compounds
Ha(Ca)
Hb‑f(Cb‑f)
-N(CH2)2−(CH2)2O
-N(CH2)2−(CH2)2O
H2bihyat (DMSO-d6)
1 (D2O pH = 9.5)
1 (DMSO-d6)
3.276(37.51)
3.651(37.85)
3.598(37.50)
3.604(37.60)
3.731(37.79)
3.598(37.50)
3.627(66.48)
3.680(66.55)
3.670(66.57)
3.746(66.49)
3.766(66.55)
3.670(66.57)
3.736(43.81)
3.722(43.99)
3.800(44.13)
3.748(43.93)
3.816(43.99)
3.800(44.13)
2 (D2O pH = 9.5)
3 (D2O pH = 9.5)
4 (DMSO-d6)
3.636(38.21)
a
NMR (13C) shifts from 2D {1H, 13C} grHMQC. Labeling according to Scheme 2.
E
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Scheme 4. Drawings of the UVI, VV, and FeIII Species Formed with H2bihyat and H2dipic
Figure 4. 1H NMR spectra, assignments of the peaks (A) and speciation (based on the 1H NMR spectra) of the uranyl complexes (B) of DMSO-d6
VI
2−
solutions containing [UVIO2(NO3)2(H2O)2]·4H2O (10.0 mM) and H2bihyat (5.00−25.0 mM). 5 and [UVIO2(bihyat)2]2− ( ), [(U O2)3(bihyat)3]
■
VI
2+
◆
( ). Labeling according to Scheme 2.
●
( ), H2bihyat (red triangles), U O2
ppm was assigned to the formation of complex 2. However, the
quantity of 2 was not measured because of the overlap of the
peaks of 2 with those of 5.
complexes 2 and 3. The 1H NMR spectra of the D2O solutions
containing [UVIO2(NO3)2(H2O)2]·4H2O (5.00 and 10.0 mM)
and H2bihyat (2.00−30.0 mM) at various pDs gave also peaks
assigned to the proton complex 1 and anions of complexes 2 and
3, being in dynamic equilibria (Figure 5). 1 and the anion of 3 are
more stable at 1:1 UVIO22+/H2bihyat molar ratio, whereas
addition of more H2bihyat results in the formation of the anion of
2, which is the only species present in the solution at 1:2
UVIO22+/H2bihyat molar ratio. The stability of 2 increases over 1
and 3 at higher pDs. At 1:2 UVIO22+/H2bihyat molar ratio no
observed peaks originated from the free ligand, and this fact
reveals that H2bihyat forms hydrolytically stable complexes with
NMR in Aqueous Solution. The 1H NMR spectrum of the
ligand H2byhyat in D2O at pD 9.5 gave a peak at 3.25 and a
multiplet at 3.70 ppm, which were assigned to the methyl
hydroxylamino (Hf) and the -N(CH2)-(CH2)O- morpholino
protons, respectively.
In D2O solutions of UVIO22+ and H2bihyat the species 1, 2, and
3 are formed, as it is evident by 1H NMR spectroscopy (Scheme
4). The 1H NMR spectra of the complexes 1−4 in D2O at pDs >
5 gave peaks that were assigned to complex 1 and anions of
F
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
protons (Hd) and two discrete triplets at 3.766 and 3.816 ppm,
which were assigned to -N(CH2)- and -(CH2)O- morpholino
protons, respectively. Small quantities of the anion of 2 are
formed at high pDs, pD ≈ 9.
D2O solutions containing [UVIO2(NO3)2(H2O)2]·4H2O and
H2bihyat in a molar ratio of ∼1:2 (10.0/18.0 mM) show mainly
the formation of the anion of 2, whereas 1 and the anion of 3 are
present in minor quantities. The quantity of the anion of 2 in this
solution increases by increasing the pD value. At pDs 7.3, and 9.0,
80% and 95% of H2bihyat is bound to the anion of 2, respectively.
1
The H NMR spectrum of complex 2 in D2O shows a peak at
3.60 ppm, which was assigned to methyl hydroxylamino protons
(Hg) and only one peak for the morpholino protons at 3.75 ppm.
Dynamic NMR in Organic Solvents. The 2D {1H } EXSY
NMR of 4 in DMSO-d6/CD3CN (1:4, v/v) shows off-diagonal
exchange cross peaks, starting from the strongest to the weakest,
between Ha and Hb, Ha and Hf, and Hc and Hf (Figure S3), which
were assigned to three different exchange pathways (Scheme 5,
pathways 1−3). The Ha−Hb exchange is attributed to the change
of the hybridization, from sp3 to sp2 and the reverse, of the two
nonequivalent hydroxylamine nitrogen atoms located on each of
the two bihyat2− ligands ligated to the central uranyl moiety
(pathway 1, Scheme 5).The Ha−Hf is attributed to the exchange
of the central bihyat2− ligands with the free H2bihyat (pathway 2,
Scheme 5). However, the fact that Hb does not exchange with the
free ligand as fast as Ha does supports a stepwise mechanism,
whereas the chelate rings of the central bihyat2− initially open at
1
Figure 5. H NMR spectra of the D2O solutions, at various pDs,
containing 10.0 mM [UVIO2(NO3)2(H2O)2]·4H2O and H2bihyat (9.50
mM) (solid black line), 10.0 mM [UVIO2(NO3)2(H2O)2]·4H2O and
H2bihyat (18.0 mM) (red dashed line), and 5.00 mM
[UVIO2(NO3)2(H2O)2]·4H2O and H2bihyat (4.75 mM) (solid green
line). Labeling according to Scheme 2.
UVI O22+ . More specifically, solutions containing
[UVIO2(NO3)2(H2O)2]·4H2O and H2bihyat at a molar ratio
∼1:1 (10.0/9.50 mM) show the formation of complex 1, the
anion of 3, and minor quantities of the anion of 2 in the pD range
1
of 4−12. The H NMR spectrum of complex 1 in D2O gave
broad peaks at 3.65, 3.68, and 3.72, which were assigned to the
He, -N(CH2)-, and -(CH2)O- morpholino protons, respectively.
Complex 1 is more stable at pDs < 5, where it precipitates out due
to its limited solubility in D2O. At pDs > 5 the anion of 3 is the
dominant species in solution giving in 1H NMR spectra a sharp
peak, relative to the peaks of the other UVIO22+/bihyat2−species,
at 3.731 ppm, which was assigned to methyl hydroxylamino
Nsp3 hydroxylamine; then, the coordinated Nsp2 turns to Nsp3
,
-
2+
and finally H2bihyat dissociates. The lability of the UVIO2
O(Nsp3) bond compared to that of UVIO22+-O(Nsp2) might be
attributed to the more efficient protonation of O(Nsp3
)
compared to O(Nsp2). However, if someone considers that all
metal complexes with bihyat2−, including the rest of the uranium
complexes in this study, coordinate to Nsp2 hydroxylamines, the
Scheme 5. Exchange Mechanisms of Complex 4 in DMSO-d6/CD3CN 1:4 (v/v)
G
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
1
Nsp3 hydroxylamine in 4 must exhibit higher energy than Nsp2,
which is stabilized by the side-on coordination with the second
uranium atom, and thus, it is more labile. The much lower
exchange rate of Hc−Hf was attributed to the exchange of the
spectroscopy (Scheme 4). The H NMR spectra of the D2O
solutions containing [UVIO2(NO3)2(H2O)2]·4H2O (5.00 mM),
H2bihyat (13.0 mM), and various concentrations of H2dipic (0−
20.0 mM) at pDs 7.5 and 9.0 are shown in Figure 6A. Each 1H
NMR spectrum contains peaks assigned to the free H2bihyat and
H2dipic, to the anion of complex 2, and to a new complex that
contains both bihyat2− and dipic2− ligated to the uranyl moiety,
that is, [UVIO2(bihyat)(dipic)]2−(6) (Figure 6A, Scheme 4). The
1H NMR spectrum of complex 6 exhibits a multiplet at 8.44
assigned to the aromatic protons of the ligated dipic2−, a triplet at
3.79 assigned to the -(CH2)O- morpholino protons of bihyat2−, a
triplet at 3.75 assigned to the -N(CH2)- morpholino protons of
bihyat2−, and a singlet at 3.685 ppm assigned to the methyl-
hydroxylamine protons of bihyat2−. The diagram of the
concentrations of the anion of 2 and 6 versus the concentration
bihyat2− in complex 5 with the free ligand (pathway 3, Scheme
2+
5), supporting that UVIO22+-O(Nsp2) is more inert than UVIO2
-
O(Nsp3).
Dynamic NMR in Aqueous Solutions. The 2D {1H} EXSY
N M R s p e c t r a o f D 2 O s o l u t i o n s c o n t a i n i n g
[UVIO2(NO3)2(H2O)2]·4H2O and H2bihyat at pD 8.0 and 9.5
are shown in Figure S4. The spectra gave off-diagonal exchange
cross peaks between the protons Hd-He and He-Hg. The Hd-He
were assigned to the dimerization of 1 to 3 and the reverse
(Scheme 6, pathway 1). The less-intense He-Hg cross peaks were
1
Scheme 6. Exchange Mechanisms of 1−3 in D2O
of the added H2dipic is shown in Figure 6B. The H NMR
spectrum of a D2O solution containing [UVIO2(NO3)2(H2O)2]·
4H2O (5.00 mM), H2bihyat (13.0 mM), and H2dipic (10.0 mM)
reveals the presence of complex 6 (67%) and of the anion of 2
(33%) at pD 7.5, while at pD 9 the ratio changes to 7% and 93%
for 6 and the anion of 2, respectively. The equilibrium constants
calculated for reaction 4 are 0.60 0.05 and 52 5 at pDs 7.5
and 9.0, respectively.
[UVIO2(bihyat)(dipic)]2− + H2bihyat
⇄ [UVIO2(bihyat)2]2− + H2dipic
(4)
The stability of complex 6 is related to the UVIO2/bihyat2−
species that exists in D2O at various pDs. At low pDs the 1:1
UVIO2/bihyat2− species, that is, [UVIO2(bihyat)(H2O)2] (1′), is
the most stable complex, and at the equatorial plane of 1′ there is
space for dipic2− to bind to the uranium atom, while at high pDs
the complex [UVIO2(bihyat)2] (2′) is the most stable, and in 2′
there is not any space for dipic2− to ligate to the uranyl moiety.
Thus, the speciation in D 2 O of the system
assigned to the ligation−deligation of a bihyat2− in the
conversion of 1 to 2 and the reverse (Scheme 6, pathway 2).
The exchange of the ligated bihyat2− to UVIO2 with the free
2+
H2bihyat in D2O is a slow process in agreement with the results in
DMSO-d6/CD3CN.
[UVIO2(NO3)2(H2O)2]·4H2O−H2bihyat−H2dipic is entirely
2+
controlled by the ligation of bihyat2− to UVIO2
.
2+
NMR Experiments with H2dipic and H2bihyat. In the
Furthermore, despite the high affinity of H2dipic for UVIO2
D2O solutions containing UVIO22+, H2bihyat, and H2dipic the
{the stability constants, log(βi), for the two complexes
1
species 1, 2, 3, and 6 are formed, as it is evident by H NMR
[UVIO2(dipic)] and [UVIO2(dipic)2]2− are 10.7 0.1 and 16.3
1
1
Figure 6. H NMR spectra (A) and speciation of the uranyl complexes on the basis of H NMR spectra (B) of D2O solutions containing
[UVIO2(NO3)2(H2O)2]·4H2O (5.00 mM) and H2bihyat (13.0 mM) and various concentrations of H2dipic (0−20.0 mM) at pD 7.5 (red lines) and pD 9
(black lines). Labeling according to Scheme 2.
H
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Figure 7. Speciation and 1H NMR spectra of the uranyl complexes of D2O solutions containing [UVIO2(NO3)2(H2O)2]·4H2O (10.0 mM), H2bihyat
(20.8 mM), and NaVO3 (0−15.0 mM) at pDs 8.0 (A, C) and 10.0 (B, D).
0.1 {Xu, 2013}, respectively} H2dipic cannot displace bihyat2−
from UVIO22+/bihyat2− species. This means that the thermody-
namic stability of UVIO22+/bihyat2− complexes is much higher
than that of the corresponding UVIO22+/dipic2− complexes.
NMR Experiments with Glutarimidedioxime and
H2bihyat. The 1H NMR spectra of the D2O solutions containing
[UVIO2(NO3)2(H2O)2]·4H2O (5.00 mM), H2bihyat (13.0
mM), and various concentrations of glutarimidedioxime (2.5−
27.0 mM) at pDs 7.5 and 9.0 are shown in Figure S5. The spectra
show that, in the presence of H2bihyat, glutarimidedioxime does
both pDs. The stepwise addition of NaVVO3 to the solution
results in the decrease of the anion of 2 and the free ligand and
the simultaneous formation of a new complex with peaks at 3.255
[-(CH3)NOH], 3.664 [-N(CH2)-], and 3.742 [-(CH2)O-] ppm.
Stability studies of the mixed inorganic UVIO22+/VVO4
3−
solutions have shown the formation of (UVIO2)3(VVO4)2,
which is the dominant species at pH range of 1.5−9.5.63 The
1
integration of the peaks in the H and 51V spectra of the new
UVIO22+/VVO43−/H2bihyat complex reveals that its stoichiom-
etry is 3:2:2, that is, [(UVIO2)3(VVO4)2(H2bihyat)2] (7). The
chemical shifts of the peaks of the ligand of complex 7 are only
slightly shifted to weaker field compared to the free ligand, and
this indicates that the ligand is likely to be in the protonated form
H2bihyat. In addition, the peaks of the ligated H2bihyat do not
show any broadening, although they are very close to the peaks of
free H2bihyat. Apparently, the ligation of the H2bihyat to the
(UVIO2)3(VVO4)2 is inert. 51V NMR spectroscopy shows a broad
peak at −514 ppm assigned to 7 (Figure S6).
not form any complex with UVIO2 even if the molar ratio of
2+
glutarimidedioxime/H2bihyat is greater than or equal to 2. Thus,
considering the high stability of UVIO22+-glutarimidedioxime
complex,41,54 these results support the high affinity of H2bihyat
for the uranyl moiety.
2+
3−
H2bihyat Binding of UVIO2 in UVIO22+/VVO4 Sol-
utions by 1H NMR Spectroscopy. In D2O solutions
containing UVIO22+, H2bihyat, and VVO4 the species 1, 2, 3,
3−
7, and [VVO2(bihyat)]− are formed, as it evident by H NMR
Complex 7 is the major species (59%), in a solution containing
10.0 mM UOVI2(NO3)2, 20.8 mM H2bihyat, and 10.0 mM
NaVVO3, at pD = 8.0, while at pD = 10.0 the anion of 2 is the
major species (50%), and 42% is complex 7. A small quantity of
H2bihyat, less than 5%, is bound to the complex cis-
[VVO2(bihyat)]−. The concentration of cis-[VVO2(bihyat)]−
decreases when the concentration of NaVVO3 is increased to
15 mM with a simultaneous increase of 7. In any case, the data
show that bihyat2− ligates to UVIO22+ much more strongly than to
1
spectroscopy (Scheme 4). The 1H NMR spectra of D2O
solutions containing [UVIO2(NO3)2(H2O)2]·4H2O (10 mM),
H2bihyat (20.8 mM), and various quantities of NaVVO3 (0−15.0
mM) at pDs 8.0 and 10.0 are shown in Figure 7C,D. The
diagrams of the concentrations of the UVIO22+/bihyat2−and
VVO2 /bihyat2− species versus the concentration of the added
+
NaVVO3 at pDs 8.0 and 10.0 are shown in Figure 7A,B. The 1H
NM R s pec t ru m o f D 2 O s o l u t i o n c o n t a i n i n g
[UVIO2(NO3)2(H2O)2]·4H2O (10.0 mM) and H2bihyat (20.8
mM) reveals the presence of the anion of 2 and the free ligand at
VVO2 , despite the high stability of the VO2 -bihyat2− complexes
+
+
(the stability constants [log(βi)] for [HVVO2(bihyat)] and cis-
I
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
Figure 8. 1H NMR spectra of a D2O solution containing H2bihyat (10.5 mM) and [UVIO2(NO3)2(H2O)2]·4H2O (5.00 mM) and FeIIICl3 (0−5.0 mM)
at pD 7.5 (A) and at pD 9.0 (B). (C) Concentrations of UVIO22+/bihyat2− species vs the added quantity of FeIIICl3 based on the NMR spectra of (A, B).
Labeling according to Scheme 2.
[VVO2(bihyat)]− are 19.36 (6) and 17.87 (1), respectively),52
Fe(OH)3 does not precipitate from the solution, suggesting that
interactions of UVIO22+-bihyat2− species with FeIII keep it in
solution.
2+
whereas the selectivity of the ligand to bind UVIO2 in the
UVIO22+/VO43− solutions increases at higher pDs.
H2bihyat Binding of UVIO22+ in UVIO22+/FeIII Solutions by
H2bihyat Binding of UVIO22+in UVIO22+/ FeIII Solutions by
UV−Vis Spectroscopy. The UV−vis spectra of 2 (prepared
from an aqueous solution containing 1.125 mM
[UVIO2(NO3)2(H2O)2]·4H2O and 2.270 mM H2bihyat and
1H NMR Spectroscopy. In D2O solutions containing UVIO2
,
2+
bihyat2−, and FeIII the species 1, 2, 3, [FeIII(bihyat)]+, and
[FeIII(bihyat)2]− are formed (Scheme 4). The 1H NMR spectra
of D2O solutions containing [UVIO2(NO3)2(H2O)2]·4H2O (5
mM), H2bihyat (10.4 mM), and various quantities of FeIIICl3
(0−5.00 mM) at pDs 7.5 and 9.0 are shown in Figure 8. The
diagrams of the concentrations of the UVIO22+ species versus the
concentration of the added FeIIICl3 at pDs 7.5 and 9.0 are also
shown in Figure 6. The FeIII-bihyat2− complexes, namely,
[FeIII(bihyat)]+ and [FeIII(bihyat)2]−, are NMR-silent, and
1
characterized by H NMR) at pH of 7.5 and 9.0 are shown in
Figure S7. The spectra have a shoulder at 440 nm (ε = 1100 M−1
cm−1, pH = 9.0; ε = 1200 M−1 cm−1, pH = 7.5) and a long tail up
to 700 nm.
The UV−vis spectra of the aqueous solutions containing
[UVIO2(NO3)2(H2O)2]·4H2O (1.125 mM), H2bihyat (2.500
mM), and various concentrations of FeIIICl3 (0−1.125 mM) at
pH 7.5 and 9.0 are shown in Figures S9 and S10. The
concentrations of the UVIO22+ and FeIII species were calculated
by SQUAD, taking into account the uranium compounds 1, 2,
and the iron(III) species [FeIII(bihyat)]+ and [FeIII(bihyat)2]−.
The speciation diagrams of the UVIO22+/bihyat2− and FeIII/
bihyat2− species versus the concentration of the added FeIIICl3
are shown in Figure S10. The anion of the dinuclear species 3 was
not taken into account, because only negligible quantities are
1
2+
thus, the peaks in H NMR spectra originate from UVIO2
-
bihyat2− complexes and the free H2bihyat. The 1H NMR
spectrum of a D2O solution containing [UVIO2(NO3)2(H2O)2]·
4H2O (5.00 mM) and H2bihyat (10.4 mM) reveals the existence
of the anion of 2 and the free ligand at both pDs. At pD 7.5 the
stepwise addition of FeIIICl3 to the solution results in the
decrease of the anion of 2 and the free ligand and the increase of
1, that is, the D2O solution containing 5.00 mM UVIO22+/10.4
mM H2bihyat/5.00 mM FeIII contains 0.50 mM of the anion of 2
and 3.5 mM of 1, and 80% of the UVIO22+ is bound to bihyat2−,
while at pD 9.0 the solution contains 3.40 mM of the anion of 2
and 1.60 mM of 1; 100% of the UVIO22+ is bound to bihyat2−. At
pD > 10.5, bihyat2− is entirely bound to UVIO22+ in the anion of 2.
Although FeIII is released in solution at these high pD values (>7)
1
formed under these conditions, as it was evident by H NMR
spectroscopy. Most of the UVIO22+ is bound to bihyat2− at both
pH values, but at pH 7.5 the major UVIO22+ species is complex 1,
whereas at pH 9.0 it is the anion of 2, in agreement with the
results obtained by 1H NMR. Thus, it is evident on the basis of
J
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
both spectroscopies (NMR and UV−vis) that bihyat2− prefers to
Author Contributions
ligate with UVIO22+ in alkaline UVIO22+/FeIII aqueous solutions.
The manuscript was written through contributions of all authors.
All authors have given approval to the final version of the
manuscript
CONCLUSIONS
■
Notes
In conclusion, a series of uranyl complexes with the bis-
(hydroxylamino)triazine ligand H2bihyat and various composi-
tions of UVIO22+/bihyat2−, depending on the molar ratio of
[UVIO2(NO3)2(H2O)2]·4H2O/H2bihyat, the solvent (water or
acetonitrile), and the pHs, was synthesized. The X-ray structure
analysis of the uranyl/bihyat2− reveals very strong binding of
bihyat2−. Kinetic studies of UVIO22+/bihyat2− complexes in
aqueous and organic solutions show that these complexes are in
dynamic equilibrium with the ligation−deligation of bihyat2− to
be a slow process. The high strength of H2bihyat to ligate to
The authors declare no competing financial interest.
REFERENCES
■
(1) Ansoborlo, E.; Prat, O.; Moisy, P.; Den Auwer, C.; Guilbaud, P.;
Carriere, M.; Gouget, B.; Duffield, J.; Doizi, D.; Vercouter, T.; Moulin,
C.; Moulin, V. Actinide speciation in relation to biological processes.
Biochimie 2006, 88 (11), 1605−1618.
(2) Taylor, D. M.; Taylor, S. K. Environmental uranium and human
health. Rev. Environ. Health 1997, 12 (3), 147−157.
(3) Starck, M.; Laporte, F. A.; Oros, S.; Sisommay, N.; Gathu, V.;
Solari, P. L.; Creff, G.; Roques, J.; Den Auwer, C.; Lebrun, C.; Delangle,
P. Cyclic Phosphopeptides to Rationalize the Role of Phosphoamino
Acids in Uranyl Binding to Biological Targets. Chem. - Eur. J. 2017, 23
(22), 5281−5290.
(4) Winde, F.; Erasmus, E.; Geipel, G. Uranium contaminated drinking
water linked to leukaemiaRevisiting a case study from South Africa
taking alternative exposure pathways into account. Sci. Total Environ.
2017, 574, 400−421.
(5) Keramidas, A. D.; Rikkou, M. P.; Drouza, C.; Raptopoulou, C. P.;
Terzis, A.; Pashalidis, I. Investigation on uranyl interaction with
bioactive ligands. Synthesis and structural studies of the uranyl
complexes with glycine and N-(2-mercaptopropionyl)glycine. Radio-
chim. Acta 2002, 90 (9−11), 549−554.
UVIO2 is demonstrated by its ability to displace from the
2+
equatorial plane other strong ligands, such as H2dipic and
2+
glutarimidedioxime, from the equatorial plane of UVIO2
.
Thermodynamic (stability-selectivity) NMR and UV−vis studies
show that H2bihyat has a high affinity toward the UVIO22+ moiety
and presents high selectivity to bind UVIO22+ in UVIO22+/VVO42+
3−
and UVIO22+/FeIII solutions. The affinity of bihyat2− for UVIO2
increases by increasing the pH from 7 to 10. This is attributed to
the large space around the equatorial plane of uranyl and the
availability of the f-orbitals of the UVIO22+ to accommodate two
strong ligands, in contrast to the smaller space of VV and FeIII
ions.
We should also note that the BHT ligand H2bihyat is (i) easily
prepared, (ii) very stable in the atmosphere and water, (iii)
inexpensive, and (iv) nontoxic. Thus, tridentate chelators, based
on an N,N′-disubstituted BHT motif, represent very promising
chelators for the detoxification of uranyl from biological
organisms and sorbents for cheap and effective separation
technologies of UVIO22+ from either wastes and groundwater or
seawater.
(6) Ni, C.; Shuh, D. K.; Raymond, K. N. Uranyl sequestration:
Synthesis and structural characterization of uranyl complexes with a
tetradentate methylterephthalamide ligand. Chem. Commun. 2011, 47
(22), 6392−6394.
́
(7) Leydier, A.; Lecercle, D.; Pellet-Rostaing, S.; Favre-Reguillon, A.;
Taran, F.; Lemaire, M. Sequestering agent for uranyl chelation: New
binaphtyl ligands. Tetrahedron Lett. 2011, 52 (31), 3973−3977.
́ ́
(8) Sawicki, M.; Lecercle, D.; Grillon, G.; Le Gall, B.; Serandour, A. L.;
Poncy, J. L.; Bailly, T.; Burgada, R.; Lecouvey, M.; Challeix, V.; Leydier,
A.; Pellet-Rostaing, S.; Ansoborlo, E.; Taran, F. Bisphosphonate
sequestering agents. Synthesis and preliminary evaluation for in vitro
and in vivo uranium(VI) chelation. Eur. J. Med. Chem. 2008, 43 (12),
2768−2777.
ASSOCIATED CONTENT
■
S
* Supporting Information
The Supporting Information is available free of charge on the
ACS Publications website at DOI: 10.1021/acs.inorg-
chem.8b00582.
(9) Sawicki, M.; Siaugue, J. M.; Jacopin, C.; Moulin, C.; Bailly, T.;
Burgada, R.; Meunier, S.; Baret, P.; Pierre, J. L.; Taran, F. Discovery of
powerful uranyl ligands from efficient synthesis and screening. Chem. -
Eur. J. 2005, 11 (12), 3689−3697.
(10) Gorden, A. E. V.; Xu, J.; Raymond, K. N.; Durbin, P. Rational
design of sequestering agents for plutonium and other actinides. Chem.
Rev. 2003, 103 (11), 4207−4282.
(11) Gorden, A. E. V.; DeVore, M. A.; Maynard, B. A. Coordination
chemistry with f-element complexes for an improved understanding of
factors that contribute to extraction selectivity. Inorg. Chem. 2013, 52
(7), 3445−3458.
(12) Feng, M. L.; Sarma, D.; Qi, X. H.; Du, K. Z.; Huang, X. Y.;
Kanatzidis, M. G. Efficient Removal and Recovery of Uranium by a
Layered Organic-Inorganic Hybrid Thiostannate. J. Am. Chem. Soc.
2016, 138 (38), 12578−12585.
(13) Sarma, D.; Malliakas, C. D.; Subrahmanyam, K. S.; Islam, S. M.;
Kanatzidis, M. G. K2xSn4-xS8-x(x = 0.65−1): A new metal sulfide for
rapid and selective removal of Cs+, Sr2+and UO22+ions. Chem. Sci.
2016, 7 (2), 1121−1132.
(14) Ma, S.; Huang, L.; Ma, L.; Shim, Y.; Islam, S. M.; Wang, P.; Zhao,
L. D.; Wang, S.; Sun, G.; Yang, X.; Kanatzidis, M. G. Efficient Uranium
Capture by Polysulfide/Layered Double Hydroxide Composites. J. Am.
Chem. Soc. 2015, 137 (10), 3670−3677.
1D and 2D NMR spectra, UV spectra, concentration of
UVIO2 species versus the added quantity of FeIIICl3,
2+
crystal data and structure refinement, bond lengths, bond
angles (PDF)
Accession Codes
CCDC 1825543−1825546 contain the supplementary crystallo-
graphic data for this paper. These data can be obtained free of
charge via www.ccdc.cam.ac.uk/data_request/cif, or by emailing
data_request@ccdc.cam.ac.uk, or by contacting The Cambridge
Crystallographic Data Centre, 12 Union Road, Cambridge CB2
1EZ, UK; fax: +44 1223 336033.
AUTHOR INFORMATION
■
Corresponding Authors
*E-mail: akeramid@ucy.ac.cy. (A.D.K.)
*E-mail: tkampano@cc.uoi.gr. (T.A.K.)
(15) Riley, B. J.; Chun, J.; Um, W.; Lepry, W. C.; Matyas, J.; Olszta, M.
J.; Li, X.; Polychronopoulou, K.; Kanatzidis, M. G. Chalcogen-based
aerogels as sorbents for radionuclide remediation. Environ. Sci. Technol.
2013, 47 (13), 7540−7547.
ORCID
Epameinondas Leontidis: 0000-0003-4427-0398
Anastasios D. Keramidas: 0000-0002-0446-8220
K
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
(16) Manos, M. J.; Kanatzidis, M. G. Layered metal sulfides capture
uranium from seawater. J. Am. Chem. Soc. 2012, 134 (39), 16441−
16446.
(17) Durbin, P. W.; Kullgren, B.; Ebbe, S. N.; Xu, J.; Raymond, K. N.
Chelating agents for uranium(VI): 2. Efficacy and toxicity of
tetradentate catecholate and hydroxypyridinonate ligands in mice.
Health Phys. 2000, 78 (5), 511−521.
(18) Durbin, P. W.; Kullgren, B.; Xu, J.; Raymond, K. N. In vivo
chelation of Am(III), Pu(IV), Np(V) AND U(VI) in mice by TREN-
(Me-3,2-HOPO). Radiat. Prot. Dosim. 1994, 53 (1−4), 305−309.
(19) Durbin, P. W.; Kullgren, B.; Xu, J.; Raymond, K. N. New agents
for in vivo chelation of uranium(VI): Efficacy and toxicity in mice of
multidentate catecholate and hydroxypyridinonate ligands. Health Phys.
1997, 72 (6), 865−879.
(20) Durbin, P. W.; Kullgren, B.; Xu, J.; Raymond, K. N. Development
of decorporation agents for the actinides. Radiat. Prot. Dosim. 1998, 79
(1−4), 433−443.
Uncovering the competitive role of vanadium in uranium extraction
from seawater. Radiochim. Acta 2017, 105 (7), 541−553.
(36) Ivanov, A. S.; Leggett, C. J.; Parker, B. F.; Zhang, Z.; Arnold, J.;
Dai, S.; Abney, C. W.; Bryantsev, V. S.; Rao, L. Origin of the unusually
strong and selective binding of vanadium by polyamidoximes in
seawater. Nat. Commun. 2017, 8 (1), 1 DOI: 10.1038/s41467-017-
01443-1.
(37) Kuo, L. J.; Gill, G. A.; Tsouris, C.; Rao, L.; Pan, H. B.; Wai, C. M.;
Janke, C. J.; Strivens, J. E.; Wood, J. R.; Schlafer, N.; D’Alessandro, E. K.
Temperature Dependence of Uranium and Vanadium Adsorption on
Amidoxime-Based Adsorbents in Natural Seawater. ChemistrySelect
2018, 3 (2), 843−848.
(38) Chatterjee, S.; Bryantsev, V. S.; Brown, S.; Johnson, J. C.; Grant,
C. D.; Mayes, R. T.; Hay, B. P.; Dai, S.; Saito, T. Synthesis of
naphthalimidedioxime ligand-containing fibers for uranium adsorption
from seawater. Ind. Eng. Chem. Res. 2016, 55 (15), 4161−4169.
(39) Leggett, C. J.; Parker, B. F.; Teat, S. J.; Zhang, Z.; Dau, P. D.;
Lukens, W. W.; Peterson, S. M.; Cardenas, A. J. P.; Warner, M. G.;
Gibson, J. K.; Arnold, J.; Rao, L. Structural and spectroscopic studies of a
rare non-oxido V(v) complex crystallized from aqueous solution. Chem.
Sci. 2016, 7 (4), 2775−2786.
(40) Sun, X.; Xu, C.; Tian, G.; Rao, L. Complexation of
glutarimidedioxime with Fe(iii), Cu(ii), Pb(ii), and Ni(ii), the
competing ions for the sequestration of U(vi) from seawater. Dalton
Trans. 2013, 42 (40), 14621−14627.
(41) Tian, G.; Teat, S. J.; Rao, L. Thermodynamic studies of U(vi)
complexation with glutardiamidoxime for sequestration of uranium
from seawater. J. Chem. Soc., Dalton Trans. 2013, 42 (16), 5690−5696.
(42) Li, B.; Zhou, J.; Priest, C.; Jiang, D. E. Effect of Salt on the Uranyl
Binding with Carbonate and Calcium Ions in Aqueous Solutions. J. Phys.
Chem. B 2017, 121 (34), 8171−8178.
(43) Wu, W.; Priest, C.; Zhou, J.; Peng, C.; Liu, H.; Jiang, D. E.
Solvation of the Ca2UO2(CO3)3Complex in Seawater from Classical
Molecular Dynamics. J. Phys. Chem. B 2016, 120 (29), 7227−7233.
(44) Xu, C.; Tian, G.; Teat, S. J.; Rao, L. Complexation of U(VI) with
dipicolinic acid: Thermodynamics and coordination modes. Inorg.
Chem. 2013, 52 (5), 2750−2756.
(45) Drouza, C.; Gramlich, V.; Sigalas, M. P.; Pashalidis, I.; Keramidas,
A. D. Synthesis, structure, and solution dynamics of UO22+-hydroxy
ketone compounds [UO2(ma)2(H 2O)] and [UO2(dpp)(Hdpp)2-
(H2O)] ClO4 [ma = 3-hydroxy-2-methyl-4-pyrone, Hdpp = 3-hydroxy-
1,2- dimethyl-4(1H)-pyridone]. Inorg. Chem. 2004, 43 (26), 8336−
8345.
(46) Cousson, A.; Nectoux, F.; Pages, M. Crystal Structure of
̀
Tetrakis(dipicolinato)triurany. Radiochim. Acta 1993, 61 (3−4), 177−
180.
(47) Harrowfield, J. M.; Lugan, N.; Shahverdizadeh, G. H.; Soudi, A.
A.; Thuery, P. Solid-state luminescence and π-stacking in crystalline
́
uranyl dipicolinates. Eur. J. Inorg. Chem. 2006, 2006, 389−396.
(48) Ekeltchik, I.; Gun, J.; Lev, O.; Shelkov, R.; Melman, A.
Bis(hydroxyamino)triazines: Versatile and high-affinity tridentate
hydroxylamine ligands for selective iron(III) chelation. Dalton Trans.
2006, 6 (10), 1285−1293.
(49) Gun, J.; Ekeltchik, I.; Lev, O.; Shelkov, R.; Melman, A. Bis-
(hydroxyamino)triazines: Highly stable hydroxylamine-based ligands
for iron(III) cations. Chem. Commun. 2005, 42, 5319−5321.
(50) Peri, D.; Alexander, J. S.; Tshuva, E. Y.; Melman, A. Distinctive
structural features of hydroxyamino-1,3,5-triazine ligands leading to
enhanced hydrolytic stability of their titanium complexes. Dalton Trans.
2006, 34, 4169−4172.
(51) Nikolakis, V. A.; Stathopoulos, P.; Exarchou, V.; Gallos, J. K.;
Kubicki, M.; Kabanos, T. A. Unexpected synthesis of an unsymmetrical
μ-oxido divanadium(V) compound through a reductive cleavage of a N-
O bond and cleavage-hydrolysis of a C-N bond of an N,N-disubstituted
Bis-(hydroxylamino) ligand. Inorg. Chem. 2010, 49 (1), 52−61.
(52) Nikolakis, V. A.; Tsalavoutis, J. T.; Stylianou, M.; Evgeniou, E.;
Jakusch, T.; Melman, A.; Sigalas, M. P.; Kiss, T.; Keramidas, A. D.;
Kabanos, T. A. Vanadium(V) compounds with the bis-(hydroxylami-
no)-1,3,5-triazine ligand, H2bihyat: Synthetic, structural, and physical
(21) Leoncini, A.; Huskens, J.; Verboom, W. Ligands for f-element
extraction used in the nuclear fuel cycle. Chem. Soc. Rev. 2017, 46 (23),
7229−7273.
(22) Zarrougui, R.; Mdimagh, R.; Raouafi, N. Highly efficient
extraction and selective separation of uranium (VI) from transition
metals using new class of undiluted ionic liquids based on H-
phosphonate anions. J. Hazard. Mater. 2018, 342, 464−476.
(23) Nigond, L.; Condamines, N.; Cordier, P. Y.; Livet, J.; Madic, C.;
Cuillerdier, C.; Musikas, C.; Hudson, M. J. Recent advances in the
treatment of nuclear wastes by the use of diamide and picolinamide
extractants. Sep. Sci. Technol. 1995, 30 (7−9), 2075−2099.
(24) Nigond, L.; Musikas, C.; Cuillerdier, C. Extraction by n,n,n′,n′-
tetraalkyl −2 alkyl propane −1,3 dia mides. ii. u(vi) and pu(iv). Solvent
Extr. Ion Exch. 1994, 12 (2), 297−323.
(25) Ali, O.; Osman, H. H.; Sayed, S. A.; Shalabi, M. E. H. The removal
of uranium and thorium from their aqueous solutions via glauconite.
Desalin. Water Treat. 2015, 53 (3), 760−767.
(26) Mustafa, J.; Kausar, A.; Bhatti, H. N.; Ilyas, S. Sequestering of
uranium (VI) onto eucalyptus bark: kinetic, equilibrium and
thermodynamic studies. Desalin. Water Treat. 2016, 57 (31), 14578−
14589.
(27) Yakout, S. M.; Rizk, M. A. Adsorption of uranium by low-cost
adsorbent derived from agricultural wastes in multi-component system.
Desalin. Water Treat. 2015, 53 (7), 1917−1922.
(28) Yi, Z. J.; Yao, J.; Kuang, Y. F.; Chen, H. L.; Wang, F.; Xu, J. S.
Uptake of hexavalent uranium from aqueous solutions using coconut
husk activated carbon. Desalin. Water Treat. 2016, 57 (4), 1749−1755.
(29) Sholl, D. S.; Lively, R. P. Seven chemical separations to change the
world. Nature 2016, 532 (7600), 435−437.
(30) Parker, B. F.; Zhang, Z.; Leggett, C. J.; Arnold, J.; Rao, L. Kinetics
of complexation of V(v), U(VI), and Fe(III) with glutaroimide-dioxime:
Studies by stopped-flow and conventional absorption spectroscopy.
Dalton Trans. 2017, 46 (33), 11084−11096.
(31) Parker, B. F.; Zhang, Z.; Rao, L.; Arnold, J. An overview and recent
progress in the chemistry of uranium extraction from seawater. Dalton
Trans. 2018, 47 (3), 639−644.
(32) Abney, C. W.; Mayes, R. T.; Saito, T.; Dai, S. Materials for the
Recovery of Uranium from Seawater. Chem. Rev. 2017, 117 (23),
13935−14013.
(33) Chen, L.; Bai, Z.; Zhu, L.; Zhang, L.; Cai, Y.; Li, Y.; Liu, W.; Wang,
Y.; Chen, L.; Diwu, J.; Wang, J.; Chai, Z.; Wang, S. Ultrafast and Efficient
Extraction of Uranium from Seawater Using an Amidoxime Appended
Metal-Organic Framework. ACS Appl. Mater. Interfaces 2017, 9 (38),
32446−32451.
(34) Piechowicz, M.; Abney, C. W.; Thacker, N. C.; Gilhula, J. C.;
Wang, Y.; Veroneau, S. S.; Hu, A.; Lin, W. Successful Coupling of a Bis-
Amidoxime Uranophile with a Hydrophilic Backbone for Selective
Uranium Sequestration. ACS Appl. Mater. Interfaces 2017, 9 (33),
27894−27904.
(35) Wang, C. Z.; Wu, Q. Y.; Lan, J. H.; Chai, Z. F.; Wu, G. Z.; Shi, W.
Q. Complexation of vanadium with amidoxime and carboxyl groups:
L
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX

Inorganic Chemistry
Article
studies of [V 2VO3(bihyat)2] and of the enhanced hydrolytic stability
species cis-[VVO2(bihyat)]. Inorg. Chem. 2008, 47 (24), 11698−11710.
(53) Stylianou, M.; Nikolakis, V. A.; Chilas, G. I.; Jakusch, T.; Vaimakis,
T.; Kiss, T.; Sigalas, M. P.; Keramidas, A. D.; Kabanos, T. A.
Molybdenum(VI) coordination chemistry of the N,N-disubstituted
bis(hydroxylamido)-1,3,5-triazine ligand, H2bihyat. Water-assisted
activation of the MoVIO bond and reversible dimerization of cis-
[MoVIO2(bihyat)] to [MoVI2O 4(bihyat)2(H2O)2]. Inorg. Chem.
2012, 51 (24), 13138−13147.
(54) Tian, G.; Teat, S. J.; Zhang, Z.; Rao, L. Sequestering uranium from
seawater: Binding strength and modes of uranyl complexes with
glutarimidedioxime. Dalton Trans. 2012, 41 (38), 11579−11586.
(55) Pattenaude, S. A.; Coughlin, E. J.; Collins, T. S.; Zeller, M.; Bart, S.
C. Expanding the Library of Uranyl Amide Derivatives: New Complexes
Featuring the tert -Butyldimethylsilylamide Ligand. Inorg. Chem. 2018,
57 (8), 4543−4549.
́ ́
(56) Tourneux, J. C.; Berthet, J. C.; Cantat, T.; Thuery, P.; Mezailles,
N.; Ephritikhine, M. Exploring the uranyl organometallic chemistry:
From single to double uranium-carbon bonds. J. Am. Chem. Soc. 2011,
133 (16), 6162−6165.
(57) Berthet, J. C.; Nierlich, M.; Ephritikhine, M. Oxygen and nitrogen
Lewis base adducts of [UO2(OTf) 2]. Crystal structures of polypyridine
complexes with out-of-plane uranyl equatorial coordination. Dalton
Trans. 2004, 17, 2814−2821.
́
(58) Berthet, J. C.; Thuery, P.; Dognon, J. P.; Guillaneux, D.;
Ephritikhine, M. Sterically congested uranyl complexes with seven-
coordination of the UO2 unit: The peculiar ligation mode of nitrate in
[UO 2(NO3)2(Rbtp)] complexes. Inorg. Chem. 2008, 47 (15), 6850−
6862.
(59) Charushnikova, I. A.; Den Auwer, C. Crystal structures of
molecular adducts between uranyl nitrate and 2,2′:6′,2″-Terpyridine or
2,2′-Bipyridyl. Russ. J. Coord. Chem. 2004, 30 (7), 511−519.
(60) Kawasaki, T.; Kitazawa, T. Crystal structure of μ-peroxido-
κ4O1,O2:O1′,O2′-bis[(nitrato-κO)(2,2′:6′,2″-terpyridine-
κ3N,N′,N″)dioxidouranium(VI)]. Acta Crystallogr. Sect. Sect. E: Struct.
Commun. 2015, 71, m122−m123.
(61) Kiernicki, J. J.; Cladis, D. P.; Fanwick, P. E.; Zeller, M.; Bart, S. C.
Synthesis, Characterization, and Stoichiometric U-O Bond Scission in
Uranyl Species Supported by Pyridine(diimine) Ligand Radicals. J. Am.
Chem. Soc. 2015, 137 (34), 11115−11125.
(62) McSkimming, A.; Su, J.; Cheisson, T.; Gau, M. R.; Carroll, P. J.;
Batista, E. R.; Yang, P.; Schelter, E. J. Coordination Chemistry of a
Strongly-Donating Hydroxylamine with Early Actinides: An Inves-
tigation of Redox Properties and Electronic Structure. Inorg. Chem.
2018, 57 (8), 4387−4394.
(63) Nipruk, O. V.; Chernorukov, N. G.; Volochai, A. A.; Arova, M. I.
Study of the state of uranyl orthovanadate (UO2) 3(VO4)2·4H2O in
aqueous solutions. Russ. J. Gen. Chem. 2013, 83 (4), 636−641.
M
DOI: 10.1021/acs.inorgchem.8b00582
Inorg. Chem. XXXX, XXX, XXX−XXX