Bismuth(III) halide complexes of aromatic thiosemicarbazones: Synthesis, structural characterization and biological evaluation

Article abstract of DOI:10.1016/j.poly.2021.115388

Four new bismuth(III) thiosemicarbazone complexes, {BiCl₃(η¹-S-Hacptsc)₃} (1), {[BiBr₃(η¹-S-Hacptsc)₃]·CH₃OH} (2), {[BiI₂(μ₂-I](η¹-S-Hacptsc)]₂} (3) and {[BiCl₂(μ₂-Cl)(η¹-S-Hbztsc)₂]₂} (4), were prepared with the ligands acetophenone thiosemicarbazone (Hacptsc) and benzaldehyde thiosemicarbazone (Hbztsc). The complexes were characterized by a series of spectroscopic techniques. The crystal structures of 1–4 were also determined by X-ray diffraction. To the best of our knowledge, complexes 1–4 are the first examples of bismuth(III) halide aromatic thiosemicarbazones. Hirshfeld surface analysis studies show that H^…H and X^…H/H^…X interactions of complexes 1–4 play an important role in the formation of supramolecular aggregation. Complexes 1–4 have been tested for their in vitro cytotoxic activity against human breast adenocarcinoma (MCF-7) cells. The toxicity of 1–4 has been evaluated on normal human fetal lung fibroblast cells (MRC-5). Complexes 1–4 appeared to show low cytotoxic activity and low toxicity. The antibacterial activity of 1–4 and their ligands was evaluated against the Gram negative species Pseudomonas aeruginosa (P. aeruginosa) and Escherichia coli (E. coli) and Gram positive ones Staphylococcus epidermidis (S. epidermidis) and Staphylococcus aureus (S. aureus) by the Inhibition Zone (IZ) method. The influence of 1–4 on the catalytic peroxidation of linoleic acid by the enzyme lipoxygenase (LOX) has been determined experimentally. The IC₅₀ values reveal that the synthesized bismuth(III) aromatic thiosemicarbazone complexes have good potential to inhibit lipoxygenase, with values better than the free aromatic thiosemicarbazone ligands and cisplatin.

Full text of DOI:10.1016/j.poly.2021.115388

Polyhedron 208 (2021) 115388
Contents lists available at ScienceDirect
Polyhedron
journal homepage: www.elsevier.com/locate/poly
Bismuth(III) halide complexes of aromatic thiosemicarbazones: Synthesis,
structural characterization and biological evaluation
,
I.I. Ozturka *, C.N. Bantib, S.K. Hadjikakoub, N. Panagiotouc, A.J. Tasiopoulosc
a Section of Inorganic Chemistry, Department of Chemistry, Tekirdag Namık Kemal University, 59030 Tekirdag, Turkey
b Section of Inorganic and Analytical Chemistry, Department of Chemistry, University of Ioannina, 45110 Ioannina, Greece
c Department of Chemistry, University of Cyprus, Nicosia, Cyprus
A R T I C L E I N F O
A B S T R A C T
1-S-Hacptsc)3} (1), {[BiBr3( 1-S-Hacptsc)3]⋅
η
Keywords:
Four new bismuth(III) thiosemicarbazone complexes, {BiCl3(
η
1-S-Hacptsc)]2} (3) and {[BiCl2(µ2-Cl)(
η
1-S-Hbztsc)2]2} (4), were prepared with the
Bismuth(III) halide
Aromatic thiosemicarbazone
Crystal structure
CH3OH} (2), {[BiI2(µ2-I](
η
ligands acetophenone thiosemicarbazone (Hacptsc) and benzaldehyde thiosemicarbazone (Hbztsc). The com-
plexes were characterized by a series of spectroscopic techniques. The crystal structures of 1–4 were also
determined by X-ray diffraction. To the best of our knowledge, complexes 1–4 are the first examples of bismuth
(III) halide aromatic thiosemicarbazones. Hirshfeld surface analysis studies show that H… H and X… H/H… X in-
teractions of complexes 1–4 play an important role in the formation of supramolecular aggregation. Complexes
1–4 have been tested for their in vitro cytotoxic activity against human breast adenocarcinoma (MCF-7) cells. The
toxicity of 1–4 has been evaluated on normal human fetal lung fibroblast cells (MRC-5). Complexes 1–4 appeared
to show low cytotoxic activity and low toxicity. The antibacterial activity of 1–4 and their ligands was evaluated
against the Gram negative species Pseudomonas aeruginosa (P. aeruginosa) and Escherichia coli (E. coli) and Gram
positive ones Staphylococcus epidermidis (S. epidermidis) and Staphylococcus aureus (S. aureus) by the Inhibition
Zone (IZ) method. The influence of 1–4 on the catalytic peroxidation of linoleic acid by the enzyme lipoxygenase
(LOX) has been determined experimentally. The IC50 values reveal that the synthesized bismuth(III) aromatic
thiosemicarbazone complexes have good potential to inhibit lipoxygenase, with values better than the free ar-
omatic thiosemicarbazone ligands and cisplatin.
Hirshfeld surface analysis
Biological activity
1. Introduction
[9–16].
Bismuth is considered to be the least toxic metal and due to this
Thiosemicarbazones, which are usually obtained by condensation of
thiosemicarbazide with suitable aldehydes and ketones, have become
the focus of attention in recent years because of their various applica-
tions in industry and chemistry [1,2]. Thiosemicarbazones are prom-
ising compounds in the treatment of many diseases and the development
of these compounds is still continuing today [3–6]. After the success of
cisplatin, the synthesis of antitumor and antimicrobial drugs by forming
metal complexes associated with organic ligands has become a new
strategy [7]. The presence of amide, imine and thione groups makes
thiosemicarbazones polydentate ligands, and due to these properties,
many thiosemicarbazone complexes with different coordination modes
have been prepared and characterized [8]. Some of these metal thio-
semicarbazone complexes have shown a range of activities such as
anticancer, antitumor, antibacterial, antimicrobial and antifungal
feature bismuth compounds have many applications in medicine [17].
The unpredictable structural variations of bismuth, because of its one
inert electron pairs (6s2), and the polydentate ligands of thio-
semicarbazones allow the synthesis of compounds with a wide variety of
coordination structures for bismuth(III) thiosemicarbazone complexes
[18–26]. Although structural studies on bismuth(III) complexes con-
taining heterocyclic thiosemicarbazone have been published in the
literature [18–26], there is no structural study on bismuth(III) halide
complexes containing aromatic thiosemicarbazones.
Aiming to contribute to the investigations on the coordination
chemistry and biological action of bismuth(III) aromatic thio-
semicarbazone complexes, in the present work we have synthesized two
monomeric (1 and 2) and two dimeric (3 and 4) bismuth(III) thio-
semicarbazone complexes. Complexes 1–4 were characterized by
* Corresponding author.
E-mail address: iiozturk@nku.edu.tr (I.I. Ozturk).
https://doi.org/10.1016/j.poly.2021.115388
Received 4 July 2021; Accepted 19 July 2021
Available online 27 July 2021
0277-5387/© 2021 Elsevier Ltd. All rights reserved.

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
spectroscopic techniques, thermal analysis, and single crystal X-ray
diffraction (XRD) analysis. Complexes 1–4 and the free thio-
semicarbazone ligands (Hacptsc and Hbztsc) were evaluated for their in
vitro cytotoxic activity against MCF-7 cells, along with the non-
cancerous cells MRC-5. Their in vitro antimicrobial activity against
Gram positive and negative bacteria was also checked. The LOX inhib-
itory activity caused by complexes 1–4 and the free thiosemicarbazone
ligands was studied.
m, 1076 m, 1022w, 966w, 827 s, 758 s, 685 s, 630w, 586 m, 528 s, 415 s.
1H NMR (400 MHz, DMSO‑d6, δ, ppm): 10.25 (s, 3H, N2H), 8.32 (br, s,
6H, N1H2), 7.95 (m, 6H, C4H, C8H), 7.42 (m, 9H, C5H, C6H, C7H), 2.34
(s, 9H, –CH3). 13C NMR (400 MHz, DMSO‑d6, δ, ppm): 179.68 (C1),
148.96 (C2), 138.54 (C3), 130.17 (C5-7), 129.18 (C4-8), 127.53 (C6),
14.98 (–CH3).
2.3.2. Synthesis of {[mer-BiBr3(
η
1-S-Hacptsc)3]⋅CH3OH} (2)
Bismuth(III) bromide (0.224 g, 0.0005 mol) was dissolved in 10 mL
methanol, then a 10 mL methanolic solution of acetophenone thio-
semicarbazone was added (0.290 g, 0.0015 mol). The yellow solution
that formed was refluxed for 4 h and cooled to room temperature. Yel-
low crystals were obtained by slow evaporation of the solution at room
temperature. The crystals were filtered, washed with a small amount of
cold methanol and dried in vacuo over silica gel. Yellow crystals, yield:
87% (0.461 g), melting point: 210–212 ◦C, m.w.: 1060.54 g/mol. Anal.
Calc. for C28H37BiBr3N9OS3: C, 31.71; H, 3.52; N, 11.89; S, 9.07%.
Found: C, 31.34; H, 3.46; N, 11.63; S, 8.94%. Soluble in methanol,
acetonitrile, acetone, tetrahydrofuran and dimethyl sulfoxide. ΛM
(DMSO, Ωꢀ 1 cm2 molꢀ 1): 17.95 ± 0.72. IR (cmꢀ 1): 3433 m, 3298 s,
3240 s, 1583 s, 1524 s, 1491 m, 1471w, 1441 m, 1365w, 1284 s, 1182w,
1084 m, 1072 m, 1018w, 999w, 823 s, 756 s, 681 s, 631 m, 552 s, 521 s,
444 m. 1H NMR (400 MHz, DMSO‑d6, δ, ppm): 10.25 (s, 3H, N2H), 8.33
(br, s, 6H, N1H2), 7.95 (m, 6H, C4H, C8H), 7.42 (m, 9H, C5H, C6H, C7H),
2.34 (s, 9H, –CH3). 13C NMR (400 MHz, DMSO‑d6, δ, ppm): 179.42 (C1),
149.12 (C2), 138.51 (C3), 130.20 (C5-7), 129.18 (C4-8), 127.54 (C6),
15.01 (–CH3).
2. Experimental
2.1. Materials and instrumentation
The precursors acetophenone, benzaldehyde, thiosemicarbazide,
bismuth(III) chloride, bismuth(III) bromide and bismuth(III) iodide
were procured from Sigma Aldrich and used without purification.
Elemental analyses for C, H, N and S were carried out with a Carlo Erba
EA MODEL 1108 elemental analyzer. Melting points were measured in
open tubes with a STUART SMP30 scientific apparatus and are uncor-
rected. The molar conductivity of the complexes in DMSO was measured
by means of a VWR Phenomenal conductometer CO 3000 L. FT-IR
spectra were recorded in the 4000–400 cmꢀ 1 region with a Bruker Op-
tics, Vertex 70 FT-IR spectrometer using ATR techniques. Micro Raman
spectra (64 scans) were recorded at room temperature by using a low-
power (~30 mW) green (514.5 nm) laser on a Renishaw In Via spec-
trometer set at 2.0 resolution. Thermogravimetric–Differential Thermal
Analysis (TG–DTA) of the complexes was carried out on a Seiko SII TG/
DTA 7200 apparatus under an N2 flow (50 cm3 minꢀ 1) with a heating
rate of 5 ◦C minꢀ 1. 1H and 13C NMR spectra were recorded with a Varian
Unity Inova 500 MHz spectrometer in DMSO‑d6 with chemical shifts
given in parts per million referenced to internal TMS (H). The UV spectra
were collected with a Shimadzu UV-2600 UV–Vis spectrophotometer.
2.3.3. Synthesis of {[BiI2(µ -I)(
η
1-S-Hacptsc)]2} (3)
The procedure was the s2ame as that for compound 1, but the bismuth
(III) iodide was added to acetophenone thiosemicarbazone in a molar
stoichiometric ratio of 1:1 for complex 3 (BiI3: 0.295 g, 0.0005 mol;
HAcptsc: 0.097 g, 0.0005 mol). Red crystals, yield: 79% (0.619 g),
melting point: 185–187 ◦C, m.w.: 1565.92 g/mol. Anal. Calc. for
2.2. Preparation of acetophenone thiosemicarbazone (Hacptsc) and
benzaldehyde thiosemicarbazone (Hbztsc)
C18H22B2I6N6S2: C, 13.81; H, 1.42; N, 5.37; S, 4.09%. Found: C, 13.64;
H, 1.48; N, 5.26; S, 4.22%. Soluble in methanol, ethanol, acetonitrile,
acetone, tetrahydrofuran and dimethyl sulfoxide. ΛM (DMSO, Ωꢀ 1 cm2
molꢀ 1): 21.03 ± 0.76. IR (cmꢀ 1): 3425 m, 3292 s, 1579 s, 1520 s, 1491
m, 1441 m, 1367w, 1279 m, 1236w, 1182w, 1082 m, 1070 m, 1018w,
999w, 962w, 822 s, 758 s, 683 s, 631 m, 540 s, 519 s, 442 m. 1H NMR
(400 MHz, DMSO‑d6, δ, ppm): 10.26 (s, 2H, N2H), 8.34 (br, s, 4H, N1H2),
7.95 (m, 4H, C4H, C8H), 7.42 (m, 6H, C5H, C6H, C7H), 2.34 (s, 6H,
–CH3). 13C NMR (400 MHz, DMSO‑d6, δ, ppm): 179.22 (C1), 149.25
(C2), 138.48 (C3), 130.22 (C5-7), 129.18 (C4-8), 127.55 (C6), 15.05
(–CH3).
The thiosemicarbazone ligands were prepared according to the
literature procedure [27]. The thiosemicarbazide (5 mmol) and aceto-
phenone or benzaldehyde (5 mmol) were dissolved in 20 mL ethanol. A
few drops of hydrochloric acid were added to the mixture. The mixture
was stirred and refluxed for 5 h (78 ◦C). Completion of the reaction was
monitored by TLC for the disappearance of the starting material. The
mixture was then cooled to room temperature and filtered. After a slow
evaporation of the filtrate at room temperature, the crystals that formed
were collected by filtration. Hacptsc (C9H11N3S), m.w.: 193.27 g/mol,
colorless crystals, melting point: 116–118 ◦C, yield: 84% (0.081 g).
Hbztsc (C8H9N3S), m.w.: 179.24 g/mol, colorless crystals, melting point:
158–160 ◦C, yield: 86% (0.077 g).
2.3.4. Synthesis of {[BiCl2(µ -Cl)(
η
1-S-Hbztsc)2]2} (4)
The procedure was the sa2me as that for compound 1, but the bismuth
(III) chloride to benzaldehyde thiosemicarbazone molar stoichiometric
ratio was 1:2 for complex 4 (BiCl3: 0.158 g, 0.0005 mol; HBztsc: 0.179 g,
0.0010 mol). Yellow crystals, yield: 82% (0.277 g), melting point:
204–206 ◦C, m.w.: 1347.62 g/mol. Anal. Calc. for C32H36Bi2Cl6N12S4: C,
28.52; H, 2.69; N, 12.47; S, 9.52%. Found: C, 28.64; H, 2.46; N, 12.65; S,
9.64%. Soluble in methanol, acetonitrile, acetone, tetrahydrofuran and
dimethyl sulfoxide. ΛM (DMSO, Ωꢀ 1 cm2 molꢀ 1): 7.16 ± 1.18. IR (cmꢀ 1):
3441 m, 3402 m, 3290 m, 3226 m, 1608 s, 1597 s, 1556 m, 1527 s,
1498w, 1444 m, 1369 s, 1275 s, 1225 m, 1173 m, 1093 m, 1053 m,
1024w, 993w, 953 s, 918w, 868 m, 800 s, 752 s, 688 s, 642w, 604 s, 565
s, 530 m, 505w, 478 m. 1H NMR (400 MHz, DMSO‑d6, δ, ppm): 11.47 (s,
4H, N2H), 8.23, 8.03 (d, 8H, N1H2), 8.09 (s, 4H, C2H), 7.82 (m, 8H, C4H,
C8H), 7.43 (m, 12H, C5H, C6H, C7H). 13C NMR (400 MHz, DMSO‑d6, δ,
ppm): 178.85 (C1), 143.27 (C2), 135.09 (C3), 130.78 (C5-7), 129.59
(C4-8), 128.23 (C6).
2.3. Synthesis of the new bismuth(III) halide complexes
2.3.1. Synthesis of {mer-BiCl3(
η
1-S-Hacptsc)3} (1)
Bismuth(III) chloride (0.158 g, 0.0005 mol) was dissolved in 10 mL
ethanol and a few drops of HCl were added. Next a 10 mL ethanolic
solution of acetophenone thiosemicarbazone was added (0.290 g,
0.0015 mol). The yellow solution that formed was refluxed for 3 h and
cooled to room temperature. Yellow crystals were obtained by slow
evaporation of the solution at room temperature. The crystals were
filtered, washed with a small amount of cold ethanol and dried in vacuo
over silica gel. Yellow crystals, yield: 85% (0.381 g), melting point:
185–186 ◦C, m.w.: 895.13 g/mol. Anal. Calc. for C27H33BiCl3N9S3: C,
36.23; H, 3.72; N, 14.08; S, 10.74%. Found: C, 35.59; H, 3.79; N, 13.96;
S, 10.49%. Soluble in methanol, acetonitrile, acetone, tetrahydrofuran
and dimethyl sulfoxide. ΛM (DMSO, Ωꢀ 1 cm2 molꢀ 1): 5.13 ± 0.89. IR
(cmꢀ 1): 3433w, 3371 m, 3257 s, 3171 m, 3057w, 2361w, 2341w, 1591
s, 1514 s, 1491 s, 1444 m, 1367w, 1334w, 1281 s, 1252 m, 1186w, 1092
2

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
2.4. Single X-ray structure determination
interaction. Points on the plot with no contribution on the surface are
left uncolored, and points with a contribution to the surface are colored
in blue for a small contribution, through green to red for points with the
greatest contribution [35,36].
Single crystal X-ray diffraction data for complexes 1–4 were
collected on a Rigaku Supernova A diffractometer, equipped with a CCD
area detector utilizing Mo/Cu-Kα (λ = 0.71073/1.5418 Å) radiation. A
suitable crystal was mounted on a Hampton cryoloop with Paratone-N
oil and transferred to a goniostat, where it was cooled for data collec-
tion. The structures were solved by direct methods using SHELXT and
refined on F2 using full-matrix least squares using SHELXL14.1 [28].
Software packages used: CrysAlis CCD for data collection, CrysAlis RED
for cell refinement, data reduction and absorption correction (Empirical
absorption correction using spherical harmonics, implemented in the
SCALE3 ABSPACK scaling algorithm) [29] and WINGX for geometric
calculations [30]. The non-H atoms were treated anisotropically,
whereas the aromatic hydrogen atoms were placed in calculated, ideal
positions and refined as riding on their respective carbon atoms. The
crystal data and refinement parameters are presented in Table 1.
2.6. Cytotoxic activity
Biological experiments were carried in dimethyl sulfoxide Dulbec-
co’s Modified Eagle’s Medium solutions (DMEM) DMSO/DMEM
(0.02–0.2% v/v) for complexes 1–4 and the free ligands. Stock solutions
of complexes 1–4 and the free ligands (0.01 M) in DMSO were freshly
prepared and diluted in with the cell culture medium to the desired
concentrations (0.5–30 μM). The results are expressed in terms of IC50
values, which is the concentration of drug required to inhibit cell growth
by 50% compared to the control after a 48 h incubation of the complexes
and free ligands with the cell lines. The cell viability was determined by
a Sulforhodamine B (SRB) assay, as previously described [37].
2.7. Effect on the growth of microbial strains
2.5. Hirshfeld surface analysis
The procedure was performed as previously reported [38]. Briefly,
bacterial strains plated onto trypticase soy agar were incubated at 37 ◦C
for 18–24 h. Three to five isolated colonies of the same morphological
appearance were selected from a fresh agar plate using a sterile loop and
transfer into a tube containing 2 mL of a sterile saline solution. The
optical density at 620 nm was adjusted to 0.1, which corresponds to 108
cfu/mL [38]. For the evaluation of IZ, filter paper discs (about 9 mm in
diameter), were been soaked with the compounds as well as their ligands
at concentrations of 1 mM and they were placed on the agar surface and
the petri plates were incubated for 20 hrs.
The determination of the Hirshfeld surface (HS) and analysis of the
corresponding fingerprint plot (FP) provide us an efficient and reason-
ably effective method for the aims of the visualization and comparison of
various intermolecular interactions present within a crystal structure
[31]. The three-dimensional HSs mapped to the normalized contact
distance (dnorm) and their associated two-dimensional FP analyses as
well as shape-index and curvedness presented in this study were
generated for the bismuth(III) compounds 1–4 using Crystal Explorer
17.5 [32]. The identification of the close contacts is possible via the
normalized contact distance (dnorm) relative to the distances from the
surface to the nearest nucleus inside and outside the surface (di and de
respectively) and the van der Waals (vdW) radii of the atom. For the
visualization of dnorm, a red-blue-white (RBW) color scale was selected
[33,34]. 2D-fingerprint plots are derived from the Hirshfeld surface and
provide a visual summary of the frequency of each de and di combination
along the surface of a molecule. Thus, the two-dimensional fingerprint
graph reveals the relative area of the surface corresponding to each
2.8. Lipoxygenase activity inhibition
2.8.1. Preparation of solutions
The buffer solution: 0.1 mol boric acid (H3BO3, 6.18 g) was added to
300 cm3 distilled water. The pH was adjusted to 9 with 50% w/v NaOH.
Finally, the solution was diluted to 500 cm3 [39]. Linoleic acid substrate
Table 1
Crystal data and structure refinement details for the bismuth(III) thiosemicarbazone complexes 1–4.
1
2
3
4
Empirical formula
Formula weight
T (K)
C
27H33BiCl3N9S3
C28H37BiBr3N9OS3
1060.54
C18H22Bi2I6N6S2
1565.92
C32H36Bi2Cl6N12S4
1347.62
895.13
104(2)
105(1)
102(1)
101.3(3)
Wavelength (Å)
Crystal system
Space group
a (Å)
0.71073
1.54184
1.54184
0.71073
Triclinic
Monoclinic
I 2/a
Monoclinic
I 2/a
Triclinic
P ꢀ 1
P ꢀ 1
7.9486(3)
15.0186(3)
8.4527(2)
20.9566(7)
8.6174(3)
9.4389(5)
b (Å)
19.1734(5)
23.5942(6)
69.954(2)
10.9253(7)
12.6558(8)
68.617(6)
c (Å)
57.4824(15)
90
23.5241(7)
90
α
(◦)
β (◦)
γ (◦)
V (Å3)
Z
85.063(2)
94.871(2)
93.272(3)
89.936(5)
80.202(2)
90
90
69.763(5)
3327.19(18)
4
7270.9(3)
4241.3(2)
1128.52(13)
1
8
4
D
calc (g cmꢀ 3
)
1.787
1.936
2.452
1.983
μ
(mmꢀ 1
)
5.763
15.295
51.438
8.367
F(000)
1760
4088
2752
644
Crystal size (mm3)
0.032x0.041x0.140
3.222 to 27.499
ꢀ 10 ≤ h ≤ 10
ꢀ 24 ≤ k ≤ 23
ꢀ 29 ≤ l ≤ 26
32,089
0.013x0.025x0.138
4.632 to 66.998
ꢀ 17 ≤ h ≤ 17
ꢀ 10 ≤ k ≤ 7
ꢀ 68 ≤ l ≤ 68
23,093
0.011x0.015x0.046
3.764 to 66.987
ꢀ 24 ≤ h ≤ 25
ꢀ 8 ≤ k ≤ 10
ꢀ 28 ≤ l ≤ 26
6937
0.010x0.029x0.060
3.260 to 27.495
ꢀ 12 ≤ h ≤ 12
ꢀ 12 ≤ k ≤ 14
ꢀ 16 ≤ l ≤ 13
9339
θ Range for data collection (◦)
Index ranges
Reflections collected
Independent reflections
Data/restraints/parameters
GOF on F2
14803[Rint = 0.0532]
14803/0/775
0.970
6464 [Rint = 0.0389]
6464/0/408
1.057
3778 [Rint = 0.0250]
3778/0/154
1.150
5003 [Rint = 0.0456]
5003/0/253
1.010
Final R indices [I > 2
R Indices (all data)
σ
(I)]
R1 = 0.0422 wR2 = 0.0657
R1 = 0.0696 wR2 = 0.0740
1.563 and ꢀ 1.837
R1 = 0.0303 wR2 = 0.0802
R1 = 0.0344 wR2 = 0.0822
1.228 and ꢀ 1.179
R1 = 0.0795 wR2 = 0.2158
R1 = 0.0826 wR2 = 0.2177
2.483 and ꢀ 3.972
R1 = 0.0410 wR2 = 0.0634
R1 = 0.0519 wR2 = 0.0680
1.967 and ꢀ 1.847
Largest diff. peak and hole (e Åꢀ 3
)
3

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
solution: 0.05 cm3 of linoleic acid was dissolved in 0.05 cm3 95% ethanol
in a volumetric flask (50 cm3). The appropriate volume of H2O was
gradually added in the flask. 5 cm3 of the prepared solution was added to
30 cm3 of the borate buffer. Enzyme solution (lipoxygenase): a solution of
10,000 U of enzyme for each cm3 of borate buffer was prepared in ice
cold bath [39]. An amount of 500 U for every 3 cm3 of reaction mixture
was used in every experiment. A unit of lipoxygenase causes an increase
in absorption at 234 nm equal to 0.001 per minute.
values are compatible with the formation of complexes 1–4. The sta-
bility of complexes 1–4 in dimethyl sulfoxide solution were tested by
molar conductivity measurements. No significant change was observed
between the initial molar conductivity values and the corresponding
ones measured after 0, 24 and 48 h for complexes 1–4 (Table S1). This
shows that the compounds are stable in dimethyl sulfoxide solution.
3.2. Spectroscopy
2.9. Procedure
The IR and Raman spectra of the bismuth(III) thiosemicarbazone
complexes (1–4) provide information about the bismuth ligand bonding
[25]. The important IR and Raman bands of the free thiosemicarbazone
ligands and their bismuth(III) halide complexes are summarized in
Table 2 (Figs. S1-S10). In the IR spectra of complexes 1–4, the bands at
The enzyme activity was monitored by UV analysis. The 0.05 cm3 of
enzyme solution was added to a cuvette containing 2 cm3 linoleic acid
solution and the appropriate amounts of buffer and inhibitor solutions in
a thermostatic water bath at 25 ◦C. There was no pre-incubation period
for the enzyme with an inhibitor solution. The activity of the enzyme
was determined by monitoring the increase in the absorption caused by
the oxidation of linoleic acid at 234 nm and 25 ◦C [40]. Standard so-
lutions of the complexes in DMSO were used for the inhibition activity
experiments (three sets). In this case, the substrate concentration was
kept constant (0.3 mM), whereas the amounts of buffer and inhibitor
solutions were varied according to the inhibitor final concentration
needed. The total experiment volume was 3 cm3.
3440–3371 and 3298–3257 cmꢀ 1 are due to
ν(NH2) asymmetric and
symmetric stretching vibrations, respectively. The IR band due to ν(NH)
is observed in the 3244–3171 cmꢀ 1 region for complexes 1–4. These
stretching vibrations
(ν(NH2) and ν(NH)) suggest that the non-
involvement of the –NH2 group in the bonding with the bismuth atom
and there is no deprotonation of the NH group [42]. The thioamide
–
–
bands of the complexes, namely, ν(C S) and ν(C N), appear in the
–
ranges, 827–800 and 966–953 cmꢀ 1, respectively. The coordination of
the thione S-donor atom to the bismuth(III) ion was suggested by a shift
ꢀ 1
–
of the
ν
(C S) bands to lower stretching frequencies (ca. 16–25 cm
)
–
compared to the free thiosemicarbazone ligands [43]. In contrast, the
3. Results and discussion
–
ν(C N) stretching vibrations remained unchanged
bands due to the
upon bismuth coordination. No vibrational bands were observed in the
IR spectra of the complexes due to the thiol group (C-SH), in the region
3.1. Synthesis
ν
2600–2400 cmꢀ 1. This suggests that the thiosemicarbazone ligands
(Hacptsc and Hbztsc) coordinate with the bismuth(III) ion through the S-
donor atom in their thione form. The region from 500 to 100 cmꢀ 1 was
investigated for Bi-S and Bi-X (X: Cl, Br and I) vibration bands in the
Raman spectra of complexes 1–4 [44–47]. These characteristic bands
are given in Table 2. The Raman spectra of complexes 1–4 show Bi-S
vibration bands at 254–233 cmꢀ 1. In the region between 216 and 144
cmꢀ 1, Bi-X (X: Cl (1 and 4), Br (2) and I (3)) vibration bands are
observed in the Raman spectra of the complexes. These results show that
the thiosemicarbazone ligands are bound to the bismuth ion only via the
sulfur atom. The 1H and 13C NMR chemical shifts of the bismuth(III)
thiosemicarbazone complexes in DMSO‑d6 are given in the experimental
part (Figs. S11-S18). The presence of N(2)H signals suggested coordi-
nation of the thiosemicarbazone ligands to the bismuth(III) ion in the
thione form [48].
The reactions of BiCl3 and BiBr3 with acetophenone thio-
semicarbazone (Hacptsc) in a 1:3 M ratio yielded the yellow complexes
{mer-BiCl3
(
η
1-S-Hacptsc)3} (1) and {[mer-BiBr3
(
η
1-S-Hacptsc)3]⋅
CH3OH} (2). The reaction of BiI3 with the same ligand in a 1:1 M ratio
yielded the red complex {[BiI2(µ2-I](
η
1-S-Hacptsc)]2} (3), and the re-
action of BiCl3 with benzaldehyde thiosemicarbazone (Hbztsc) in a 1:2
M ratio yielded the yellow complex {[BiCl2(µ2-Cl)(
η
1-S-Hbztsc)2]2} (4)
(Scheme 1). The compounds were stable to air in the solid state, with
melting points in the range between 185 and 212 ◦C, and were produced
in reasonably good yields. These compounds are readily soluble in
common solvents. Their low molar conductivity values in dimethyl
sulfoxide at 25 ◦C (5.13 ± 0.82 Ωꢀ 1 cm2 molꢀ 1 (1), 17.95 ± 0.82 Ωꢀ 1
cm2 molꢀ 1 (2), 19.23 ± 0.65 Ωꢀ 1 cm2 molꢀ 1 (3) and 7.16 ± 1.18 Ωꢀ 1
cm2 molꢀ 1 (4)) show that they are non-electrolytic in nature [41]. These
To confirm the resistance of the Bi(III) thiosemicarbazone complexes
1–4 to degradation in dimethyl sulfoxide over time, the complexes were
analyzed by UV–vis spectroscopy. The Bi(III) thiosemicarbazone com-
plexes were dissolved in DMSO at room temperature and then their
respective UV–visible spectra were tested at different times (0–48 h).
Table 2
Selected mid-IR and Raman spectroscopic data (cmꢀ 1) for the bismuth(III) thi-
osemicarbazone complexes 1–4 and the free ligands.
IR (cmꢀ 1
)
Raman (cmꢀ 1
)
–
–
(C N)
–
Compounds
ν(NH2)
ν(NH)
ν
ν
(C S)
ν
(Bi-
ν(Bi-X)
S)
Hacptsc
3406,
3217
3371,
3257
3433,
3298
3425,
3292
3400,
3228
3440,
3290
3142
3171
3242
3244
3140
3226
962
966
964
962
945
953
843
827
823
822
818
800
–
–
1
239
236
233
–
202, 171,
154
2
186, 163,
146
3
180, 128,
114
Hbztsc
4
–
254
216, 174,
152
Scheme 1. The molecular formulae of the aromatic thiosemicarbazone ligands
used in this study and reaction scheme for the synthesis of complexes 1–4.
4

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
There was no obvious red or blue shift in the absorption peak of each
complex and no new absorption peaks appeared (Fig. S19). These results
show that the structures of Bi(III) thiosemicarbazone complexes do not
change in solution and do not degrade in solution over 48 h.
mass losses in different temperature ranges by thermogravimetric
studies.
3.4. Crystal and molecular structures of {BiCl3(
η
1-S-Hacptsc)3} (1),
{[BiBr3(
η
1-S-Hacptsc)3]⋅CH3OH} (2), {[BiI2(µ -I](
η
1-S-Hacptsc)]2} (3)
2
and {[BiCl2(µ2-Cl)(
η
1-S-Hbztsc)2]2} (4)
3.3. Thermal analysis
Aromatic thiosemicarbazone ligands usually bind to metal ion either
in the neutral thione form or in the anionic thiolate form. In the neutral
The thermal stability of the bismuth(III) thiosemicarbazone com-
plexes 1–4 was analyzed by TG-DTA analysis. The weight loss of com-
plexes was monitored while the temperature was increased at a rate of
10 ◦C minꢀ 1 from ambient up to 1000 ◦C, under a nitrogen atmosphere
(Figs. S20-S23). The thermal analysis of complex 1 includes four
decomposition steps (180–996 ◦C) with a total mass loss of 92.40%. The
first stage of decomposition (180–300 ◦C) involves a 43.07% mass loss
due to the evolution of two ligand molecules (calc. 43.18%). The second
decomposition stage (300–680 ◦C) involves a 20.33% mass loss due to
the evolution of one ligand molecule (calc. 21.59%). The third stage of
decomposition (680–885 ◦C) of 11.61% mass loss is due to the evolution
of three chlorine atoms (calc. 11.88%). Finally, the last stage of
decomposition (885–990 ◦C) of 17.39% mass loss corresponds to bis-
muth residues. The thermal analysis of complex 2 consists of four main
steps (75–992 ◦C), which sum up to a total mass loss of 92.27%. The first
stage (75–110 ◦C) involves a 3.03% mass loss, corresponding to evolu-
tion of one methanol molecule (calc. 3.02%). The second stage of
decomposition (110–380 ◦C) corresponds to a 55.50% mass loss for
three ligand molecules (calc. 54.67%). The third stage of decomposition
(380–700 ◦C) of 23.23% mass loss is due to the evolution of three
bromine atoms (calc. 22.60%). The last stage of decomposition
(700–992 ◦C) of 10.30% mass loss corresponds to bismuth residues. The
thermal analysis of complex 3 consists of two main steps (185–993 ◦C),
which sum up to a total mass loss of 94.98%. The first stage
(185–410 ◦C) involves a 74.15% mass loss, corresponding to evolution
of two ligand molecules and six iodine atoms (calc. 73.31%). The second
stage of decomposition (410–885 ◦C) of 20.84% mass loss corresponds
to bismuth residues. The thermal analysis of complex 4 includes three
decomposition steps (200–988 ◦C) with a total mass loss of 98.9%. The
first stage of decomposition (200–475 ◦C) involves a 52.99% mass loss
due to the evolution of four ligand molecules (calc. 53.20%). The second
decomposition stage (475–830 ◦C) involves a 15.99% mass loss due to
the evolution of six chlorine atoms (calc. 15.78%). The third stage of
decomposition (830–988 ◦C) of 29.92% mass loss corresponds to bis-
muth residues.
form, the binding occurs via only the S atom in the
η
1-S and µ2-S modes.
In the anionic thiolate form, the binding occurs via the thiolate sulfur
and azomethine nitrogen atoms as bidentate, forming five member
chelate rings (
η
2-N3,S chelation), or via thiolate sulfur, azomethine ni-
trogen and one ortho carbon atom of the phenyl ring as terdentate (
η
3-C,
N3,S chelation) (Scheme 2). The modes (
η
1-S and µ2-S) shown by the
neutral thione form are also exhibited by the anionic thiolate form [8].
Thiosemicarbazone ligands usually bind to the bismuth ion in the
anionic thiolate form [18–26].
The crystal data for complexes 1–4 are given in Table 1 and impor-
tant bond parameters are presented in Table 3. Complexes 1 and 4
crystallized in the triclinic crystal system with the space group P1, while
complexes 2 and 3 crystallized in the monoclinic crystal system with the
space group I2/a.
The molecular structure of complex 1 shows a mononuclear neutral
bismuth(III) chloride complex in the solid state (Fig. 1). The crystal
structure of 1 comprises two complexes in the asymmetric unit; both
exhibiting similar geometries. In both molecules, the thiosemicarbazone
–
ligands exhibit an E-configuration with respect to the C N bond and
–
they coordinate in a monodentate fashion via their sulfur atom in the
neutral thione form, but the CNNC(S)N backbone in the thio-
semicarbazone ligands in molecule B is more planar than the CNNC(S)N
backbone in the thiosemicarbazone ligands in molecule A (C8-N2-N3-
C7: ꢀ 178.8(5)◦, C17-N5-N6-C16: ꢀ 178.8(5)◦ and C26-N8-N9-C25:
158.4(5)◦ in molecule A; C35-N11-N12-C34: 176.4(5)◦, C44-N14-N15-
C43: ꢀ 168.5(5) and C53-N17-N18-C52: ꢀ 173.2(5)◦ in molecule B).
The bismuth(III) ion in both molecules is octahedrally coordinated by
three chlorine and three sulfur atoms, which are arranged in a meridi-
onal conformation. The geometry of the central atom in both molecules
is distorted octahedral, as reflected by the slight deviation of the cis
(88.75(4)-101.60(4)◦) and trans (169.64(4)-172.40(4)◦) angles from the
ideal values. The Bi-S bond distances vary from 2.818(1) to 2.928(1) Å
and the Bi-Cl bond distances vary from 2.580(1) to 2.846(1) Å. These
distances are in agreement with those found previously for similar
Thus, we determined the thermal stability of the complexes and their
Scheme 2. Possible coordination modes of neutral thione and anionic thiolate forms of aromatic thiosemicarbazones.
5

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
Table 3
Selected bond lengths (Å) and angles (◦) for the bismuth(III) thiosemicarbazone complexes 1–4.
1
2
3
4
(a) bond lengths
(a) bond lengths
(a) bond lengths
(a) bond lengths
Bi1-Cl1
2.846(1)
Bi1-S1
2.818(1)
Bi1-Br1
2.812(1)
Bi1-I1
2.890(2)
Bi1-Cl1
2.598(1)
Bi1-Cl2
Bi1-Cl3
Bi2-Cl4
Bi2-Cl5
Bi2-Cl6
S1-C8
2.650(2)
2.580(1)
2.602(1)
2.664(2)
2.838(1)
1.726(6)
1.711(6)
1.710(7)
Bi1-S2
Bi1-S3
Bi2-S4
Bi2-S5
Bi2-S6
S4-C35
S5-C44
S6-C53
2.868(2)
2.906(1)
2.928(1)
2.756(1)
2.860(2)
1.712(5)
1.732(6)
1.716(5)
Bi1-Br2
Bi1-Br3
Bi1-S1
Bi1-S2
Bi1-S3
S1-C9
2.949(8)
2.842(2)
2.810(1)
2.741(1)
2.830(1)
1.700(5)
1.732(5)
1.713(4)
Bi1-I2
Bi1-I3
Bi1-I3*
Bi1-S1
S1-C9
2.884(2)
3.128(2)
3.212(2)
2.703(6)
1.670(2)
Bi1-Cl2
Bi1-Cl3
Bi1-Cl3*
Bi1-S1
Bi1-S2
S1-C8
2.572(2)
2.809(2)
2.903(2)
2.752(2)
2.947(2)
1.753(7)
1.721(5)
S2-C17
S3-C26
S2-C27
S3-C18
S2-C16
(b) bond angles
(b) bond angles
(b) bond angles
(b) bond angles
Cl1-Bi1-Cl2
Cl1-Bi1-Cl3
Cl1-Bi1-S1
Cl1-Bi1-S2
Cl1-Bi1-S3
Cl2-Bi1-Cl3
Cl2-Bi1-S1
Cl2-Bi1-S2
Cl2-Bi1-S3
Cl3-Bi1-S1
Cl3-Bi1-S2
Cl3-Bi1-S3
S1-Bi1-S2
S1-Bi1-S3
S2-Bi1-S3
98.05(4)
170.17(4)
88.68(4)
95.32(4)
90.83(4)
91.76(4)
86.63(4)
165.74(4)
83.19(4)
91.18(5)
74.85(4)
91.06(4)
88.75(4)
169.64(4)
101.60(4)
Cl4-Bi2-Cl5
Cl4-Bi2-Cl6
Cl4-Bi2-S4
Cl4-Bi2-S5
Cl4-Bi2-S6
Cl5-Bi2-Cl6
Cl5-Bi2-S4
Cl5-Bi2-S5
Cl5-Bi2-S6
Cl6-Bi2-S4
Cl6-Bi2-S5
Cl6-Bi2-S6
S4-Bi2-S5
S4-Bi2-S6
S5-Bi2-S6
91.72(4)
172.40(4)
88.57(4)
89.96(4)
81.18(4)
95.67(4)
87.35(4)
84.17(4)
172.82(4)
90.03(4)
92.52(4)
91.46(4)
171.35(4)
93.47(4)
94.73(4)
Br1-Bi1-Br2
Br1-Bi1-Br3
Br1-Bi1-S1
Br1-Bi1-S2
Br1-Bi1-S3
Br2-Bi1-Br3
Br2-Bi1-S1
Br2-Bi1-S2
Br2-Bi1-S3
Br3-Bi1-S1
Br3-Bi1-S2
Br3-Bi1-S3
S1-Bi1-S2
94.03(3)
174.70(3)
82.53(3)
91.60(3)
85.18(3)
86.89(2)
88.92(3)
173.99(3)
106.14(3)
102.72(3)
87.71(3)
89.55(3)
89.70(4)
161.19(4)
76.44(3)
I1-Bi1-I2
I1-Bi1-I3
I1-Bi1-I3*
I1-Bi1-S1
I2-Bi1-I3
I2-Bi1-I3*
I2-Bi1-S1
I3-Bi1-I3*
I3-Bi1-S1
I3*-Bi1-S1
95.54(5)
92.02(5)
171.35(5)
87.7(1)
Cl1-Bi1-Cl2
Cl1-Bi1-Cl3
Cl1-Bi1-Cl3*
Cl1-Bi1-S1
Cl1-Bi1-S2
Cl2-Bi1-Cl3
Cl2-Bi1-Cl3*
Cl2-Bi1-S1
Cl2-Bi1-S2
Cl3-Bi1-Cl3*
Cl3-Bi1-S1
Cl3-Bi1-S2
Cl3*-Bi1-S1
Cl3*-Bi1-S2
S1-Bi1-S2
97.71(5)
170.11(5)
92.34(4)
89.66(5)
83.41(5)
89.91(5)
169.04(5)
88.63(5)
88.19(5)
79.64(4)
84.20(5)
103.21(5)
87.04(5)
97.35(4)
171.93(5)
172.38(6)
88.83(6)
91.8(1)
83.82(6)
87.5(1)
99.7(1)
S1-Bi1-S3
S2-Bi1-S3
*½-x, y, 1-z
*1-x, -y, 1-z
Fig. 1. Molecular structure of two independent molecules of {BiCl3(η1-S-Hacptsc)3} (1) with the atomic numbering scheme.
bismuth(III) thioamide complexes [37,45]. Between the independent
molecules, there are intermolecular weak hydrogen bonds (N13-
H13A… N7 and N7-N7B… N13), which link them together. In the crystal
distances are in agreement with those found previously for similar bis-
muth(III) thioamide complexes [46]. Different types of non-covalent
…
…
…
…
interactions (N
H
Br, N
… Br) are
–
O, O H
–
–
H
–
O, C H
–
Br, C H
…
…
…
structure of 1, intermolecular N
Cl, N
… S
responsible for the stability of the solid-state architecture of 2 (Fig. S25)
–
H
–
H
–
S, C H
–
Cl, C H
…
...
– –
and N H Br and C H Br intermolecular interactions play a dominant
interactions are effective for the stabilization of the 3D supramolecular
…
… Cl intermolec-
–
H
role in the stability of the solid state architecture of the molecule. The
intermolecular contacts are summarized in Table S2.
–
H
structure (Fig. S24). In complex 1, N
Cl and C
ular interactions play a dominant role in the formation of supramolec-
ular aggregation. The intermolecular contacts are summarized in
Table S2.
The asymmetric unit of complex 3 consist of one thiosemicarbazone
ligand, three iodine atoms and one bismuth(III) ion (Fig. 3a). The ge-
ometry around the bismuth center in each monomeric unit is see-saw,
with a τ4 value of 0.71 [49]. One sulfur atom from thiosemicarbazone
ligand with an E-configuration (the CNNC(S)N backbone is planar; C9-
N2-N1-C7: 178(2)◦) and one terminal iodine atom occupy equatorial
positions (Bi1-S1: 2.703(6) Å and Bi1-I1: 2.890(2) Å) and one terminal
and one bridging iodine atom are located in each of the axial positions
(Bi1-I2: 2.884(2) Å and Bi1-I3: 3.128(2) Å). Two strong intermolecular
interactions between the µ-I and Bi atoms (Bi1… I3: 3.212(2) Å) lead to a
The molecular structure of complex 2 consists of a mononuclear
neutral bismuth(III) bromide complex and one solvent molecule of
methanol in the solid state (Fig. 2). Three sulfur atoms from three thi-
osemicarbazone ligands and three bromide ions form an octahedral
environment with a meridional conformation. The thiosemicarbazone
ligands coordinate in a monodentate fashion in the neutral thione form.
In complex 2, the CNNC(S)N backbone in the two thiosemicarbazone
ligands is planar (C9-N2-N3-C7: ꢀ 178.1(4)◦ and C18-N8-N9-C16: 174.5
(4)◦), but the CNNC(S)N backbone in the third ligand is not planar (C27-
N5-N6-C25: 159.8(4)◦). The geometry of the central atom is distorted
octahedral as reflected from the slight deviation of the cis (76.44(3)-
106.14(3)◦) and trans (161.19(4)-174.70(3)◦) angles from the ideal
values. The Bi-S bond distances vary from 2.741(1) to 2.830(1) Å and
the Bi-Br bond distances vary from 2.812(1) to 2.949(8) Å. These
dimeric structure with a base-edge sharing bi-square pyramidal geom-
…
… I contacts
–
H
–
H
etry (Fig. 3b). The weak intermolecular N
I and C
stabilize the supramolecular self-assembly of complex 3 (Fig. S26). The
intermolecular contacts are summarized in Table S2.
The molecular structure of complex 4 is shown in Fig. 4. Compound 4
exists as a doubly bridged dimer, bearing a Bi2(µ-Cl)2 core, and it is
6

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
Fig. 2. Molecular structure of {[BiBr3(η1-S-Hacptsc)3]⋅CH3OH} (2) with the atomic numbering scheme.
formed as edge sharing bioctahedral, with both bismuth atoms exhib-
iting a distorted octahedral environment. Compound 4 consists of two
[Bi(LS)2Cl3] units with a square pyramidal geometry around each bis-
muth center (the calculated tau (τ5) value is 0.030) (Fig. 4a) [50]. Each
thiosemicarbazone ligand in compound 4 coordinates in a monodentate
fashion via the sulfur donor atom in the neutral thione form and the
CNNC(S)N backbone in the thiosemicarbazone ligands is planar (C8-N2-
N1-C7: ꢀ 174.8(6)◦ and C16-N5-N4-C15: ꢀ 178.8(6)◦). The equatorial
plane in the square pyramidal units is formed by two sulfur (Bi1-S1:
2.752(2) Å, Bi1-S2: 2.947(2) Å) and two chlorine (Bi1-Cl1: 2.598(1) Å,
Bi1-Cl3: 2.809(2) Å) atoms, with a trans-S, trans-Cl arrangement, and
one chlorine (Bi1-Cl2: 2.572(2) Å) atom is in the apical position. Two
strong intermolecular interactions between the µ-Cl and Bi atoms
(Bi1⋯Cl3: 2.903 Å) lead to dimerism, with a distorted octahedral ge-
ometry around the bismuth(III) ion (Fig. 4b). Two bismuth atoms and
two chlorine atoms build a Bi2Cl2 parallelogram. Edge-shared bio-
ctahedral complexes of bismuth(III) halide with sulfur containing li-
gands show four different arrangements (cis-sulfur/cis-halide, cis-sulfur/
trans-halide, trans-sulfur/cis-halide and bridging-sulfur) [45]. The config-
uration of the edge-shared bioctahedral compound 4 shows the trans-
sulfur/cis-halide arrangement. The cis bond angles around the bismuth
ion are between 79.64(4) and 103.21◦. The trans bond angles around the
bismuth ion are between 169.04(5) and 171.93(5)◦. These values indi-
cate that the geometry of the central atom deviates slightly from the
ideal geometry. The intermolecular hydrogen bonds and the van der
[19,25]
3.5. Hirshfeld surface analysis
Hirshfeld surface analysis is a powerful tool to gain additional in-
formation about the intermolecular interactions of molecular crystals.
The size and shape of the Hirshfeld surface allow qualitative and
quantitative investigations and visualization of intimate intermolecular
contacts. The three-dimensional Hirshfeld surfaces were generated as
depicted in Fig. 5. The 3D Hirshfeld surface were mapped based on dnorm
having the ranges ꢀ 0.3559 to 1.3447 Å (for 1), ꢀ 0.5219 to 1.3302 Å (for
2), ꢀ 0.2466 to 2.6637 Å (for 3) and ꢀ 0.3289 to 1.3813 Å (for 4), the
shape index range ꢀ 1.0 to 1.0 Å and the curvedness range ꢀ 4.0 to 4.0 Å.
For optimum resolution, standard (high) surface resolution criteria were
chosen and the surface transparency option was enabled. The red re-
gions on the dnorm surface indicate close-contact interactions, which are
mainly responsible for the significant hydrogen bonding contacts. For
the present four complexes, these red regions (bright and pale) are
indicative of short contacts of X… H/H… X (X: Cl, Br and I) interactions.
The bright red regions on the dnorm surfaces correspond to significant
–
N
H
… X (X: Cl, Br and I) interactions, while the pale red regions
correspond to significant C
… X (X: Cl, Br and I) interactions. These
–
H
X… H/H… X (X: Cl, Br and I) type interactions play a leading role in the
crystal packing of the bismuth(III) complexes 1–4.
The two-dimensional fingerprint plots of the H… H, X… H/H… X and
C… H/H… C interactions for compounds 1–4 are depicted in Fig. S28. In
the 2D fingerprint plots, grey represents the whole fingerprint, while the
blue area represents the proportion of each short-range effect. Fig. S29
shows the schematic of the relative percentage contributions to the
Hirshfeld surface area of the various intermolecular contacts in the
crystal structures of 1–4. The percentage of H… H contacts of 1–4, which
are reflected in the middle of the scattered points of the 2D fingerprint
plots, is 40.2 (A), 41.6 (B), 40.7, 21.8 and 32.5%, respectively. The
X… H/H… X (X = Cl, Br and I) interaction is one of the most significant
Waals contacts give rise to a three-dimensional construction of the
…
… Cl
–
H
–
H
structure and add to its stability. In complex 4, the N
Cl, C
and N
H
… S intermolecular interactions play a dominant role in the
–
formation of the supramolecular aggregation (Fig. S27). The intermo-
lecular contacts are summarized in Table S2.
–
–
The C S bond lengths in the complexes 1–4 vary from 1.670(2) to
1.753(7) Å. These bonds are slightly longer than those observed in the
free thiosemicarbazone ligands [51,52]. They are, however, in the range
of those measured in other bismuth(III) thiosemicarbazone compounds
7

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
Fig. 3. Molecular structure of {[BiI2(µ2-I](η1-S-Hacptsc)]2} (3) with the atomic numbering scheme ((A) monomeric and (B) dimeric formations; symmetry code: 1/2-
x,y,1-z).
contacts for compounds 1–4. For compounds 1–4, the H… X interactions
are represented by a spike in the upper left (donor) area of the finger-
print plot, whilst the X… H interactions are represented by a spike in the
lower right (acceptor) region of the fingerprint plot. The percentage of
X… H/H… X contacts of 1–4 is 19.0 (A), 18.5 (B), 16.0, 44.9 and 26.0%,
respectively. The H… H contacts represent the dominant interactions in
compounds 1, 2 and 4, while the dominant interactions in compound 3
fibroblast), after incubation for a period of 48 h. The IC50 values of 1–4
are higher than 30 М against the cancerous (MCF-7) and non-cancerous
μ
cell line (MRC-5) (Table 4), indicating that these compounds are not
active against the tested cells and they exhibit less activity than
cisplatin. The free ligands are also inactive. Bismuth(III) complexes of
acetophenone thiosemicarbazone and benzaldehyde thiosemicarbazone
are less active against cancer cells, in comparison to bismuth(III) com-
plexes of dithiocarbamate derivatives [53,54]. Therefore, the ligand
type, which is bound to the bismuth(III) ion, describes the activity of a
compound against cells.
are the I… H/H… I contacts. The other non-negligible weak C… H/H…
C
and S… H/H… S contacts were found to be 15.5 and 13.0% for 1A, 14.6
and 13.2% for 1B, 19.5 and 8.1% for 2, 11.6 and 6.5% for 3 and 13.7 and
12.3% for 4, respectively. Table S3 summarizes the various weak contact
contributions to the Hirshfeld surfaces that are observed for 1–4.
Fig. 5.
3.7. Antibacterial activity:
Inhibition zone (IZ): The antibacterial activity of compounds 1–4 and
their ligands were evaluated upon incubation with P. aeruginosa, E. coli,
S. epidermidis and S. aureus for 20 h, as summarized in Table 5 and
presented in Fig. 6.
3.6. Cytotoxic activity
The cell viability of compounds 1–4 and the free ligands (Hacptsc
and Hbztsc) was evaluated against human adenocarcinoma breast (MCF-
7) and the non-cancerous cell line MRC-5 (on normal human fetal lung
The compounds 1–4 are more active than their ligands against the
tested bacterial strains. Compounds 1–4 are more active towards Gram
8

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
strains lie between 9.0 and 11.5 mm. No inhibition zones were devel-
oped when the ligands were tested (Table 5, Fig. 6).
3.8. Study of the peroxidation of linoleic acid by the enzyme lipoxygenase
in the presence of compounds 1–4 and the free thiosemicarbazone ligands
A survey of the literature reveals that LOX inhibition induces
apoptosis [55], so the influence of the bismuth(III) compounds 1–4 and
the free thiosemicarbazone ligands on the oxidation of linoleic acid by
the enzyme LOX was studied over a wide concentration range. The de-
gree of LOX activity (A, %) in the presence of each compound was
Table 4
IC50 values for cell viability found for complexes 1–4 and other Bi(III) dithio-
carbamate complexes against MCF-7 (breast) and MRC-5 cells (normal human
fetal lung fibroblast cells).
Compounds
IC50 values (μМ)
Ref.
MCF-7
MRC-5
Hacptsc
>30
>30
>30
>30
>30
>30
>30
*
Hbztsc
>30
*
1
>30
*
2
>30
*
3
>30
*
4
>30
*
{[BiCl(Me2DTC)2]}n
{[BiBr(Me2DTC)2]}n
{[BiBr2(Et2DTC)]}n
{[BiI2(Me2DTC)]}n
Cisplatin
0.023 ± 0.003
0.08 ± 0.01
0.08 ± 0.006
0.1 ± 0.003
5.5 ± 0.4
–
[53]
[54]
[54]
[54]
[54]
0.25 ± 0.01
0.32 ± 0.02
0.29 ± 0.01
± 0.2
*In this work, Me2DTCH
diethyldithiocarbamate
=
dimethyldithiocarbamate, Et2DTCH
=
Table 5
IZs of 1–4 and their ligands against P. aeruginosa, E. coli, S. epidermidis and
S. aureus.
Fig. 4. (A) Molecular structure of {[BiCl2(µ2-Cl)(η1-S-Hbztsc)2]2} (4) with the
atomic numbering scheme ((A) monomeric and (B) dimeric formations; sym-
metry code: 1-x,-y,1-z).
P. aeuroginosa
E. coli
S. epidermidis
S. aureus
1
10.8 ± 0.9
11.0 ± 1.1
10.5 ± 0.6
10.0 ± 0.0
9.0 ± 0.0
9.7 ± 0.7
11.3 ± 0.7
12.0 ± 1.1
11.3 ± 0.7
12.5 ± 0.9
9.3 ± 0.7
9.5 ± 0.9
9.0 ± 0.0
9.6 ± 0.9
9.25 ± 0.5
9.2 ± 0.3
9.0 ± 0.0
9.2 ± 0.3
10.0 ± 1.4
9.8 ± 1.6
10.3 ± 1.3
11.5 ± 0.6
9.0 ± 0.0
9.0 ± 0.0
2
3
negative (P. aeuroginosa, E. coli) than Gram positive strains
(S. epidermidis, S. aureus). The IZs of 1–4 against Gram negative strains
lie between 10.0 and 12.5 mm while the IZs against Gram positive
4
Hacptsc
Hbztsc
Fig. 5. View of the Hirshfeld surfaces mapped with (a) dnorm (b) shape-index, (c) curvedness for complexes 1–4.
9

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
Fig. 6. IZ developed in P. aeruginosa, E. coli, S. epidermidis and S. aureus by 1–4 and their ligands at 1 mM.
calculated according to the method described previously [56,57]. The
IC50 values determined are 65.3 (1), 72.5 (2), 25.8 (3) and 24.5 µM (4),
whilst the values for the free ligands are 230.8 (Hacptsc) and 248.4 µM
(Hbztsc) (Fig. 7). According to this study, it is seen that the bismuth(III)
thiosemicarbazone compounds (1–4) have a much higher inhibitory
activity than the free thiosemicarbazone ligands (Hacptsc and Hbztsc)
and the bismuth(III) iodide compound of acetophenone thio-
semicarbazone (3) has a higher inhibitory activity than the bismuth(III)
chloride and bismuth(III) bromide compounds of acetophenone thio-
semicarbazone (1 and 2). Also, it is observed that the dimeric bismuth
(III) thiosemicarbazone compounds (3 and 4) show higher inhibition
activity than the monomeric bismuth(III) thiosemicarbazone com-
pounds (1 and 2) and cisplatin (IC50: 65.9 µM) [58].
this study, bismuth(III) halide complexes of aromatic thio-
semicarbazones have been synthesized for the first time. The chemical
structures of these four new complexes, with the molecular formulae
{BiCl3(
η
1-S-Hacptsc)3} (1), {[BiBr3(
η
1-S-Hacptsc)3]⋅CH3OH} (2),
{[BiI2(µ2-I](
η
1-S-Hacptsc)]2} (3) and {[BiCl2(µ2-Cl)(
η
1-S-Hbztsc)2]2}
(4), were characterized by various spectroscopic methods and the
crystal structures of 1–4 were determined by single crystal X-ray
diffraction. In all the complexes (1–4), the thiosemicarbazone ligands
–
–
exhibit the E-configuration with respect to the C N bond and coordi-
nate in a monodentate fashion through the sulfur atoms in the neutral
thione form. Complexes 1 and 2 are mononuclear octahedral com-
pounds with a meridional conformation. Complexes 3 and 4 exist as
double-bridged dimers. Complex 3 has a base-edge sharing bi-square
pyramidal structure and complex 4 has an edge sharing bioctahedral
structure. The H… H and X… H/H… X interactions of complexes 1–4 play
an important role in the formation of supramolecular aggregation.
Complexes 1–4 appeared to show low cytotoxicity and toxicity against
MCF-7 and MRC-5 cells, respectively, although these complexes have
4. Conclusion
To date, there have been many studies on transition metal and non-
transition metal complexes of thiosemicarbazones in the literature. In
Fig. 7. The inhibitory effect against LOX caused by ( ) {BiCl3(η1-S-Hacptsc)3} (1), ( ) {[BiBr3(η1-S-Hacptsc)3]⋅CH3OH} (2), ( ) {[BiI2(µ2-I](η1-S-Hacptsc)]2} (3),
(
)
{[BiCl2(µ2-Cl)(η1-S-Hbztsc)2]2} (4), (■) acetophenone thiosemicarbazone (Hacptsc) and
( ) benzaldehyde thiosemicarbazone (Hbztsc) in various
concentrations.
10

I.I. Ozturk et al.
Polyhedron 208 (2021) 115388
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