Synthesis, characterization and biological applications of bismuth(III) complexes with aroylthiourea ligands

Article abstract of DOI:10.1016/j.ica.2020.119871

This work describes the synthesis, structural characterization and biological applications of three new bismuth(III) complexes with aroylthiourea-based ligands: [Bi(L^a)₃(HL^a)] (1), [Bi₂(L^b)₄(μ-L^b)₂]?2(C₃H₆O) (2), and [Bi₆(μ-L^c)₆(μ₃-NO₃)₂(μ₆-NO₃)](NO₃)₃?4H₂O (3), where HL^a = N-benzoyl(N′,N′-diethylthiourea), HL^b = N-benzoyl(morpholinylthiourea), and H₂L^c = N²,N⁶-bis(diethylcarbamothioyl)pyridine-2,6-dicarboxamide. The ligands HL^a and HL^b were considered as monopodal, while H₂L^c as bipodal. All compounds were characterized by melting point determination, Fourier-transform infrared spectroscopy (FTIR), proton proton and carbon-13 nuclear magnetic resonance spectroscopy (NMR), mass spectrometry (MS), elemental analysis (EA) and single-crystal X-ray diffraction (SC-XRD). Structural analysis showed that compound 1 was a mononuclear heptacoordinate complex, while compound 2 presented a dinuclear structure and compound 3 was built up by a hexanuclear framework. The proligands, the new complexes, and Bi(NO₃)₃?5H₂O had their antibacterial activities evaluated against E. coli (ATCC 25922), S. aureus (ATCC 25923), and P. aeruginosa (ATCC 27853). The in vitro disk-diffusion (DD) method showed the ability of compound 2 to inhibit two types of bacteria (P. aeruginosa and S. aureus). In the results of minimum inhibitory concentration (MIC), all complexes showed significant activity against the tested microorganisms except for compound 1. The inorganic salt used for comparison showed antibacterial activity only against P. aeruginosa and the ligands showed no apparent activity. Compound 2 presented the best antibacterial activity among the tested substances, and its performance was remarkable even when compared to other similar compounds found in the literature, attesting the importance of targeting bismuth(III) aroylthioureas for further research on new drugs development.

Full text of DOI:10.1016/j.ica.2020.119871

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Synthesis, characterization and biological applications of bismuth(III) com‐
plexes with aroylthiourea ligands
Marcielli Indiara de Oliveira, Gabriela Pereira Chuy, Bruno Stefanello
Vizzotto, Robert Alan Burrow, Ernesto Schulz Lang, Sailer Santos dos Santos
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Please cite this article as: M.I. de Oliveira, G.P. Chuy, B.S. Vizzotto, R.A. Burrow, E.S. Lang, S.S. dos Santos,
Synthesis, characterization and biological applications of bismuth(III) complexes with aroylthiourea ligands,
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Synthesis, characterization and biological applications of bismuth(III)
complexes with aroylthiourea ligands
Marcielli Indiara de Oliveiraa, Gabriela Pereira Chuyb, Bruno Stefanello Vizzottob, Robert
Alan Burrowa, Ernesto Schulz Langa and Sailer Santos dos Santosa*
a Laboratório de Materiais Inorgânicos - Departamento de Química, CCNE, UFSM, Santa
Maria – RS – Brazil – 97105-900.
b Laboratório de Biologia Molecular, Universidade Franciscana - UFN, 1614 Andradas Street,
Santa Maria – RS – Brazil – 97010-032.
* Corresponding author:
E-mail: sailer.santos@ufsm.br or sailer.santos@gmail.com
Fax number: +55 55 3220 8031
Marcielli Indiara de Oliveira
Gabriela Pereira Chuy
Bruno Stefanello Vizzotto
Robert Alan Burrow
0000-0003-0696-4452
0000-0001-6760-4851
0000-0001-6819-4081
0000-0003-4909-5007
0000-0002-6852-8667
0000-0002-7086-8871
Ernesto Schulz Lang
Sailer Santos dos Santos
1

Abstract
This work describes the synthesis, structural characterization and biological applications of
three new bismuth(III) complexes with aroylthiourea-based ligands: [Bi(La)3(HLa)] (1),
[Bi2(Lb)4(-Lb)2]2(C3H6O) (2), and [Bi6(-Lc)6(3-NO3)2(6-NO3)](NO3)34H2O (3), where
HLa = N-benzoyl(N’,N’-diethylthiourea), HLb = N-benzoyl(morpholinylthiourea), and H2Lc =
N2,N6-bis(diethylcarbamothioyl)pyridine-2,6-dicarboxamide. The ligands HLa and HLb were
considered as monopodal, while H2Lc as bipodal. All compounds were characterized by melting
point determination, Fourier-transform infrared spectroscopy (FTIR), hydrogen and carbon-13
nuclear magnetic resonance spectroscopy (NMR), mass spectrometry (MS), elemental analysis
(EA) and single-crystal X-ray diffraction (SC-XRD). Structural analysis showed that com-
pound 1 was a mononuclear heptacoordinate complex, while compound 2 presented a dinuclear
structure and compound 3 was built up by a hexanuclear framework. The proligands, the new
complexes, and Bi(NO3)35H2O had their antibacterial activities evaluated against E. coli
(ATCC 25922), S. aureus (ATCC 25923), and P. aeruginosa (ATCC 27853). The in vitro disk-
diffusion (DD) method showed the ability of compound 2 to inhibit two types of bacteria (P.
aeruginosa and S. aureus). In the results of minimum inhibitory concentration (MIC), all com-
plexes showed significant activity against the tested microorganisms except for compound 1.
The inorganic salt used for comparison showed antibacterial activity only against P. aeruginosa
and the ligands showed no apparent activity. Therefore, compound 2 presented the best anti-
bacterial activity among the tested substances, and its performance was remarkable even when
compared to other similar compounds found in the literature, attesting the importance of target-
ing bismuth(III) aroylthioureas for further research on new drugs development.
Keywords: aroylthioureas; bismuth(III) complexes; crystal structure; antibacterial activity.
1. Introduction
Thiourea-based molecules and their metal complexes have several pharmacological applica-
tions, especially on antimicrobial activity against pathogenic bacteria and fungi [1]. Amongst
the most interesting thiourea-based ligands, aroylthioureas and their anions exhibit a rich and
2

very well documented coordination chemistry [2,3]. Aroylthiourea compounds of general for-
mula Ar(C=O)NH(C=S)NR2 (Ar = aryl; R = alkyl, aryl) (Figure 1a), constitute an important
class of versatile bidentate ligands, which have hard (O), soft (S) and intermediary donor atoms
(N). This structural characteristic allows these ligands to present different coordination modes,
producing complexes with several distinct metals. In addition to the monopodal structure (HL')
represented in Figure 1(a), aroylthiourea ligands can also be bipodal, (H2L''), where they differ
by the presence of two branches in relation to the central aromatic ring used as a spacer, as
shown schematically in Figure 1(b) [4]. The removal of the acidic amidic hydrogens enhances
the coordination capacity of these ligands, affording since mononuclear [5,6] to metallamacro-
cyclic [7-10] and heterobimetallic complexes [11-13].
INSERT Figure 1 ABOUT HERE
Bismuth compounds are commonly used in medicine, and some have clinical applications such
as treatment of syphilis (sodium/potassium bismuth tartrate, bismuth chloride, etc.), wound in-
fections (bismuth oxide), diarrhea (bismuth subsalicylate, nitrate bismuth, etc.), and ulcer (bis-
muth citrate, bismuth subnitrate, etc.) [14]. In the antimicrobial activity, its main use is in the
treatment of gastric disorders related to the bacterium Helicobacter pylori (H. pylori) [15], a
gram-negative bacterium found in the stomach where it causes damage to epithelial cells caus-
ing gastritis and ulcers [16]. Although bismuth is considered a heavy metal, its drugs are safe
if used according to the recommended dosages. Side effects from overdosing are reversible
when intake is interrupted [17,18].
Recently, the broad-spectrum antimicrobial applications of bismuth-based compounds have
been reviewed, including carboxylates, thiolates, phosphinic acid derivatives, and dithiocarba-
mate complexes [19-23]. Surprisingly, there have been no reports in the literature about bismuth
complexes with aroylthiourea based proligands. Due to the extensive chemistry of aroylthiourea
compounds with different types of metals with a wide variety of biological applications, and
also to the well-spread uses of bismuth in commercially available drugs, we decided to inves-
tigate potential applications of bismuth(III) benzoylthioureas as antimicrobial agents. In this
work, we describe the synthesis, structural characterization, and biological applications of three
new bismuth(III) compounds with aroylthioureas as ligands: [Bi(La)3(HLa)] 1, [Bi2(Lb)4(-
3

Lb)2]2(C3H6O) 2, and [Bi6(-Lc)6(3-NO3)2(6-NO3)](NO3)34H2O 3, where HLa = N-ben-
zoyl(N’,N’-diethylthiourea), HLb = N-benzoyl(morpholinylthiourea), and H2Lc = N2,N6-bis(di-
ethylcarbamothioyl)pyridine-2,6-dicarboxamide (Figure 2).
INSERT Figure 2 ABOUT HERE
2. Experimental
2.1 Materials and general instrumentation
Commercially available solvents and reagents (Sigma-Aldrich) were purified by standard meth-
ods prior to use [24]. The bismuth source, Bi(NO3)35H2O, was used as received. N,N-diethyl-
thiourea was obtained from acidic hydrolysis of in situ prepared N-benzoyl(N’,N’-diethylthio-
urea) [25]. Synthetic manipulations involving air-sensitive compounds were carried out using
a standard argon atmosphere. CHNS elemental analyses were performed at a Heraeus Vario EL
microanalysis instrument. Melting points (m.p.) were recorded using a MicroQuímica,
MQAPEF-301 digital melting point apparatus and were not corrected. Fourier-transform infra-
red (FTIR) spectra, in attenuated total reflectance (ATR) sampling mode, were recorded on a
Bruker Vertex 70 spectrometer with a Bruker Platinum ATR accessory, equipped with a dia-
mond crystal window. A total of 32 scans were performed at 4 cm−1 resolution in the 4000-
400 cm–1 spectral range and then converted to transmission mode. 1H and 13C nuclear magnetic
resonance (NMR) spectra were recorded on a Bruker DPX-400 or on a Bruker Avance III HD-
600 spectrometers. CDCl3, DMSO-d6, and acetone-d6 were used as solvents and TMS as the
internal reference. Chemical shifts are reported in parts per million (δ, ppm) and were refer-
enced to the residual solvent peak. Multiplicities are expressed as: s (singlet), t (triplet), q (quar-
tet), m (multiplet), and br (broad). The electrospray-ionization Fourier-transform ion-cyclotron-
resonance (ESI-FTICR) mass spectrometric (MS) experiments were performed with a Varian
IonSpec QFT-7 FTICR mass spectrometer in positive mode. All MS results are given in the
form: m/z, assignment (M stands for the corresponding molecular ion peak).
2.2 Single-crystal X-ray diffractometry (SC-XRD)
Data were collected on a Bruker D8 Venture diffractometer equipped with an Incoatec IµS high
brilliance Mo-Kα X-ray tube with two-dimensional Montel micro-focusing optics and a Photon
100 detector. The structures were solved by dual space methods with Bruker SHELXTL XT
[26]. Fourier-difference map analyses yielded the positions of the non-hydrogen atoms, and
4

refinements were carried out with the Bruker SHELXTL XL package [27]. All refinements
were made by full-matrix least-squares on F2 with anisotropic displacement parameters for all
non–hydrogen atoms. Hydrogen atoms were included in the refinement in calculated positions
according to the molecular skeletons. Drawings were done using Crystal Impact Diamond 3
[28]. Crystal data and more details of the data collection and refinements of the bismuth(III)
complexes 1, 2, and 3 are presented in Table S1 of Supplementary Information file.
2.3 Disk Diffusion Assay (DD)
The antimicrobial susceptibility was performed by the agar disk diffusion method in cation
adjusted Mueller-Hinton agar (CAMH) as recommended by the Clinical and Laboratory Stand-
ards Institute (CLSI) [29], with the microorganisms Escherichia coli (ATCC 25922), Staphy-
lococcus aureus (ATCC 25923) and Pseudomonas aeruginosa (ATCC 27853). Isolated pure
colonies were transferred into a sterile saline solution to form homogenous bacterial suspen-
sions, in a standard turbidity inoculum equivalent to 0.5 McFarland (1108 CFU mL–1), then
poured over the agar plates and allowed to dry for 5 min. Sterile filter paper disks (Whatman
No. 1, diameterꢀ=ꢀ6 mm) were placed over the agar surface and impregnated with 10 L of a
solution of each compound (freshly dissolved in deionized water at 0.01 M), and incubated for
24 h at 37 °C. Cefotaxime (30 μg) and Ceftazidime (30 μg) disks were used as positive controls.
The inhibition zones were measured in millimeters as the diameter of the growth-free zones.
All tests were performed in triplicate.
2.4 Minimal Inhibitory Concentration (MIC)
The broth microdilution method was used to determine the MIC according to CLSI [29], as
described previously. All analyses were performed in triplicate. Twofold serial dilutions of
compounds were prepared directly in a microtiter plate containing Mueller Hinton broth to ob-
tain concentrations ranging from 10 mM to 0.019 mM. Bacterial inoculum was added at a final
concentration of 5×104 CFU mL–1 per well. Plates were then covered and incubated for 24 h at
37 °C. The MIC of the samples was detected using spectrophotometric reading at 595 nm after
the addition of 20 µL triphenyl-tetrazolium chloride (TTC) solution (0.02 g mL–1) incubated at
37 ºC for 2 h. The growth of bacteria changes the dye from colorless to red, indicating positive
5

growth, whereas the colorless indicates growth inhibition. MIC was defined as the lowest sam-
ple concentration which prevented this change and exhibited inhibition of microorganism
growth.
2.5 Synthetic procedures
2.5.1 Synthesis of the ligands
The syntheses of the monopodal ligands N-benzoyl(N’,N’-diethylthiourea) (HLa) and N-ben-
zoyl(morpholinylthiourea) (HLb) were adapted from Douglass and Dains [30]. The preparation
of the bipodal ligand N2,N6-bis(diethylcarbamothioyl)pyridine-2,6-dicarboxamide (H2Lc) was
adapted from reported procedures [31-33].
2.5.1.1 Synthesis of HLa and HLb
In a 250 mL three-neck round-bottom flask, equipped with a magnetic stirring system and re-
flux condenser, ammonium thiocyanate (7.61 g, 100 mmol) was suspended in 100 mL of dry
acetone. Then, 12.0 mL of benzoyl chloride (14.8 g, 105 mmol) was slowly added dropwise.
During the addition, the mixture changed from colorless to yellow. After completion of the
addition, the system was heated to reflux for 2 h. The reaction mixture was cooled with an ice
bath, and 120 mmol of the corresponding amine (see below) was added dropwise. After the end
of the addition, the system was kept at room temperature with magnetic stirring for 2 h. After-
wards, 200 mL of a 6 mol L–1 HCl solution was added to the reaction mixture and extraction
was performed with ethyl acetate (3  100 mL). The solvent was removed by a rotatory evap-
orator, and the product was purified by recrystallization from a mixture of ethyl ether and meth-
anol (4:1). The crystalline product was dried under high vacuum for 4 h.
HLa: 12.0 mL of diethylamine (8.78 g). Yield: 61.5% (14.5 g; 61.5 mmol); C12H16N2OS
(F.W.= 236.33 g mol–1); Elem. Anal.: Calcd: C = 60.99%; H = 6.82%; N = 11.85%;
S = 13.57%; Found: C = 60.37%; H = 6.72%; N = 12.11%; S = 13.24%; m.p.: 102 °C; FTIR
(ATR, cm–1): (N-H) 3264; (C=O) 1651; 1H NMR (DMSO-D6; δ/ppm; J/Hz): 10.33 (br, 1H,
NH); 7.93 (d, 2H, CH, J = 7.14); 7.59 (t, 1H, CH, J = 7.35); 7.50 (t, 2H, CH, J = 7.72); 3.95 (q,
2H, CH2, J = 6.94); 3.52 (q, 2H, CH2, J = 7.04); 1.25 (t, 3H, CH3, J = 7.00); 1.18 (t, 3H, CH3,
6

J = 7.10); 13C NMR (DMSO-D6; δ/ppm): 180.98 (C=S), 164.52 (C=O), 133.45 (CH); 132.73
(CH); 128.92 (CH); 128.55 (CH); 48.99 (CH2); 47.71 (CH2); 13.81 (CH3); 11.58 (CH3).
HLb: 11.0 mL of morpholine (10.8 g). Yield: 67.5% (16.9 g; 67.5 mmol); C12H14N2O2S (F.W.=
250.32 g mol–1); Elem. Anal.: Calcd: C = 57.58%; H = 5.64%; N = 11.19%; S = 12.81%;
Found: C = 57.43%; H = 5.63%; N = 10.99%; S = 12.73%; m.p.: 149 ºC; FTIR (ATR, cm–1):
(N-H) 3236; (C=O) 1662; 1H NMR (acetone-D6; δ/ppm; J/Hz): 9.68 (br, 1H, NH); 8.00 (d,
2H, CH, J = 7.21); 7.62 (t, 1H, CH, J = 7.43); 7.52 (t, 2H, CH, J = 7.80); 4.21 (br, 2H, CH2);
3.76 (br, 4H, CH2); 3.69 (br, 2H, CH2); 13C NMR (DMSO-D6; δ/ppm): 180.85 (C=S); 164.55
(C=O); 133.91 (CH); 133.42 (CH); 129.39 (CH); 129.07 (CH); 66.75 (CH2); 52.55 (CH2); 51.91
(CH2).
2.5.1.2 Synthesis of H2Lc
In a 250 mL three-neck round-bottom flask, equipped with a magnetic stirring system and re-
flux condenser, 9.30 mL of triethylamine (6.75 g; 66.7 mmol) were added dropwise into a so-
lution of N,N-diethylthiourea (5.00 g; 37.8 mmol) in 100 mL of dry acetone. A suspension of
pyridine-2,6-dicarbonyl dichloride (3.86 g; 18.9 mmol) in 50.0 mL of anhydrous acetone was
slowly added dropwise. After completion of the addition, the system was stirred for 1 h at room
temperature (r.t.). Then, the system was kept between 50 – 60 ºC with an oil bath for 2 h. After
cooling down to r.t., the reaction mixture was filtered, and the filtrate was concentrated to dry-
ness. The brown oily product was washed several times with an ethyl ether/methanol 10:1 so-
lution, and the resulting white solid was collected by filtration and dried under high vacuum for
4 h.
H2Lc: Yield: 68.0% (5.09 g; 12.9 mmol); C17H25N5O2S2 (F.W.= 395.54 g·mol–1); Elem. Anal.:
Calcd: C = 51.62%; H = 6.37%; N = 17.71%; S = 16.21%; Found: C = 51.64%; H = 6.36%;
N = 17.63%; S = 16.07%; m.p.: 179 ºC; FTIR (ATR, cm–1): (N-H) 3265; (C=O) 1672; 1H
NMR (DMSO-D6; δ/ppm; J/Hz): 11.29 (s, 2H, NH); 8.33 (m, 2H, m-Py); 8.28 (m, 1H, p-Py,
J = 8.65); 4.00 (q, 4H, CH2, J = 7.03); 3.59 (q, 4H, CH2, J = 7.11); 1.29 (t, 6H, CH3, J = 7.05);
1.20 (t, 6H, CH3, J = 7.14); 13C NMR (DMSO-D6; δ/ppm): 180.28 (C=S); 160.61 (C=O);
148.34 (CH); 140.62 (CH); 126.44 (CH); 47.89 (CH2); 47.25 (CH2); 14.09 (CH3); 11.56 (CH3).
7

2.5.2 Synthesis of the bismuth(III) complexes
Bismuth(III) complexes with the selected ligands were obtained using a similar protocol. A
general optimized procedure is described below.
The ligand was dissolved in 4.0 mL of solvent under magnetic stirring. After complete disso-
lution, three drops of NEt3 were added.* A solution of Bi(NO3)3·H2O (0.048 g, 0.10 mmol) in
2.0 mL of solvent was added dropwise to the first solution causing the formation of a yellow
solution to be observed. The reaction mixture was kept under magnetic stirring for 1 h in open
atmosphere. The solution was filtered, and crystals suitable for SC-XRD measurements were
obtained after slow evaporation of the mother liquor.
* Ligand H2Lc required gentle heating for dissolution, and no NEt3 was added.
[Bi(La)3(HLa)] (1) - Ligand: HLa (0.070 g, 0.30 mmol); Solvent: EtOH; Yield: 86% (0.073 g;
64 mmol); C48H62BiN8O4S4 (F.W.= 1151.29 g·mol–1); Elem. Anal. Calcd: C = 50.08%;
H = 5.34%; N = 9.73%; S = 11.14%; Found: C = 50.25%; H = 5.34%; N = 9.77%; S = 11.16%;
m.p.: 110 ºC; FTIR (ATR, cm–1): (C=O) = 1682; (C=O) = 1494; (C=S) = 1222; ESI+-MS:
1151.2613 [M+H]+ (Calcd: 1151.3575); 1150.2808 [M]+ (Calcd: 1150.3502); 679.1599
a
+
1
[Bi(L )2] (Calcd: 679.1609); H NMR (CDCl3; δ/ppm; J/Hz): 8.66 (br, 1H, NH); 7.83 (d,
8H,CH, J = 7.54); 7.54 (t, 4H, CH, J = 7.41); 7.43 (t, 8H, CH, J = 7.65); 3.13 (q, 16H, CH2,
J = 7.33); 1.29 (t, 24H, CH3, J = 7.34); 13C NMR (CDCl3; δ/ppm): 179.49 (C=S), 163.49
(C=O), 133.08 (CH); 132.47 (CH); 128.92 (CH); 127.93 (CH); 65.85 (CH2); 52.11 (CH2); 46.59
(CH2); 8.69 (CH3).
[Bi2(µ-Lb)2(Lb)4]·2(CO)Me2 (2) - Ligand: HLb (0.075 g, 0.30 mmol); Solvent: (CO)Me2;
Yield: 90% (0.091 g; 0.05 mmol); C78H90Bi2N12O14S6 (F.W.= 2029.93 g·mol–1); Elem. Anal.:
Calcd: C = 46.15%; H = 4.47%; N = 8.28%; S = 9.48%; Found: C = 45.41%; H = 4.28%; N=
8.73%; S = 9.51%; m.p.: 160 ºC; FTIR (ATR, cm–1): (C=O)acetone = 1702; (C=O) = 1484;
(C=S) = 1222; ESI+-MS: 1663.2958 [M–(Lb)]+ (Calcd: 1663.3096); 707.1156 [Bi(Lb)2]+
1
(Calcd: 707.1199); H NMR (acetone-D6; δ/ppm; J/Hz): 8.01 (d, 6H, CH, J = 7.53); 7.63 (t,
3H, CH, J = 7.45); 7.53 (t, 6H, CH, J = 7.74); 2.83 (br, 24H, CH2); 13C NMR (acetone-D6;
δ/ppm): 179.11 (C=S); 163.21 (C=O); 133.36 (CH); 130.62 (CH); 129.36 (CH); 129.04 (CH);
66.94 (CH2); 66.70 (CH2).
8

[Bi6(µ-Lc)6(µ3-NO3)2(µ6-NO3)](NO3)34H2O (3) - Ligand: H2Lc (0.039 g, 0.10 mmol);
Solvent: MeOH; Yield: 52% (0.035 g; 0.0086 mmol); C102H146Bi6N36O34S12 (F.W.=
4059.13 g/mol); Elem. Anal. Calcd: C = 30.18%; H = 3.63%; N = 12.42%; S = 9.48%; Found:
C = 29.10%; H = 3.35%; N = 12.50%; S = 8.88%; m.p.: 228 ºC; FTIR (ATR, cm–1): (O-H)
3430,05; (C=O) 1642; (C-O) 1520; (N-O) 1331, 1346; ESI+-MS: 2594.3883
[Bi4(Ld)4(NO3)3]+ (Calcd: 2594.4018); 1930.2931 [Bi3(Ld)3(NO3)2]+ (Calcd: 1930.3042);
d
+
d
+
1
1266.2003 [Bi2(L )2(NO3)] (Calcd: 1266.2067); 602.1066 [Bi(L )] (Calcd: 602.1092; H
NMR (DMSO-D6; δ/ppm; J/Hz): 7.95 (d, 12H, m-Py, J = 7.06); 7.60 (t, 6H, p-Py, J = 7.14);
13
3.12 (q, 24H, CH2, J = 7.28); 1.20 (t, 36H, CH3, J = 7.29); C NMR (DMSO-D6; δ/ppm):
179.91 (C=S); 163.90 (C=O); 132.56 (CH); 132.21 (CH); 128.14 (CH); 65.47 (CH2); 50.47
(CH2); 45.93 (CH2); 8.50 (CH3); 8.43 (CH3).
3. Results and discussions
3.1. Molecular and crystal structures
Compounds 1-3 were obtained as crystalline materials and had their crystal and molecular struc-
tures determined.
3.1.1. Compound 1
Compound 1, [Bi(La)3(HLa)], crystallized in the monoclinic system, with space group C2/c,
forming a heptacoordinate BiIII complex. It was possible to observe that the ligand acquired two
different coordination modes in the structure: anionic bidentate coordination mode, where three
La-2S,O chelating ligands were coordinated to the metal, and one monodentate coordination,
where only the sulfur atom of a neutral HLa-S was coordinated to the BiIII ion (Figure 3(a)).
This asymmetry in the behavior of the ligands occurred due to a change in the configuration of
one of the ligands, which underwent a rotation around the sp3 nitrogen atom of the amide resi-
due, changing the torsion angle of the system -(CO)NH(CS)-. This change in conformation
caused the atoms of oxygen and sulfur to be very distant, preventing the formation of the fourth
chelate. In complex 1, the geometry around bismuth was a highly distorted pentagonal bipyra-
9

mid (PBPY-7), where three oxygen and two sulfur atoms were occupying the equatorial posi-
tions (O1, O2, O3, S1, S3) while the axial positions were occupied by two sulfur atoms (S2,
S4) (Figure 3(b)).
INSERT Figure 3 ABOUT HERE
The bismuth(III) ion has an ionic radius large enough to form complexes with greater numbers
of coordination, as already reported in some examples in the literature, e.g. 7 [34], 8 [35] and 9
[36]. The three La-2S,O chelating ligands presented Bi-O bond lengths range between
2.3704(03) - 2.4072(03) Å, and Bi-S bond lengths between 2.6192(12) - 2.8462(11) Å, while
the seventh coordination consisted of a bond of a sulfur atom from an adjacent neutral ligand
(3.2147(11) Å), much longer than the Bi-S bonds observed for the chelating ligands. The high
degree of distortion of the pentagonal bipyramidal geometry can be related to the stereochemi-
cal activity of the BiIII lone pair that led to an hemidirected coordination environment [37- 41].
This hemidirected coordination was also evidenced by the relatively high values found for the
O2-Bi1-S4 and S1-Bi1-S3 angles (118.792(2) – 137.643(1)°), which made the O2-S3-S4-S1
quadrilateral system almost planar (torsion angle -12.360(1)°). Selected bond lengths and an-
gles are shown in Table 1.
INSERT Table 1 ABOUT HERE
3.1.2. Compound 2
Compound 2, [Bi2(µ-Lb)2(Lb)4]·2(CO)Me2, crystallized in the triclinic system with space
III
̅
group P1 as a dinuclear Bi complex that had six anionic ligands derived from N-benzoyl-
morpholinylthiourea, and two acetone molecules as solvates in its molecular structure. Four Lb
moieties behaved as S,O chelating ligands while the two remaining acted as -Lb-
(12O,S,2S) and -Lb-(1S,22O,S) ligands, respectively (Figure 4 (a)).
The two BiIII ions presented equivalent coordination spheres. The bismuth coordination number
was also seven in a strongly distorted pentagonal bipyramidal geometry, where three oxygen
and two sulfur atoms (O11, O21, O31, S11, and S33) were occupying the equatorial positions
while the axial positions were occupied by two sulfur atoms (S22, S33') (Figure 4(b)).
INSERT Figure 4 ABOUT HERE
10

As well as for 1, the hemidirected pentagonal bipyramidal coordination in 2 was due to the
effect of the stereochemically active BiIII electron lone pair, and the distortion, in this case, was
also enhanced due to the sterical hindrance imposed by the bridging ligands. The O21-Bi1-S33'
and S11-Bi1-S33 bond angles were very large for a PBPY-7 coordination (137.750(5) and
146.157(3)°, respectively), which made the system O21-S33-S33'-S11 almost planar (torsion
angle –9.520(6)°). Selected bond distances and angles are shown in Table 2, where Bi-O bond
lengths range between 2.3140(14) and 2.4998(17) Å and the chelate Bi-S bond lengths between
2.6616(07) and 2.6955(07) Å, while the sixth and seventh coordination positions were consti-
tuted by μ-S bonds of bridging ligands with bond lengths between 3.0946(07) - 3.1542(07) Å.
INSERT Table 2 ABOUT HERE
3.1.3. Compound 3
Compound 3, [Bi6(µ-Lc)6(µ3-NO3)2(µ6-NO3)](NO3)34H2O, crystallized in the monoclinic sys-
tem, with space group P21/n. The molecular structure of 3 consisted in a hexanuclear cluster
built up by six dianionic bridging Lc ligands connecting the BiIII ions in a distorted trigonal
antiprismatic structure. Three nitrate ions were encapsulated in the central void of this frame-
work, with the other three nitrate ions acting as counterions, and four water molecules as solv-
ates. The encapsulated nitrate ions assembled a very intricate bonding net with the BiIII ions,
forming µ3 (marginal nitrates) and µ6 (central nitrate) systems. The central nitrate ion was situ-
ated on a crystallographic inversion center and exhibited a static disorder, being 50% eclipsed
to each vicinal nitrate moiety. Figure 5 shows the structure of the cationic fragment of com-
pound 3 and the nitrate ions encapsulated in its central void.
INSERT Figure 5 ABOUT HERE
The Lc moieties intercalated the BiIII ions in pairs showing a 4O,N,N’,S tetradentate coordina-
tion to one cation and a 2O,S’ bidentate coordination to the second cation, in which both BiIII
ions were connected by the same oxygen atom. This coordination scheme was possible due to
a modification in the conformation of one of the amide residues of the ligand side chains (Figure
11

6). This structure was quite different from those observed for indium(III) complexes with sim-
ilar ligands [41, 42].
INSERT Figure 6 ABOUT HERE
There were three crystallographic independent BiIII ions: Bi1, Bi2, and Bi3. Atom Bi1 was
nonacoordinate, while Bi2 and Bi3 were decacoordinate. For all BiIII species, the 4O,N,N’,S
tetradentate chelate rings built up a hemidirected pentagonal pyramidal coordination in which
the fifth basal position was completed by an oxygen atom from a 2O,S’ chelate provided by a
second Lc ligand, and the apical position was occupied by the sulfur atom of this same second
chelate ring. The complete coordination spheres were holodirected if taking into account the
secondary bonds with the encapsulated nitrate groups. The coordination environments of the
independent BiIII species are depicted in Figure 7.
INSERT Figure 7 ABOUT HERE
This tangled structure imposed a high steric hindrance that introduced longer bond lengths than
the observed for the other complexes, especially for the Bi-O bonds. The Bi-O bonds from the
Lc skeleton were in the range of 2.6162(3) - 2.6761(3) Å, while longer Bi···O contacts provided
by the enclosed nitrate groups were in the range of 2.8025(3) - 3.1825(2) Å. The coordinate
bonds between the Bi-N and Bi-S atoms had bond length ranges between 2.3100(04) -
2.5403(4) Å and 2.6150(16) – 2.7635(15) Å, respectively. The basal N-Bi-S bond angles were
in the range of 60.616(5) - 61.119(5)º while the apical N-Bi-S bond angles were between
69.432(5) - 92.431(5)º, which were significantly different due to the irregularity of the bond
framework. Selected bond lengths and angles are shown in Table 3.
INSERT Table 3 ABOUT HERE
3.2. Fourier-transform infrared (FTIR) spectroscopy
Fourier-transform infrared (FTIR) spectra of all compounds are similar. The strong NH stretch-
ing bands occurred between 3110-3265 cm–1 for the free ligands and were not observed in the
complexes, except for 1 that presented a weak peak at 3243 cm–1 since it had one neutral HLa
molecule coordinated to bismuth(III). The strong C=O stretching bands were observed between
1651-1688 cm–1 for the free ligands. A strong red shift was observed for these bands in the
12

complexes spectra (1484-1520 cm–1) as a result of coordination. A similar bathochromic effect
was observed for the C=S stretching modes, that relied on 1266-1278 cm–1 for the free ligands
and in 1245-1258 cm–1 for the complexes [43, 44]. For compound 3, nitrate modes were ob-
served in 1331 and 1346 cm–1 [45]. Table 4 summarizes the main bands observed in the FTIR
spectra and the respective assignment attempts of the synthesized ligands and complexes for
comparison.
INSERT Table 4 ABOUT HERE
3.3. 1H and 13C Nuclear Magnetic Resonance (NMR) spectroscopy
1
Essentially, the H NMR spectra of the proligands and their corresponding complexes were
13
quite similar. Also, no significant differences were observed in the C NMR spectra of the
proligands in comparison to their respective complexes.
1
Comparing the H NMR spectra of HLa and 1, the chemical shifts observed for the complex
were slightly shielded in comparison to the ligand, especially for the N-H acidic hydrogen.
However, a direct discussion regarding the coordination effect was not possible because these
spectra were collected using different solvents. The CH3-triplets (1.18 and 1.25 ppm) and the
CH2-quartets (3.52 and 3.95 ppm) of the ethyl groups appeared split for HLa, but only one triplet
(1.29 ppm) and one quartet (3.13 ppm) were observed for complex 1, which can be related to a
decrease in the degree of freedom of the individual methyl and methylene moieties upon coor-
dination.
1
Comparing the H NMR spectra of HLb and 2, the main difference was related to the CH2-
morpholinyl resonances: in HLb, these resonances were distributed between 3.69-4.21 ppm,
while in 2 they were apparently merged in one single broad signal centered at 2.83 ppm (resid-
ual water peak could overlap the other peak). The aromatic region of the spectra was almost
identical, and the NH signal observed at 9.68 ppm for HLb was absent in complex 2.
1
The ethyl moiety resonances in the H NMR spectra of H2Lc and 3 followed the same trend
observed for HLa and 1: CH3-triplets (1.20 and 1.29 ppm) and CH2-quartets (3.59 and 4.00 ppm)
were split for the ligand, but only one resonance of each group was observed for the complex
(triplet: 1.20 ppm; quartet: 3.12 ppm ). The H-aromatic resonances were not resolved for H2Lc
(multiplets at 8.28 and 8.33 ppm), but a clear doublet (7.95 ppm) and a triplet (7.60 ppm) were
observed for the complex 3. The NH resonance observed at 11.29 ppm for H2Lc was absent in
the 1H NMR spectrum of 3, as expected.
13

3.4. Antibacterial activity
Given the well-known antimicrobial activity of bismuth compounds, we tested the inhibition
ability of the synthesized ligands, complexes as well as the starting salt Bi(NO3)3·5H2O against
the selected two Gram-Negative (E. coli and P. aeruginosa) and Gram-Positive (S. aureus)
bacteria by the disc diffusion and broth microdilution assays (Table 5). Based on the disc dif-
fusion assay, only compound 2 showed stronger inhibiting bacterial abilities producing inhibi-
tion of zones of 13.0 mm and 12.0 mm for P. aeruginosa and S. aureus, respectively. These
data indicated that the antibacterial performance of 2 was about three times greater than those
found in the literature for copper compounds containing similar ligands [46]. This pronounced
increase in activity can be attributed to the morpholine ring present in the structure in which the
heterocyclic compounds activate biological activity [46].
INSERT Table 5 ABOUT HERE
For the antimicrobial activities evaluated by broth microdilution assay, the tested compounds
presented distinct behaviors. Bismuth(III) nitrate showed activity only against P. aeruginosa,
while the ligands did not show any apparent activity. A minimum inhibitory concentration
(MIC) for bismuth compounds is between 0.019 and 5.0 µg mL–1. Compound 1 does not
demonstrate satisfactory activity for the tested bacteria, while compounds 2 and 3 demonstrate
interesting activities. Among them, compound 2, was the most active for the three different
types of bacteria (E. coli = 0.156 µg mL–1, P. aeruginosa = 1.250 µg mL–1, and S. aureus =
0.019 µg mL–1). Compound 3 was shown to be more efficient against P. aeruginosa and S.
aureus with a minimum inhibition concentration of 2.5 µg mL–1 for both.
4. Conclusions
The new bismuth(III) aroylthioureas complexes were synthesized from monopodal (HLa and
HLb) and bipodal (H2Lc) ligands with the following compositions [Bi(La)3(HLa)] (1),
[Bi2(Lb)4(-Lb)2]2(C3H6O) (2), and [Bi6(-Lc)6(3-NO3)2(6-NO3)](NO3)34H2O (3). The syn-
thesized ligands and complexes were satisfactorily characterized by different analytical meth-
odologies. Single-crystal X-ray diffraction studies were carried out for the crystalline com-
pounds 1, 2, and 3, revealing mononuclear, dinuclear, and hexanuclear structures, respectively.
14

Antimicrobial activity in the DD assay showed that compound 2 presented a significant inhibi-
tion zone against two types of bacteria (P. aeruginosa and S. aureus) with a performance close
to three times better than those found for similar compounds against the same bacteria. In the
MIC test, all synthesized complexes proved to be efficient against the three selected bacteria
(E. coli, S. aureus, and P. aeruginosa). Compound 2 presented the best values, even when com-
pared to other bismuth compounds found in the literature, attesting the importance of targeting
bismuth(III) aroylthioureas for further research on new drugs development.
5. Abbreviations
ATCC
ATR
Calcd.
CAMH
CCDC
CFU
American type culture collection
Attenuated total reflectance
Calculated
Cation adjusted Mueller-Hinton agar
Cambridge Crystallographic Data Centre
Colony-forming unit
CLSI
DD
Clinical and Laboratory Standards Institute
Disk Diffusion Assay
DMSO
Dimethylsulfoxide
Elem. Anal. Elemental analysis
ESI-FTICR Electrospray-ionization Fourier-transform ion-cyclotron-resonance
ESI-MS
FTIR
F.W.
HLa
Electrospray-ionization mass spectrometry
Fourier-transform infrared spectroscopy
Formula weight
N-benzoyl(N’,N’-diethylthiourea)
N-benzoyl(morpholinylthiourea)
N2,N6-bis(diethylcarbamothioyl)pyridine-2,6-dicarboxamide
molecular ion peak
HLb
H2Lc
M
M
molar (mol L–1)
MIC
m.p.
MS
Minimal Inhibitory Concentration
Melting point
Mass spectrometry
m/z
mass/charge ratio
NMR
PBPY-7
ppm
r.t.
Nuclear magnetic resonance spectroscopy
Seven-coordination pentagonal bipyramid
parts per million
room temperature
SC-XRD
TMS
TTC
Single-crystal X-ray diffractometry
Tetramethylsilane
Triphenyl-tetrazolium chloride
6. Supplementary data
15

A crystallographic data table, ellipsoid representations, and spectroscopic data are available
free of charge as electronic supplementary information. CCDC 1984604, 1984603, and
1984605 contain the supplementary crystallographic data for the complexes 1, 2, and 3, respec-
tively. These data can be obtained free of charge via http://www.ccdc.cam.ac.uk/conts/retriev-
ing.html, or from the Cambridge Crystallographic Data Centre, 12 Union Road, Cambridge
CB2 1EZ, UK; fax: (+44) 1223–336–033; or e–mail: deposit@ccdc.cam.ac.uk.
7. CRediT author statement
Marcielli Indiara de Oliveira: Investigation, Validation, Formal analysis, Gabriela Pereira
Chuy: Investigation, Validation, Bruno Stefanello Vizzotto: Supervision, Methodology, Re-
sources, Writing - Review & Editing, Robert Alan Burrow: Formal analysis, Writing - Review
& Editing, Ernesto Schulz Lang: Funding acquisition, Resources, Writing - Review & Editing,
Sailer Santos dos Santos: Funding acquisition, Supervision, Resources, Methodology, Con-
ceptualization, Project administration, Writing - Original Draft, Writing - Review & Editing.
8. Declaration of interest
The authors declare that they have no known competing financial interests or personal relation-
ships that could have appeared to influence the work reported in this paper.
9. Acknowledgments
We would like to thank the financial agencies: Brazilian Research Councils (CNPq), Coor-
denação de Aperfeiçoamento de Pessoal de Nível Superior via CAPES-PrInt, and CAPES-
PROEX programs- Finance Code 001, and also CAPES/PROBRAL (88881.144118/2017-01).
M.I.O. gratefully acknowledges a scholarship from PPGQ/UFSM CAPES/PROEX program.
S.S.S. gratefully acknowledges grants sponsored by FIPE/CCNE/UFSM projects. The X-ray
diffractometer and the FTIR spectrometer were purchased with funding from FINEP/CT-Infra.
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20

Tables
Table 1. Selected bond lengths (Å) and angles (º) for compound 1.
Bond lengths (Å)
Bond angles (º)
O1-Bi1-O2
O1-Bi1-S1
O1-Bi1-S2
O1-Bi1-S3
O2-Bi1-S2
O2-Bi1-S3
O2-Bi1-S4
O3-Bi1-O1
O3-Bi1-O2
O3-Bi1-S1
O3-Bi1-S2
S1-Bi1-O2
S1-Bi1-S3
S2-Bi1-S1
S2-Bi1-S3
S2-Bi1-S4
S3-Bi1-O3
2.3704(03)
138.350(11)
75.215(08)
80.803(9)
Bi1-O1
Bi1-O2
Bi1-O3
Bi1-S1
Bi1-S2
Bi1-S3
Bi1-S4
2.4072(03)
2.4070(03)
2.8287(12)
2.6192(11)
2.8462(11)
3.2147(11)
146.572(8)
79.018(7)
71.923(07)
118.792(2)
70.255(10)
143.053(10)
143.776(7)
86.097(7)
75.532(08)
137.643(4)
99.070(4)
96.052(3)
162.176(10)
76.339(07)
21

Table 2. Selected bond lengths (Å) and angles (º) for compound 2.
Bond lengths (Å)
Bond angles (º)
O11-Bi1-O21
O11-Bi1-O31
O11-Bi1-S11
O11-Bi1-S33'
O11-Bi1-S22
O21-Bi-O31
O21-Bi-S22
2.3140(14)
140.150(7)
71.670(6)
79.200(4)
70.346(04)
79.632(5)
137.190(6)
78.310 (4)
72.300(5)
137.054(5)
83.710 (5)
149.640(4)
70.050(05)
146.157(3)
92.443(18)
99.540(3)
144.894(02)
Bi1-O11
Bi1-O21
Bi1-O31
Bi1-S11
Bi1-S22
Bi1-S33
Bi1-S33'
2.4245(15)
2.4998(17)
2.6955 (07)
2.6616(08)
3.0946(07)
3.1542(07)
O21-Bi1-S11
O21-Bi1-S33'
O31-Bi-S22
O31-Bi1-S11
O31-Bi1-S33'
S11-Bi1-S33
S11-Bi1-S33'
S22-Bi1-S11
S22-Bi1-S33'
22

Table 3. Selected bond lengths (Å) and angles (º) for compound 3.
Bond lengths (Å)
Bi1-N11
Bond angles (º)
N11-Bi1-N14
N11-Bi1-O11
N11-Bi1-S32
N14-Bi1-S12
N14-Bi1-S32
O11-Bi1-O32
O11-Bi1-S32
O32-Bi1-S32
S12-Bi1-S32
2.5403(4)
2.3133(4)
2.6162(3)
2.7779(3)
2.7635(15)
2.6296(16)
3.1029(4)
2.9218(3)
2.8025(3)
66.238(6)
60.989(5)
69.752(5)
60.616(5)
91.616(5)
96.357(6)
82.266(5)
78.406(5)
91.709(5)
Bi1-N14
Bi1-O32
Bi1···O11
Bi1-S12
Bi1-S32
Bi1···O21N'
Bi1···O22N'
Bi1···O31N
2.5300(4)
2.3100(4)
2.6761(3)
2.8016(3)
2.6150(16)
2.7420(16)
2.9020(2)
3.1825(2)
3.0050(3)
3.1002(3)
66.794(5)
60.780(5)
69.432(5)
92.431(5)
61.119(5)
95.380(5)
76.182(5)
79.707(5)
92.007(5)
Bi2-N21
N21-Bi2-N22
N21-Bi2-O23
N21-Bi2-S11
N22-Bi2-S11
N22-Bi2-S21
O11-Bi2-O23
O11-Bi2-S11
O23-Bi2-S11
S11-Bi2-S21
Bi2-N22
Bi2-O11
Bi2-O23
Bi2-S11
Bi2-S21
Bi2···O21N
Bi2···O23N
Bi2···O31N
Bi2···O32N
2.5316(4)
2.3267(4)
2.6419(3)
2.8032(2)
2.6302(15)
2.7320(16)
3.0993(3)
3.0525(3)
2.9413(3)
3.1773(4)
66.828(5)
60.874(5)
70.175(5)
92.156(5)
61.049(5)
94.976(5)
77.563(5)
80.785(5)
92.278(5)
Bi3-N31
N31-Bi3-N32
N31-Bi3-O32
N31-Bi3-S22'
N32-Bi3-S22'
N32-Bi3-S31
O23'-Bi3-O32
O23'-Bi3-S22'
O32-Bi3-S22'
S22'-Bi3-S31
Bi3-N32
Bi3-O23'
Bi3···O32
Bi3-S22'
Bi3-S31
Bi3···O33N
Bi3···O22N
Bi3···O23N
Bi3···O31N
23

Table 4. FTIR spectra main bands for the synthesized ligands and complexes.
Assignment
(O-H)i
HLa
HLb
H2Lc
1
-
2
3
-
-
-
-
3430
3264m
1651s
3236m
1662s
3243w
1682mii
1494s
1245m
-
3265m
1672s
-
-
(N-H)
1702miii
1484s
1258m
-
1642mii
1520s
1253m
1331s
1346s
(C=O)
1278m
-
1266s
-
1275m
-
(C=S)
(N-O)iv
i H2O solvate; ii non-coordinated C=O; iii non-coordinated C=O from acetone solvate; iv nitrate ions.
Table 5. Inhibition of zones (mm) and MIC values (µg mL–1) of compounds against tested
bacteria.
P. aeruginosa
S. aureus
E. coli
ATCC 25922
ATCC 27853
ATCC 25923
Compound
IZ
MIC
>10.0
>10.0
>10.0
>10.0
0.156
5.0
IZ
MIC
>10.0
>10.0
>10.0
>10.0
1.250
2.5
IZ
MIC
>10.0
>10.0
>10.0
>10.0
0.019
2.5
HLa
HLb
-
-
-
-
-
-
-
-
-
-
-
H2Lc
-
-
-
-
1
13.0
12.0
2
-
-
-
-
3
Bi(NO3)3·5H2O
>10.0
5.0
>10.0
IZ: inhibition zones; MIC: minimum inhibitory concentration. The “-“ signals indicate no inhibition zone
observed.
24

Figures
Figure 1. Molecular structures of: (a) monopodal aroylthioureas; (b) bipodal aroylthioureas.
Figure 2. Schematic route to obtain complexes 1 – 3, with HLa = N-benzoyl(N’,N’-diethylthi-
ourea), HLb = N-benzoyl(morpholinylthiourea), and H2Lc = N2,N6-bis(diethylcarbamothi-
oyl)pyridine-2,6-dicarboxamide. Solvate molecules are omitted in this representation.
25

Figure 3. (a) Molecular structure of 1 (hydrogen atoms attached to carbon were omitted for
clarity). (b) Coordination environment for bismuth(III) in compound 1.
Figure 4. (a) Molecular structure of 2 (hydrogen atoms and solvate molecules were omitted
for clarity). (b) Coordination geometry around bismuth in complex 2. Symmetry operations
used to generate equivalent atoms: ' = –x, –y, –z.
26

Figure 5. Two different projections of the molecular structure of 3: (a) the cationic fragment
built up by BiIII and Lc moieties, with emphasis in the central void; (b) the cationic framework
and the encapsulated nitrate ions. Hydrogen atoms, ethyl groups, solvate molecules, and pe-
ripheral nitrate counterions were omitted for clarity. Symmetry operations used to generate
equivalent atoms: ' = 1–x, 1–y, 1–z.
Figure 6. Representation of the coordination scheme provided by the ligands Lc in compound
3, with emphasis in the distinct chelating systems to two adjacent bismuth(III) ions.
Figure 7. The coordination environments of the independent BiIII species in compound 3.
Symmetry operations used to generate equivalent atoms: ' = 1–x, 1–y, 1–z.
27

Table 1. Selected bond lengths (Å) and angles (º) for compound 1.
Bond lengths (Å)
Bond angles (º)
O1-Bi1-O2
O1-Bi1-S1
O1-Bi1-S2
O1-Bi1-S3
O2-Bi1-S2
O2-Bi1-S3
O2-Bi1-S4
O3-Bi1-O1
O3-Bi1-O2
O3-Bi1-S1
O3-Bi1-S2
S1-Bi1-O2
S1-Bi1-S3
S2-Bi1-S1
S2-Bi1-S3
S2-Bi1-S4
S3-Bi1-O3
2.3704(03)
138.350(11)
75.215(08)
80.803(9)
Bi1-O1
Bi1-O2
Bi1-O3
Bi1-S1
Bi1-S2
Bi1-S3
Bi1-S4
2.4072(03)
2.4070(03)
2.8287(12)
2.6192(11)
2.8462(11)
3.2147(11)
146.572(8)
79.018(7)
71.923(07)
118.792(2)
70.255(10)
143.053(10)
143.776(7)
86.097(7)
75.532(08)
137.643(4)
99.070(4)
96.052(3)
162.176(10)
76.339(07)
Table 2. Selected bond lengths (Å) and angles (º) for compound 2.
Bond lengths (Å)
Bond angles (º)
O11-Bi1-O21
O11-Bi1-O31
O11-Bi1-S11
O11-Bi1-S33'
O11-Bi1-S22
O21-Bi-O31
O21-Bi-S22
2.3140(14)
140.150(7)
71.670(6)
79.200(4)
70.346(04)
79.632(5)
137.190(6)
78.310 (4)
72.300(5)
137.054(5)
83.710 (5)
149.640(4)
70.050(05)
146.157(3)
Bi1-O11
Bi1-O21
Bi1-O31
Bi1-S11
Bi1-S22
Bi1-S33
Bi1-S33'
2.4245(15)
2.4998(17)
2.6955 (07)
2.6616(08)
3.0946(07)
3.1542(07)
O21-Bi1-S11
O21-Bi1-S33'
O31-Bi-S22
O31-Bi1-S11
O31-Bi1-S33'
S11-Bi1-S33
28

S11-Bi1-S33'
S22-Bi1-S11
S22-Bi1-S33'
92.443(18)
99.540(3)
144.894(02)
Table 3. Selected bond lengths (Å) and angles (º) for compound 3.
Bond lengths (Å)
Bi1-N11
Bond angles (º)
N11-Bi1-N14
N11-Bi1-O11
N11-Bi1-S32
N14-Bi1-S12
N14-Bi1-S32
O11-Bi1-O32
O11-Bi1-S32
O32-Bi1-S32
S12-Bi1-S32
2.5403(4)
2.3133(4)
2.6162(3)
2.7779(3)
2.7635(15)
2.6296(16)
3.1029(4)
2.9218(3)
2.8025(3)
66.238(6)
60.989(5)
69.752(5)
60.616(5)
91.616(5)
96.357(6)
82.266(5)
78.406(5)
91.709(5)
Bi1-N14
Bi1-O32
Bi1···O11
Bi1-S12
Bi1-S32
Bi1···O21N'
Bi1···O22N'
Bi1···O31N
2.5300(4)
2.3100(4)
2.6761(3)
2.8016(3)
2.6150(16)
2.7420(16)
2.9020(2)
3.1825(2)
3.0050(3)
3.1002(3)
66.794(5)
60.780(5)
69.432(5)
92.431(5)
61.119(5)
95.380(5)
76.182(5)
79.707(5)
92.007(5)
Bi2-N21
N21-Bi2-N22
N21-Bi2-O23
N21-Bi2-S11
N22-Bi2-S11
N22-Bi2-S21
O11-Bi2-O23
O11-Bi2-S11
O23-Bi2-S11
S11-Bi2-S21
Bi2-N22
Bi2-O11
Bi2-O23
Bi2-S11
Bi2-S21
Bi2···O21N
Bi2···O23N
Bi2···O31N
Bi2···O32N
2.5316(4)
2.3267(4)
2.6419(3)
2.8032(2)
66.828(5)
60.874(5)
70.175(5)
92.156(5)
Bi3-N31
Bi3-N32
Bi3-O23'
Bi3···O32
N31-Bi3-N32
N31-Bi3-O32
N31-Bi3-S22'
N32-Bi3-S22'
29