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11 (
6
); 739-746
doi:
10.1016/j.arabjc.2017.12.014

Synthesis, characterizations, and antibacterial properties of PbMoO4 nanocrystals

, , , , , , , , , ,
a Departamento de Física, Universidade Federal do Ceará, P. O. Box 6030, CEP 60455-970 Fortaleza, CE, Brazil
b Universidade Federal do Cariri, CEP 63000-000 Juazeiro do Norte, CE, Brazil
c Laboratório de Microbiologia e Biologia Molecular, Universidade Regional do Cariri, CEP 63105-000 Crato, CE, Brazil
d Departamento de Física, Campus Ministro Petrônio Portella, Universidade Federal do Piauí, CEP 64049-550 Teresina, PI, Brazil

⁎Corresponding author at: Universidade Regional do Cariri, Departamento de Química Biológica, Av. Cel. Antônio Luiz, 1161, CEP 63105-000 Crato, CE, Brazil. hdmcoutinho@gmail.com (H.D.M. Coutinho) hdmcoutinho@urca.br (H.D.M. Coutinho)

Received: , Accepted: ,
© The Author(s) 2017
Disclaimer:
This article was originally published by Elsevier and was migrated to Scientific Scholar after the change of Publisher.

Peer review under responsibility of King Saud University.

Abstract

This study reports the synthesis and characterization of PbMoO4 nanocrystals and the antibacterial properties and modulation of their antibiotic activity. Lead molybdate nanocrystals were obtained through the conventional hydrothermal method, and the structural, vibrational and morphological properties of the sample were determined using X-ray diffraction, Raman and infrared spectroscopy, and scanning electron microscopy images. The obtained samples present scheelite-type tetragonal structure (space group I41/a) without secondary phases, and the Raman spectrum shows the formation of PbMoO4 structurally ordered at short-range, confirming the quality of the samples. The antibacterial and antibiotic-modulation activities were performed in triplicate using the microdilution method. The minimum inhibitory concentration (MIC) of antibiotics alone or in association with PbMoO4, were demonstrated using geometric mean. When assayed directly, the PbMoO4 presented a MIC ≥ 1024 μg/mL against all bacterial strains tested. When in association with the gentamicin against Staphylococcus aureus, a synergism was observed reducing 37.5% the MIC. However, in the assays against the Gram-negative strains was observed that the presence of lead affected the effect of the antibiotic, leading to an antagonism.

Keywords

Lead molybdate
Hydrothermal method
Characterizations
Antibacterial properties
1

1 Introduction

Molybdates constitute an important class of materials belonging to the group of transition metal oxides that exhibit various functional properties dependent on the structure (Maczka et al., 2012). The molybdates have attracted wide attention due to their characteristics and applications in various fields such as photoluminescence (Gouveia et al., 2014), photocatalytic properties (Li et al., 2015; Moura et al., 2017a), humidity sensor (Suresh et al., 2002), magnetic properties (Ding et al., 2007), anode for lithium-ion batteries (Zheng et al., 2015), pressure induced amorphization (Moura et al., 2016a), phase transition (Moura et al., 2016b) and antibacterial activity (Tang et al., 2013). The structural stability and pressure-induced phase transitions of scheelite-type molybdates have been extensively studied. Raman and X-ray diffraction experiments have allowed the discovery of pressure-induced phase transitions at pressures values higher than 5 GPa depending upon the compound, making this class of materials very interesting from a scientific point of view (Errandonea et al., 2008; Errandonea et al., 2010; Errandonea et al., 2013; Errandonea et al., 2011).

Among several applications, the molybdates have presented the potential to be used as antibacterial substance, although there are still few papers addressing this subject. Microbial infections have become one of the principal problems of public health in the world, and the nanomaterials have emerged as possible new antimicrobial agents and as alternative strategies against bacterial resistance (Oliveira et al., 2015). In recent years, the interest in the antibacterial materials has grown due to several applications such as food packaging, sanitary materials, medical and military items (Liu et al., 2005; Machida et al., 2005; Tankhiwale and Bajpai, 2009). Tang et al. (2013) reported the synthesis of Ag2Mo2O7 nanoparticles in the microporous structure of the chitin matrix and the antibacterial activities were studied on Escherichia coli and Staphylococcus aureus by the disk-diffusion method. Moura et al. (2017b) show the evaluation of antibacterial and antibiotic-modulation activity on Staphylococcus aureus, Pseudomonas aeruginosa and Escherichia coli, using the microdilution method to determine the minimum inhibitory concentration (MIC) of the β-Ag2MoO4. Mardare et al. (2016) reported the growth inhibition of Escherichia coli by zinc molybdate synthesized through the hydrothermal method with different crystalline structures, utilizing optical density measurements and by the observation of cultures growth on agar Petri dishes. Meng and Xiong (2008) show the antibacterial studies using the inhibition zone method on Staphylococcus aureus and Escherichia coli by Ag2MoO7, ZnMoO4 and CoMoO4 synthesized via solid-state reaction, co-precipitation and hydrothermal route, respectively.

Among the molybdates, lead molybdate (PbMoO4), belonging to the large family of alkaline earth metal molybdates with the general formula AMoO4 (A = Ca2+, Sr2+, Ba2+, and Pb2+), has recently gained increasing interest because of their applications in many fields, e.g. scintillation detectors (Minowa et al., 1992), photocatalysis (Bi et al., 2009), photoluminescence (Bomio et al., 2013), thermoluminescence (Hofstaetter et al., 1978) and fiber optics (Taylor et al., 1993). Usually, PbMoO4 appears in a scheelite-type tetragonal structure at atmospheric conditions, and no phase changes were detected when subjected to extreme conditions of pressure (∼5 GPa) and temperature (−150 °C to 600 °C), exhibiting high thermodynamic stability (Bayne and Butler, 2014).

In the present study, we report on the synthesis of PbMoO4 nanocrystals by the hydrothermal method without the use of surfactants or organic additives. The structural, vibrational and morphological characterization of PbMoO4 samples were performed using X-ray diffraction (XRD), Raman and infrared spectroscopy and scanning electron microscopy (SEM), respectively. Previous works show several technological and scientific applications of lead molybdate as mentioned previously. However, its antibacterial activity was not discussed before, and the present work contributes to fill this gap. It is investigated the antibacterial properties and antibiotic-modulation activity by PbMoO4 nanocrystals against the standard and multidrug-resistant (MDR) bacterial strains of Staphylococcus aureus, Escherichia coli and Pseudomonas aeruginosa, verifying their efficacy combined with conventional antibiotics. This would enable the use of PbMoO4 not only for antimicrobial surfaces and coatings, but also as a powder which can be embedded in polymers used for catheters, implants and in others domestic or hospital materials.

2

2 Materials and methods

2.1

2.1 Synthesis of PbMoO4 nanocrystals

The synthesis of PbMoO4 nanocrystals was performed by the conventional hydrothermal method, using 1 mmol of sodium molybdate dihydrate (Na2MoO4·2H2O) and 1 mmol of lead chloride (PbCl2) as reagents, separately dissolved in 30 ml of deionized water and after that stirred for 15 min. These two aqueous solutions were mixed, submitted to 3 min of ultrasound treatment and then transferred into a Teflon autoclave, which was sealed and kept at 150 °C for 2 h with a heating rate of 10 °C/min. We observed the formation of a white precipitate compound which was washed several times with deionized water, and then it was dried with acetone for 6 h in the air.

2.2

2.2 Characterization

The structural characterization of the obtained sample was done by X-ray diffraction technique using a Bruker D-8 Advance XRD diffractometer with the CuKα radiation (λ = 1.5418 Å) in the 2θ range of 5–80°, with a step size of 0.02° and a counting time of 2 s/step. Structural parameters of PbMoO4 nanocrystals have been obtained by the Rietveld method (Rietveld, 1969) from the crystal data available in the Inorganic Crystal Structure Database (ICSD) – Card No. 67493. The Rietveld refinement was performed using the GSAS software package (Larson and Von Dreele, 2004). Fourth-order Chebyshev polynomials were used to fit the inelastic scattering background. The peak profile analysis was carried out using the modified Thompson–Cox–Hasting pseudo-Voigt profile function. Optimized parameters were scale factor, background, sample position in relation to the goniometer, lattice parameters (a, b, c), Lorentzian width related to crystallite size (LX), profile half-width parameters (GU, GV, GW), peak asymmetry related to axial divergence (S/L), atomic coordinates (x, y, z), isotropic temperature parameter (U), ratio between Kα1 and Kα2 (Ratio), and polarization of the diffraction beam (Pola). The full width at half maximum (FWHM) was used to calculate the crystallite size by the Scherrer equation (Azaroff, 1968). The crystallite size, micro-strain and homogeneity of the crystallites were evaluated through the value of correlation coefficient and were calculated using the Williamson–Hall equation (WH) (Williamson and Hall, 1953). Raman measurements were performed using a micro-Raman Senterra Bruker spectrometer, and the 532 nm line of a laser was used as the excitation source. The spectrometer slit was set for a resolution of 3 cm−1. An Olympus microscope (BX-50) was used to focus the laser on the sample surface. The Fourier-transform infrared (FT-IR) spectrum was measured in the spectral range of 350–4000 cm−1 on a spectrometer model Perkin Elmer Spectrum Two, using a KBr pallet in a transmittance mode. The spectrum was recorded with 180 scans with a spectral resolution of 2 cm−1. Morphological aspects of the microcrystals were observed using scanning electron microscopy (SEM) and the elemental analysis was done by energy dispersive spectroscopy (EDS) using a Quanta 450 FEG scanning electron microscope and an EDAX X-ray detector.

2.3

2.3 Bacterial strains, compounds and antibacterial activity assay

The microorganisms were obtained from the Laboratório de Microbiologia e Biologia Molecular (LMBM) of Universidade Regional do Cariri (URCA). In this study were used standard (Escherichia coli ATCC 25922, Staphylococcus aureus ATCC 6538 and Pseudomonas aeruginosa ATCC 9027) and MDR (Escherichia coli 06, Staphylococcus aureus 10 and Pseudomonas aeruginosa 15) bacterial strains. The resistance profile of MDR bacterial strains is shown in Table 1. The drugs and the compound were dissolved using water and diluted to a final concentration of 1024 μg/mL. Norfloxacin was dissolved using DMSO according to CLSI (2008) guidelines. To determine the MIC was used the microdilution procedure. The inoculum was performed using bacterial strains previously cultivated in heart infusion agar (HIA), and the cell concentration was adjusted to 0.5 McFarland (1 × 108 CFU/mL) in saline solution 0.9%. Tubes containing 1350 μL of brain heart infusion broth (BHI) at 10% and 150 μL of bacterial inoculum were prepared. An amount of 100 μL of this solution were dropped into each well of a 96 well microtiter plate, followed by a serial dilution of the lead compound solution, ranging between 512 and 0.5 μg/mL. Each test was performed in triplicate. The microtiter plates were incubated for 24 h at 37 °C. After this time, the MIC was estimated by the addition of 20 μL of resazurin and after a time of 1 h, the color change was evaluated. The lower concentration that inhibited the bacterial growth indicated the MIC (Gallucci et al., 2009; Sales et al., 2014).

Table 1 Resistance profile of the used strains.
Bacteria Source Resistance profile
Escherichia coli 06 Urine culture Cf, Cef, Ca, Cro, Com
Staphylococcus aureus 10 Swab retal Ca, Cef, Cf, Oxa, Pen, Amp, Amox, Mox, Cip, Lev, Asb, Amc, Eri, Cla, Azi, Clin
Pseudomonas aeruginosa 15 Catheter tip Cpm, Ctz, Imi, Cip, Ptz, Lev, Mer

Ast – aztreonam; Amp – Ampicilin; Asb – Ampicilin + Sulbactam; Ami – Amikacin; Amox – Amoxicilin; Amc – Amoxicilin + Clavulamic acid; Azi – Azitromicine; Ca – Cefadroxil; Cfc – Cefaclor; Cf – Cefalotine; Cef – Cefalexin; Cla – Claritromicin; Cro – Ceftriaxone; Ctz – ceftazidime; Cip – Ciprofloxacin; Clo – Cloranphenicol; Clin – Clindamicine; Imi – imipenem; Can – Kanamicin; Szt – sulphametrim; Tet – Tetracycline; Tob – Tobramicin; Oxa – Oxacilin; Gen – Gentamicin; Lev – Levofloxacin; Mer – meropenem; Mox – Moxifloxacin; Neo – Neomicin; To – paromomicin; But – Butirosine; Sis – sisomicine; Net – Netilmicin; Pen – Penicilin; Ptz – Piperacilin + Tazobactam.

2.4

2.4 Modulation of drugs assay

The antibiotic-modulation activity of the lead compound was evaluated using the method described by Coutinho et al. (2008). For each bacterial strain, a tube containing 1162 μL of BHI at 10%, 188 μL of lead molybdate (corresponding to the MIC/8) and 150 μL of bacterial inoculum was prepared. As a control, a solution with 1350 μL of BHI (at 10%) and 150 μL of bacterial inoculum was done for each strain. For each solution, an amount of 100 μL was dropped into each well of a 96 well microtiter plate, followed by a serial dilution of the antibiotic solution with 1024 μg/mL, ranging between 512 and 0.5 μg/mL. All tests were performed in triplicate. The microtiter plates were incubated for 24 h at 37 °C.

2.5

2.5 Statistical analysis

The data was analyzed through the statistical package GraphPad Prism 5.0 software. The data was analyzed using a One-way ANOVA test, followed by Bonferroni’s post hoc test (where p < .05 and p < .0001 were considered significant and p > .05 was not significant).

3

3 Results

3.1

3.1 X-ray diffraction (XRD)

The observed and calculated XRD patterns by Rietveld method are shown in Fig. 1. The crystalline nature of the samples was confirmed by XRD analysis. The XRD patterns indicate that PbMoO4 crystals have a tetragonal structure with space group C64h (I41/a) containing four molecular formulas per unit cell (Z = 4), without secondary phases when compared with ICSD Card No. 67493. In the scheelite-type structure, each Mo atom is surrounded by four equivalent O sites in tetrahedral symmetry. On the other hand, each Pb atom shares corners with eight adjacent MoO4 tetrahedra, forming AO8 bisdisphenoids (Errandonea et al., 2010). A schematic representation of the tetragonal unit cell of PbMoO4 crystals is shown in the inset of Fig. 1, where one can observe the Mo atoms (green color) coordinated by four oxygen atoms (red color) forming tetrahedral clusters [MoO4], and the Pb atoms (gray color) coordinated by eight oxygen atoms (red color) forming the dodecahedral clusters [PbO8]. The Rietveld refinement showed a good correlation between the observed and the calculated XRD patterns, confirming the phase purity of PbMoO4 crystals. The structural refinement data are listed in Table 2. From the full width at half maximum of the diffraction peaks and based on the Scherrer and Williamson–Hall equations, it was possible to calculate the average crystallite size and the micro-strain. The average crystallite size according to the Scherrer equation is DSC = 81.70 nm and by the Williamson-Hall equation is DW-H = 87.71 nm. The obtained values of the crystallite size from both equations are similar, indicating that the sample has a low strain in the lattice. The micro-strain obtained by the Williamson-Hall equation presents a very low-value (ε = 9 ∗ 10−5 nm), indicating high homogeneity of the sample.

X-ray diffraction patterns observed and calculated by the Rietveld method of the PbMoO4 nanocrystals. Inset: Schematic representation of the scheelite-type tetragonal unit cells corresponding to PbMoO4 crystals in atmospheric conditions.
Fig. 1 X-ray diffraction patterns observed and calculated by the Rietveld method of the PbMoO4 nanocrystals. Inset: Schematic representation of the scheelite-type tetragonal unit cells corresponding to PbMoO4 crystals in atmospheric conditions.
Table 2 Lattice parameters, quality indicators of structural refinement (R-values), site occupation and atomic coordinates obtained by Rietveld refinement of PbMoO4 nanocrystals.
Lattice parameters R-values Atoms Wyckoff x y z
a = 5.435086 (24) Å Rp = 2.90% Pb 4b 0.00000 0.25000 0.62500
c = 12.106621 (83) Å Rwp = 3.85% Mo 4a 0.00000 0.25000 0.12500
α = β = γ = 90° R(F2) = 3.68% O 16f 0.207127 (618) 0.118218 (700) 0.050633 (297)
V = 357.63 Å χ2 = 2.160 – – – – –

3.2

3.2 Vibrational spectroscopy

The group theory analysis for the PbMoO4 crystals predicts a total of 33 optical modes at the center of the Brillouin zone. The optical modes are distributed among the irreducible representations of the factor group C4h as described by Eq. (1):

(1)
Γ = 3 A g + 4 A u + 5 B g + 3 B u + 5 E g + 4 E u .

The selection rules stand that only Ag, Bg and the doubly degenerated Eg modes are Raman active, only the Au and Eu modes are infrared active and Bu modes are silent. The unpolarized Raman spectrum of the PbMoO4 at atmospheric conditions in the spectral range 1100–30 cm−1, presents a total of 10 vibrational modes located at 869, 766, 743, 351, 318, 193, 168, 104, 73 and 62 cm−1 as can be seen in Fig. 2. The Raman mode at 869 cm−1 (Ag) corresponds to the symmetric stretching (υ1) vibration and appears as a very intensive band, as occurs with many other molybdates (Maczka et al., 2012). The modes at 766 (Bg) and 743 cm−1 (Eg) correspond to the antisymmetric stretching (υ3) vibrations of O–Mo–O bonds of MoO4 units. Regarding the bending modes of the MoO4 tetrahedra, they are expected to appear in the Raman spectrum as bands with wavenumber lower than 500 cm−1. So, the bands at 351 (Eg) and 318 cm−1 (Ag, Bg) are assigned as antisymmetric (υ4) and symmetric bending (υ2) modes of the molybdate ions, respectively. The Raman modes at 193 cm−1 (Eg) and 168 cm−1 (Ag) corresponds to the rotational (R) modes. The Raman peaks at 104 (Eg), 73 (Eg) and 62 cm−1 (Bg) correspond to the translational (T) modes. The well-defined active-Raman modes confirm that PbMoO4 crystals are structurally ordered at short-range, and the relative positions of all Raman modes are in agreement with the literature confirming the quality of the obtained sample (Manjón et al., 2006; Sezancoski et al., 2009; Vilaplana et al., 2012; Bomio et al., 2013). The infrared spectrum of the PbMoO4 at atmospheric conditions in the spectral range 1100–350 cm−1 presents three vibrational modes located at 850, 760 and 375 cm−1 as can be seen in Fig. 3. The strong absorption bands with two modes located at 850 (Au) and 760 (Eu) cm−1 are related to internal modes originating from antisymmetric stretching (υ3) vibrations from MoO4 units. The absorption band at 375 cm−1 corresponds to the antisymmetric bending (υ4) vibrational mode of O–Mo–O bonds of the molybdate ions. The infrared modes are in good agreement with the reported in the literature (Manjón et al., 2006; Bomio et al., 2013).

Raman spectra of the PbMoO4 nanocrystals at room temperature in the spectral region 1100–30 cm−1.
Fig. 2 Raman spectra of the PbMoO4 nanocrystals at room temperature in the spectral region 1100–30 cm−1.
FT-IR spectrum of the PbMoO4 nanocrystals at room temperature in the spectral region 1100–350 cm−1.
Fig. 3 FT-IR spectrum of the PbMoO4 nanocrystals at room temperature in the spectral region 1100–350 cm−1.

3.3

3.3 Morphology and composition analysis

Fig. 4 shows the (a) low- and (b and c) high-magnification SEM images of PbMoO4 nanocrystals obtained by the hydrothermal method. It is possible to note that the samples have a nanometric size and irregular form. The particle size distribution histogram (See inset of Fig. 4c) shows that the average particle size obtained is 76.86 nm. It is interesting to note that the average particle sizes (range) obtained by the SEM images are close to the values determined by Scherrer (DSC = 81.70 nm) and Williamson-Hall (DW-H = 87.71 nm) equations. Thus, the images confirm that the synthesis method (hydrothermal) leads to the formation of nanoparticles. The EDS spectrum (Fig. 3(d)) demonstrates that the molybdate is composed of only Pb, Mo and O atoms, confirming the quality of the sample obtained. This agrees very well with our Rietveld analysis as previously discussed. The theoretical and experimental results of the weight percentages obtained from the EDS spectra are shown in Table 3. From these results, one can see that the experimental percentages are close to the stoichiometric values. When calculating the Pb/(Mo + 4O) ratio, the similar values of 1.3 and 1.2 are obtained for theoretical and experimental percentages, respectively. Therefore, the EDS analysis (Fig. 4 and Table 3) allowed to determine the chemical composition and the atomic fractions of Pb, Mo and O present in the nanocrystal, which are close to the stoichiometric proportion. Also, a very weak signal of C is observed and certainly is originated from the tape used as the support for the measurements.

(a) Low- and (b and c) high-magnification SEM images of PbMoO4 prepared by hydrothermal route showing the nanostructures formed. (b) The corresponding EDS spectrum of the sample. In the inset (Fig. 4(c)), particle size distribution of the nanocrystals.
Fig. 4 (a) Low- and (b and c) high-magnification SEM images of PbMoO4 prepared by hydrothermal route showing the nanostructures formed. (b) The corresponding EDS spectrum of the sample. In the inset (Fig. 4(c)), particle size distribution of the nanocrystals.
Table 3 Theoretical elemental percentages obtained from the stoichiometry PbMoO4, and their respective experimental values obtained from EDS.
PbMoO4
Element Wt% stoichiometric Wt% experimental
C – 11.7
Pb 56.4 47.3
Mo 26.1 19.5
4O 17.4 21.6
Rate Pb/(Mo + 4O) 1.3 1.2

3.4

3.4 Antibacterial activity and modulation of antibiotic activity by PbMoO4 nanocrystals

The results obtained on the antibacterial effect of PbMoO4 are described in Table 4. The PbMoO4 have not demonstrated a clinically relevant antibacterial activity, with a MIC higher than 1000 μg/mL in previous works (Rios and Recio 2005; Holetz et al., 2002). However, studies performed by Al-Noor and Ibraheem (2012) and Xie et al., (2013) using lead complexes demonstrated an antibacterial activity against Staphylococcus aureus, Escherichia coli, Pseudomonas aeruginosa and Bacillus cereus.

Table 4 Minimum inhibitory concentration (μg/mL).
Compound Strains
S.A. ATCC P.A. ATCC E.C. ATCC S.A. 10 P.A. 15 E.C. 06
PbMoO4 ≥1024 ≥1024 ≥1024 ≥1024 ≥1024 ≥1024

S.A., Staphylococcus aureus; P.A., Pseudomonas aeruginosa; E.C., Escherichia coli.

4

4 Discussion

This effect is related to the spatial geometry of these metal complexes and the presence of carboxyl groups in the ligand (Al-Noor and Ibraheem 2012; Xie et al., 2013; El-Ajaily et al., 2007). This fact indicates that the antibacterial effect is dependent on the metallic ion, the ligand and the interaction between them (Anacona et al., 1999). Metallic molybdate nanoparticles (Ag2MoO4) demonstrated an antibacterial effect against Gram-positive and -negative strains (Moura et al., 2017b), suggesting the antibacterial activity is related to a particular ion.

In addition to antibacterial activity, some compounds can inhibit the bacterial mechanisms of antibiotic-resistance, enhancing their effect against multidrug-resistant (MDR) bacteria (Nogueira et al., 2014; Coutinho et al., 2009). These compounds enhance the bacterial cell membrane permeability, thus increasing the concentration of the antibiotics inside the cell (Burt, 2004). Synthetic or natural products with the property to inhibit the resistance mechanisms are defined as modulators of the antibiotic activity, being one of the main mechanism involved in this modulation the inhibition of efflux pumps (Tintino et al., 2014; Tintino et al., 2016).

The results of the antibiotic-modulation activity of lead molybdate are demonstrated in Fig. 5. The compound demonstrated a synergism with the gentamicin against S. aureus, reducing the MIC of 16 μg/mL to 10 μg/mL (37.5%). However, against P. aeruginosa and E. coli, the same result was observed: the compound demonstrated an antagonism against norfloxacin and imipenem. In other tested associations, no interactions were observed.

Modulatory effect of the PbMoO4 in association with different antibiotcs: norfloxacin, gentamicin and imipenem in comparision with the effect of these antibiotic alone em Staphylococcus aureus (A), Pseudomonas aeruginosa (B) e Escherichia coli (C). The (*) express the significance level between the treatments, with **** representing p < .0001 when compared to the control.
Fig. 5 Modulatory effect of the PbMoO4 in association with different antibiotcs: norfloxacin, gentamicin and imipenem in comparision with the effect of these antibiotic alone em Staphylococcus aureus (A), Pseudomonas aeruginosa (B) e Escherichia coli (C). The (*) express the significance level between the treatments, with **** representing p < .0001 when compared to the control.

The better modulatory effect of PbMoO4 against the Gram-positive strain can be explained by the cytological differences between them (Andrade, 2013). Gram-positive bacteria present a large cell wall composed by peptidoglycan. The Gram-negative has a thin cell wall but presents a protection formed by lipopolysaccharide in the outer membrane of the bacterial cell. These differences represent an additional barrier against the influx of some substances, as some kinds of drugs (Schaechter et al., 2002; Tortora et al., 2008). By this way, a putative interaction between the Gram-positive cell membrane and the PbMoO4 can be a probable cause of the synergism observed against this bacteria.

Antagonism was observed in the study of Moura et al. (2017b) using Ag2MoO4 in association with Norfloxacin against P. aeruginosa and E. coli. The lead compound possibly chelated the antibiotics or affected their structure, reducing the effect of these drugs (Sousa et al., 2016; Sobral et al., 2016). More assays are necessary to determine the possibility of these last interactions. However, if positive, the use of antibiotics associated with lead compound must be evaluated carefully in persons previously exposed to this metal.

This study described the synthesis and the structural, vibrational, morphological and antibacterial properties of PbMoO4 crystals. Lead molybdate was obtained by the conventional hydrothermal method without the use of surfactants or organic additives. XRD and Rietveld analysis revealed that the PbMoO4 nanocrystals present scheelite-type tetragonal structure. The Raman spectroscopy, revealing the presence of 10 modes, and EDS, showing all expected chemical elements of the molybdate, confirmed the quality of the obtained samples. About the antibacterial activity, the PbMoO4 have not demonstrated a clinically relevant antibacterial effect. However, this compound modulated the antibiotic activity, causing a synergism against Gram-positive bacteria and an antagonism against Gram-negative ones. These results indicated the necessity of more studies about the interaction between lead and antibiotics, mainly to evaluate the risk of the usage by patients exposed to lead.

Acknowledgements

The authors thank CNPq, CAPES and FUNCAP for the financial support and the Central Analítica-UFC by the support.

Conflict of interest

The authors declare that they have no conflict of interest.

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