Cashew-gum-based silver nanoparticles and palygorskite as green nanocomposites for antibacterial applications

Materials Science & Engineering C 115 (2020) 110927

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Cashew-gum-based silver nanoparticles and palygorskite as green nanocomposites for antibacterial applications

T

Cristiany Marinho Araújoa,b, Moisés das Virgens Santanaa, Antonio do Nascimento Cavalcantec, Lívio César Cunha Nunesd, Luiz Carlos Bertolinoe, Carla Adriana Rodrigues de Sousa Britof, ⁎ Humberto Medeiros Barretof, Carla Eirasa, a

Laboratório de Pesquisa e Desenvolvimento de Novos materiais e Sistemas Sensores – MatSens - Departamento de Engenharia de Materiais – Centro de Tecnologia (CT), Campus Ministro Petrônio Portela, Universidade Federal do Piau í-UFPI, Teresina, PI 64049-550, Brazil b Instituto Federal de Educação, Ciência e Tecnologia do Piauí - IFPI, Teresina, PI 64018-900, Brazil c Instituto Federal de Educação, Ciência e Tecnologia do Maranhão – IFMA, Campus Presidente Dutra, Maranhão, MA 65760-000, Brazil d Núcleo de Tecnologia Farmacêutica, Universidade Federal do Piauí – UFPI, Teresina, PI 64049-550, Brazil e Centro de Tecnologia Mineral – CETEM, Cidade Universitária, Ilha do Fundão 21941-908, Rio de Janeiro – RJ, Brazil f Departamento de Parasitologia e Microbiologia, Universidade Federal do Piauí – Campus Universitário Ministro Petrônio Portella, Teresina, PI, Brazil

ARTICLE INFO

ABSTRACT

Keywords: Biopolymer Clay minerals Green synthesis Nanocomposite Antibacterial agent

Nanocomposite materials have been proposed to enhance the properties of different materials. In this study, palygorskite (Pal) clay is proposed as a support matrix for silver nanoparticles stabilised with cashew gum (Anacardium occidentale L.) (AgNPs-CG), producing the Pal/AgNPs-CG nanocomposite, whose bactericidal activity was studied. AgNPs-CG was synthesised using a green method in which CG acted as a reducing and stabilising agent for these nanostructures. AgNPs-CGs were subsequently characterised then adsorbed to the Pal surface, which was previously treated to remove impurities such as quartz. Pal and Pal/AgNPs-CG were characterised by X-ray diffraction, specific surface area, thermal analysis, Fourier transform infrared spectroscopy, scanning electron microscopy, energy dispersive spectroscopy, and transmission electron microscopy. The antibacterial activity assay by the direct contact method showed that the synergistic effect of the combination of AgNPs-CG and Pal increased the bactericidal effect of the nanomaterial compared with the AgNPs-CG activity, reaching a percentage inhibition of up to 70.2% against E. coli and 85.3% against S. aureus. Nanocomposite atoxicity was demonstrated by the Artemia Salina model. Thus, the Pal/AgNPs-CG nanocomposite emerges as a nanomaterial with potential antibacterial applications.

1. Introduction Silver nanoparticles (AgNPs) have been long reported in the literature as antimicrobial agents. In the form of nanoparticles, the antimicrobial activity of silver is increased due to the higher number of particles per unit area (increase of area/surface/volume ratio) [1]. Interest in research using silver as an antimicrobial agent is due to its high toxicity to pathogenic microorganisms among the chemical elements of the periodic table, considering the following sequence (as bulk state): Ag > Hg > Cu > Cr > Pb > Co > Au > Zn > Fe > Mn > Mo > Sn [2], besides their low toxicity to animal cells. Also, AgNPs have been proposed as viable alternatives against antibiotic-resistant bacteria [3,4]. AgNPs have applications in various sectors, such as in water

⁎

purification, catalysis, nanoelectronics, food packaging, biomedicine, biosensors, cosmetics, dressings, catheters, and bone prostheses and nanoplasmonics [5–9]. In pharmacological applications, they are used as antiplasmodial, anticancer, anti-inflammatory, and antifungal agents [10]. AgNPs can be synthesised using a variety of routes, including physical, chemical, photochemical, and biological. Among these routes, “green methods” are attractive because they do not use environmentally aggressive chemical reagents. Green synthesis employs products of natural origin that act as reducing or stabilising agents, providing the final product with antibacterial, antioxidant, and antitumor activity [11,12]. Several biological methods have been proposed for the synthesis of nanoparticles. These methods include the use of microorganisms, enzymes, plant extracts, and plant exudates as possible

Corresponding author. E-mail address: [email protected] (C. Eiras).

https://doi.org/10.1016/j.msec.2020.110927 Received 10 January 2020; Received in revised form 9 March 2020; Accepted 1 April 2020 Available online 03 April 2020 0928-4931/ © 2020 Elsevier B.V. All rights reserved.

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ecologically correct alternatives to conventional methods [13]. Among common exudates, cashew gum (CG) is attractive because it is an acid polysaccharide extracted from the Anacardium occidentale L. tree that has been successfully used in the green synthesis of metallic nanoparticles, especially AgNPs. This biopolymer can act both as a metal reducing agent and a stabilising agent for nanostructures, thus favouring the reduction of the aggregation processes [14,15]. CG polysaccharide also has several biological applications such as antibacterial activity [16], anti-inflammatory activity [17], antidiarrheal activity [18], and application as a film in wound dressings [19]. An additional property of AgNPs reported by medical practitioners is a support matrix capable of the controlled release of these nanoparticles [20]. Another reported limitation is the possible aggregation of these nanoparticles, thus limiting its application [21]. A viable alternative to remedy these issues is to combine AgNPs with other environmentally friendly materials that can act as a nanoparticle support matrix [22]. Clays are attractive support materials for the immobilization of nanoparticles due to their low cost, attractive chemical and physical properties, availability, high surface area, and high thermal and mechanical stability [23]. Also, they have “swelling” and adsorption properties, which rank them as excellent support materials for nanoparticles [24]. Palygorskite (Pal), Si8Mg5O20(OH)2(OH2)4·4H2O, is a hydrated silicate of magnesium and aluminium with reactive hydroxyl groups on the surface [25]. Pal is a non-planar clay mineral with an open channel structure, forming elongated crystals and a fibrous morphology of type 2:1, with a double layer of silicon tetrahedron and a central layer of magnesium, aluminium, or iron octahedron [26,27]. Due to its unique structure, stability, and large surface area, there are several efforts to use Pal in new applications in its natural or modified form [28]. Pal is characterised as a biocompatible and eco-friendly clay mineral [29,30], still having anti-inflammatory properties and non-cytotoxicity, what has allowed its application as gastrointestinal protector [31,32], treatment of renal failure [33] and tuberculosis [34], cosmetic products such as deodorants, creams and shampoos [35]. Pal also has been used in nanoformulations for diclofenac delivery [36]. In this context, the objective of this work was to produce a nanocomposite material with antimicrobial properties using Pal as a support material for AgNPs synthesised by a green method, using CG as a reduction and stabilising agent (Pal/AgNPs-CG nanocomposite). The antibacterial activity of Pal/AgNPs-CG was tested against Gram-positive (Staphylococcus aureus) and Gram-negative (Escherichia coli) bacterial strains. A toxicity test was also carried out using the Artemia salina model.

2.2. Palygorskite (pal) treatment Pal samples were macerated to reduce their size then sieved using a 200 mesh (0.074 mm) screen. Then the samples underwent successive washes with ultrapure water obtained from the Milli-Q system. After each wash, the samples were centrifuged for 3 min at 5000 rpm using a Nova Instruments model NI 1812. The samples then underwent a chemical treatment adapted from the literature [26,38]. In this procedure, aqueous H2O2 (1:2 m/v) was employed to remove impurities and organic matter. Removal was performed by mechanical stirring for 24 h at 100 rpm. The samples were then washed and centrifuged. The supernatant was discarded, and the residue dried in a lyophilizer then macerated, sieved, and autoclaved for 15 min at 121 ± 1 °C. 2.3. Synthesis of silver nanoparticles (AgNPs-CG) and the palygorskite/ silver (Pal/AgNPs-CG) nanocomposite The synthesis of AgNPs-CG was adapted from the procedure outlined by Quelemes et al. (2013). A 0.3% (w/v) CG solution was added to an aqueous solution of AgNO3 (v/v) then heated at 78 ± 2 °C with magnetic stirring for 1 h. The product formed was centrifuged for 3 min at 5000 rpm. Pal was added (0.8 g) to the colloidal AgNPs-CG solution, and the samples were taken to a shaker table where the mixture was stirred at 200 rpm for 24 h. The nanocomposite obtained was centrifuged, the supernatant discarded, and the solid residue oven-dried, macerated and stored protected from light and moisture. 2.4. Characterization of AgNPs-CG, Pal and the Pal/AgNPs-CG nanocomposite 2.4.1. AgNPs-CG spectroscopic characterization Spectroscopic characterization of AgNPs-CG was performed by ultraviolet-visible (UV–Vis) spectroscopy using a Hitachi U-300 spectrophotometer. 2.4.2. Average hydrodynamic size, polydispersion index (PDI) and zeta potential (ζ) The average hydrodynamic size, polydispersion index (PDI) and zeta potential (ζ) of AgNPs-CG were determined by a Dynamic Light Scattering (DLS) technique using a Zetasizer model Nano Series ZS-90 from Malvern Instruments, with a 90° measurement angle, 633-nm HeeNe gas laser, and photodiode detector. Analyses were performed by diluting 1/10 (v/v) suspensions of AgNPs-CG in ultrapure water. 2.4.3. Electronics microscopies The morphology was analysed by Pal in natura and purified Pal were performed by scanning electron microscopy (SEM). Subsequently, in order to evaluate whether the Pal purification process (removal of impurities) was effective, energy dispersive spectroscopy (EDS) analyses were performed, which enable a qualitative and semi-quantitative microanalysis of chemical elements present in the sample. The images were obtained on a Quanta FEG 250 F electron microscope with an energy-dispersive x-ray detector (SEM/EDS) with an acceleration voltage from 1 to 30 kV, equipped with an SDD (silicon drift detector), Ametek, model HX-1001 (Apollo X-SDD detector). In prior analyses, the samples were covered with a thin layer of gold deposited using a Quorum Q150R metalliser for 30 s at 20 mA under an argon atmosphere. Transmission electron microscopy (TEM) was employed to verify the morphology of AgNPs-CG and Pal/AgNPs-CG. The images were obtained using a JEOL model JEM - 2100 with a lanthanum hexaboride (LaB6) filament operating at 200 kV. From the images obtained, counts were made, and the particle size distribution was measured with the aid of ImageJ software. The data obtained in the program were processed using Origin 10.1 software.

2. Materials and methods 2.1. Materials and reagents Pal from Guadalupe, Piauí, Brazil was purchased from the JL company, located at BR-316, 19 km from Teresina, Piauí, Brazil. During the beneficiation process, Pal was acid-activated using sulfuric acid (H2SO4) following the instructions provided by JL. The CG used in the synthesis of silver nanoparticles (AgNPs-CG) was isolated from the exudate of the Anacardium occidentale L. tree, following the procedure described by De Paula et al. (1998) [37]. The collection process occurred in Ilha Grande, Piauí, Brazil, in April 2016. The entire process of isolation and purification was carried out by the Biodiversity and Biotechnology Research Center (BIOTEC), Federal University of Piauí, Ministro Reis Veloso campus, Parnaíba, Piauí, Brazil. All reagents used in the research were analytical-purity grade and were used as received. Hydrogen peroxide (H2O2) was obtained from Merck, Brazil. Silver nitrate (AgNO3) was obtained from Vetec, Brazil. In all experiments, ultrapure water was obtained from a MillliQ system. 2

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2.4.4. X-ray diffraction (XRD) Pal and Pal/AgNPs-CG x-ray diffractograms were obtained using a Shimadzu D6000-RX diffractometer with CuKα radiation (λ = 1.5406 Å), a nickel filter with a voltage of 40 kV, 30 mA current, 2°·min−1 sweep rate, and 2θ in the range 5° to 75°.

transferred to a sterile falcon tube, containing 2000 μg of a solid sample or 2000 μL of a liquid sample. To determine the inhibitory effect, 100 μL of this solution was transferred to Petri dishes containing the MuellerHinton Agar culture medium and seeded with a Drigalski loop using the spread plate method. The plates were incubated in a microbiological oven at 37 °C for 24 h, and the inhibitory effect was determined by CFU counting. All analyses were performed in triplicate. The inhibitory effect produced by each sample analysed was calculated using the following equation:

2.4.5. Specific surface area (SBET) Specific surface area measurements were calculated using the BET method [39] using the adsorption/desorption isotherms of nitrogen at 77 K. Analyses were performed on a Quantachrome (version 10.01). Before the adsorption/desorption measurements, the samples were treated at 200 °C for 12 h under N2 gas flow. Surface area calculations were performed using nitrogen physisorption data, and a linear regression from graphing 1/v[(p/p0)-1] vs (p/p0) and Eq. (1).

VA =

(P0

Vm. Ct .P P )[1 + (Ct

1) P / P0

=

N1

N2 N1

x 100%

(2)

where ƞ is defined as the inhibitory effect, N1 is the arithmetic mean of the colony-forming units of the control plates, and N2 is the arithmetic average of the colony-forming units of each of the tested solutions.

(1)

2.6. Toxicity test

where:

The lethality test against Artemia salina (A. salina) was performed using the procedure described by Meyer [40], with some modifications. All assays were performed in triplicate. Pal and Pal/AgNPs-CG suspensions were prepared at 10.0 mg·mL−1, from which dilutions were obtained (1.0 mg·mL−1, 0.5 mg·mL−1, and 0.1 mg·mL−1). In the test, synthetic seawater (1.0 L) was prepared and used by dissolving the following substances with their respective masses: 15.153 g NaCl, 1.398 g MgCl, 1.888 g MgSO4, 0.652 g CaCl2, 0.414 g of KCl, and 0.116 g of NaHCO3. A. salina hatching was performed using 50 mg of eggs added to 1.0 L of previously prepared synthetic seawater that was sat under artificial illumination and aeration for 48 h. After hatching, ten nauplii (with adequate movement) were separated for each test tube containing the triplicate test concentrations. Synthetic seawater (9.0 mL) and 1.0 mL of the test concentration were added to each tube. A negative control containing only ten nauplii and 10 mL of synthetic seawater was also prepared. After incubation of the tubes, surviving nauplii were counted with a magnifying glass after 24 and 48 h.

Ct = adsorption energy constant; P = pressure; P0 = gas saturation pressure; VA = amount of adsorbed gas (in mL); Vm = amount of adsorption on monolayer (in mL). 2.4.6. Thermal analysis Thermogravimetric analysis/derived thermogravimetric analysis (TG/DTG) and differential scanning calorimetry (DSC) were performed using an SDT Q600 V.20.9 Build TA, model DSC-TGA Standard, under an argon atmosphere with a flow rate of 100 mL·min−1, a heating rate of 10 °C·min−1 and a temperature range from 20 °C to 900 °C. 2.4.7. Fourier transform infrared spectroscopy (FTIR) Fourier transform infrared (FTIR) spectra were recorded on a Perkin-Elmer (USA) Paragon 1000 spectrophotometer using KBr pellets. Measurements were taken in the wavelength range of 4000 to 400 cm−1 during 32 scans and a resolution of 4 cm−1.

3. Results and discussion

2.5. Study of antibacterial activity

3.1. AgNPs-CG characterization

2.5.1. Bacterial strains Bacterial strains of Staphylococcus aureus (ATCC 25923) and Escherichia coli (ATCC 25922) from the collection of microorganisms at the Laboratory of Microbiology Research (LPM) of the Federal University of Piauí - UFPI were used for the study of antibacterial activity.

Fig. 1 presents the UV–Vis, TEM, and size distribution results obtained from the characterization of AgNPs-CG produced via green synthesis. The first evidence of the successful formation of AgNPs-CG was the change in colour of the reaction medium, in which the silver ion solution (AgNO3) changed from colourless to light yellow (colloidal suspension of AgNPs-CG), confirming the reduction of Ag+ to Ag (insert in Fig. 1A). The UV–Vis absorption spectrum (Fig. 1A) confirmed the formation of AgNPs-CG by the presence of an absorption band characteristic of the surface plasmon resonance at 409 nm, which is assigned to the formation of spherically shaped AgNPs, as previously reported in the literature [41,42]. Araruna et al. (2013) [14] and Quelemes et al. (2013) [16] identified maximum absorption bands around 420 nm using cashew gum for silver nanoparticle synthesis. Cashew gum acted as both a silver ion reducing agent and a stabilising agent for the nanoparticles formed in the process of obtaining AgNPs-CG using a green synthesis method, as reported in the literature. This dual role can be explained by the fact that CG is an anionic heteropolysaccharide, derived from OH– groups that involve the surface of nanoparticles [14,17]. The negative charges on OH– create an electrostatic repulsion between the nanoparticles, avoiding the aggregation process [17,43]. Nanoparticles obtained from biopolymers have a large number of hydroxyl groups that can complex with metal ions [17], which is an advantage over the use of conventional synthetic chemical agents, such as macromolecular chains of biopolymers [44,45].

2.5.2. Bacterial inoculum preparation Bacterial cultures were maintained on nutrient agar at 4.0 °C. A bacterial growth loop was transferred from this bacterial culture to a falcon tube containing 3.0 mL of 3% brain heart infusion (BHI) culture medium. The falcon tube sample was incubated at 37 °C for 24 h. From this culture in BHI, a standard bacterial suspension with a density equivalent of 0.5 on the Mac Farland scale, with approximately 1.5 × 108 CFU·mL−1 (Colony Forming Units) was prepared. After this step, serial decimal dilutions were made (in physiological saline solution) with a suspension of 1.5 × 104 CFU·mL−1 for both microorganisms. 2.5.3. Direct contact test The antibacterial activity of Pal, AgNPs-CG, and the Pal/AgNPs-CG nanocomposite was investigated by the direct contact method, following the procedure of Zheng and Zhu [78], the results being expressed in CFU. For the tests, a standardised bacterial suspension was subjected to decimal serial dilutions until 1.5 × 104 CFU·mL−1 in BHI medium was obtained. Then, 2000 μL of this diluted suspension was 3

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Fig. 1. A) Ultraviolet-visible (UV–Vis) absorption spectrum of a colloidal suspension of silver nanoparticles stabilised with cashew gum (AgNPs-CG) (insert shows the colour change after the reaction producing the nanoparticles); B) shows a transmission electron microscopy (TEM) image of AgNPs-CG; C) corresponds to the size histogram obtained from transmission electron microscopy (TEM) data and processed by ImageJ software. D) shows the size histogram obtained by dynamic light scattering (DLS).

classify this system as stable. Finally, it is important to emphasise that the negative charge observed for ζ for AgNPs-CG in an aqueous medium is due to the presence of free hydroxyls from the monosaccharide groups present in the CG, which occur due to the acidic, branched, and anionic character of heteropolysaccharides [16]. Also, the stability of the AgNPs-CG colloidal system may be due to the presence of free hydroxyl groups in the CG structure. These groups can be oxidized in the presence of free electrons. This fact leads to a further reduction of Ag+ to Ag and a better stabilisation of AgNPs-CG, preventing the process of agglomeration of these nanoparticles [49].

The TEM micrographs obtained for AgNPs-CG shown in Fig. 1B corroborate the UV–Vis data concerning the expected spherical shape of these nanoparticles [46,47], since the maximum absorption was observed close to 409 nm. These micrographs also show that AgNPs-CG is dispersed at a moderate interparticle distance, which likely hinders the process of agglomeration. The average diameter distribution of the nanoparticles was determined using 200-nm-scale images (Fig. 1C), counting about 98 nanoparticles. In the supplementary material (Fig. S1), additional TEM micrographs of AgNPs-CG can be viewed. As shown in Fig. 1C, the size of AgNPs-CG follows a normal Gaussian-shaped distribution, with maximum diameters of 5.5 ± 8.94 nm and 12.3 ± 4.53 nm. These results are consistent with the broadband absorption shown in the UV–Vis spectrum, characteristic of polydisperse nanosystems. Dynamic Light Scattering (DLS) was also used to observe the size of the nanoparticles. Fig. 1D shows a histogram of the distribution of AgNPs-CG in which populations range in size from 3 to 10 nm, agreeing with the data obtained by TEM. However, the mean diameter values obtained by DLS (3.8 ± 0.95 nm) were slightly lower (0.9%) than those obtained by TEM. The DLS technique measures the average hydrodynamic diameter, which encompasses the actual diameter and the passivating layer of nanoparticles, thus making more representative measurements of the sample as a whole. In the TEM results, the size distribution was performed only with image magnification and generally corresponded to a small fraction of the total sample, which may explain the difference in the average diameters observed between the two techniques. The polydispersion index (PDI) obtained by DLS was approximately 0.3. According to Costa [79], PDI values between 0.08 and 0.7 are characteristic of systems that show an average polydispersity, per the results found by UV–Vis and TEM in this study. Using DLS, ζ can be determined, which is related to the electrostatic repulsion between the nanoparticles and the stability of the colloidal system. The higher the value of ζ, the greater the stability of the suspension, since the force with which particles repel each other is higher than the natural tendency to aggregate [48]. Thus, ζ for AgNPs-CG, estimated at −33 ± 3.72 mV at pH = 6.7 and 25 °C allows us to

3.2. Characterization of pal in natura, purified pal, and the pal/AgNPs-CG nanocomposite 3.2.1. X-ray diffraction (XRD) To investigate the Pal crystalline structure, the influence of physical and chemical treatments, and the incorporation of AgNPs-CG on the Pal surface, XRD was used, whose diffractograms are shown in Fig. 2. The characteristic diffraction peaks of Pal and quartz (SiO2) are identified with the aid of crystallographic card no. 01–082-1873 and 01–085-0794, respectively, which were obtained from the Joint Committee on Powder Diffraction Standards (JCPDS) database. Pal characteristic peaks and their respective diffraction planes are identified in the samples at 8.4° (110), 12.3° (211), 13.8° (200), 16.3° (130), and 19.7° (121). These peaks are well described in the literature [26,27,50]. The presence of the peak at 2θ = 8.4° is assigned to the 1.05-nm interplanar distance attributed to the basal plane of the Pal structure, that is, to the primary plane of the crystal face [51]. Reflections at 2θ = 13.74°, 16.5°, 19.7°, 20.8°, and 28.1° are assigned to the Si-O-Si groups of crystalline clay layers. The peak at 2θ = 12.3° is assigned to the hydrated sodium cation oxides present between the clay layers. The reflections at 2θ = 21.02°, 26.76°, 36.68°, 39.60°, 42.60°, 50.26°, 55.00°, and 60.10° are due to quartz [26,52]. The high quartz contents are characteristic of the palygorskite of Guadalupe, PI, Brazil. After in natura chemical and physical treatment of Pal, there was a decrease in the intensity of these peaks and a consequent decrease of the quartz 4

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Ag (111)

P Q

P

P Q P

36

38

40

42

44

46

2 (degree)

P Q

Q

Q

Q

Intensity (a.u.)

PP P

Ag (200)

Pal/AgNPs-CG

Purified Pal

Pal in natura

0

10

20

30 2

40 50 degree)

60

70

80

Fig. 2. X-ray diffractogram of (a) Pal in natura, (b) purified Pal, and (c) Pal/AgNPs-CG nanocomposite. (P = Palygorskite, Q = Quartz and Ag = Silver).

content in the purified Pal. The presence of other impurities was also detected, which was confirmed by EDS analysis (Figs. S1 and S2). The peaks present in the Pal/AgNPs-CG nanocomposite (blue curve, Fig. 2) are almost identical to the peaks observed in the in natura Pal and purified Pal samples, showing small displacements. This behaviour suggests that the structure of Pal is preserved after its modification with AgNPs-CG. The Pal/AgNPs-CG diffractogram shows a rapid decrease in the crystalline profile when compared with the Pal diffractogram. Also, after incorporation of AgNPs-CG, new discrete reflection peaks are observed, such as peaks at 2θ = 38.1° (111) and 44.2° (200), which correspond to the centre-faced cubic crystals of silver, according to JCPDS 04–0783. These results indicate the incorporation of nanoparticles on the clay surface, which is later confirmed by the FTIR and TEM results (Figs. 3 and 4, respectively).

Transmittance (a.u.)

3432

630

1645

646

CG 3404

2927

1649 1270 1122

882 777 1040 1082

Purified Pal 3266 3370

3543

1665 1104

3400 3707

3.2.2. Fourier-transform infrared spectroscopy (FTIR) Fig. 3 shows the FTIR spectra obtained for CG, AgNPs-CG, Pal, and the Pal/AgNPs-CG nanocomposite. In the CG FTIR spectrum (red curve, Fig. 3), that is, of the biopolymer used in the synthesis of AgNPs-CG, a broadband at 3404 cm−1 is observed due to the stretching vibrations of the OeH bonds present in the CG hydroxyl groups [17]. The absorption bands at 2927 cm−1 and 1649 cm−1 are respectively attributed to the CeH bond stretching vibrations and angular deformation of the OeH plane of the monosaccharide units (galactose, glucose, glucuronic acid, rhamnose, and arabinose) or water present in the biopolymer structure [53]. The band at 1270 cm−1 is due to the stretching of CeO groups in the carboxylic acids bonded to the aromatic ring. The bands at 1040 cm−1, 1082 cm−1, and 1122 cm−1 are assigned to C-O-C glycosidic bonds, as well as OeH bonds of alcohols [16]. The bands at 777 cm−1 and 646 cm−1 correspond to the out-of-plane deformations in the OH– groups [14]. In the AgNPs-CG spectrum (black curve), the bands previously observed for CG at 3404 cm−1 and 1649 cm−1 shift to 3432 cm−1 and 1645 cm−1, respectively, due to the interaction of silver with the

AgNPs-CG

470 450 1030

3404

Pal/AgNPs-CG

1419

3624 3543

650 419

370

-1

Wave number (cm ) Fig. 3. Fourier transform infrared (FTIR) spectra of silver nanoparticles stabilised with cashew gum (AgNPs-CG) obtained via green synthesis and the Pal/ AgNPs-CG (Pal is palygorskite) nanocomposite. For comparative purposes, the FTIR of CG and Pal is also shown. (For interpretation of the references to colour in this figure, the reader is referred to the web version of this article.)

biopolymer. More significant evidence of this interaction is observed in the AgNPs-CG spectrum below 1300 cm−1. This behaviour suggests that the primary interaction between AgNPs and CG occur through OH groups since the 777 cm−1 and 646 cm−1 bands observed in CG correspond to the out-of-plane deformation of these groups [14]. In the FTIR spectrum for purified Pal (Fig. 3, violet curve), it is 5

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Fig. 4. Scanning electron microscopy (SEM) micrographs of palygorskite (Pal) in natura (A and B) and purified Pal (C and D) enlarged to 20,000× and 100,000×, respectively.

observed that the bonds present in its crystalline structure correspond to three types of interactions between water and clay: 1) coordinated or crystalline water that binds the magnesium ions to the hydroxyls in the octahedral sheet, 2) zeolitic water located in the channels that interact with coordinated water and the octahedral leaf, and 3) water physically adsorbed on the clay surface [54]. The bands at 3543 cm−1, 3400 cm−1, and 3370 cm−1 are water molecules present in the octahedral leaf terminal positions (coordinated water) and the water molecules present in the Pal channels (zeolitic water). These bands are also attributed to OH stretching in the Al-Mg-OH or Al-Fe+3-OH present in Pal groups [55]. The band observed at 1655 cm−1 is caused by the deformation of zeolitic water, adsorbed and coordinated [56]. The band at 1030 cm−1 refers to the stretching vibration of the SieO bond in the tetrahedral sheet [57]. The bands at 450 cm−1 and 470 cm−1 refer to the AleO stretching vibrations and O-Si-O strain on the tetrahedral sheet [58]. In the Pal/AgNPs-CG FTIR spectrum (blue curve, Fig. 3) changes in intensity, displacement, and the appearance of new bands are observed when compared with isolated spectra of the materials that make up the nanocomposite. In the region between 3624 cm−1 and 3404 cm−1, it is possible to observe a reduction in the intensity of the stretching bands of the OeH groups. This behaviour is caused by the intermolecular interactions between the OeH groups in CG that bind with metals (Fe, Al, and Mg) present in the Pal structure, reinforcing the formation of the Pal/AgNPs-CG nanocomposite. Besides, the Pal bands observed at 3543, 3400 and 3370 cm−1 shift to 3707, 3624 and 3543 cm−1 respectively, due to the interaction with AgNPs-CG. In the Pal/AgNPs-CG spectrum, a new band was observed at 650 cm−1 and may be related to the stretching vibration of zeolitic and adsorbed water bound to the Mg present in the octahedral sheet in the region of the Pal canal ends [59].

3.2.3. Morphological characterization of Pal and Pal/AgNPs-CG nanocomposite Before examining the nanocomposite morphology, we investigated the effect of the Pal purification process on its morphology using SEM (see Fig. 4). In addition to this study, analyses were performed by EDS seeking to clarify the composition of the clay mineral after the purification process (Supplementary Material, Figs. S2 and S3). Finally, the incorporation of AgNPs-CG on the Pal surface was confirmed by TEM (see Fig. 5). The SEM micrographs, Fig. 4, show that in natura Pal has a fibrous structure and can appear as agglomerates of tapes and needles of varying sizes. Such results are in agreement with the studies described in the literature [60,61]. Purified Pal presented little difference in its morphology, maintaining the tendency to form irregular agglomerates and distribution of its fibres. Pal fibre agglomerates may be caused by impurities and organic matter still present in the clay, or due to the dehydration process in the Pal drying process [62]. A summary of the results obtained from the EDS analyses (Figs. S2 and S3) are presented in Table 1, where a reduction in the concentration of K, Ca, and Fe can be seen, which are generally reported as impurities present in Pal. An increase in the intensity of the peaks related to O and Mg, which are among the main constituents (Si, O, Mg, and Al) of this clay are also seen. Although the EDS technique is semi-quantitative, it is observed that the Pal purification process is successful and promotes a decrease in the number of impurities present in Pal in natura. Fig. 5 shows the TEM micrographs of the Pal/AgNPs-CG nanocomposite in various amplifications. Pal fibbers present in nanocomposite have size varying between 200 and 500 nm and average diameter around 10–25 nm, as well as observed in other studies

6

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Fig. 5. Transmission electron microscopy (TEM) images of the Pal supporting the silver nanoparticles stabilised with cashew gum (Pal/AgNPs-CG) nanocomposite. A) and B) show magnifications that allow observing the nanocomposite aggregates. C) and D) show more details of the material.

[63,64]. The Pal/AgNPs-CG nanocomposite keeps this same format; however, AgNPs appears decorating its surface after nanocomposite synthesis. These rods and nanoparticles can appear as aggregates depending of sample preparation. Besides, most silver nanoparticles are found to be adsorbed on the Pal fibres. These results corroborate the data obtained by XRD, FTIR, and thermal analysis (Fig. 6), which confirm that there are interactions between Pal and AgNPs-CG during the formation of the Pal/AgNPs-CG nanocomposite.

physical and chemical treatment processes, the surface area increased from 106.3 m2·g−1 to 118.5 m2·g−1. The surface area value found for Pal increased after impurities were removed (confirmed by the XRD and EDS results). According to the literature, Pal sourced from the Guadalupe-PI region has a specific area of ~113 m2/g [61], corroborating the results obtained here. This high specific surface area is due to the combination of microcrystals on the Pal structure and its fibrillar morphology and small grain size. The increase in the surface area observed after the Pal purification process may be due to the cleanliness of the channels and the elimination of aggregate impurities such as carbonates, quartz, mica, smectites, and feldspars [51]. The treatment performed for Pal in natura possibly aids the disintegration of Pal particles, leading to the formation

3.2.4. Specific surface area (SBET) Table 2 shows the results obtained in determining the surface area of Pal in natura, purified Pal, and the Pal/AgNPs-CG nanocomposite. The results listed in Table 2 show that after Pal in natura passed the

Table 1 Elements present in the structure of Pal in natura and purified Pal (obtained by EDS).

Pal in natura Elements Oxygen Magnesium Aluminum Silicon Potassium Iron Calcium

% mass 45.5 3.3 9.6 27.0 3.5 7.9 3.2

% atomic 61.3 3.0 7.6 22.1 1.9 3.1 1.0

% error 8.3 7.7 5.9 5.2 3.7 2.2 3.9

Purified Pal % mass % atomic 54.4 68.7 4.6 3.8 9.0 6.8 23.7 17.8 2.0 1.0 4.4 1.6 0.6 0.3

% error 7.8 7.3 5.9 5.2 3.9 2.6 4.1

Potassium, Iron and calcium are among the main impurities found in Pal and their values are reduced after purification (highlighted in yellow).

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85ºC

7%

90

0.06

484ºC

196ºC

0.04 7.3%

0.02

85

0.7

294 ºC

0.6

0.08 DTG (%/ºC)

95

241 ºC

100

Mass loss (%)

Mass Loss (%)

0.10

2.5% 1.8%

80

0.5 0.4

60

0.3

40

0.2

80 ºC

0.1 20

0.00

0.0

80 0

A

DTG (%/ºC)

708ºC

100

200

400

600

800

1000

B

0

200

Temperature (°C)

400

600

800

1000

800

1000

Temperature (ºC)

0.10

100

700ºC

1.6% 1.9%

Endo 1.2%

10

0.08

0

90

84 ºC

0.04

294 ºC 484 ºC 7.0% 763 ºC

85

0.4%

C

241ºC

80 0

200

400

600

800

0.02

Heat flow (mW)

0.06

5.6 %

DTG (%/ºC)

Mass loss (%)

95 -10 -20 -30

CG Pal Pal/AgNPs-CG

-40 -50

0.00

D

1000

0

200

400

600

Temperature (ºC)

Temperature (ºC)

Fig. 6. Thermogravimetric/differential thermogravimetric (TG/DTG) curves for A) Pal, B) CG and C) Pal/AgNPs-CG. D) shows the differential scanning calorimetry (DSC) results obtained for these systems. (Pal is Palygorskite, AgNPs-CG is silver nanoparticles stabilised with cashew gum.)

loss (7.3%) for Pal is observed at a Tm of 708 °C and is attributed to the dehydroxylation processes of the Pal Mg-OH groups [68]. In this temperature range, the elimination of water molecules is accompanied by partial destruction of the Pal structure. Another point to be considered in the fourth mass loss is the release of carbon dioxide, since above 500 °C the carbonates present in Pal are thermally unstable, and their decomposition releases CO2 [69]. It is noteworthy that studies conducted with Pal extracted from different geographic regions suggest that the thermal behaviour may vary with Pal's physicochemical properties, as well as with its origin and quantity of impurities [60]. The TG/DTG curve for the Pal/AgNPs-CG nanocomposite (Fig. 6C) shows six phases of mass loss. The first mass loss of 1.6% occurred at Tm = 84 °C, which is attributed to the loss of physically adsorbed molecules on the Pal surface and a portion of the zeolitic water. The second and third mass loss of 1.9% and 1.2% for Pal/AgNPs-CG occurs at the Tm of 241 °C and 294 °C, respectively, and are attributed to CG decomposition (also shown in Fig. 6B), generating H2O, CO, and CH4 [70,71]. Also, the change from an endothermic to exothermic processes is observed at Tm = 241 °C, suggesting interactions between CG and AgNPs. The fourth mass loss of 5.6% for the nanocomposite occurs at Tm = 484 °C, equivalent to the maximum temperature shown by the Pal TG curve, which is due to the loss of coordination water molecules and condensation of silanol and aluminol groups. The fifth mass loss of 7.0% at Tm = 703 °C occurs due to dehydroxylation of the Mg-OH groups, elimination of water and carbonate molecules, as described above for the Pal TG curve. The sixth mass loss observed at Tm of 761 °C (which starts at 700 °C) is due to the crystalline phase formation of Pal, such as olivine (Mg2SiO4), spinel (MgAl2O4), enstatite (MgSiO3), sillimanite (Al2SiO5), and cristobalite (SiO2) [72]. Table S1 (supplemental material) shows a summary of all TG/DTG events occurring for Pal, CG, and the Pal/AgNPs-CG nanocomposite. All values of initial temperature (Ti), final temperature (Tf), and mass loss for the Pal/AgNPs-CG nanocomposite are lower than the values obtained for Pal. These results prove that, besides the nanocomposite

Table 2 Specific surface area values for Pal in natura, purified Pal, and the Pal/AgNPs-CG nanocomposite. Sample

Surface area (m2·g−1)

Pal in natura Purified Pal Pal/AgNPs-CG

106.3 118.5 69.4

of more available spaces for nitrogen adsorption [65,66]. For the Pal/ AgNPs-CG nanocomposite, a considerable decrease in specific surface area (almost half) was observed when compared to Pal, whether purified or not. This result was probably due to AgNPs-CG on the Pal surface, thus preventing the entry of nitrogen molecules into the clay pores [67]. The results obtained by TEM reinforce these conclusions. 3.2.5. Thermal analysis by thermogravimetry/derived thermogravimetry (TG/DTG) and differential scanning calorimetry (DSC) The thermogravimetric analysis (TG) and derived thermogravimetry (DTG) curves show information about the thermal stability of the samples in the decomposition process. Differential scanning calorimetry (DSC) analysis provides information on the chemical and physical processes involving energy variations. Fig. 6 shows TG/DTG curves for Pal (Fig. 6A), CG (Fig. 6B), and Pal/ AgNPs-CG (Fig. 6C). Fig. 6D shows the DSC results for all these systems. Pal's TG/DTG curve (Fig. 6A) shows four major mass losses: the first 2.5% mass loss occurs at a maximum temperature (Tm) of 85 °C, which corresponds to the loss of water molecules physically adsorbed, and a part of zeolitic water (located in the channels of Pal). The second mass loss of 1.8% occurs with a Tm of 196 °C, which corresponds to the thermal dehydration of the remaining zeolitic water of the Pal structural layer. The third mass loss (approximately 7%) occurs at Tm = 484 °C and is attributed to the coordination water loss linked to Pal's octahedral sheet ions and structural hydroxyls, as well as the condensation of silanol and aluminium groups [26]. The fourth mass 8

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Table 3 The inhibitory effect on bacterial growth of E. coli (ATCC 25922) and S. aureus (ATCC 25923) promoted by the Pal/AgNPs-CG nanocomposite and their constituents. (Pal = palygorskite; AgNPs-CG = silver nanoparticles stabilised with cashew gum.) Samples

Saline solution (control) Pal AgNPs-CG Pal/AgNPs-CG ⁎

Inhibitory effect (%) E. coli (UFC/mL – %)

S. aureus (CFU/mL - %)

0.0 0.0 64.7 ± 1.23 70.2 ± 1.34⁎

0.0 0.0 43.1 ± 0.82 85.3 ± 1.62⁎

Statistically significant by Student's t-test (p < 0.05).

and 245 °C and 245–302 °C, with a maximum temperature of 241 °C and 294 °C, respectively, corroborating the CG data obtained using TG/ DTG. 3.3. Evaluation of the antibacterial activity of the Pal/AgNPs-CG nanocomposite The antibacterial activity of the Pal/AgNPs-CG nanocomposite was evaluated by the direct contact method against E. coli (gram-negative) and S. aureus (gram-positive). The results are presented in Fig. 7 and Table 3. For comparative purposes, the inhibitory effect of AgNPs-CG and Pal also was evaluated. From the results shown in Fig. 7, we can see that Pal has no inhibitory effect against E. coli (Fig. 7C) or S. aureus (Fig. 7D) when compared with the control groups (Fig. 7A and B, respectively). It is possible that the presence of Pal in the culture medium favours the growth of a larger amount of CFUs compared with the control groups, probably due to the occurrence of impurities and organic matter that was not completely removed during the purification process. On the other hand, AgNPs-CG inhibits the growth of E. coli (Fig. 7E) at 64.7% and S. aureus (Fig. 7F) at 43.1%. The lower AgNPs-CG activity (Table 3) observed against S. aureus can be explained by the fact that these bacteria have a thicker cell wall (composed of peptidoglycan) when compared with the cell wall of gram-negative bacteria. Therefore, the gram-positive bacterial cell wall has greater physical protection, which may hinder the action of AgNPsCG on its cell wall. The peptidoglycan layer in gram-negative bacteria is thinner, favouring faster action of AgNPs-CG on the cell wall of these bacteria, leading to inactivation or alteration of the bacterial protein structure that leads to cell death [73]. A surprising effect was observed when AgNPs-CG were incorporated into Pal as a support matrix, generating the nanocomposite of interest. The synergistic effect between these nanomaterials increased the bactericidal activity previously observed for AgNPs-CG. The inhibitory effect of the nanocomposite against E. coli was 70.2% (Fig. 7G) while for S. aureus, it was 85.3% (Fig. 7H), almost double that observed when AgNPs-CG were used alone. Although the mechanisms of action between the nanocomposite and bacterial strains are not entirely understood, it is believed that the increased bactericidal effect against S. aureus may be related to the controlled release of AgNPs-CG from their support matrix (Pal) onto the membrane of these microorganisms. The high Pal surface area facilitates the contact of the nanocomposite with bacteria, improving the action of the AgNPs-CG. In Lyu et al. [74] study, the authors synthetized AgNPs using amylose and added curcumin to increase the antibacterial effect, reaching an approximate 50% for S. aureus and 70% for P. aeruginosa (gram-negative, as well as E. coli), even when the concentration of antibacterial reagents was increased. In the study by Menazea et al. [75] the antibacterial activity of selenium/carbonated hydroxyapatite/ ε-polycaprolactone fibres coated with AgNPs was 45% against E. coli

Fig. 7. Inhibitory effect of Pal/AgNPs-CG nanocomposite against gram-positive and gram-negative bacteria. The left column shows the results obtained using an E. coli strain (ATCC 25.922): A) control; C) Pal vs E. coli; E) AgNPs-CG vs E. coli and G) Pal/AgNPs-CG vs E. coli. The right column shows the results obtained using S. aureus strain (ATCC 25.923): B) control; D) Pal vs S. aureus; F) AgNPs vs S. aureus; H) Pal/AgNPs-CG vs S. aureus. (Pal = palygorskite; AgNPsCG = silver nanoparticles stabilised with cashew gum.)

formation, there is an improvement in thermal stability after modification of Pal with silver nanoparticles. At the end of the thermal analysis, the amount of total residual mass of the Pal/AgNPs-CG nanocomposite was 82.3%, higher than Pal (81.4%). In DSC analysis, Fig. 6D, Pal shows four low-intensity endothermic peaks, the first being observed between 120 and 230 °C (Tmax ~196 °C), the second between 230 and 526 °C (Tmax ~484 °C), and the third between 566 and 756 °C (Tmax ~708 °C). These peaks corroborate the results obtained from the mass loss on the Pal TG/DTG curve. The DSC curve of the Pal/AgNPs-CG nanocomposite (Fig. 6D) shows the four endothermic peaks also reported for Pal DSC, as well as two other CGrelated peaks, which occurred in the temperature range between 117 9

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Table 4 Toxicity test results (in triplicate) against A. salina using Pal, AgNPs-CG and Pal/AgNPs-CG. Concentration

Number of living A. Salina (n) Pal

Controla 0.1 mg·mL−1 0.5 mg·mL−1 1 mg·mL−1 5 mg·mL−1 10 mg·mL−1 0.1 mM 0.01 mM 0.001 mM a

Pal/AgNPsCG

AgNPs-CG

t = 24 h

t = 48 h

t = 24 h

t = 48 h

t = 24 h

t = 48 h

10 10 10 10 10 10 – – –

10 ± 0.0 9 ± 0.33 9 ± 0.33 9 ± 0.33 9 ± 0.33 9 ± 0.33 – – –

10 10 10 10 10 10 – – –

10 ± 0.0 9 ± 0.33 9 ± 0.33 9 ± 0.33 9 ± 0.33 9 ± 0.33 – – –

10 ± 0.0 10 ± 0.0 10 ± 0.0

10 ± 0.0 10 ± 0.0 9 ± 0.33

± ± ± ± ± ±

0.0 0.0 0.0 0.0 0.0 0.0

± ± ± ± ± ±

0.0 0.0 0.0 0.0 0.0 0.0

Control: Artificial saline solution.

and 43% against S. aureus. Comparing these results with those obtained in this work, it is evident that the Pal/AgNPs-CG nanocomposite is an excellent candidate for antibacterial applications. The zeta potential (charge) of Pal/AgNPs-CG nanocomposite in solution is −12.2 mV (pH = 6.7), thus presenting a negative surface charge. This value is less than that observed for AgNPs-CG (−33 ± 3.72 mV), since the free hydroxyls previously present in AgNPs-CG are now interacting with Pal surface during the nanocomposite formation. The negative charge may have favored an electrostatic interaction of the nanocomposite with the cell wall of S. aureus (positively charged), causing structural changes and degradation, leading these cells to death [76]. However, while negative charge may contribute, there are many other properties in nanocomposite that can assist in antibacterial activity. For a more detailed elucidation of the action mechanisms, further studies should be carried out.

applications in biotechnology and related applications. CRediT authorship contribution statement Cristiany Marinho Araújo:Conceptualization, Data curation, Investigation, Methodology, Writing - original draft, Writing - review & editing.Moisés das Virgens Santana:Data curation, Investigation, Methodology.Antonio do Nascimento Cavalcante:Data curation, Investigation, Methodology, Visualization, Writing - review & editing.Lívio César Cunha Nunes:Methodology, Validation, Supervision, Writing - review & editing.Luiz Carlos Bertolino:Data curation, Investigation, Methodology, Visualization, Validation.Carla Adriana Rodrigues de Sousa Brito:Data curation, Methodology, Validation, Investigation.Humberto Medeiros Barreto:Data curation, Investigation, Methodology, Validation, Writing - review & editing.Carla Eiras:Conceptualization, Data curation, Investigation, Funding acquisition, Methodology, Project administration, Resources, Supervision, Visualization.

3.4. Toxicity test with Artemia salina (acute toxicity test) The bioassay with A. salina nauplii is considered useful for preliminary general toxicity assessments and is widely used because it is low cost and fast [77]. Results on the exposure of Artemia salina at different concentrations of Pal and Pal/AgNPs-CG nanocomposite are shown in Table 4. In Table 4, it can be seen that no death of A. Salina nauplii occurred after the first 24 h in the five concentrations tested when Pal or Pal/ AgNPs-CG were used. After 48 h, only one A. saline nauplii died for both samples tested. Due to the high survival rate of organisms exposed to the samples and concentrations tested, it was not possible to calculate the lethal dose 50% (LD50%). Through the test performed, it is possible to suggest that the proposed nanocomposite presents low toxicity or is nontoxic since the LD50 > 10 mg·mL−1. According to the World Health Organization (WHO), toxic substances are those with LD50 values below 1000 ppm [52].

Declaration of competing interest The authors declare that they have no known competing financial interests or personal relationships that could have appeared to influence the work reported in this paper. Acknowledgements The authors would like to thank the Coordination for the Improvement of Higher Education Personnel (CAPES), National Council for Scientific and Technological Development (CNPq) for the financial support received through the process 431275/2018-1 (Call MCTIC/ CNPq No. 28/2018 - Universal/Range B) and the Research Productivity Grant process 311802/2017-6 (Call CNPq No. 12/2017). Authors also thank to Foundation for Research Support of Piauí (FAPEPI) for their financial support and the Federal University of Piauí (UFPI) and Federal Institute of Piauí (IFPI) for providing working and research conditions.

4. Conclusion The present study proposes a green synthesis and characterization of a new nanocomposite based on palygorskite and silver nanoparticles reduced and stabilised with cashew gum (Pal/AgNPs-CG). The AgNPsCG were adsorbed on the Pal surface, which acts as a support matrix for the nanoparticles. The incorporation of AgNPs-CG into Pal considerably increases the thermal stability and bactericidal effect of this nanocomposite against E. coli and S. aureus bacteria. For S. aureus, the inhibitory effect is 85.3% when Pal/AgNPs-CG is used, almost double that observed for AgNPs-CG (43.1%). A preliminary toxicity test using A. salina nauplii shows that the proposed nanocomposite has low toxicity. Therefore, this material is an excellent candidate for antimicrobial

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