Review Article | Open Access
Carlos Enrique Escárcega-González, Javier A. Garza-Cervantes, Augusto Vázquez-Rodríguez, José Rubén Morones-Ramírez, "Bacterial Exopolysaccharides as Reducing and/or Stabilizing Agents during Synthesis of Metal Nanoparticles with Biomedical Applications", International Journal of Polymer Science, vol. 2018, Article ID 7045852, 15 pages, 2018. https://doi.org/10.1155/2018/7045852
Bacterial Exopolysaccharides as Reducing and/or Stabilizing Agents during Synthesis of Metal Nanoparticles with Biomedical Applications
Bacterial exopolysaccharides (EPSs) are biomolecules secreted in the extracellular space and have diverse biological functionalities, such as environmental protection, surface adherence, and cellular interactions. EPSs have been found to be biocompatible and eco-friendly, therefore making them suitable for applications in many areas of study and various industrial products. Recently, synthesis and stabilization of metal nanoparticles have been of interest because their usefulness for many biomedical applications, such as antimicrobials, anticancer drugs, antioxidants, drug delivery systems, chemical sensors, contrast agents, and as catalysts. In this context, bacterial EPSs have been explored as agents to aid in a greener production of a myriad of metal nanoparticles, since they have the ability to reduce metal ions to form nanoparticles and stabilize them acting as capping agents. In addition, by incorporating EPS to the metal nanoparticles, the EPS confers them biocompatibility. Thus, the present review describes the main bacterial EPS utilized in the synthesis and stabilization of metal nanoparticles, the mechanisms involved in this process, and the different applications of these nanoparticles, emphasizing in their biomedical applications.
1. Generalities of Exopolisaccharides (EPSs)
Microbial exopolysaccharides (EPSs) are biopolymers produced and secreted by microbial cells to the extracellular medium, forming a capsule or slime loosely attached to the cell surface . These compounds can be soluble or insoluble polymers released into the surrounding environment to accumulate outside the cells [2, 3]. Thus, they can be encountered attached to the microbial cell surface or within the fermentation medium . Synthesis of EPSs is important to microbial cells since EPSs play crucial biological roles in their survival. Among these functions include cell protection, attachment to solid surfaces, cell aggregation, and cell-cell interactions [4, 5]. There are various groups of microorganisms that can produce EPS; bacteria (including extreme and marine bacteria) [4–6], cyanobacteria , fungi and yeasts , and microalgae . Some of the most studied EPSs produced by microorganisms are xanthan, dextran, alginate, gellan, levan, cellulose, curdlan, pullulan, succinoglycan, and hyaluronic acid [9–11]. In this context, based on their functionality, EPSs have been classified in the following categories: constructive or structural, sorptive, surface active, informative, redox active, and nutritive . Moreover, EPSs from extreme bacteria possess unique and specific properties of interest since metabolic products from these types of bacteria have evolved to adapt to extreme environmental conditions .
The structure of EPSs is mainly conformed of carbohydrates such as monomers of D-glucose, D-galactose, D-mannose, L-fucose, L-rhamnose, D-glucuronic acid, D-galacturonic acid, L-guluronic acid, D-mannuronic acid, N-acetyl-D-glucosamine, and N-acetyl-D-galactosamine, as well as noncarbohydrate components that confers an anionic nature to the EPSs such as carboxyl, phosphate, sulfate, and pyruvate substituents [10, 13–16]. In addition of the negative charge, these organic groups increase the lipophilicity of the EPSs and have influence in the interaction with other polysaccharides and cations . The structure of some microbial EPSs is shown in Figure 1.
2. Main Bacterial EPSs
Xanthan gum is a heteropolysaccharide EPS produced by the genus Xanthomonas and is the first natural biopolymer produced at an industrial scale [10, 17]. Dextran is a homopolysaccharide composed of α-glucans and produced by the Leuconostoc, Streptococcus, and Lactobacillus genera [10, 18]. Curdlan is a nonbranching linear polysaccharide composed of β-glucan and produced by Alcaligenes faecalis . Gellan gum is a sphingan heteropolysaccharide synthesized by the genera Sphingomonas and is composed of acetyl and glyceryl substituents . Cellulose is another β-glucan that can be produced by the genera Gluconacetobacter, Agrobacterium, Aerobacter, Achromobacter, Azotobacter, Rhizobium, Sarcina, and Salmonella . Levan is a homopolyfructose-branched EPS produced by microorganisms from the genera Zymomonas, Pseudomonas, Mycobacterium, Corynebacterium, Erwinia, Bacillus, and Azotobacter [22, 23]. Succinoglycan is a biopolymer composed of one galactose and seven glucose residues with succinyl, acetyl, and pyruvyl as nonsaccharide substituents; this EPS has been found to be produced by some genera such as Rhizobium, Alcaligenes, Pseudomonas, and Agrobacterium [10, 24]. Other more recent bacterial EPSs that have been reported are FucoPol, a heteropolysaccharide produced by Enterobacter A47, which is composed of fucose, galactose, glucose, and glucoronic acid with the nonsaccharide substituents pyruvate, succinate, and acetate  and GalactoPol, a polysaccharide produced by Pseudomonas oleovorans aNRRL B-14682 mainly formed by galactose and other saccharides as glucose, mannose, and rhamnose in lower amounts . Both of these EPSs are obtained by their respective bacteria using glycerol as sole carbon source. The information of this section is summarized in Table 1.
3. Application of EPSs
Many areas such as chemistry, food, cosmetics, hydrocolloids, pharmaceuticals, medicine, packaging industries, textiles, detergents, adhesives, agriculture, wastewater treatment, and nanotechnology have benefited from the use of EPS [2, 10, 27]. These industrial areas have taken advantage of the properties of EPS to elaborate many different products; such as adhesives, absorbents, lubricants, rheology modifiers, viscosifiers, emulsifiers, chelating agents, biomaterials intended to serve as drug delivery vehicles encapsulating bioactive biomolecules, anticancer agents, imaging, tissue engineering, antimicrobial agents, and as a reducting and stabilizer agent in the synthesis of metal nanoparticles [2, 6, 28–32]. Moreover, EPS have been reported to be generally recognized as safe (GRAS) compounds, meaning that they do not represent a health risk in their use . Due to these properties, other applications of EPS are currently being explored, among them are sorption, their use in the removal of toxic metals and carbon dioxide [34, 35], improving activated sludge settleability , and designing aqueous foams with clay nanoparticles to avoid the emission of volatile organic compounds during oil or gasoline loading and storage . In regard to this, EPS from marine microorganism have also been found to have interesting properties such as good antioxidant activity [38, 39], blocking effect to avoid the adherence of gastrointestinal pathogens, anticancer and antiviral effect in human cell lines [40–42], restoration of bone integrity, and anticoagulant properties . Thus, as described in this section, EPSs offer a wide range of applications. In this review, we focus on the ability of bacterial EPSs to act as reducing and stabilizing agents during the synthesis of metallic nanoparticles for applications in biology and the medical field.
3.1. EPS Used in the Synthesis of Metal Nanoparticles
Metal nanoparticles have been the target of research within the last two decades, since they have been found to have different and enhanced properties when compared to those exhibited by the bulk metals . These nanoparticles also present high reactivity due to their crystallographic surface structure and large surface area . All of these properties allow for metallic nanoparticles to be applied in areas such as medicine, electronics, environment, agriculture, health care, and pharmaceutical products.
There are physical, chemical, and biological methods to produce and synthesize metal nanoparticles. Biological methods or green synthesis mainly use plant extracts. Fungal and bacterial strains and their cultures have been explored recently since they provide an environmentally friendly and cost-effective synthesis platform that employs nontoxic reagents and procedures . Green synthesis has been used to elaborate many different metal nanomaterials such as Ag, Au, Zn, Ti, TiO2 Ni FeO, Fe3O4, Cu, Co, Pd, Ba, CdS, and Pt nanoparticles [47–51]. Thus, much emphasis has been placed in the discovery of effective reducing and stabilizing agents to synthesize metallic nanoparticles. In this context, EPSs contain various functional groups in their structure that can serve as reductive and stabilizing agents in the synthesis of metal nanoparticles by a chelating and capping process . These processes allow control on size, shape, and particle dispersion . Further, during synthesis of metal nanoparticles in the presence of EPSs, their mucoadhesion properties lead to a neutral, low surface energy and low level of nonspecific protein receptor recognition capping, making these nanoparticles more adequate to utilize in broader applications . A general representation of possible interactions between EPS and metal ions to form metal nanoparticles is shown in Figure 2.
In this context, it is important to mention that in most cases in which EPSs are utilized to synthesized metal nanoparticles, the EPSs act both as a reducing and stabilizing agents at the same time due to their properties and structures with many functional groups; which consequently make EPSs suitable and advantageous to produce metal nanoparticles destined to be applied in the biomedical sciences [53–57]. However, there are also studies in which metal nanoparticles are produced with other reducing agents or other reducing methods, where the EPSs act only as a stabilizing or capping agent [58–60].
3.2. Differences between Polysaccharides and Exopolysaccharides in the Preparation of Metal Nanoparticles
There are differences between commercial polysaccharides and extracted microbial exopolysaccharides, mainly regarding their composition. As mentioned previously, polysaccharides are mainly composed by carbohydrates. Cellulose, as well as starch, is composed by D-glucose; alginate is composed by β-D-mannuronate and α-L-guluronate; carboxymethyl cellulose is a polymer of D-glucose with carboxymethyl groups bonded to the hydroxyl groups; pectin is mainly composed by galacturonic acid, linked to other components as acetic acid, D-apiose, glucorinic acid, etc. Polysaccharides have many functionalities, which include the capability of their hydroxyl groups and hemiacetal ends to reduce metal precursor salts . Metallic nanoparticles synthesized with polysaccharides are often reduced in alkaline conditions to achieve better pH conditions for the synthesis or to hydrolyze the polysaccharide to increase the amount of available reducing sugars [62, 63].
On the other hand, exopolysaccharides, besides being composed primarily of carbohydrates, may have organic and inorganic substituents, as shown in Table 2 . Some EPS of cyanobacteria are mostly heteropolysaccharides, containing S functional groups linked to the sugar backbone . Similarly, there are reports of carbohydrate backbones containing S in their chemical composition in the EPS of some Bacillus strains [66, 67]. There are some N-acetylamino sugars that have been not found in commercial microbial polysaccharides . The introduction of these amino functionality in the reducing end of EPS make them capable of complexing and stabilizing much better metallic nanoparticles .
4. Role of Bacterial EPSs in the Synthesis of Metallic Au and Ag Nanoparticles with Biomedical and Other Applications
Among the most studied and broadly produced nanoparticles, through green synthesis methods, are silver (Ag-NPs) and gold (Au-NPs) nanoparticles. Many of these studies report the use of EPS as reducing and stabilizing agents during their synthesis. For instance, xanthan gum has been used in the synthesis of Au-NPs and these EPSs proved to be an effective drug delivery carrier for doxorubicin hydrochloride to human lung cancer cells . Furthermore, xanthan gum EPSs have been shown to aid in the synthesis of Ag-NPs with enhanced catalytic properties and antibacterial activity against Escherichia coli and Staphylococus aureus .
Dextran is a well-known EPS used to produce Ag-NPs with applications as chemical sensors for cysteine . Moreover, Ag-NPs with antibacterial and antifungal properties have also been synthesized using dextran sulfate . For the case of Au-NPs, these particles have been obtained using dextran as a capping and reducing agent . In this study, the Au-NPs showed antitumor effects against Ehrlich ascites carcinoma and solid carcinoma transplanted in mice through tests performed to evaluate liver and kidney biochemical function, as well as oxidation stress ratio and histopathological studies.
Curdlan and other modified compounds of EPSs have been useful to produce Ag-NPs using 4-acetamido-2,2,6,6-tetramethypiperidine-1-oxyl radical- (TEMPO-) oxidized curdlan , and also, nontoxic and biocompatible Au-NPs were produced using carboxylic curdlan. For the last study, the interaction of Au-NPs with bovine serum albumin were tested, indicating that these nanoparticles do not produce significant changes in protein structure .
Sphingans, such as gellan, have been used as reducing and stabilizing agents to elaborate Au-NPs for drug delivery formulations with cytotoxic effects against human glioma cell lines LN-18 and LN-229 . Using gellan gum, a highly stable water dispersion of antibacterial Ag-NPs was synthesized and tested their cytotoxicity in mouse embryonic fibroblast cells (NIH3T3), as well as their diffusion across rat skin . Finally, Au-NPs were produced with the same EPS revealing that these nanoparticles are uptaken by the human glioma cell line LN-229 and do not possess toxicity after oral administration in rats .
For the case of cellulose, previous works have stated that microbial cellulose in comparison to plant cellulose can be extracted with greater purity and a higher level of polymerization and crystallinity . Bacterial cellulose has been employed as a stabilizing agent of metallic nanoparticles, such is the case of Ag-NPs that coat the surface of bacterial cellulose nanofibers . Ag-NPs stabilized by microbial cellulose have also been synthesized to be used as optical sensors of cyanide ions and 2-mercaptobenzothiazole in water samples . Bacterial cellulose nanofibers have been shown to act as templates for synthesis of Au-NPs to produce nanocomposites formed by Au-NPs nanofibers in aqueous suspension. These nanocomposites have been used to immobilize the horseradish peroxidase enzyme to make a biosensor to detect H2O2 .
Levan is another microbial EPS, obtained from Acetobacter xylinum NCIM 2526, that has been used for the synthesis of Ag-NPs and Au-NPs with catalytic activity, tested by reduction of 4-nitrophenol and methylene blue . In this study, levan acted as an additional reducing and stabilizer agent during thermal reduction method and as stabilizer or capping during chemical reduction method.
Succinoglycan (sinorhizobial octasaccharide) isolated form Sinorhizobium meliloti is an EPS used to stabilize Ag-NPs . The presence of this EPS has been shown to confer biocompatible characteristics to the nanoparticles . In addition, it is important to note other novel EPSs extracted from bacteria that have been useful in the synthesis of Ag-NPs and Au-NPs. EPS from Lactobacillus rhamnosus has been reported to be used in the synthesis of Ag-NPs with antimicrobial activity against bacterial (Pseudomonas aeruginosa, Klebsiella pneumonia, and Listeria monocytogenes) and fungal pathogens (Aspergillus and Penicillium spp.) . Ag-NPs with antibacterial and antibiofilm activity against gram (+) and gram (−) bacteria were produced using an EPS extracted from Lactobacillus brevis NM101-1 . These Ag-NPs were effective as antibiotic adjuvants to enhance their antimicrobial activity. EPS from Lactobacillus plantarum was utilized in the production of Au-NPs to design a drug delivery agent against multidrug-resistant bacteria. The design involved the use of antibiotics to functionalize the Au-NPs to improve their antimicrobial properties . An additional strain of Lactobacillus plantarum-605 was used to produce nonglucan EPS-605 useful for the synthesis of Ag-NPs and Au-NPs . Antibacterial Ag-NPs have been synthesized in the presence of EPSs from Lactobacillus casei (LPW2E) and Lactobacillus fermentum (LPF6) . Moreover, Ag-NPs with applications in the degradation of azo dyes have been synthesized using EPS produced by Leuconostoc lactis KC117496 EPS .
The genera Bacillus has also been found to produce EPSs with applications in the synthesis of metal nanoparticles. A bioflocculant EPS from marine Bacillus subtilis MSBN17 was used to elaborate Ag-NPs tested as an antibacterial agent in sewage water and also as an antibiotic enhancer against pathogenic microorganisms when combined . Au-NPs with antibacterial activity against clinical pathogenic bacteria were produced using EPS from marine Bacillus megaterium MSBN04 . Additionally, Ag-NPs were produced on the basis of low and high molar mass of EPS obtained from diazotrophic Bradyrhizobium japonicum 36 strain. In this study, the nanoparticles were synthetized using low molecular mass EPS and had antibacterial and antifungal activities against Escherichia coli, Staphylococcus aureus, and Candida albicans .
To summarize this section, the silver and gold nanoparticles as well as their uses in which EPSs have been used as a reducing and/or stabilizing agent to synthesize them are showed in Table 3.
Nanoparticles produced by 50 : 50 solution of alginate/gellan mixture.
5. Role of Bacterial EPSs in the Synthesis of Other Metal Nanoparticles with Biomedical and Other Applications
EPSs have also been used in the synthesis of other metal nanoparticles, such is the case of xanthan gum, that has been used as a reducing and stabilizing agent to produce palladium nanoparticles (Pd-NPs) with very good catalytic activity during the reduction of 4-nitrophenol to 4-aminophenol by sodium borohydride . Xanthan gum has also been used to stabilize Pd/Fe-NPs employed to remediate polychlorinated biphenyl- (PCB-) contaminated soil in combination with surfactant BriJ35 by means of electrokinetic nanoparticle method, showing an enhancing of the degradation of PCB28 .
Dextran has been used to produce iron oxide nanoparticles. Indeed, this EPS was used to coat magnetic nanoparticles to produce biocompatible ferrofluids using the coprecipitation method. In this study, the dextran-coated iron oxide nanoparticles presented significant less cytotoxicity to L929 cells in comparison to the same bare nanoparticles making them more suitable for diagnostic and therapeutic purposes . Likewise, dextran was used as a stabilizing agent of iron oxide magnetic nanoparticles which were evaluated on in vitro and in vivo toxicological assays, showing them as nontoxic and safe nanoparticles to be used for biomedical applications .
Furthermore, carboxylic curdlan (Cur-4, Cur-8, and Cur-24) offers reducing and stabilizing agent properties in the production of selenium nanoparticles (Se-NPs) . These nanoparticles presented a strong antioxidant capacity and low cytotoxic activity against SPCA-1 and HeLa cell lines in vitro. Similarly, zinc oxide nanoparticles (ZnO-NPs) were obtained by carboxylic curdlan, evaluating the interaction of these nanoparticles with bovine serum albumin showing mild modification of its conformation .
Interestingly, with a combination of alginate and gellan (50 : 50 solution), Pd-NPs were stabilized and used as a catalyst system . In this study, the EPSs combination were carried out looking for improvement of the catalytic function of alginate/gellan-stabilized Pd-NPs taking advantage of synergistic interactions among EPSs [58, 97, 98], showing that combining the appropriately different EPSs may be useful in the synthesis, stabilization, and improving properties of metal nanoparticles. In this context, magnetic nanoparticles tested as drug carrier system of the anticancer drug 2,4-dihydroxy-5-fluoruracil (5FU) against the cancer cells MCF7, G1, and L929 were stabilized and coated using gellan gum and mauran .
Cellulose has also been employed to make other metal nanoparticles such as cadmium sulfide (CdS-NPs). These particles were produced by means of bacterial cellulose nanofibers and were proposed to be used as photocatalyst, luminescence, and photoelectron transfer devices . Evenly, antibacterial nanocomposites formed of bacterial cellulose-cooper oxide nanoparticles were obtained by hydrothermal deposition .
Levan has been used to produce and coat cerium oxide nanoparticles as both reducing and stabilizing agents. These nanoparticles were suggested to have applications to treat diseases related to oxidative stress, due to their antioxidant activity tested in H2O2-stimulated NIH3T3 cells . The above nanoparticles resulted nontoxic and biocompatible in cytotoxic studies with mouse fibroblast NIH3T3 cells and HEK293T cells. Likewise, levan was applied to coat and stabilize biocompatible Se, Fe, and Co nanoparticles as a strategy to obtain better food supplements with micronutrients safer and more efficient for humans .
In addition, recent EPSs such as FucoPol have been used to coat functionalized iron oxide magnetic nanoparticles. For instance, these nanoparticles functionalized with synthetic ligand applied for purification and recovery of antibodies were coated with FucoPol . In another study, nanoprobes of the same nanoparticles, in this case, functionalized with meso-2,3-dimercaptosuccinic acid (DMSA), were also coated with the same EPS and tested for cell labeling in magnetic resonance imaging (MRI) .
It is important to that note other bacterial EPSs have been used as reducing and stabilizing agents such is the case of EPSs obtained from Bacillus licheniformis Dahb1 used to synthetize ZnO nanoparticles by the coprecipitation method . These nanoparticles presented effective antibacterial and antibiofilm activity against both gram negative and gram positive bacteria, as well as antifungal and larvicidal activity with low cytotoxicity in hemolytic assays. In addition, magnetic iron oxide nanoparticles were produced and stabilized by a spore-forming strain of Bacillus subtilis EPS . The nanoparticles mentioned presented antibacterial activity, high bioavailability, and cytotoxicity against human epidermoid carcinoma cell line (A431).
To summarize this section, other metal nanoparticles as well as their uses in which EPSs have been used as a reducing and/or stabilizing agent to synthesize them are shown in Table 3.
6. Potential Mechanisms That Explain the Synthesis of Metal Nanoparticles by Bacterial EPSs
In general, it has been noted that once metal ions are in contact with EPSs that contain reducing sugars, they are chelated and then reduced and stabilized by various functional groups. Polyanionic groups are the best known chemical moieties to be involved in the reduction and stabilization of metal nanoparticles . Moreover, electrostatic interactions between metal cationic ions and anionic groups such as carboxylic and phosphoric functional groups of EPS have been mentioned to be an advantage for the synthesis of metal nanoparticles . Among these functional groups, hydroxyl, carboxyl, phosphoric, hemiacetal, and amino end groups have been proposed to reduce metal ions from the precursor salts to obtain the respective nanoparticles [52, 68, 104]. In relation with the above, hydroxyl groups have been attributed the ability to coordinate with metal ions . In fact, during the reducing process, oxidation of hydroxyl groups to form carbonyl groups as well as oxidation of alcoholic and aldehydic groups to form carboxylic groups has been reported to be an important factor during synthesis of metal nanoparticles . In regard with this, reaction conditions such as temperature, time of reaction, concentration of reactants, and pH have an influence in the morphological characteristics and mechanisms of producing nanoparticles [92, 103]. Once the nanoparticles are made, the EPS matrix forms a film or layer that acts as a capping and stabilizer, thereby obtaining metal nanoparticles with a small and tight size distribution, preventing agglomeration [52, 107]. These processes can be explained by the adsorption of the EPSs in the nanoparticle surface, promoting steric repulsion between them and augmenting the viscosity of the complex nanoparticles-EPS impeding their aggregation . In this context, it is noteworthy to mention that capping agents affect characteristics of metal nanoparticles such as surface charge and colloidal stability .
Thus, in relation to the EPSs described in this study, the structure of xanthan gum has been described to be helical with many hydroxyl groups that can carry out reduction of ions. In addition, this structure creates a network by hydrogen bonding in which nanoparticles stabilize . Further, xanthan gum has negative charge due to acetyl groups and pyruvic acid linked with mannose and provides this charge to nanoparticle surface creating a steric repulsion among them . Dextran, is useful in the synthesis of metal nanoparticles since their hydroxyl, ketone, aldehydes, and carboxyl groups interact and allow the reduction of Ag+ ions to form Ag-NPs, preventing their agglomeration as well [71, 72]. At this point, it was mentioned that oxygen from dextran functional groups can donate their pair of electrons to gold ions thereby producing Au-NPs . As it is well known, dextran is rich in hydroxyl groups that can interact with magnetic nanoparticles by hydrogen bonds stabilizing them [95, 109].
For curdlan, the carboxylic groups of curdlan derivatives such as carboxylic curdlan and carboxymethyl curdlan have the ability to adsorb metal ions by electrostatic attractive forces. These functional groups reduce the metal ions, and the necessary nucleation is created to form stabilized clusters during synthesis of Au-NPs, Ag-NPs, and ZnO-NP, as well as stabilization of Se-NPs [57, 60, 73, 74]. In this context, it is noteworthy to mention that curdlan is not soluble in water; therefore, it is carboxymethylated, oxidized, and its sodium salt is formed, in order to improve their properties .
Moreover, for the case of gellan gum, this anionic EPS envelope itself, which has been attributed to the stabilization of nanoparticles, and also it has abundant carbohydrate units that form the capping of Au-NPs [75, 77]. Similar to others bacterial EPSs, gellam gum has acyl groups and abundant carboxyl groups that may interact with metal ions to reduce and stabilize the respective nanoparticles .
Oxidizing bacterial cellulose by TEMPO allows the introduction of carboxylate groups that carry out ion-exchange reactions with metal ions to reduce them and synthesize metal nanoparticles [79, 111]. These EPSs have been utilized in nanofibers which are responsible of reduction and adsorption of metal as Ag+ and Cd+2 to form nanoparticles by hydroxyl groups, as well as attracting other metal nanoparticles like Au-NPs due to electrostatic repulsion [80, 81, 99, 112]. The hydroxyl groups have been described to be abundant in cellulose nanofibers and very important factor to explain physical properties of cellulose [113, 114].
In the case of levan, it has a lot of keto sugar units, and similar to other bacterial EPSs, it has numerous hydroxyl functional groups that may interact electrostatically with ions such as Ag+ leading to the formation of the respective nanoparticles . In this context, succinoglycan has been proposed to act as a reducing and stabilizing agent also due to hydroxyl groups that may give an electron to Ag+ to form Ag and is also capable to be involved in the formation of a complex matrix that carries out the stabilization acting as a capping agent . FucoPol has been used as a capping agent for magnetic nanoparticles being described to have a negative character because of its substituents that exhibit suitable stabilizing properties due to its good flocculation and emulsification process . During stabilizing function of FucoPol, it has been mention that this effect is dependent of steric and electrostatic interactions .
Additionally, related to similar mechanisms involved during synthesis and stabilization of metal nanoparticles reported with other EPSs, it has been described abundant functional groups as hydroxyl and hemiacetal ends in EPSs that carried out the reduction and stabilization of nanoparticles making them more suitable for application in different fields of study [86, 89]. Actually, sugar monomers like glucose, galactose, mannose, and fructose have been mentioned to reduce Ag+ ions to produce Ag-NPs when used EPSs of lactic acid bacteria [89, 116]. In general, many functional groups have been mentioned to carry out the reduction and stabilization of metal nanoparticles (Ag-NPs, Au-NPs, and FeO-NPs) by bacterial EPS such as hydroxyl, carboxyl, ester, aldehydes, methoxyl, sulfated, phosphate, amino, amide, and N-acetylated sugar molecules that possess negative charge and interact with metal ions by electrostatic attractive forces, thereby producing metal nanoparticles as described above [33, 87, 88, 90, 91, 103]. Thus, the above information may explain the reduction process of metal ions to form the respective nanoparticles, as well as their mechanisms to the effective stabilization that bacterial EPSs can carry out during the obtaining of metal nanoparticles. A representation of the information in this section is shown in Figure 3.
7. Main Techniques Used to Characterize Metal Nanoparticles and Biomedical Measurements
7.1. Instrumental Techniques to Characterize Metal Nanoparticles
After the production of metal nanoparticles (in this study, by means of bacterial exopolysaccharides), there are some characteristics that required their proper characterization, such as shape, size, surface, and dispersity . These characterization can be achieved by various instrumental techniques. In this context, ultraviolet-visible spectroscopy (UV-visible spectroscopy) has been very useful to rapidly detect the formation of different metal nanoparticles (silver, copper, gold, and platinum nanoparticles) since the surface plasmon resonance (SPR) phenomenon can be measured . For the case of shape, size, morphology, and particle size distribution of metal nanoparticles, transmission electron microscopy (TEM), high-resolution electron microscopy (HRTEM), scanning electron microscopy, atomic force microscopy (AFM), and dynamic light scattering are suitable techniques that have been used to measure these physical properties of metal nanoparticles [117, 119–124]. Crystallinity and the structure of metal nanoparticles are other physical characteristics which can be measured by X-ray diffraction and selected area electron diffraction (SAED) technique [125, 126]. To identify and confirm the elemental composition of metal nanoparticles and their capping, energy-dispersive spectrometry (EDS) is a proper technique for this purpose . When metal nanoparticles possess a capping or stabilizing agent, Fourier-transform infrared spectroscopy (FTIR) is applied to identify the functional groups present in the nanoparticle surface, and Zeta potential is used to determine the surface charge [128, 129]. In addition, when magnetic nanoparticles are produced, vibrating sample magnetometry (VSM) and superconducting quantum interference device (SQUID) magnetometry are adequate techniques to measure magnetic properties .
7.2. Biomedical Measurements Applied to Metal Nanoparticles Synthesized by EPSs as a Reducing and/or Stabilizing Agents
In relation to biomedical measurements carried out during biomedical applications of metal nanoparticles synthesized by bacterial EPSs, the antimicrobial activity of metal nanoparticles synthesized by bacterial EPSs has been measured by determination of minimum inhibitory concentration (MIC) [85, 86, 102, 120], minimum bactericidal concentration (MBC) [86, 120], fluorescence microscopy imaging (FMI) , skin infection model in vivo by colony counting method using the pour plate technique , agar disc diffusion method [53, 70, 72, 90, 91], agar well diffusion method [33, 85, 86, 88, 90–92, 102], colony counting method , antibiofilm activity [85, 102], bacterial growth kinetics tests, and kill time assays [85, 86, 92, 102]. Moreover, antifungal activity was measured by agar well and disk diffusion method [72, 102] as well as larvicidal activity using the World Health Organization method [102, 131].
On the other hand, metal nanoparticles produced by EPS as an anticancer agent and drug delivery carrier has been tested by some of biomedical measurements such as in vitro drug-released studies by dialysis method , in vivo studies of biochemical parameters and histopathological assays of liver and kidney functions and oxidation stress ratio , in vitro cytotoxicity and anticancer assays against tumor cell lines by MTT (3-(4,5-dimethylthiazol-2-yl)-2,5-diphenyltetrazolium bromide) colorimetric method [75, 103, 132], tumor cellular uptake by confocal laser scanning microscopy [75, 77], internalization of metal nanoparticles in tumor cells by cellular imaging and flow cytometry studies , cell viability by in vitro cytotoxicity and biocompatibility tests by alamar blue assay , antiproliferation of cancer cells using magnetic hyperthermia method (MHM) and qualitatively determination of live and dead cells after MHM , and measuring of tumor cell death by acridine orange/ethidium bromide staining assay .
In this context, other biomedical measurements related with other applications are cysteine detection by absorption spectroscopy and visual inspection during color change , biocompatibility assays by cytotoxicity studies using MTT method [54, 95, 96], toxicological tests by measuring in vivo studies of oral, dermal, and immunotoxicity, as well as genotoxicity, carcinogenicity, biochemical and hematological parameters, and histopathological analysis , interaction with protein assay employing fluorescence, circular dichroism spectroscopies and UV-visible spectroscopy [60, 74], in vitro ROS scavenging assay and antioxidant activities by DPPH (2,2-diphenyl-1-picrylhydrazyl), Trolox and ferric-reducing ability of plasma (FRAP) tests [54, 57], and in vitro MRI of cell phantoms to assess nanoprobes for cell labeling by MRI . Thus, there are many ways to measure the potential of metal nanoparticles synthesized by EPSs as a reducing and/or stabilizing agent in different important biomedical applications today.
Metal nanoparticles have been an important research target within the last decades, mainly because they have different properties than when in the bulk. Metal nanoparticles have been found to have beneficial properties for biomedical applications such as antimicrobial, anticancer, antioxidant, drug delivery, chemical sensors, contrast agents, and also in other applications such as catalysts and environmental remediation agents. Therefore, there is an interest in finding different compounds capable of effectively reducing and stabilizing metal nanoparticles. Green synthesis methods have gotten a lot of attention in the production of metallic nanoparticles, since these synthesis follow a process that involves almost exclusively the metallic salt precursor and a biological compound that performs either the chelation of the reduced metal, its stabilization, or both functions at the same time. Moreover, green synthesis methods have a wide array of advantages when comparing them with physical and chemical production methods; green synthesis provides and environmental friendly and cost-effective synthesis platform, employing nontoxic reagents and procedures. Bacterial EPSs are biomolecules that possess attractive properties to be exploited, in green synthesis production of metallic nanoparticles, due to their chemical composition. Bacterial EPS are heteropolysaccharides containing different functional groups in their backbone including amino, sulfate, phosphate, and hydroxyl substituents as well as N-acetylamino sugars and hemiacetal ends; all of these functional groups are great candidates in the reduction, complexation, and stabilization of metal nanoparticles during their synthesis. However, there are still several challenges in the use of bacterial EPS to aid in the synthesis of metallic nanoparticles, mainly the wide variability of the EPS chemical composition. Depending on the composition of the chosen EPS, the reaction conditions change, such as the temperature, reaction time, concentration, and rate of precursor salts to EPS. Furthermore, all of these synthesis parameters have shown to have a direct influence on the morphological characteristics of the produced nanoparticles.
Thus, bacterial EPSs are a suitable option to synthesize different functionalized metal nanoparticles to be used in biomedical and other types of applications. Using some bacterial EPS allows the production of metal nanoparticles, with a wide variety of applications, in an eco-friendly and nontoxic manner, conferring interesting characteristics through the functionalization of these nanomaterials. However, more research is needed related to the understanding of mechanisms involved in the process of reduction and stabilization during synthesis of metal nanoparticles, as well as more thorough toxicological and environmental studies to measure their impact on our society and the environment. Figure 4 illustrates a summary of the main content of this review.
Conflicts of Interest
The authors declare that there is no conflict of interest regarding the publication of this paper.
This work was supported by Paicyt 2016-2017 Science Grant from the Universidad Autónoma de Nuevo León and CONACYT grants for Basic Science grant 221332, Fronteras de la Ciencia grant 1502, and Infraestructura grant 279957.
- B. H. A. Rehm, Ed., Microbial Production of Biopolymers and Polymer Precursors: Applications and Perspectives, Caister Academic Press, 2009.
- O. Ates, “Systems biology of microbial exopolysaccharides production,” Frontiers in Bioengineering and Biotechnology, vol. 3, 2015.
- M. Moscovici, “Present and future medical applications of microbial exopolysaccharides,” Frontiers in Microbiology, vol. 6, 2015.
- B. Nicolaus, M. Kambourova, and E. T. Oner, “Exopolysaccharides from extremophiles: from fundamentals to biotechnology,” Environmental Technology, vol. 31, no. 10, pp. 1145–1158, 2010.
- U. Nwodo, E. Green, and A. Okoh, “Bacterial exopolysaccharides: functionality and prospects,” International Journal of Molecular Sciences, vol. 13, no. 12, pp. 14002–14015, 2012.
- P. Laurienzo, “Marine polysaccharides in pharmaceutical applications: an overview,” Marine Drugs, vol. 8, no. 9, pp. 2435–2465, 2010.
- S. Mahapatra and D. Banerjee, “Fungal exopolysaccharide: production, composition and applications,” Microbiology Insights, vol. 6, 2013.
- G. J. C. Underwood and D. M. Paterson, “The importance of extracellular carbohydrate productionby marine epipelic diatoms,” Advances in Botanical Research, vol. 40, pp. 183–240, 2003.
- F. Donot, A. Fontana, J. C. Baccou, and S. Schorr-Galindo, “Microbial exopolysaccharides: main examples of synthesis, excretion, genetics and extraction,” Carbohydrate Polymers, vol. 87, no. 2, pp. 951–962, 2012.
- F. Freitas, V. D. Alves, and M. A. M. Reis, “Advances in bacterial exopolysaccharides: from production to biotechnological applications,” Trends in Biotechnology, vol. 29, no. 8, pp. 388–398, 2011.
- A. Mishra and B. Jha, “Microbial exopolysaccharides,” in The Prokaryotes, pp. 179–192, Springer, 2013.
- H.-C. Flemming and J. Wingender, “The biofilm matrix,” Nature Reviews Microbiology, vol. 8, no. 9, pp. 623–633, 2010.
- T. Gutierrez, G. Morris, and D. H. Green, “Yield and physicochemical properties of EPS from Halomonas sp. strain TG39 identifies a role for protein and anionic residues (sulfate and phosphate) in emulsification of n-hexadecane,” Biotechnology and Bioengineering, vol. 103, no. 1, pp. 207–216, 2009.
- I. W. Sutherland, “The biofilm matrix – an immobilized but dynamic microbial environment,” Trends in Microbiology, vol. 9, no. 5, pp. 222–227, 2001.
- I. W. Sutherland, “EPS—A complex mixture,” in The Perfect Slime—Microbial Extracellular Polymeric Substances, H.-C. Flemming, J. Wingender, and T. R. Neu, Eds., pp. 15–24, IWA Publishing, 2016.
- D. C. O. Thornton, E. M. Fejes, S. F. DiMarco, and K. M. Clancy, “Measurement of acid polysaccharides in marine and freshwater samples using alcian blue,” Limnology and Oceanography: Methods, vol. 5, no. 2, pp. 73–87, 2007.
- H. Habibi and K. Khosravi-Darani, “Effective variables on production and structure of xanthan gum and its food applications: a review,” Biocatalysis and Agricultural Biotechnology, vol. 10, pp. 130–140, 2017.
- L. Casettari, G. Bonacucina, G. A. Morris et al., “Dextran and its potential use as tablet excipient,” Powder Technology, vol. 273, pp. 125–132, 2015.
- M. Xiao, M. Jiang, K. Wu et al., “Investigation on curdlan dissociation by heating in water,” Food Hydrocolloids, vol. 70, pp. 57–64, 2017.
- R. J. Coleman, Y. N. Patel, and N. E. Harding, “Identification and organization of genes for diutan polysaccharide synthesis from Sphingomonas sp. ATCC 53159,” Journal of Industrial Microbiology & Biotechnology, vol. 35, no. 4, pp. 263–274, 2008.
- M. Shoda and Y. Sugano, “Recent advances in bacterial cellulose production,” Biotechnology and Bioprocess Engineering, vol. 10, no. 1, pp. 1–8, 2005.
- T. A. A. Moussa, S. A. S. Al-Qaysi, Z. A. Thabit, and S. B. Kadhem, “Microbial levan from Brachybacterium phenoliresistens: characterization and enhancement of production,” Process Biochemistry, vol. 57, pp. 9–15, 2017.
- R. Srikanth, C. H. S. S. S. Reddy, G. Siddartha, M. J. Ramaiah, and K. B. Uppuluri, “Review on production, characterization and applications of microbial levan,” Carbohydrate Polymers, vol. 120, pp. 102–114, 2015.
- S. A. Glenn, N. Gurich, M. A. Feeney, and J. E. González, “The ExpR/Sin quorum-sensing system controls succinoglycan production in Sinorhizobium meliloti,” Journal of Bacteriology, vol. 189, no. 19, pp. 7077–7088, 2007.
- A. R. V. Ferreira, C. A. V. Torres, F. Freitas, M. A. M. Reis, V. D. Alves, and I. M. Coelhoso, “Biodegradable films produced from the bacterial polysaccharide FucoPol,” International Journal of Biological Macromolecules, vol. 71, pp. 111–116, 2014.
- F. Freitas, V. D. Alves, J. Pais et al., “Characterization of an extracellular polysaccharide produced by a Pseudomonas strain grown on glycerol,” Bioresource Technology, vol. 100, no. 2, pp. 859–865, 2009.
- G. Sathiyanarayanan, K. Dineshkumar, and Y.-H. Yang, “Microbial exopolysaccharide-mediated synthesis and stabilization of metal nanoparticles,” Critical Reviews in Microbiology, vol. 43, no. 6, pp. 731–752, 2017.
- J. M. Aguilera, P. J. Lillford, and H. Watzke, “Why food materials science?” in Food Materials Science, pp. 3–10, Springer, 2008.
- A. Banerjee, U. Halder, and R. Bandopadhyay, “Preparations and applications of polysaccharide based green synthesized metal nanoparticles: a state-of-the-art,” Journal of Cluster Science, vol. 28, no. 4, pp. 1803–1813, 2017.
- A. Imeson, Ed., Food Stabilisers, Thickeners and Gelling Agents, John Wiley & Sons, 2011.
- E. Rodríguez-Carmona and A. Villaverde, “Nanostructured bacterial materials for innovative medicines,” Trends in Microbiology, vol. 18, no. 9, pp. 423–430, 2010.
- A. Vazquez-Rodriguez, X. G. Vasto-Anzaldo, D. Barboza Perez et al., “Microbial competition of Rhodotorula mucilaginosa UANL-001L and E. coli increase biosynthesis of non-toxic exopolysaccharide with applications as a wide-spectrum antimicrobial,” Scientific Reports, vol. 8, no. 1, p. 798, 2018.
- P. Kanmani and S. T. Lim, “Synthesis and structural characterization of silver nanoparticles using bacterial exopolysaccharide and its antimicrobial activity against food and multidrug resistant pathogens,” Process Biochemistry, vol. 48, no. 7, pp. 1099–1106, 2013.
- S. K. Kazy, P. Sar, and S. F. D'Souza, “Studies on uranium removal by the extracellular polysaccharide of a Pseudomonas aeruginosa strain,” Bioremediation Journal, vol. 12, no. 2, pp. 47–57, 2008.
- S. W. Park, B. S. Choi, K. W. Song, K. J. Oh, and J. W. Lee, “Absorption of carbon dioxide into aqueous xanthan gum solution containing monoethanolamine,” Separation Science and Technology, vol. 42, no. 16, pp. 3537–3554, 2007.
- Y. M. Lin, L. Wang, Z. M. Chi, and X. Y. Liu, “Bacterial alginate role in aerobic granular bio‐particles formation and settleability improvement,” Separation Science and Technology, vol. 43, no. 7, pp. 1642–1652, 2008.
- A. M. Sani and K. K. Mohanty, “Incorporation of clay nano-particles in aqueous foams,” Colloids and Surfaces A: Physicochemical and Engineering Aspects, vol. 340, no. 1–3, pp. 174–181, 2009.
- C. Sun, C. Y. Shan, X. D. Gao, and R. X. Tan, “Protection of PC12 cells from hydrogen peroxide-induced injury by EPS2, an exopolysaccharide from a marine filamentous fungus Keissleriella sp. YS4108,” Journal of Biotechnology, vol. 115, no. 2, pp. 137–144, 2005.
- H.-H. Sun, W.-J. Mao, Y. Chen et al., “Isolation, chemical characteristics and antioxidant properties of the polysaccharides from marine fungus Penicillium sp. F23-2,” Carbohydrate Polymers, vol. 78, no. 1, pp. 117–124, 2009.
- M. A. Guzman-Murillo and F. Ascencio, “Anti-adhesive activity of sulphated exopolysaccharides of microalgae on attachment of red sore disease-associated bacteria and Helicobacter pylori to tissue culture cells,” Letters in Applied Microbiology, vol. 30, no. 6, pp. 473–478, 2000.
- T. Hayashi, K. Hayashi, M. Maeda, and I. Kojima, “Calcium spirulan, an inhibitor of enveloped virus replication, from a blue-green alga Spirulina platensis,” Journal of Natural Products, vol. 59, no. 1, pp. 83–87, 1996.
- M. Matsuda, T. Yamori, M. Naitoh, and K. Okutani, “Structural revision of sulfated polysaccharide B-1 isolated from a marine Pseudomonas species and its cytotoxic activity against human cancer cell lines,” Marine Biotechnology, vol. 5, no. 1, pp. 13–19, 2003.
- S. Colliec-Jouault, P. Zanchetta, D. Helley et al., “Les polysaccharides microbiens d’origine marine et leur potentiel en thérapeutique humaine,” Pathologie Biologie, vol. 52, no. 3, pp. 127–130, 2004.
- H. R. Moon, D.-W. Lim, and M. P. Suh, “Fabrication of metal nanoparticles in metal–organic frameworks,” Chemical Society Reviews, vol. 42, no. 4, pp. 1807–1824, 2013.
- J. R. Morones, J. L. Elechiguerra, A. Camacho et al., “The bactericidal effect of silver nanoparticles,” Nanotechnology, vol. 16, no. 10, pp. 2346–2353, 2005.
- K. Arunachalam and S. Annamalai, “Chrysopogon zizanioides aqueous extract mediated synthesis characterization of crystalline silver and gold nanoparticles for biomedical applications,” International Journal of Nanomedicine, vol. 8, no. 1, pp. 2375–2384, 2013.
- O. V. Kharissova, H. V. Rasika Dias, B. I. Kharisov, B. O. Pérez, and V. M. Jiménez Pérez, “The greener synthesis of nanoparticles,” Trends in Biotechnology, vol. 31, no. 4, pp. 240–248, 2013.
- V. Makarov, A. Love, O. Sinitsyna et al., ““Green” nanotechnologies: synthesis of metal nanoparticles using plants,” Acta Naturae, vol. 6, no. 1, pp. 35–44, 2014.
- K. Quester, M. Avalos-Borja, and E. Castro-Longoria, “Biosynthesis and microscopic study of metallic nanoparticles,” Micron, vol. 54-55, pp. 1–27, 2013.
- S. Shamaila, A. K. L. Sajjad, N. U. A. Ryma et al., “Advancements in nanoparticle fabrication by hazard free eco-friendly green routes,” Applied Materials Today, vol. 5, pp. 150–199, 2016.
- Z. Vaseghi, A. Nematollahzadeh, and O. Tavakoli, “Green methods for the synthesis of metal nanoparticles using biogenic reducing agents: a review,” Reviews in Chemical Engineering, vol. 34, no. 4, pp. 529–559, 2018.
- H. E. Emam and H. B. Ahmed, “Polysaccharides templates for assembly of nanosilver,” Carbohydrate Polymers, vol. 135, pp. 300–307, 2016.
- I. M. S. Araújo, R. R. Silva, G. Pacheco et al., “Hydrothermal synthesis of bacterial cellulose–copper oxide nanocomposites and evaluation of their antimicrobial activity,” Carbohydrate Polymers, vol. 179, pp. 341–349, 2018.
- S.-J. Kim and B. H. Chung, “Antioxidant activity of levan coated cerium oxide nanoparticles,” Carbohydrate Polymers, vol. 150, pp. 400–407, 2016.
- D. Medhat, J. Hussein, M. E. El-Naggar et al., “Effect of Au-dextran NPs as anti-tumor agent against EAC and solid tumor in mice by biochemical evaluations and histopathological investigations,” Biomedicine & Pharmacotherapy, vol. 91, pp. 1006–1016, 2017.
- S. I. C. J. Palma, C. A. V. Rodrigues, A. Carvalho et al., “A value-added exopolysaccharide as a coating agent for MRI nanoprobes,” Nanoscale, vol. 7, no. 34, pp. 14272–14283, 2015.
- J.-K. Yan, W.-Y. Qiu, Y.-Y. Wang, W.-H. Wang, Y. Yang, and H.-N. Zhang, “Fabrication and stabilization of biocompatible selenium nanoparticles by carboxylic curdlans with various molecular properties,” Carbohydrate Polymers, vol. 179, pp. 19–27, 2018.
- S. Cacchi, E. Caponetti, M. A. Casadei et al., “Suzuki-Miyaura cross-coupling of arenediazonium salts catalyzed by alginate/gellan-stabilized palladium nanoparticles under aerobic conditions in water,” Green Chemistry, vol. 14, no. 2, pp. 317–320, 2012.
- B. Sivakumar, R. G. Aswathy, R. Sreejith et al., “Bacterial exopolysaccharide based magnetic nanoparticles: a versatile nanotool for cancer cell imaging, targeted drug delivery and synergistic effect of drug and hyperthermia mediated cancer therapy,” Journal of Biomedical Nanotechnology, vol. 10, no. 6, pp. 885–899, 2014.
- J.-K. Yan, Y.-Y. Wang, L. Zhu, and J.-Y. Wu, “Green synthesis and characterization of zinc oxide nanoparticles using carboxylic curdlan and their interaction with bovine serum albumin,” RSC Advances, vol. 6, no. 81, pp. 77752–77759, 2016.
- Y. Park, Y. N. Hong, A. Weyers, Y. S. Kim, and R. J. Linhardt, “Polysaccharides and phytochemicals: a natural reservoir for the green synthesis of gold and silver nanoparticles,” IET Nanobiotechnology, vol. 5, no. 3, pp. 69–78, 2011.
- H. B. Ahmed, M. K. Zahran, and H. E. Emam, “Heatless synthesis of well dispersible Au nanoparticles using pectin biopolymer,” International Journal of Biological Macromolecules, vol. 91, pp. 208–219, 2016.
- H. E. Emam, M. K. Zahran, and H. B. Ahmed, “Generation of biocompatible nanogold using H2O2–starch and their catalytic/antimicrobial activities,” European Polymer Journal, vol. 90, pp. 354–367, 2017.
- I. W. Sutherland, Biotechnology of Microbial Exopolysaccharides, Cambridge University Press, 1990.
- S. Pereira, A. Zille, E. Micheletti, P. Moradas-Ferreira, R. De Philippis, and P. Tamagnini, “Complexity of cyanobacterial exopolysaccharides: composition, structures, inducing factors and putative genes involved in their biosynthesis and assembly,” FEMS Microbiology Reviews, vol. 33, no. 5, pp. 917–941, 2009.
- M. C. Manca, L. Lama, R. Improta, E. Esposito, A. Gambacorta, and B. Nicolaus, “Chemical composition of two exopolysaccharides from Bacillus thermoantarcticus,” Applied and Environmental Microbiology, vol. 62, no. 9, pp. 3265–3269, 1996.
- R. P. Singh, M. K. Shukla, A. Mishra, P. Kumari, C. R. K. Reddy, and B. Jha, “Isolation and characterization of exopolysaccharides from seaweed associated bacteria Bacillus licheniformis,” Carbohydrate Polymers, vol. 84, no. 3, pp. 1019–1026, 2011.
- V. D. Nadkarni, A. Pervin, and R. J. Linhardt, “Directional immobilization of heparin onto beaded supports,” Analytical Biochemistry, vol. 222, no. 1, pp. 59–67, 1994.
- D. Pooja, S. Panyaram, H. Kulhari, S. S. Rachamalla, and R. Sistla, “Xanthan gum stabilized gold nanoparticles: characterization, biocompatibility, stability and cytotoxicity,” Carbohydrate Polymers, vol. 110, pp. 1–9, 2014.
- W. Xu, W. Jin, L. Lin et al., “Green synthesis of xanthan conformation-based silver nanoparticles: antibacterial and catalytic application,” Carbohydrate Polymers, vol. 101, pp. 961–967, 2014.
- S. Davidović, V. Lazić, I. Vukoje et al., “Dextran coated silver nanoparticles — chemical sensor for selective cysteine detection,” Colloids and Surfaces B: Biointerfaces, vol. 160, pp. 184–191, 2017.
- M. Cakić, S. Glišić, G. Nikolić, G. M. Nikolić, K. Cakić, and M. Cvetinov, “Synthesis, characterization and antimicrobial activity of dextran sulphate stabilized silver nanoparticles,” Journal of Molecular Structure, vol. 1110, pp. 156–161, 2016.
- J.-K. Yan, P.-F. Cai, X.-Q. Cao et al., “Green synthesis of silver nanoparticles using 4-acetamido-TEMPO-oxidized curdlan,” Carbohydrate Polymers, vol. 97, no. 2, pp. 391–397, 2013.
- J.-K. Yan, J.-L. Liu, Y.-J. Sun, S. Tang, Z.-Y. Mo, and Y.-S. Liu, “Green synthesis of biocompatible carboxylic curdlan-capped gold nanoparticles and its interaction with protein,” Carbohydrate Polymers, vol. 117, pp. 771–777, 2015.
- S. Dhar, E. M. Reddy, A. Shiras, V. Pokharkar, and B. L. V. Prasad, “Natural gum reduced/stabilized gold nanoparticles for drug delivery formulations,” Chemistry - A European Journal, vol. 14, no. 33, pp. 10244–10250, 2008.
- S. Dhar, P. Murawala, A. Shiras, V. Pokharkar, and B. L. V. Prasad, “Gellan gum capped silver nanoparticle dispersions and hydrogels: cytotoxicity and in vitro diffusion studies,” Nanoscale, vol. 4, no. 2, pp. 563–567, 2012.
- S. Dhar, V. Mali, S. Bodhankar, A. Shiras, B. L. V. Prasad, and V. Pokharkar, “Biocompatible gellan gum-reduced gold nanoparticles: cellular uptake and subacute oral toxicity studies,” Journal of Applied Toxicology, vol. 31, no. 5, pp. 411–420, 2011.
- P. R. Chawla, I. B. Bajaj, S. A. Survase, and R. S. Singhal, “Microbial cellulose: fermentative production and applications,” Food Technology & Biotechnology, vol. 47, no. 2, pp. 107–124, 2009.
- S. Ifuku, M. Tsuji, M. Morimoto, H. Saimoto, and H. Yano, “Synthesis of silver nanoparticles templated by TEMPO-mediated oxidized bacterial cellulose nanofibers,” Biomacromolecules, vol. 10, no. 9, pp. 2714–2717, 2009.
- N. Pourreza, H. Golmohammadi, T. Naghdi, and H. Yousefi, “Green in-situ synthesized silver nanoparticles embedded in bacterial cellulose nanopaper as a bionanocomposite plasmonic sensor,” Biosensors and Bioelectronics, vol. 74, pp. 353–359, 2015.
- T. Zhang, W. Wang, D. Zhang et al., “Biotemplated synthesis of gold nanoparticle–bacteria cellulose nanofiber nanocomposites and their application in biosensing,” Advanced Functional Materials, vol. 20, no. 7, pp. 1152–1160, 2010.
- K. B. A. Ahmed, D. Kalla, K. B. Uppuluri, and V. Anbazhagan, “Green synthesis of silver and gold nanoparticles employing levan, a biopolymer from Acetobacter xylinum NCIM 2526, as a reducing agent and capping agent,” Carbohydrate Polymers, vol. 112, pp. 539–545, 2014.
- S. A. Cumberland and J. R. Lead, “Synthesis of NOM-capped silver nanoparticles: size, morphology, stability, and NOM binding characteristics,” ACS Sustainable Chemistry & Engineering, vol. 1, no. 7, pp. 817–825, 2013.
- C. Kwon, B. Park, H. Kim, and S. Jung, “Green synthesis of silver nanoparticles by sinorhizobial octasaccharide isolated from Sinorhizobium meliloti,” Bulletin of the Korean Chemical Society, vol. 30, no. 7, pp. 1651–1654, 2009.
- E. Z. Gomaa, “Exopolysaccharide-mediated silver nanoparticles produced by Lactobacillus brevis NM101-1 as antibiotic adjuvant,” Microbiology, vol. 85, no. 2, pp. 207–219, 2016.
- Pradeepa, S. M. Vidya, S. Mutalik, K. U. Bhat, P. Huilgol, and K. Avadhani, “Preparation of gold nanoparticles by novel bacterial exopolysaccharide for antibiotic delivery,” Life Sciences, vol. 153, pp. 171–179, 2016.
- C. Li, L. Zhou, H. Yang et al., “Self-assembled exopolysaccharide nanoparticles for bioremediation and green synthesis of noble metal nanoparticles,” ACS Applied Materials & Interfaces, vol. 9, no. 27, pp. 22808–22818, 2017.
- B. C. Adebayo-Tayo and A. O. Popoola, “Biogenic synthesis and antimicrobial activity of silver nanoparticle using exopolysaccharides from lactic acid bacteria,” International Journal of Nano Dimension, vol. 8, no. 1, pp. 61–69, 2017.
- C. Saravanan, R. Rajesh, T. Kaviarasan, K. Muthukumar, D. Kavitake, and P. H. Shetty, “Synthesis of silver nanoparticles using bacterial exopolysaccharide and its application for degradation of azo-dyes,” Biotechnology Reports, vol. 15, pp. 33–40, 2017.
- G. Sathiyanarayanan, G. Seghal Kiran, and J. Selvin, “Synthesis of silver nanoparticles by polysaccharide bioflocculant produced from marine Bacillus subtilis MSBN17,” Colloids and Surfaces B: Biointerfaces, vol. 102, pp. 13–20, 2013.
- G. Sathiyanarayanan, V. Vignesh, G. Saibaba et al., “Synthesis of carbohydrate polymer encrusted gold nanoparticles using bacterial exopolysaccharide: a novel and greener approach,” RSC Advances, vol. 4, no. 43, pp. 22817–22827, 2014.
- B. Rasulov, N. Rustamova, A. Yili, H.-Q. Zhao, and H. A. Aisa, “Synthesis of silver nanoparticles on the basis of low and high molar mass exopolysaccharides of Bradyrhizobium japonicum 36 and its antimicrobial activity against some pathogens,” Folia Microbiologica, vol. 61, no. 4, pp. 283–293, 2016.
- A. Santoshi kumari, M. Venkatesham, D. Ayodhya, and G. Veerabhadram, “Green synthesis, characterization and catalytic activity of palladium nanoparticles by xanthan gum,” Applied Nanoscience, vol. 5, no. 3, pp. 315–320, 2015.
- G. Fan, L. Cang, W. Qin, C. Zhou, H. I. Gomes, and D. Zhou, “Surfactants-enhanced electrokinetic transport of xanthan gum stabilized nanoPd/Fe for the remediation of PCBs contaminated soils,” Separation and Purification Technology, vol. 114, pp. 64–72, 2013.
- Z. Shaterabadi, G. Nabiyouni, and M. Soleymani, “High impact of in situ dextran coating on biocompatibility, stability and magnetic properties of iron oxide nanoparticles,” Materials Science and Engineering: C, vol. 75, pp. 947–956, 2017.
- N. S. Remya, S. Syama, A. Sabareeswaran, and P. V. Mohanan, “Toxicity, toxicokinetics and biodistribution of dextran stabilized iron oxide nanoparticles for biomedical applications,” International Journal of Pharmaceutics, vol. 511, no. 1, pp. 586–598, 2016.
- F. M. Goycoolea, E. R. Morris, and M. J. Gidley, “Screening for synergistic interactions in dilute polysaccharide solutions,” Carbohydrate Polymers, vol. 28, no. 4, pp. 351–358, 1995.
- Y. Nitta, B. S. Kim, K. Nishinari et al., “Synergistic gel formation of xyloglucan/gellan mixtures as studied by rheology, DSC, and circular dichroism,” Biomacromolecules, vol. 4, no. 6, pp. 1654–1660, 2003.
- X. Li, S. Chen, W. Hu et al., “In situ synthesis of CdS nanoparticles on bacterial cellulose nanofibers,” Carbohydrate Polymers, vol. 76, no. 4, pp. 509–512, 2009.
- O. M. Bondarenko, A. Ivask, A. Kahru et al., “Bacterial polysaccharide levan as stabilizing, non-toxic and functional coating material for microelement-nanoparticles,” Carbohydrate Polymers, vol. 136, pp. 710–720, 2016.
- V. L. Dhadge, P. I. Morgado, F. Freitas et al., “An extracellular polymer at the interface of magnetic bioseparations,” Journal of the Royal Society Interface, vol. 11, no. 100, article 20140743, 2014.
- M. Abinaya, B. Vaseeharan, M. Divya et al., “Bacterial exopolysaccharide (EPS)-coated ZnO nanoparticles showed high antibiofilm activity and larvicidal toxicity against malaria and Zika virus vectors,” Journal of Trace Elements in Medicine and Biology, vol. 45, pp. 93–103, 2018.
- V. Vignesh, G. Sathiyanarayanan, G. Sathishkumar, K. Parthiban, K. Sathish-Kumar, and R. Thirumurugan, “Formulation of iron oxide nanoparticles using exopolysaccharide: evaluation of their antibacterial and anticancer activities,” RSC Advances, vol. 5, no. 35, pp. 27794–27804, 2015.
- S. Raveendran, N. Chauhan, V. Palaninathan et al., “Extremophilic polysaccharide for biosynthesis and passivation of gold nanoparticles and photothermal ablation of cancer cells,” Particle & Particle Systems Characterization, vol. 32, no. 1, pp. 54–64, 2015.
- S. Pandey, G. K. Goswami, and K. K. Nanda, “Green synthesis of biopolymer–silver nanoparticle nanocomposite: an optical sensor for ammonia detection,” International Journal of Biological Macromolecules, vol. 51, no. 4, pp. 583–589, 2012.
- Y. N. Mata, E. Torres, M. L. Blázquez, A. Ballester, F. González, and J. A. Muñoz, “Gold(III) biosorption and bioreduction with the brown alga Fucus vesiculosus,” Journal of Hazardous Materials, vol. 166, no. 2-3, pp. 612–618, 2009.
- U. Shah, A. Gani, B. A. Ashwar et al., “A review of the recent advances in starch as active and nanocomposite packaging films,” Cogent Food & Agriculture, vol. 1, no. 1, 2015.
- R. Jain, N. Jordan, S. Weiss et al., “Extracellular polymeric substances govern the surface charge of biogenic elemental selenium nanoparticles,” Environmental Science & Technology, vol. 49, no. 3, pp. 1713–1720, 2015.
- V. M. Khot, A. B. Salunkhe, N. D. Thorat, R. S. Ningthoujam, and S. H. Pawar, “Induction heating studies of dextran coated MgFe2O4 nanoparticles for magnetic hyperthermia,” Dalton Transactions, vol. 42, no. 4, pp. 1249–1258, 2013.
- Y. Jin, H. Zhang, Y. Yin, and K. Nishinari, “Comparison of curdlan and its carboxymethylated derivative by means of rheology, DSC, and AFM,” Carbohydrate Research, vol. 341, no. 1, pp. 90–99, 2006.
- T. Saito and A. Isogai, “Ion-exchange behavior of carboxylate groups in fibrous cellulose oxidized by the TEMPO-mediated system,” Carbohydrate Polymers, vol. 61, no. 2, pp. 183–190, 2005.
- H. Dong, J. F. Snyder, D. T. Tran, and J. L. Leadore, “Hydrogel, aerogel and film of cellulose nanofibrils functionalized with silver nanoparticles,” Carbohydrate Polymers, vol. 95, no. 2, pp. 760–767, 2013.
- K. Missoum, M. Belgacem, and J. Bras, “Nanofibrillated cellulose surface modification: a review,” Materials, vol. 6, no. 5, pp. 1745–1766, 2013.
- G. Siqueira, J. Bras, and A. Dufresne, “Cellulosic bionanocomposites: a review of preparation, properties and applications,” Polymer, vol. 2, no. 4, pp. 728–765, 2010.
- F. Freitas, V. D. Alves, C. A. V. Torres et al., “Fucose-containing exopolysaccharide produced by the newly isolated Enterobacter strain A47 DSM 23139,” Carbohydrate Polymers, vol. 83, no. 1, pp. 159–165, 2011.
- N. Cioffi and M. Rai, Eds., Nano-Antimicrobials: Progress and Prospects, Springer, 2012.
- C. P. Devatha and A. K. Thalla, “Green synthesis of nanomaterials,” in Synthesis of Inorganic Nanomaterials, pp. 169–184, Elsevier, 2018.
- S. K. Kailasa, J. R. Koduru, M. L. Desai, T. J. Park, R. K. Singhal, and H. Basu, “Recent progress on surface chemistry of plasmonic metal nanoparticles for colorimetric assay of drugs in pharmaceutical and biological samples,” TrAC Trends in Analytical Chemistry, vol. 105, pp. 106–120, 2018.
- Y. Choi, M. J. Choi, S. H. Cha, Y. Kim, S. Cho, and Y. Park, “Catechin-capped gold nanoparticles: green synthesis, characterization, and catalytic activity toward 4-nitrophenol reduction,” Nanoscale Research Letters, vol. 9, no. 1, p. 103, 2014.
- C. E. Escárcega-González, J. A. Garza-Cervantes, A. Vazquez-Rodríguez et al., “In vivo antimicrobial activity of silver nanoparticles produced via a green chemistry synthesis using Acacia rigidula as a reducing and capping agent,” International Journal of Nanomedicine, vol. 13, pp. 2349–2363, 2018.
- P. Logeswari, S. Silambarasan, and J. Abraham, “Synthesis of silver nanoparticles using plants extract and analysis of their antimicrobial property,” Journal of Saudi Chemical Society, vol. 19, no. 3, pp. 311–317, 2015.
- F. Luo, D. Yang, Z. Chen, M. Megharaj, and R. Naidu, “One-step green synthesis of bimetallic Fe/Pd nanoparticles used to degrade Orange II,” Journal of Hazardous Materials, vol. 303, pp. 145–153, 2016.
- S. S. Poguberović, D. M. Krčmar, B. D. Dalmacija et al., “Removal of Ni(II) and Cu(II) from aqueous solutions using ‘green’ zero-valent iron nanoparticles produced by oak and mulberry leaf extracts,” Water Science & Technology, vol. 74, no. 9, pp. 2115–2123, 2016.
- G. R. Salunke, S. Ghosh, R. J. S. Kumar et al., “Rapid efficient synthesis and characterization of silver, gold, and bimetallic nanoparticles from the medicinal plant Plumbago zeylanica and their application in biofilm control,” International Journal of Nanomedicine, vol. 9, p. 2635, 2014.
- I. Uddin, “Mechanistic approach to study conjugation of nanoparticles for biomedical applications,” Spectrochimica Acta Part A: Molecular and Biomolecular Spectroscopy, vol. 202, pp. 238–243, 2018.
- T. Wang, J. Lin, Z. Chen, M. Megharaj, and R. Naidu, “Green synthesized iron nanoparticles by green tea and eucalyptus leaves extracts used for removal of nitrate in aqueous solution,” Journal of Cleaner Production, vol. 83, pp. 413–419, 2014.
- M. Hamelian, K. Varmira, and H. Veisi, “Green synthesis and characterizations of gold nanoparticles using thyme and survey cytotoxic effect, antibacterial and antioxidant potential,” Journal of Photochemistry and Photobiology B: Biology, vol. 184, pp. 71–79, 2018.
- R. Dobrucka and J. Długaszewska, “Biosynthesis and antibacterial activity of ZnO nanoparticles using Trifolium pratense flower extract,” Saudi Journal of Biological Sciences, vol. 23, no. 4, pp. 517–523, 2016.
- M. P. Patil, R. D. Singh, P. B. Koli et al., “Antibacterial potential of silver nanoparticles synthesized using Madhuca longifolia flower extract as a green resource,” Microbial Pathogenesis, vol. 121, pp. 184–189, 2018.
- M. Faraji, Y. Yamini, and M. Rezaee, “Magnetic nanoparticles: synthesis, stabilization, functionalization, characterization, and applications,” Journal of the Iranian Chemical Society, vol. 7, no. 1, pp. 1–37, 2010.
- WHO and Special Programme for Research, Training in Tropical Diseases, Dengue: Guidelines for Diagnosis, Treatment, Prevention and Control, World Health Organization, 2009.
- M. Buttacavoli, N. N. Albanese, G. Di Cara et al., “Anticancer activity of biogenerated silver nanoparticles: an integrated proteomic investigation,” Oncotarget, vol. 9, no. 11, pp. 9685–9705, 2018.
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