Structural, textural and morphological characteristics of tannins from Acacia mearnsii encapsulated using sol-gel methods: Applications as antimicrobial agents

Highlights

• Four sol-gel routes were investigated in tannins from Acacia mearnsii encapsulation.

• Textural and morphological differences between hybrid materials are discussed.

• Antimicrobial tests showed the performance of hybrid materials compared to tannins.

• The sol-gel methods preserved characteristics of original tannins.

• Hybrid materials promoted the gradual release of phenolic compounds in tests.

Abstract

Tannins from Acacia mearnsii were encapsulated using four different sol-gel methods acid (SGAR), basic (SGBR), silicate (SGSR) and non-hydrolytic (SGNHR) routes. The hybrid materials were analyzed using a set of techniques to characterize their structure, texture and morphology. The antimicrobial performance of the encapsulated materials was evaluated against different microorganisms (Staphylococcus aureus, Escherichia coli, Aspergillus niger and Candida sp.). The data showed that the encapsulation route significantly affects the characteristics of the resulting hybrid materials. Better functional performances were obtained using the silicate route, which produced mesoporous materials with a small surface area (0.96 m² g⁻¹) and small particle size (<1 nm). These characteristics promoted the gradual release of tannins in an aqueous medium and improved their interactions with microorganisms. Furthermore, the process demonstrated the preservation of tannins after synthesis and increased antimicrobial activity (via a controlled tannin release), as demonstrated by the moderate activity against filamentous fungi and yeast.

Introduction

Tannins constitute a heterogeneous group of water-soluble polyphenolic compounds that are present in a number of vegetables and in various plant parts, such as roots, twigs, flowers, leaves, fruits, and seeds. The term tannin is derived from the ability of these compounds to interact with and precipitate macromolecules, such as proteins. This ability enables the use of tannins to tan animal leather [1], [2]. The three classes of tannins are (i) hydrolysable tannins, which are esters of gallic or ellagic acids, (ii) phlorotannins, which are derivatives of phloroglucinol (1,3,5- trihydroxybenzene), and (iii) condensed tannins [3], [4]. The condensed tannins from black acacia (Acacia mearnsii) are condensed polymers composed of catechol, benzoquinone and a catechin flavonoid [5].

Tannins are essential for a variety of plant functions. These compounds are responsible for the major organoleptic (wine astringency) differences and nutritional properties of plant-derived foods. Tannins are also useful for numerous practical applications in industry [6], such as wood adhesives [7], [8], biopolymer adsorbents for water treatment [9], [10] and additives [11], [12], [13].

Tannins are also useful due to their antimicrobial properties. The astringent characteristics of tannins can induce complexation with enzymes or with microbial substrates, and the antimicrobial action mechanisms of tannins in different microorganisms, such as bacteria, fungi and yeasts, are still under investigation. The toxicity of tannins for microorganisms is well documented and involves several research fields, i.e., food science, soil science, plant pathology, pharmacology and animal and human nutrition [14], [15], [16].

Despite the numerous applications assigned to vegetable tannins, these polymers exhibit physical and chemical instabilities in aqueous phases. They undergo oxidation and auto-oxidation reactions during storage, resulting in undesirable color changes, which is especially unfavorable in the beverage industry. Examples in the literature report the use of a sol-gel process to obtain substrates (silica) that improve the stability of different materials. For instance, the immobilization of enzymes such as peroxidase [17], l-lysine [18] and essential oils [19], resulted in hybrid materials with greater chemical stability and the potential for applications in the food industry, cosmetics and pharmaceuticals. Sol-gel is the process through which a network is formed from a solution via a progressive change of the liquid precursor(s) into a sol and then to a gel and, in most cases, to a dry network [20]. The low processing temperature combined with the high sol homogeneity due to mixing on the molecular scale renders sol–gel technology ideal for the fabrication of organic–inorganic hybrid materials by entrapment of several thermolabile organic substances (polymers, drugs or biomolecules) in the glassy matrix, which enabling the modification of the morphology and physical properties of the sol–gel products [21], [22], [23].

The development of hybrid composite materials bearing hydrolysable tannins and phenolic compounds such as tannic acid has been described in the literature. Tannic acid was employed as a template in the synthesis of mesoporous silica nanoparticles, which were shown to be active in protein adsorption and enzyme encapsulation [24]. Monodisperse and mesoporous composites were prepared via the modified Stöber method in a one-pot synthesis. The resulting systems demonstrated high antioxidant activity using tannic acid with antioxidant agent. These types of composites with tunable physical and chemical properties are a novel platform for use as promising engineered nanostructures for various biomedical applications [25]. The preparation of poly (tannic acid) (p(TA)) particles by crosslinking with glycerol diglycidyl ether (GDE) and trimethylolpropane triglycidyl ether (TMPGDE) was shown to be an effective antioxidant material and exhibited a strong antimicrobial effect [26]. Modified nanoparticles of tannic acid were pre-prepared in the presence of metal ions (Ag(I) and Cu(II)), and the antimicrobial properties increased approximately four fold against three common bacterial strains compared with those of free tannic acid. In this case, some researchers suggested that smaller metal nanoparticles can directly cross and penetrate the cell membrane and damage the vital enzymes in microorganisms, as observed in the nanoparticles obtained from tannic acid and Cu(II) [27].

The mild polymerization conditions of the sol-gel method, i.e., room temperature operation and the absence of an extreme pH, make it an ideal strategy for inorganic-organic hybrid material development. Different sol-gel routes have been described in the literature. To our knowledge, comparative studies of the use of silicate-based, non-hydrolytic and hydrolytic routes catalyzed by basic and acidic catalysts have not been reported in the literature. These routes have different characteristics because the synthesis pH, the nature of the catalysts and the rate of the hydrolysis and condensation reactions can influence the final material properties [28].

Tannin extract has not been encapsulated via sol-gel methods for the evaluation of its antimicrobial activity. In the present work, the tannin extract from Acacia mearnsii was encapsulated in silica using different sol-gel process routes to obtain a powdered solid material with potential antimicrobial properties. The different routes were silicate-based, non-hydrolytic and acid- or base-catalyzed hydrolytic routes, with the aim of preserving the intrinsic properties of the tannins. The effects of the sol-gel route on the elemental, structural, textural and morphological characteristics as well as the antimicrobial performance of the tannin-encapsulated silica are discussed.