Bio-dissolution of colloidal-size clay minerals entrapped in microporous silica gels

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Abstract

Four colloidal-size fractions of strongly anisotropic particles of nontronite (NAu-2) having different ratios of basal to edge surfaces were incubated in the presence of heterotrophic soil bacteria to evaluate how changes in mineral surface reactivity influence microbial dissolution rate of minerals. To avoid any particle aggregation, which could change the reactive surface area available for dissolution, NAu-2 particles were immobilized in a biocompatible TEOS-derived silica matrix. The resulting hybrid silica gels support bacterial growth with NAu-2 as the sole source of Fe and Mg. Upon incubation of the hybrid material with bacteria, between 0.3% and 7.5% of the total Fe included in the mineral lattice was released with a concomitant pH decrease. For a given pH value, the amount of released Fe varied between strains and was two to twelve-fold higher than under abiotic conditions. This indicates that complexing agents produced by bacteria play an important role in the dissolution process. However, in contrast with proton-promoted NAu-2 dissolution (abiotic incubations) that was negatively correlated with particle size, bacterial-enhanced dissolution was constant for all size fractions used. We conclude that bio-dissolution of nontronite particles under acidic conditions seems to be controlled by bacterial metabolism rather than by the surface reactivity of mineral.

Graphical abstract

A study of the bio-dissolution of size-selected anisotropic nontronite particles immobilized in a silica gel reveals that microbial dissolution of NAu-2 is dependant on the metabolism of bacteria rather than on the reactivity of mineral surfaces.

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Highlights

► We examine how reactivity of mineral surfaces affects microbial dissolution. ► We use of size-selected anisotropic minerals (NAu-2) to vary surface reactivity. ► Bio-dissolution of NAu-2 seems to be controlled by bacterial metabolism. ► Silica gels as original approach for studying mineral–bacteria interactions.

Introduction

In soils and near subsurface environments, microorganisms play a pivotal role in the dissolution of geo-materials, thereby contributing to elements cycling, soil fertility and water quality. Microbial-mediated weathering of minerals has been documented for a wide variety of rocks and mineral phases characterized by different surface properties and solubilities, including basalts, carbonates, phosphates, felspars, oxides and phyllosilicates [1], [2], [3], [4], [5], [6], [7], [8], [9], [10], [11]. Bacteria are known to accelerate mineral dissolution either through oxido-reduction reactions or through the release of metabolic by-products [2], [4], [5]. Redox processes often involve bacteria that obtain energy from solid phase minerals. For instance, iron-reducing bacteria can use structural Fe(III) in minerals as terminal electron acceptor for anaerobic respiration. Bacterial metabolism can result in the excretion of protons, inorganic acids (e.g. carbonic acid) and a variety of low-molecular weight organic acids such as citrate, oxalate and gluconate [12], [13]. These are important chemical agents of mineral alteration due to their ability to decrease pH, thus enhancing proton-promoted dissolution and/or to withdraw cationic constituents from the mineral lattice through complexation. In response to Fe limitation, bacteria also release siderophores, a group of potent Fe(III)-scavenging compounds that contribute to the weathering of common Fe-oxyhydroxides and Fe-bearing silicate minerals [4], [14].

The extent of mineral dissolution is expected to depend on the quantity and quality of reactive species at the solid/solution interface (H+, OH, ligands, reductants, oxidants), and at the same time, on the reactivity of mineral surfaces (surface area, reactive site density). The influence of physico-chemical conditions and crystallographic and textural properties of crystal faces on abiotic dissolution process has been widely studied [13], [15], [16], [17], [18], [19]. Although it is recognized that bacteria have a significant effect on mineral weathering and dissolution, the extent to which the reactivity of mineral surfaces affects microbial dissolution remains poorly understood. This may be due to the difficulty in finding two minerals having the same chemical composition and at the same time different surface reactivity. Still, bacteria are sensitive to chemical changes in their environment, so that interaction with different mineral surfaces is expected to trigger different bacterial responses. One possible way of investigation is to use minerals having surfaces with contrasted reactivity such as 2:1 phyllosilicates. These strongly anisotropic mineral particles possess a layered structure with one octahedral sheet sandwiched between two tetrahedral sheets. Due to their anisotropic shape, two types of surfaces with different chemical composition and structure, and consequently with different surface properties and reactivity are present, i.e., edge surfaces and basal surfaces. Since the proportion of edges faces increases with decreasing particle size, comparing the extent of microbial dissolution of mineral particles for particles with varying ratios of basal to edges faces appears as a relevant way for studying the link between surface structure and bacterial alteration.

In a previous study [20], we evidenced a clear effect of the basal/edges ratio of phyllosilicates on proton-promoted dissolution by using four size-calibrated colloidal fractions of anisotropic nontronite (NAu-2). The aim of the present study is to investigate how the same changes in mineral reactivity (basal vs. edges) influence microbial dissolution, which should allow discriminating proton-promoted effects from those directly linked to bacterial metabolism. This work deals with biotic dissolution of the particles, while analysis of the proton-promoted dissolution of the same minerals is described elsewhere [20]. To avoid adsorption of colloids onto bacterial cells and uncontrolled particle aggregation that can lower the reactive surface area, the stable aqueous colloidal suspension of nontronite was homogenously dispersed in a porous silica gel before dissolution experiments.

Section snippets

Materials and methods

Two series of experiments were carried out. The first series aimed at checking the biocompatibility of synthetised hybrid silica gels, whereas the second one provided a detailed investigation of bacterial dissolution for four size fractions (Table 1) of mineral particles embedded in silica gels.

Hybrid silica gels: biocompatibility and spreading of bacteria

As shown in Fig. 1c, the inoculation of NAu-2-doped silica gel plates resulted in the formation of colonies. Silica gel plates without incorporated minerals but supplemented with dissolved Fe and Mg also supported bacterial growth (Fig. 1d). This shows that the autoclaving procedure was efficient in removing biocide alcohol traces. Furthermore, similar plating efficiencies were observed for these two culture conditions. This strongly suggests that Fe and Mg from mineral particles are available

Conclusions

Immobilizing of well-characterized size-selected colloidal clay particles in a TEOS-derived silica gel is an original way to simulate mineral–bacteria interactions in nutrient-poor mineral environment and for analyzing in detail microbial dissolution of colloidal-size mineral particles. Using such a setup and technique, we were able to demonstrate that microbial dissolution of NAu-2 is controlled by bacterial metabolism and the nature of produced metabolites rather than by reactive surface of

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