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Chin.J.Geochem.(2011)30:187–192 DOI: 10.1007/s11631-011-0500-z

Interactions between Bacillus mucilaginosus and silicate minerals (weathered adamellite and feldspar): Weathering rate, products, and reaction mechanisms MO Binbin1,2 and LIAN Bin1* 1

State Key Laboratory of Environmental Geochemistry, Institute of Geochemistry, Chinese Academy of Sciences, Guiyang 550002, China

2

Graduate University of Chinese Academy of Sciences, Beijing 100049, China

* Corresponding author, E-mail: [email protected]

Received June 20, 2010; accepted July 10, 2010 © Science Press and Institute of Geochemistry, CAS and Springer-Verlag Berlin Heidelberg 2011 Abstract Bacillus mucilaginosus is a common soil bacterium, and usually used as a model bacterium in studying microbe-mineral interactions. Several reaction mechanisms of B. mucilaginosus weathering silicate minerals were proposed. However, the molecule mechanisms and detailed processes were still unclear. In this paper, bacterium-mineral interactions were studied in terms of variations in pH value over the experimental period, variations in mineral composition, weathering rates of silicate minerals and volatile metabolites in the culture medium, etc., to further explore the bacterium-mineral interaction mechanisms. The results showed that B. mucilaginosus could enhance silicate mineral weathering obviously. The weathering rates were quite different for various kinds of silicate minerals, and the weathering rate of weathered adamellite could reach 150 mg/m2/d. Although B. mucilaginosus produced little acidic substance, pH in the microenvironment of bacterium-mineral complex might be far lower than that of the circumjacent environment; a large amount of acetic acid was found in the metabolites, and was likely to play an important role as a ligand. These results appear to suggest that acidolysis and ligand degradation are the main mechanisms of B. mucilaginosus dissolving silicate minerals, the formation of bacterium-mineral complexes is the necessary condition for the bacteria weathering silicate minerals, and extracelluar polysaccharides played important roles in bacterium-mineral interaction processes by forming bacterium-mineral complexes and maintaining the special physicochemical properties of microenvironment. Key words Bacillus mucilaginosus; silicate mineral; interaction; weathering rate; mechanism

1 Introduction Silicate minerals are the most important rockforming substances in the Earth crust, and it is acknowledged that microorganisms play a crucial role in the weathering processes of silicate minerals (Xie Xiande and Zhang Gangsheng, 2001; Ehrlich, 1996; Chen Feng, 2001). For this reason, increasing studies were carried out in this area. The available studies showed that several interaction mechanisms between microbes and silicate minerals were proposed, including acidolysis, alkaline hydrolysis, ligand degradation, enzymolysis, capsule absorption, extra-cellular polysaccharide redox and comprehensive effects (Li Sha et al., 2006; Li Fuchun et al., 2006; Lian Bin et al., 2002; Berthelin, 1988; Wu Tao et al., 2007), each of which www.gyig.ac.cn www.springerlink.com

has its reasonable basis to some extent. However, no one could elucidate clearly the detailed dissolving processes and molecular mechanisms of microbes weathering silicate minerals. For instance, acidolysis is the main accepted mechanism of microbes weathering silicate minerals (Jongmans et al., 1997; Cameselle et al., 2003; Li Sha et al., 2006), however, producing little acidic substance, yet, Bacillus mucilaginosus could promote the weathering of minerals obviously (Lian Bin et al., 2002; Basak and Biswas, 2009). Up to now, no involved enzyme was found to prove enzymolysis mechanism, and the other mechanisms proposed also lack sufficient evidence (Lian Bin et al., 2002), and further studies need to be done to perfect these mechanisms (Wu Tao et al., 2007). B. mucilaginosus, namely a silicate bacterium, is one of the common soil bacteria, and is usually used

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as a model strain in research on silicate mineral weathering (Liu Wuxing et al., 2006; Basak and Biswas, 2009; Hu Xiufang et al., 2006; Kupriyanova-Ashina et al., 1998; Malinovskaya et al., 1990). Extensive studies on the bacterium were mainly focused on the potassium releasing from soil minerals and application as a bacterial bio-fertilizer like PGPR (plant growth-promoting rhizobacteria) (Basak and Biswas, 2009), and wastewater treatment using the bacterial as biosorbent (Lian Bin et al., 2004; 2008; Li Jing et al., 2006; Cao Wenchuan et al., 2010). In many of these studies regarding B. mucilaginosus weathering silicate minerals, variations in the concentrations of various ions composing the silicates were examined, but variations in the concentrations could not reflect weathering rates because of either being adsorbed by biomass, or forming secondary silicates. In this paper, interactions between B. mucilaginosus and silicate minerals were studied in terms of pH values over the experimental period (50 d), variations in mineral compositions, weathering rates of silicate minerals, and volatile metabolites excreted by the bacterial, and the interaction mechanism was further explored.

2 Materials and methods 2.1 Bacterial culture Bacterial strain (B. mucilaginosus K02, GenBank database accession number: HM579819, stored at the Environmental Biological Science and Technology Research Center, Institute of Geochemistry, Chinese Academy of Sciences) was inoculated into 100 mL sterile medium (per 1000 mL medium containing 5 g of sucrose, 5 g of Na2HPO4·12H2O, 0.5 g of MgSO4·7H2O, 0.1 g of calcium carbonate, 1.0 mg of ferric chloride, in secondary deionized water) and incubated on a rotary shaker at 150 r/min and 28℃ for 1 day. 2.2 Mineral phases and chemical compositions of silicate minerals Silicate mineral I (collected from Rongxian County, Guangxi Province, China) and silicate mineral Ⅱ(collected from Lingshou County, Hebei Province, China) were crushed and sieved to collect grains as large as 20–40 mesh, ultrasonic-washed with secondary deionized water, and dried at 50℃ to constant weight. The mineral samples were cut into pieces, measuring 1cm×1cm×1mm in size, and burnished with 5 μm abrasive. The minerals were cut and polished into thin sheets for observation under microscope. The mineral compositions and relative contents were identified by X-ray diffractometry (XRD, Ri-

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gaku D/Max-2200, CuKα at 40 kV and 30 mA, and 3º/min scan rate), and the chemical compositions of silicate minerals were determined by using the chemical analysis method, the polished sheet mineral samples were observed under microscope (G46307, leitz, wetzlar, Germany) to determine the rock type. 2.3 Experimental settings for microbe-mineral interactions A batch of experiments was made to explore different aspects of the bacterium-mineral interactions over 50 d. Three groups of experiments were carried out as follows: 1000 mg grains of silicate mineral I, silicate mineralⅡ, and glass powder were added in 250 mL flasks (containing 100 mL culture medium), respectively, sterilized at 121℃ for 20 minutes, followed by inoculating 2 mL culture solution of B. mucilaginosus, and incubated on a rotary shaker at 150 r/min, and at 28℃. Each group has 5 samples, incubated for 10, 20, 30, 40, and 50 d, respectively. Control experiments were carried out in parallel to the experimental runs, whose experimental conditions were identical to those of the treatment experiments, but with autoclaved bacterial culture solutions instead of living bacteria. During the experimental period over 50 d, the pH values were measured every 10 d. At the end of experiments (incubation time 50 d), volatile metabolites in the cultures were extracted with ether and analyzed using HP6890/HP5973 GC/MS (Hewlett Packard, USA) (Zhou et al. 2004), and the interaction products of silicate minerals were determined by XRD. Another batch of experiments was conducted to determine silicate mineral weathering rates by measuring the weight variations of samples after the bacterium-mineral interactions over 50 d, experimental conditions were identical to those of the first batch of experiments, but with piece samples (1 cm ×1 cm ×1 mm) instead of mineral grains. Three groups of experiments were carried out. The first one allowed the minerals to be in direct contact with the bacterial cells (contact experiments) and the second one allowed the minerals to interact only with the bacterial metabolic products (separation experiments, separating the minerals and bacteria with 0.22 μm pore-size semipermeable-membrane, the samples were wrapped tightly at least in 4 layers). The third group referred to the control experiments of the first one, by adding autoclaved bacterial culture solution instead of living bacteria (control experiments).

3 Results and discussion 3.1 The chemical compositions of silicate minerals and the identification of silicate rock types

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The results of chemical compositional analysis are given in Table 1. Microscopic observation showed that silicate mineral I was weathered adamellite, the grain size of quartz ranges from 0.1 to 0.5 mm, and the grain size of clay minerals ranges from 1 to 5 μm; Silicate mineral II was identified as potassium feldspar with high purity and large crystal grains, and the weathering degree was low, little weathering occurred in the clearances between crystal grains. 3.2 Variations in pH values of the cultures during bacterium-mineral interactions In the first batch of experiments of bacterium-mineral interactions, by visual observation, the bacteria and silicate mineral grains sunk at the bottom of the flasks, and aggregated together, and no naked mineral grains were observed. Every 10 d, pH values of the cultures were measured,and then measured again after the cultures being autoclaved. The experimental results showed that all pH values of the cultures in the controls (free of living bacteria) remained almost unchanged during the experiment period (Fig. 1a, b, c, ■), pH values of the cultures (before being autoclaved) in experiments (with living bacteria) during the incubation period decreased slightly with incubation time, but the differences between experiments and controls were not obvious. After being autoclaved, pH values of the cultures in experiments decreased obviously with the incubation time, as compared with those of the control experiments (Fig. 1a, b, c, ◆). As shown in Fig. 2, in the second batch of experiments, after 50 d of incubation, there was no significant difference in pH values between experimental cultures and controls before being autoclaved, but obviously decreasing pH values of experimental cultures were measured after the cultures being autoclaved, and the difference in pH values between experiments and controls was higher than 1 pH unit. The results and previous studies indicated that because B. mucilaginosus could excrete extracellular polysaccharide and had high viscosity (Welch and Ullman, 1999; Malinovskaya et al., 1990; Lian Bin, 1998a), the bacteria existed in a form of bacterium-mineral complexes, and the metabolites were tightly enclosed in the complexes, so there was no obvious difference in pH values between experiment groups and controls before being autoclaved. After being autoclaved, metabolites, especially organic acids, were released from the bacterium-mineral comTable 1 Chemical composition Weathered adamellite Potassium feldspar

SiO2 67.20 69.70

plexes, pH values of the solutions decreased obviously (around 1.0 pH unit maximum, as compared with control experiments). Considering that the volume of bacterium-mineral complexes was relatively small (the volume of silicate minerals was less than 0.4 mL, and the culture medium volume was 100 mL), and the culture medium had some buffer capacity, we could speculate that a large amount of acidic substances existed in bacterium-mineral complexes, and the pH values might be very low (<5, by estimate) in the microenvironment of bacterium-mineral complexes. In the second batch of experiments, the results were similar to those of the first batch (Fig. 2), i.e., pH values had a little decrease relative to those of controls before being autoclaved, and pH values decreased drastically after being autoclaved. The pH values of the culture solutions containing weathered adamellite showed a continuously decreasing trend during 50 d of incubation, this might be related to continuous mineral dissolution and nutrients supply for the bacterial growth; potassium feldspar and glass powder were hardly dissolved or insoluble, the pH values tended to remain stable after 30 d of incubation. Thus, in the bacterium-silicate mineral interfaces, the pH values were low, H+ ion exchanged with cations, and the minerals were dissolved by acidolysis. 3.3 Variations in weight of samples and weathering rate calculation After 50 d of interaction, the weights of the samples were measured. The experimental data of weight variation (Table 2) showed that (1) weathered adamellite was drastically dissolved by the bacterial culture, and potassium feldspar was hardly dissolved. Potassium feldspar consists mainly of pure K-feldspar and a small amount of quartz, with large crystal grains (2–4 mm), weathering degree was relatively low, indicative of being hardly dissolved (Liu et al., 2006). However, weathered adamellite consists of several kinds of layer silicate minerals (see Table 3), characterized by smaller grain size and higher weathering degree, and it was easy to dissolve compared with feldspar. The results were similar to previous references (Lian Bin, 1998b; Wu Tao et al., 2007); (2) in case that minerals were in direct contact with bacteria, mineral weathering rates were obviously higher than those of control experiments (free of living bacteria), and at the same time, the dissolving rates of minerals in control experiments were higher than those in the separation experiments.

The chemical compositions of silicate mineral samples (%)

Al2O3 17.19 14.69

K2O 2.99 10.91

Na2O 1.45 4.13

CaO 4.98 0.37

MgO 1.49 0.077

FeO 0.17 0.13

Weight loss by burning 4.72 0.11

Total 100.19 100.007

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Fig. 1. Comparison of pH values of the cultures with the controls. Note: pH values of the cultures were measured after being autoclaved.

Table 2

Weight variations of silicate minerals after bacterium-mineral interactions (piece samples: 1 cm ×1 cm ×1 mm) Sample

Experimental condition Before experiment After experiment Decreased weight

Table 3 Mineralogical composition Before After Changing trend

Weight of weathered adamellite (mg) Contact Control Separation experiment experiment experiment 316.4 213.8 228.4 314.6 212.8 228.3 1.8 1.0 0.1

Weight of potassium feldspar (mg) Contact Control Separation experiment experiment experiment 439.6 366.9 379.7 439.4 366.8 379.7 0.2 0.1 0

Relative contents of mineralogical compositions in weathered adamellite before and after bacterium-mineral interaction Quartz 42.98 53.38 ↑

Montmorillonite 7.16 2.26 ↓

Illite 13.75 – ↓

Kaolinite 9.88 2.07 ↓

Chlorite 1.14 – ↓

Feldspar 25.07 22.58 ↓

Pyrophyllite trace 2.53 ↑

Hornblende trace 1.62 ↑

Calcite – 15.53 ↑

dissolution strongly, but in the separation experiments, the weathering rate of weathered adamellite was lowest. Potassium feldspar could hardly be dissolved. According to the decrease of weights (1.0 and 1.8 mg, control and treatment experiments, respectively), the surface area (240 mm2, sample size 1 cm ×1 cm ×1 mm) and incubation time (50 d) and the weathering rate of weathered adamellite were calculated, and the results are 83.3 and 150 mg/m2/d for control and treatment experiments, respectively. Fig. 2. Comparison of pH values of the cultures (before and after

3.4 The transformation of mineral composition

autoclave) with the controls. Note: pH values of the cultures were measured after 50 d bacterium-mineral interactions (piece samples).

Unexpectedly, the weathering rate in separation experiment was lower than that in control experiment. By analyzing the experiment data and conditions carefully, it was revealed that the result was reasonable for the following three reasons: (1) the mineral grains could not be in contact with the bacteria, there was no bacterium-mineral interaction; (2) since bacterial metabolites mainly existed in bacteria aggregates, there was no obvious decrease in pH value of bulk solution, and the minerals also could not be in direct contact with the metabolites; and (3) although the culture medium could dissolve and weather minerals, as the mineral grains were packed in a small space with, at least, 4 layers of 0.22 μm pore-size semipermeable-membrane, diffusing was restricted after reaching dissolution equilibrium, further dissolution was limited. The experimental results indicated that the culture medium could dissolve and weather the weathered adamellite, and the bacteria enhanced mineral

As bacteria could enhance the weathering degree of weathered adamellite obviously, the mineral composition of the samples was analyzed after 50 d of bacterium-mineral interactions by XRD, and the results (Table 3) showed that there were obvious variations in mineral compositions and contents. The analytical results of mineral compositions indicated that B. mucilaginosus had obvious selectivity toward different minerals in the processes of bacterium-mineral interactions. B. mucilaginosus could dissolve illite, kaolinite, and chlorite prior to other silicate minerals, and produce pyrophyllite and hornblende. The weathering products of silicate minerals were similar to those obtained in previous report (Wu Tao et al., 2007). Calcite in interaction products might be formed by the combination of CaO contained in the minerals (see Table 1) and dissolved CO2, or CO2 released by the respiration of B. mucilaginosus. Carbonic anhydrase produced by the bacterial may help Calcite formation in the culture (Zhou Xueying et al., 2010). Because of its compact structure, high purity,

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great crystal grain, and low weathering degree, potassium feldspar used in the experiments was hardly dissolved.

were dissolved by co-action of acidolysis and ligand degradation.

4 Conclusions

3.5 Analysis of volatile compositions in the cultures The volatile metabolites in the three culture solutions (containing weathered adamellite, potassium feldspar, and glass powder, respectively, incubation time 50 d) were extracted with ether and analyzed using HP6890/HP5973 GC/MS (Hewlett Packard, USA) (Zhou et al., 2004). The results (Table 4) showed that in weathered adamellite-containing culture solution, 10 volatile compositions were identified, accounting for 61.65% of the total peak area, in potassium feldspar-containing culture solution, 13 compositions were identified, accounting for 70.61% of the total peak area, in glass powder-containing culture solution, and only 2 compositions were identified, accounting for 57.58% of the total peak area. There were great differences in volatile compositions among the three samples, and acetic acid was the only composition existing in all the three culture solutions. At all conditions, acetic acid existed in culture solutions, and was the most content volatile composition. Previous studies demonstrated that due to the complexation of organic acid radicals, at the same pH value, the solubility of organic acids was far greater than that of inorganic acids (Pokrovsky et al., 2009; Welch and Ullman, 1996). This indicated that, as a main composition in the culture solutions, acetic acid was likely to play an important role as a ligand, and the minerals Table 4

B. mucilaginosus could enhance the dissolution of minerals in culture solutions, and the dissolving rates might be great different for different kinds of silicate minerals. The mechanism of B. mucilaginosus weathering silicate minerals was likely to be described as follows: in the microbe-mineral interaction processes, B. mucilaginosus contacted with mineral grains and formed bacterium-mineral complexes by its extra-cellular polysaccharide, and the physicochemical properties in the microenvironment of bacterium-mineral complexes were distinguished from those in the circumjacent environment in pH value, viscosity and concentrations of organic acid, etc. It’s in the special microenvironment (low pH, high viscosity, high acetate concentrations), and under the co-action of H+ ion exchange and acetate complexation, silicate minerals were dissolved, and further formed secondary silicate minerals. Therefore, forming bacterium-mineral complex was the necessary condition for the bacteria dissolving silicate minerals; in the processes, extra-cellular polysaccharide played important roles in the formation of complexes and maintaining the special properties of the microenvironment. Acetic acid was found in metabolites at all culture conditions, and was the most content composition in volatile metabolites, it played an important role in bacterium-mineral interactions.

Volatile compositions in culture solutions

Sample 1

Sample 2

Sample 3

No.

Compound

RC (%)

Compound

RC (%)

Compound

RC (%)

1

Acetol

14.1

Acetol

11.67

43.08

2

2-Ethyl-hexanol

1.94

Acetic acid

17.30

Acetic acid 2, 3-dihydro-3, 5-dihydroxy6-methyl-4H-Pyran-4-one

3

Acetic acid

29.15

Protoanemonine

0.66

4

1.12

2-Furanmethanol

1.02

2.82

2(5H)-Furanone

0.50

0.45

2-Hydroxy-2-cyclopenten-1-one

2.64

2.60

Furaneol

0.56

8

Furfuryl alcohol 2-Hydroxycyclopent-2-en-1-one 2-Butenoic acid 3, 5-dihydroxy2-methyl-5, 6-dihydropyran Benzoic acid

0.78

2-Propanone, 1, 3-dihydroxy-

21.1

9

5-oxymethyl furfurole

1.42

7.69

10

Palmitic acid

7.27

5 6 7

11

2-Hydroxy-γ-butyrolactone 2, 3-Dihydro-3, 5-dihydroxy-6-methyl-4H-pyran-4-one Retardex

12

Hydroxymethylfurfurole

1.60

13

Palmitic acid

3.42

Total

61.65

14.50

1.79 0.66

70.61

57.58

Note: RC (%) is relative content (%) calculated by the area-normalization method. Samples 1, 2, 3 represent weathered adamellite, potassium feldspar and glass powder contained in culture medium, respectively.

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With regard to silicate bacteria dissolving silicate minerals, Lian Bin et al. (2002) presented a comprehensive view of bacterium-mineral complex theory, and this view was worthy of further exploration. As stated above, bacterium-mineral complexes were markedly distinguished from those in the circumjacent environment in many aspects, studies on the metabolites (organic acids, polysaccharides, ligands) and physicochemical properties (pH, concentrations of various metabolites, redox potential, and viscosity) of the microenvironment were likely to be a breakthrough in the field of research on the mechanisms of bacteria weathering silicate minerals. Acknowledgements This research project was financially supported by the National High Technology Research and Development Program of China (2008AA06Z108). The authors would like to extend their thanks to Senior Engineer Feng Junming for his help in mineral identification. References

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