Biosynthesis of iron oxide nanoparticles from mineral coal tailings in a stirred tank reactor

Hydrometallurgy 184 (2019) 199–205

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Biosynthesis of iron oxide nanoparticles from mineral coal tailings in a stirred tank reactor

T

⁎

Danielle Maassa, ,1, Alexsandra Valériob,1, Luís Antonio Lourençob,1, Débora de Oliveirab, Dachamir Hotzab a b

Institute of Science and Technology (ICT), Federal University of São Paulo (UNIFESP), 12231-280 São José dos Campos, SP, Brazil Department of Chemical and Food Engineering (EQA), Federal University of Santa Catarina (UFSC), 88040-900 Florianópolis, SC, Brazil

A R T I C LE I N FO

A B S T R A C T

Keywords: Biomining Iron oxide nanoparticles Mineral coal tailings Rhomboclase Rhodococcus erythropolis

Chemical oxidation of mineral coal tailings is one of the most important environmental issues during the lifetime of a mine. The presence of sulfur compounds favors the occurrence of metal acid leaching, which contaminates water with bioaccumulative metals, rendering it unsuitable for domestic and agricultural use. The biomining of residual iron present in these tailings and its transformation into high added-value by-products is economically and environmentally attractive. The extraction of residual iron from rhomboclase and its transformation into nanoparticles by Rhodococcus erythropolis ATCC 4277 free-cells in a stirred tank reactor was studied. R. erythropolis ATCC 4277 biomining capacity was improved by diminishing stirring rate and oxygen flow rate of stirred tank reactor. According to the results of the 22 full factorial design, smaller sizes of iron-based nanoparticles (< 50 nm) were achieved when a stirring rate of 100 rpm and an oxygen flow rate of 0.1 L.min−1 were used. Composition analyses (XRD, FTIR, TEM, EDS and Mössbauer spectroscopy) showed that the synthesized nanoparticles are formed by iron oxide (β-Fe2O3 and α-Fe2O3). The proposed biomining process represents an environmental-friendly and sustainable process for the transformation of mineral coal tailings into products with greater added value.

1. Introduction Mining activity has been considered one of the major indicator of industrial development. However, this activity produces large amounts of waste and the disposal of mine tailings is one of the most important environmental issues during a mine lifetime. Some of these wastes are inert and hence not likely to represent a significant impact to the environment (Alp et al., 2009). The mine tailings are usually stored as a slurry of high water content into large tailing ponds (Evangelou, 1995; Ferrow et al., 2005; Oliveira et al., 2016). The harmfulness of tailing slurries can be decreased by adding neutralizing substances, so that they can be chemically stabilized into a form in which harmful substances cannot release to the environment (David Bonen, 1995; Oliveira et al., 2016; Poon and Lio, 1997). Other fractions of mining waste, especially tailings from processing of sulfide minerals like pyrite (FeS2) and pyrrhotite (Fe1-xS2), can cause environmental risks due to their tendency to oxidize in the presence of water or air (Hansen et al., 2013; Sánchez-Andrea et al., 2014). The stabilization of these iron sulfide minerals causes considerable costs for

mining companies since their discharge should be strictly controlled. Therefore, the reprocessing of iron sulfate minerals tailings as a source of metals and chemicals or as a raw material of construction boards has been studied (Klein et al., 1993; Nehdi and Tariq, 2007; SánchezAndrea et al., 2014). Biomining has emerged as an innovative approach for sulfide mineral processing. This process utilizes biological systems (chiefly prokaryotic microorganisms) to facilitate the extraction and recovery of metals from ores (Johnson, 2014). Biomining is considered an environmentally-friendly process when compared to traditional physicalchemical methods since less energy and chemical reagents are necessary (Brierley and Brierley, 2013). The application of these biological process for metal recovery has been widely applied commercially throughout the world to enhance the extraction of base metals from sulfide ores (Brierley and Brierley, 2013; Lang and Schüler, 2006). Currently, it is responsible for approximately 15–25% of the world's copper production, 5% of gold and smaller percentages of cobalt, nickel, uranium, and zinc (Colica et al., 2012; Nancharaiah et al., 2016).

⁎

Corresponding author. E-mail address: [email protected] (D. Maass). 1 These authors contributed equally to this work. https://doi.org/10.1016/j.hydromet.2019.01.010 Received 7 June 2018; Received in revised form 19 December 2018; Accepted 21 January 2019 Available online 23 January 2019 0304-386X/ © 2019 Elsevier B.V. All rights reserved.

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Usually biomining is used to describe both mineral “bioleaching” and “biooxidation” processes. Mineral “bioooxidation” refers to the exposition of metals that are occluded or blocked within the mineral matrix through microbial decomposition. Conversely, bioleaching should be used to describe the conversion of an insoluble metal into a soluble form, thereby extracting the target metal to the aqueous solution. Besides the simple metals bioleaching, it is possible to transform these metals into nanoparticles (NPs). In the recent years, several researches have studied the biosynthesis of metal NPs by a great variety of microorganisms (Mahmoud et al., 2017). Kundu et al. (2014) suggested that the synthesis of metal NPs by different microorganisms, e.g. Rhodococcus sp. and Bacillus licheniformis, may occur intracellularly being catalyzed by specific enzymes as well as extracellularly chemical conversion carried out by the metabolites secreted by the organisms. Also, these authors studied ZnO NPs formation by Rhodococcus pyridinivorans NT2, and proposed a sequence of reaction events behind the formation of ZnO NPs extracellularly (Eqs. 1–3).

Zn 4 (SO4 )(OH)6. xH2 O ZnSO4 . 3Zn(OH)2 + xH2 O

(1)

2[ZnSO4 . 3Zn(OH)2] 5ZnO + Zn3O(SO4 ) 2 + 6H2 O

(2)

Zn3O(SO4 )2 3ZnO + 2SO2 + O2

(3)

Tropical Culture Collection (CCT) of the André Tosello Research & Technology Foundation (Campinas, Brazil). The cells, cryopreserved in 20% (v/v) glycerol at −80 °C, were reactivated in Petri dishes containing solid Streptomyces medium (SM) (Porto et al., 2017), at 24 °C for 24 h, and subsequently stored at 4 °C. The maintenance medium consisted of: 4.0 g.L−1 of yeast extract, 10.0 g.L−1 of malt extract, 4.0 g.L−1 of glucose, 2.0 g.L−1 of calcium carbonate and 12.0 g.L−1 of agar. 2.3. Pre-culture The pre-culture for the experiments was prepared inoculating R. erythropolis ATCC 4277 colony into 100 mL of a sterilized nutrient medium with the following composition: 6.15 g.L−1 of yeast extract, 5.0 g.L−1 of malt extract, 2.0 g.L−1 of glucose, and 1.16 g.L−1 of calcium carbonate (Todescato et al., 2017). Afterwards, it was incubated for 24 h at 24 °C and 180 rpm. The cells were resuspended in the culture medium previously described to reach an optical density of 0.8 at a wavelength of 600 nm. 2.4. Biosynthesis of iron-based nanoparticles Biosynthesis of iron-based nanoparticles experiments were accomplished in a 7.0 L stirred tank reactor (Bio Tec-Flex, Tecnal, Brazil), with an initial working volume of 4.0 L. The pre-culture (10% v/v) of the initial reactor working volume and 2% (w/w) of rhomboclase was added to the culture medium in each run. The pH of culture medium containing the rhomboclase was adjust to 7.0 with 1.0 M NaOH solution. The reactor was operated with controlled temperature (30 °C) and pH (7.0) for 72 h. The pH was automatically controlled by the addition of 1.0 M HCl or 1.0 M NaOH. The oxygen flow rate was automatically adjusted during the biosynthesis experiments by the equipment probe to achieve the desired dissolved oxygen level. At the end of each cultivation run, a 100 mL sample was withdrawn from the reactor and analyzed for size distribution. A 22 full factorial design (FFD) with center points was proposed to evaluate the significant influence of operating conditions in the final particle size. Stirring rate and oxygen flow rate were selected as independent variables (Table 2). Statistical analysis of the 22 FFD was carried out using a dedicated software (Statistica® 7.0). A significance level (α) of 5% was considered to estimate the significant effects. Furthermore, a desirability profile was generated to determine the optimal process conditions. After the run using the desirability profile conditions, 200 mL samples were lyophilized for 48 h using a freeze dryer (Liotop L101, Liobras, Brazil) and characterized.

Although bioleaching be mediated by using essentially the same consortia of microorganisms (Mahmoud et al., 2017), Rhodococcus sp. has emerged as a new possibility. The remarkable genus Rhodococcus has a broad catabolic diversity and unique enzymatic capabilities, and it is a suitable industrial microorganism not only for biodegradation of many organic compounds but also for biotransformation. Rhodococcus are able to uptake and metabolize hydrophobic compounds, and persist in adverse conditions, especially in the presence of organic solvents and sulfur high contents (Kundu et al., 2014; Todescato et al., 2017). Extensive literature review revealed the synthesis of silver (Ag), gold (Au) (Ahmad et al., 2003) and Zn (Kundu et al., 2014) oxide NPs by Rhodococcus sp. To the best of our knowledge, the biosynthesis of iron NPs by Rhodococcus sp. was not studied so far. Iron nanoparticles (NPs) are a promising material for environmental applications being recently investigated for Fenton catalyst for the oxidation of organic pollutants (Khataee et al., 2017), electrocatalysis of hydrogen evolution reaction (Villalba et al., 2018), photovoltaics applications (Saxena et al., 2017) and adsorption of toxic compounds (Mohammed et al., 2017). Magnetic iron NPs can be applied for biomedical purposes such as targeted drug delivery, imaging, chemotherapy, drug formulation, hyperthermia treatment, radioimmunotherapy and peptide/antibody therapeutics (Mohammed et al., 2017). In this work, the biosynthesis process of ironbased nanoparticles (NPs) from mineral coal tailings (iron sulfate mineral) using R. erythropolis ATCC 4277 into a stirred tank reactor was studied for the first time.

2.5. Chemical and physical analyses Chemical composition of the mineral coal tailings was identified by energy-dispersive X-ray fluorescence spectrometry (EDXRF-7000, Shimadzu) with an attached silicon drift detector (SDD). Crystalline phases were identified by X-ray diffraction (XRD). The diffraction pattern was recorded between 20° and 80° (2θ) with the diffractometer (XRD 6000, Shimadzu) operating at a voltage of 20 kV and a current of 25 mA with CuKα (λ = 15,406 Å) radiation. Size distribution of the iron-based NPs was measured by dynamic light scattering (DLS, Nanoflex, Microtrac S3000/S3500, Particle Metrix). The lyophilized sample and the rhomboclase were analyzed by Fourier transform infrared spectroscopy (Prestige-21 FTIR, Shimadzu) with a diffuse reflectance mode attachment (DRS-8400). All measurements were carried out in wavenumber range of 400–4000 cm−1 at a resolution of 4 cm−1. The sample for transmission electron microscopy (TEM) determination was prepared on a carbon-coated TEM grid. Briefly, NPs sample was diluted in water and sonicated for 30 min at room temperature and then dripped on TEM grid. TEM analysis was carried out at an

2. Material and methods 2.1. Mineral coal tailings Rio Deserto Mining Company Ltd. (Criciúma, Brazil) kindly provided the iron sulfate mineral (rhomboclase) from a coal tailing pile. The ore residue was milled, sieved and used in the particle size range of 100–200 mesh (150–75 mm). 2.2. Microorganism In this work, R. erythropolis was selected for rhomboclase biomining due to its well-known application for desulfurization process (Maass et al., 2015; Todescato et al., 2017) and its capacity to grown in the presence of considered amounts of sulfur compounds. The bacterium R. erythropolis ATCC 4277 used in this study was obtained from the 200

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Table 1 Elemental composition of iron sulfate mineral. Element

C

S

Fe

P

Si

Cs

K

Mn

Pb

Cu

Zn

As

Zr

Se

wt%

58.324

21.754

17.976

0.826

0.752

0.206

0.095

0.029

0.013

0.009

0.007

0.005

0.003

0.001

accelerating voltage of 100 kV for low-resolution imaging (JEM-1011, JEOL). Energy dispersive spectroscopy (EDS) was accomplished coupled to a scanning electron microscope (SEM) (TM3030, Hitachi), after coating the samples on a double-sided carbon tape attached to the grid surface. The hyperfine analysis was accomplished through 57Fe Mössbauer spectroscopy in the transmission geometry without external field application. Measurements were carried out using a standard spectrometer at room temperature, with 57Co radioactive source dissolved in Rh matrix. The spectra were adjusted based on the discrete Gaussian lines for each hyperfine site, obtaining isomeric displacement values related to the pure metallic iron. 3. Results and discussion 3.1. Characterization of mineral coal tailings Elemental composition of rhomboclase before the biosynthesis process is presented in Table 1. The residue is predominantly composed by carbon (58 wt%), sulfur (22 wt%) and iron (18 wt%). The high content of carbon can be associated to the coal wastes and the prominent concentration of iron and sulfur is attributed to sulfides or sulfates (Oliveira et al., 2016). Crystalline phase analysis (XRD) showed that the mineral coal tailings is mostly formed by rhomboclase (JCPDS 00-0270245) (FeH(SO4)2.4H2O), as presented in Fig. 1a. Rhomboclase has a typically post-mining origin since is formed by pyrite alteration, especially in arid climates (Webmineral, n.d.). After biosynthesis, the following phases (see Fig. 1b) were identified: rhomboclase (JCPDS 00027-0245), hematite (JCPDS 01-085-0987) and magnetite (JCPDS 01076-0958). 3.2. Effect of operational conditions on iron-based particle size The biosynthesis of iron-based NPs from rhomboclase by R. erythropolis ATCC 4277 free cells in a stirred tank reactor was studied. The particle sizes obtained according to stirring rate and oxygen flow rate are presented in Table 2. Nanoparticles are generally regarded as those with at least one dimension < 100 nm (Narayanan and Sakthivel, 2010). Therefore, it can be stated that nanometric particles were obtained using the conditions of run 1. The synthesis of iron-based NPs corroborates that Rhodococcus bacteria enable removal of both pyritic and organic sulfur from mineral coal tailings (Natarajan, 2018). Analysis of variance (ANOVA) were carried out to evaluate the significance of the factors. Stirring rate (rpm) was found to be significant with p-value < 0.05 (see Table 3). Higher stirring rate resulted in larger particle sizes, as shown in Fig. 2. According to Rai and dos Santos (2017), studies performed for the production of Au nanoparticles demonstrated that higher stirring of culture medium prevented the releasing of enzymes and proteins responsible for the synthesis of nanoparticles (Ahmad et al., 2005). As the oxygen flow rate was not found to be statistically significant at the range of values studied, this operational parameter can be set at low level (see Table 3). Usually, oxygen has a role as electron acceptor in microbial oxidation and desulfurization (Gogoi and Bezbaruah, 2002; Mahmoud et al., 2017). According to Schüler (1999), Fe compounds bioleaching are favored in microaerobic environments, where the concentration of oxygen is very low, due to the sensitivity of some types of microorganisms to oxygen. Conversely, biodesulfurization of mineral coal is improved in aerobic environments (Gogoi and Bezbaruah, 2002). Despite of Rhodococcus sp. has a preferentially aerobic catabolism the lack of dissolved oxygen

Fig. 1. XRD diffraction of rhomboclase before (a) and after (b) biosynthesis. Table 2 Particle size obtained for different stirring and oxygen flow rates. Run

1 2 3 4 5

201

Stirring rate

Oxygen flow rate

rpm

Level

L.min−1

Level

100 400 100 400 250

−1 +1 −1 +1 0

0.1 0.1 5 5 2.55

−1 −1 +1 +1 0

Particle size (nm)

32.3 826 325 1089 384

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Table 3 ANOVA for factorial-designed runs. Factor

Square sum

Degrees of freedom

Mean square

F-test

p Value

(1) Stirring rate (rpm) (2) Oxygen flow rate (L.min−1) Error Total square sum

606,607.3 77,200.6 27,327.4 711,135.4

1 1 2 4

606,607.3 77,200.6 13,663.7 –

44.39553 5.65005 – –

0.021791 0.140603 – –

Fig. 3. Values predicted by the polynomial model versus experimentally observed for iron-based nanoparticle biosynthesis as a function of particle size (nm) response. Fig. 2. Surface response for particle size (nm) in terms of stirring rate (rpm) and oxygen flow rate (L.min−1).

3.3. Characterization of biosynthesized iron-based nanoparticles

may have forced the production of reductase enzymes, favored the desulfurization and enhanced the production of iron-based NPs. The estimated effects for FFD runs on particle size (nm) are described in Table 4. The most prominent effect was the stirring rate. A multiple regression analysis was applied to experimental results to obtain an equation capable to predict the particles size (Eq. (4)):

TEM analysis confirmed that the particles formed during biosynthesis process are smaller than 100 nm (see Fig. 5), thus corroborating the DLS analysis. The semi-quantitative microanalysis of chemical elements (SEM-EDS) of these iron-based NPs revealed 34 wt% oxygen, 6 wt% iron and 2 wt% sulfur (see Table 5). By comparing the data presented in Table 1, it can be seen a significant reduction in the sulfur content (from 21.754 wt% to 2.169 wt%), suggesting that the R. erythropolis was able to metabolize sulfur in coal. Expressive amounts of oxygen, iron and sulfur may be indicative of both the presence of iron oxides and iron sulfates. To clarify this point, spectroscopy analyses (Mössbauer and FTIR) were accomplished. The presence of carbon in the iron-based NPs can be attribute to intracellular/extracellular metabolites or proteins that are bound to the NPs surface. According to Kundu et al. (2014), these compounds can remain bounded to the NPs even after several washing. Moreover, it can be also associated to coal wastes in the rhomboclase and to residual culture medium. FTIR spectra of rhomboclase before and after the biosynthesis process are presented in Fig. 6. The bands obtained for the rhomboclase before biosynthesis were 490, 594, 673, 995, 1062, 1143, 1232, 1614 and 3445 cm−1. The wide bands centered at are 1614 and 3445 cm−1 are associated with the presence of moisture (Majzlan et al., 2011). The peak at 1143 cm−1 can be associated to alcohols, acetate, ethers and

(4)

PS = 531.26 + 389.425∙SR + 138.925∙OFR

where PS = particle size (nm); SR = stirring rate (rpm); OFR = oxygen flow rate (L.min−1). Predicted and observed values are similar, as shown in Fig. 3. The explained variation for this model was 92.3 to a 95% confidence limit. The coefficient of determination R2 was found to be 0.961, denoting that the model explains 96.1% of the total variations in the system. This ensures a good adjustment of the forward model to experimental data. The best process conditions identified from the desirability profile (see Fig. 4) was stirring rate of 250 rpm and an oxygen flow rate of 2.55 L.min−1. Despite the main effect of stirring rate was negative, i.e., low agitation speed results in low particle size, there are interaction effects among operational parameters, which can explain the desirability profile obtained. Characterization analyses were performed for the NPs formed under the conditions established by the desirability profile. Table 4 Effects estimated from factorial-designed runs for particle size (nm). Factor

Effect

Pure error

Student's t-Test

P-Value⁎

Confidence limit (−95%)

Confidence limit (+95%)

Coefficients

Mean/Intersection (1) Stirring rate (2) Oxygen flow rate

531.26 778.85 277.85

52.275 116.892 116.892

10.163 6.663 2.377

0.009544 0.021791 0.140603

306.336 275.905 −225.095

756.184 1281.795 780.795

531.260 389.425 138.925

⁎

Significant at P < 0.05. 202

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Fig. 4. Profiles for predicted values and desirability to particle size (nm).

Fig. 5. TEM of the iron-based NPs biosynthesized from rhomboclase. Fig. 6. FTIR spectra of rhomboclase before (—) and after (—) biosynthesis.

Table 5 Semi-quantitative microanalysis of the chemical elements in the iron-based NPs synthesized from rhomboclase by R. erythropolis ATCC 4277 free-cells. Element

wt%

Carbon Oxygen Sodium Chlorine Iron Sulfur Calcium Potassium Silicon

35.315 33.615 11.054 8.014 6.178 2.169 1.886 1.140 0.630

carboxyl compounds. Bands in the range of 900 to 1200 cm−1 (995, 1062, 1143, 1232 cm−1) indicate the presence of iron sulfates (Majzlan et al., 2011). The peaks 490, 594, 673 cm−1 are characteristic of SeS bonds, generally associated with iron disulfides (Coates, 2006; Oliveira et al., 2016). The FTIR results corroborate with XRD analysis, i.e. that the material is formed by rhomboclase and iron disulfides. After biosynthesis, the rhomboclase showed the presence of bonds Fe―O and S꞊O which are elucidated by the peaks 617 cm−1 and 1122 cm−1, respectively (Coates, 2006; Wei et al., 2012). The parameters obtained by Mössbauer spectroscopy show the presence of two phases, compatible with Fe3+. Phase 2 presented δ (isomer shift) = 0.24 mm·s−1 and Δ (quadrupole splitting) = 0.55 mm·s−1 (see Table 6). According to Cook and Hoy (2003), the doublet δ = 0.25–0.30 mm·s−1 and Δ = 0.45–0.50 mm·s−1 is the 203

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References

Table 6 Mössbauer parameters for rhomboclase after biosynthesis. Parameters

−1

Δ (mm·s ) δ (mm·s−1) Γ (mm·s−1) RA (wt%)

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Phases 1

2

0.76 0.40 0.39 53.0

0.55 0.24 0.49 47.0

δ = isomer shift, Δ = quadrupole splitting, Γ = line width, RA = relative area.

superparamagnetic spectrum due to Fe3+ in small particles of α-Fe2O3. Mössbauer parameters for phase 1 were δ = 0.40 mm·s−1 and Δ = 0.76 mm·s−1 (see Table 6). These values correspond to beta polymorph of iron(III) oxide (β-Fe2O3), since β-Fe2O3 is magnetically disordered at room temperature and exhibits paramagnetic behavior, a feature that notably distinguishes it from alpha, gamma, and epsilon polymorphs. It has a body-centered cubic bixbyite structure. To the best of our knowledge, any mention of natural occurrence of β-Fe2O3 has not been reported so far, i.e. this compound can be prepared only synthetically (Zboril et al., 2002). The relative area shows that there was 53 wt % phase 1 (β-Fe2O3) and 47 wt% phase 2 (α-Fe2O3) after biosynthesis (see Table 6). The biochemical mechanism behind the formation of iron-based nanoparticles is beyond the scope of this work. A suggested sequence of reaction events can be based on the reported by Kundu et al. (2014) as follows:

Zn 4 (SO4 )(OH)6. xH2O → ZnSO4 . 3Zn(OH)2 + xH2 O

(5)

2[ZnSO4 . 3Zn(OH)2] → 5ZnO + Zn3O(SO4 ) 2 + 6H2 O

(6)

Zn3O(SO4 )2 → 3ZnO + 2SO2 + O2

(7)

Kundu et al. (2014) studied the extracellular formation of ZnO NPs by Rhodococcus pyridinivorans NT2 using Zn4(SO4)(OH)6.0.5H2O as precursor. Thus, as the Zn4(SO4)(OH)6.0.5H2O precursor is similar to rhomboclase (FeH(SO4)2.4H2O) and the same genus of bacterium (Rhodococcus sp.) was used, it is possible to suggest that the formation of Fe2O3 NPs has a similar proposed mechanism. This aspect needs further investigation.

4. Conclusions The bacterium R. erythropolis ATCC 4277 was capable to synthesize magnetic iron oxide nanoparticles from rhomboclase. Statistical analysis of factorial design showed that the lowest levels of stirring rate and oxygen flow rate lead to smaller iron-based particles. According to FTIR, SEM-EDS, and Mössbauer analyses, the NPs synthesized are composed by β-Fe2O3 and α-Fe2O3. The biotransformation of rhomboclase into high added-value products, such as magnetic iron oxide nanoparticles, represents an important improvement to the sustainability of coal mining.

Acknowledgements The authors are thankful to Prof. João Batista Marimon da Cunha of the Federal University of Rio Grande do Sul for the Mössbauer spectroscopy analysis. We also acknowledge the LABMASSA/UFSC (Laboratório de Transferência de Massa) for the laboratory infrastructure. Danielle Maass acknowledges her postdoctoral fellowship provided by CNPq (National Council for Scientific and Technological Development) under project number 154980/2016-1. 204

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