Environmentally friendly recovery of valuable metals from spent coin cells through two-step bioleaching using Acidithiobacillus thiooxidans

Journal of Environmental Management 235 (2019) 357–367

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Research article

Environmentally friendly recovery of valuable metals from spent coin cells through two-step bioleaching using Acidithiobacillus thiooxidans

T

Tannaz Naseri, Nazanin Bahaloo-Horeh, Seyyed Mohammad Mousavi∗ Biotechnology Group, Chemical Engineering Department, Tarbiat Modares University, Tehran, Iran

ARTICLE INFO

ABSTRACT

Keywords: Bioleaching Spent coin cells Metals recovery Acidithiobacillus thiooxidans Kinetics

The technology for recycling the spent coin cells is pressing needed due to a large amount of generated spent coin cells. However, there is little information about the recycling technology of spent coin cells. In this work, a two-step bioleaching method for recovery of metals from spent coin cells by Acidithiobacillus thiooxidans is performed for the first time. In this regard, the growth characteristics of A. thiooxidans was investigated in pure culture and during the two-step bioleaching approach. The highest recovery of Li, Co and Mn was achieved at a pulp density of 30 g L−1, in values of 99%, 60%, and 20%, respectively. The structural analyzes confirmed the progress of bioleaching process. In addition, the kinetics models showed that the chemical reaction was the ratecontrolling step of the two-step bioleaching of spent coin cells. The comparative results between bioleaching and chemical leaching showed that Acidithiobacillus thiooxidans can enhance the leaching of metals. Toxicity characteristic leaching procedure of the spent coin cells powder demonstrated that the bioleached residue met the environmental limitations for safe disposal. In fact, bioleaching is an effective and promising route to reduce the environmental hazard of spent coin cells.

1. Introduction Batteries are divided into two groups: i) non-rechargeable primary batteries such as C-Zn, Zn-Mn, mercury, or primary lithium batteries and ii) rechargeable secondary batteries such as Ni-Cd, Ni-MH and lithium-ion batteries (LIBs) (Kim et al., 2016). Among rechargeable batteries, LIBs have extensively been employed in major areas from cars to microchips (Zeng et al., 2014). Small LIBs are commercially available as coin cells with a diameter of 2–5 cm. Lithium coin cells are designed to maximize energy density and suitable for applications such as memory backups (Zhang and Harb, 2013). It is anticipated that by 2020, the generation of spent LIBs will reach 200–500 ton per year (Vanitha and Balasubramanian, 2013). Generally, a battery consists of a positive electrode, negative electrode, collectors, electrolyte, separator, and metal protective shell. In LIBs, cathode contains lithium compound (LiCoO2, LiNiO2, LiMnO2, LiNi1/3Co1/3Mn1/3O2, LiMn2O4, LiNi0.8Co0.15Al0.05O2, and LiFePO4) (Li et al., 2017) and anode contains graphitic carbon. Anode collector is Cu foil and for the cathode is Al foil. Also, the electrolyte is made of lithium salts such as LiClO4, LiBF4, LiPF6, and LiCF3SO3 that is dissolved in an organic solvent (Bahaloo-Horeh et al., 2016). Furthermore, the common binder material is polyvinylidene fluoride (PVDF) (Zeng et al., 2014). ∗

Today, 35% of the global production of lithium is used in LIBs manufacturing (Swain, 2017). It is estimated that if lithium is not recycled, the world will face a severe shortage of lithium between the year of 2021 and 2023 (Sonoc and Jeswiet, 2014). Also, 25% of global production of cobalt is used in LIBs manufacturing (Santana et al., 2017). It has been shown that with an annual production of 20 million LIBs, all Co mineral deposits on earth will be depleted in less than 60 years (Swain, 2017). By recycling and reusing the LIB materials, a reduction in using natural resources and consuming the energy occurs (Dewulf et al., 2010). Also, the LIBs contain toxic materials such as heavy metals which cause serious health hazards to humans and the environment. These environmental problems reveal further the importance of recycling. Therefore, the recycling of spent LIBs is beneficial for preserving the mineral ores, producing economic revenue from valuable metals, and protecting the environment (Li et al., 2017). For both economic and environmental exploitation, the efficient, simple, eco-friendly and cost-effective technologies need to be developed (Mahmoud et al., 2017). Current efforts to recover metals from LIBs are based on the following technologies: pyrometallurgy, hydrometallurgy, and bioleaching (Vakilchap et al., 2016). Besides the release of hazardous gases such as dioxins and furans in the pyrometallurgical process, the energy consumption of this process is very

Corresponding author. E-mail addresses: [email protected] (T. Naseri), [email protected] (N. Bahaloo-Horeh), [email protected] (S.M. Mousavi).

https://doi.org/10.1016/j.jenvman.2019.01.086 Received 12 September 2018; Received in revised form 21 January 2019; Accepted 23 January 2019 0301-4797/ © 2019 Elsevier Ltd. All rights reserved.

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high (Pradhan and Kumar, 2012) as well as losses of valuable metals in slags (Fomchenko and Muravyov, 2018). Hydrometallurgical processes dominate among all the technologies owing to the share of 57.25% (Zeng et al., 2014). However, hydrometallurgical processes are also associated with environmental hazards due to the usage of toxic reagents to leach metals and a large amount of generated by-products (Pradhan and Kumar, 2012). The acid generated by these approaches could cause water and soil acidification (Zhang et al., 2018). Bioleaching is the process that utilizes the microorganisms activity to recover metals (Kaksonen et al., 2018). Currently, countries are moving towards using the green method of bioleaching because of its lower labor and energy requirements, lower capital investment (Mahmoud et al., 2017), lower hazardous risks, higher performance and needing a few industrial requirements with a mild reaction condition (Faraji et al., 2018). In bioleaching, a wide range of thermophilic, chemolithotrophic, and heterotrophic bacteria as well as fungi have been used for metals mobilization through their various mobilization mechanisms (Işıldar et al., 2016). Acidithiobacillus thiooxidans is one of the most extensively studied acidophilic chemoautotrophic bacteria in bioleaching communities (Işıldar et al., 2019) that can oxidize elemental sulfur as an electron donor in the electron transport chain and generate sulfuric acid and as a result lower the pH of the local environment (Fomchenko and Muravyov, 2018). Bioleaching can be performed through the approach of one-step or two-step based on biomass exposure to waste. In the one-step approach, the powder and bacterial inocula are added simultaneously to the culture medium. In the two-step approach, the powder is added after the bacteria reaches its maximum growth (logarithmic phase of growth). It was reported that the two-step approach is a more efficient process of metal mobilization (Heydarian et al., 2018). One limitation of bioleaching is the slow kinetics which hindered the full commercial scale of bioleaching (Ahmadi et al., 2011). Kinetics information of bioleaching process is important in order to improve the efficiency of metals leaching (Pradhan et al., 2010). For finding the kinetic order of the bioleaching process, the models of diffusion control and chemical control can be considered for a shrinking core particle (Rastegar et al., 2015a,b). Although bioleaching of metals from spent mobile phone (BahalooHoreh and Mousavi, 2017), laptop (Heydarian et al., 2018) and electric vehicle batteries (Xin et al., 2015) have already been used, a literature survey shows that the bioleaching of spent coin cells (SCCs) has not been investigated, therefore the biological knowledge for recycling of SCCs is unknown and there is a gap in this field. Furthermore, to the best of our knowledge, there is no information about kinetic aspects of metals recovery from SCCs. The present study investigated the kinetic aspects and rate controlling step of the process. This is the first report of two-step bioleaching method for the recovery of Li, Co and Mn from SCCs at various pulp densities using A. thiooxidans and also determining the rate controlling aspect. In this regard, the growth characteristics of A. thiooxidans including cell count, pH, and sulfate ion concentration was investigated in pure culture and during the two-step bioleaching approach. The analyzes of XRD, EDX, SEM, and FTIR were performed on SSCs powder before and after bioleaching to evaluate the bioleaching progress. In addition, the kinetics model was used to determine the controlling step and find the kinetic order of reaction. In the next step, the metals recovery in bioleaching were compared with chemical leaching of the SCCs powder. Toxicity characteristic leaching procedure (TCLP) of the SCCs powder was also carried out to assess the toxicity of original and bioleached SCCs powder in the environment.

Table 1 Average percentage of SCCs parts. Component

Anode & Cathode

Plastic Steel case

Electrolyte Loss

Average percentage (wt%)

30

3.8

1.6

57.3

7.3

Iran Computer Center in Tehran. The powdering procedure of SCCs was listed as follows: (a) SCCs were manually disassembled into different parts of cathodes, anodes, plastic separators, and metallic shells. The separated parts were then weighed and anodes and cathodes were dried for 12 h at 60 °C to remove the electrolyte and moisture. The electrolyte weight can be calculated as the weight differences before and after drying. The average percentage of SCCs parts is shown in Table 1. (b) The anodes and cathodes were ground by a hand mill to get a fine powder. (c) A fine powder was sieved through mesh #200 to get a homologous mixture (particle size of < 75 μm). The final powder was employed for all subsequent experiments. Fig. S1 shows the simplified powdering procedure of SCCs. 2.2. Characterization of SCCs powder 2.2.1. Thermogravimetric analysis Thermogravimetric analysis and differential scanning calorimetry (TGA/DSC) (Mettler Toledo, Switzerland) was employed to measure the mass changes of the sample as the temperature changes. In this regard, 20 mg of SCCs powder was heated with a heating rate of 10 °C min−1, in the temperature range of 25–1200 °C and an air flow rate of 50 mL min−1. 2.2.2. Initial pH determination In order to determine the alkaline, acidic or neutral nature of the SCCs powder, 1 g of the sample was added to 100 mL of distilled water and placed in a shaker incubator at 140 rpm and 30 °C (Bahaloo-Horeh et al., 2016) for 24 h. The pH measurement was carried out using a digital multi-meter (CP-500L, ISTEK, South Korea) with Ag/AgCl electrode. 2.2.3. SCCs composition The SCCs metal composition was determined by alkaline fusion method. 0.25 g of SCCs powder was melted in a platinum crucible with boric acid and sodium-potassium carbonate over a flame and then using an electric furnace at 950 °C. Then, hydrochloric acid at a ratio of 1:1 was used to dissolve the molten content. At last, 5 mL of aqua regia was added to the solution. The digest solution was filtered and made up to 100 mL by deionized water and then analyzed by using an inductively coupled plasma optical emission spectrometer (ICP-OES) (Vista-pro, Varian, Australia) in which a multi-element standard (Merck) was employed for calibration. Furthermore, in calculations, the metal concentration of a control sample was subtracted from the main sample. 2.2.4. Phase determination X-ray diffraction (XRD) was used to identify the component phase of the SCCs powder (X'Pert MPD, Philips, Netherland) with Co Kα radiation with the voltage of 40 kV, and the current of 40 mA. The scanning speed was 0.8 s step−1 with a step size of 0.04 from 10° to 90°. This analysis provides comprehensive information about the chemical structure of powder.

2. Materials and methods 2.1. Preparation of SCCs powder Spent coin cells of different sizes and brands were collected from 358

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2.2.5. FTIR analysis Fourier transform infrared spectroscopy (FT-IR) (Perkins-Elmer; USA) was employed to identify the chemical structure, molecular functional groups, and bonds in the SCCs powder before and after bioleaching with a scintillation spectral range of 400–4000 cm−1 with a precision of 2 cm−1 at room temperature. The solid samples were mixed with KBr powder, then pressed uniformly into discs and analyzed on a Perkin-Elmer Spectrum One instrument.

employed. In the approach of two-step bioleaching, when the bacteria entered the logarithmic phase, the SCCs powder was added to the culture medium. The logarithmic phase or active phase of the bacterial growth is a phase in which a cell density reaches its maximum value. For two-step bioleaching of SCCs powder, 10% (v v−1) bacterial inoculum contained 107 cells mL−1 was inoculated in 100 mL of culture medium and then incubated in a shaker-incubator at 30 °C and 140 rpm. When the bacterial cells entered to the active phase of growth, SCCs powder at different pulp densities of 10, 20, 30, 40 and 50 g L−1 was added to the pure culture medium. After the desired time and filtering the bioleaching medium, the recovery of metals was identified at all pulp densities using ICP-OES. Also, the pH, sulfate ion concentration, and cell count were measured during the bioleaching period. During the bioleaching experiment, distilled water was added to the culture medium due to compensating for water evaporation.

2.2.6. Surface morphology and EDX analysis The surface morphology of powder particles was analyzed by scanning electron microscope (SEM) (CamScan MV2300, Czech Republic) under secondary electron (SE) mode in SEM, operating at 20 kV. The solid samples were attached to sticky carbon tape and coated with a thin layer of gold-palladium alloy to increase the electrical conductivity of the sample surface, reduce charge interruptions, and produce higher resolution images. Also, the energy dispersive X-ray (EDX) and mapping analysis were employed to identify the elemental distribution of the sample using an EDX system.

2.4.1. Metals recovery For determining a proper time duration of bioleaching to achieve the maximum metals recovery, the metals recovery rate was measured daily. The recovery of metals from SCCs powder was calculated by Eq. (1):

2.3. Bacterial strains and growth condition A. thiooxidans was chosen as a mesophile bacteria to evaluate its ability to leach the metals of SCCs. This bacterium obtains its energy source through oxidation-reduction of sulfur compounds (Erüst et al., 2013). It can convert elemental sulfur to sulfuric acid and as a result, can help in heavy metals dissolution in the medium (Liang et al., 2010). A. thiooxidans (PTCC 1717) was provided by the Iranian Research Organization for Science and Technology (IROST) in Tehran, Iran in the lyophilized state. The bacteria were cultured in a medium comprised: sulfur (5 g L−1), (NH4)2SO4 (2 g L−1), K2HPO4.3H2O (0.25 g L−1), MgSO4.7H2O (0.25 g L−1) and KCl (0.1 g L−1) in 100 mL distilled water in a 250 mL Erlenmeyer flask. The culture medium was then incubated at 30 °C and 140 rpm in a shaker-incubator (WiseCube® WIS-20, Daihan Scientific, South Korea). Prior to incubation, the pH was adjusted to 2 using 98% H2SO4. Because the low pH was appropriated for the A. thiooxidans growth, there was no need to sterilize the culture medium. To monitor the A. thiooxidans growth, the pH, Eh, sulfate concentration and the cell count were measured daily.

Metal recovery =

Cs × Vs × 100% Cf × Mf

(1)

where Mf is the mass of the SCCs powder, Cf is the metal content of the SCCs powder (mg g−1), Vs is the bioleaching solution volume (L) and Cs is the metal concentration in leach liquor (mg L−1) which measured by ICP-OES. 2.5. TCLP test The TCLP test simulates the acidic condition presented in landfills and evaluates the mobility of inorganic and organic materials presented in the solid, liquid and multiphase wastes that may leach out into the soil and groundwater. The TCLP test for Li, Co and Mn from the SCCs powder before and after bioleaching were performed based on U.S. Environmental Protection Agency (EPA) SW846 Method 1311 using TCLP extraction fluid # 2 (extraction fluid # 2: 5.7 mL glacial acetic acid for 1 L of solution having pH 2.88 ± 0.05) (“U.S. Environmental Protection Agency, Method, 1311,” 1990). The SCCs powder was mixed with the extraction fluid in a solid-to-liquid ratio of 1:20. The mixture was placed in a shaker for 18 h. Then the leachate was filtered and the metals concentration were analyzed using ICP-OES. The results of TCLP were compared with toxicity threshold limits.

2.3.1. Bacterial cell count For cell counting, a hemocytometer (0.1 mm depth and 0.0025 mm2 area) under the phase-contrast microscope (Standard 25, Zeiss, Germany) was employed. The cells were counted at 400× magnification.

2.6. Chemical leaching experiment

2.3.2. Sulfate ion measurement A. thiooxidans can convert the sulfur content of the culture medium to sulfuric acid through oxidation-reduction reactions. The amount of sulfate ion in the culture medium can be an indicator of A. thiooxidans growth which measured daily using turbidimetry method by spectrophotometer (Optizen 320UV, Korea) at 420 nm (Gerayeli et al., 2013). For measuring sulfate concentration, 10 mL of sulfate buffer and 0.3 g of BaCl2 were added to 50 mL of the sample solution and then the absorbance was read at 420 nm (Rossum and Villarruz, 1961). For preparing sulfate buffer, MgCl2.6H2O (30 mg), sodium acetate (5 g), KNO3 (10 g) and acetic acid (20 mL) were dissolved in 500 mL distilled water and then made up to 1 L by distilled water.

Chemical leaching of Li, Co, and Mn from SCCs powder was performed using commercial H2SO4 in the same concentration as the bioleaching tests to define the effectiveness of leaching by inorganic acids produced by A. thiooxidans. The chemical leaching experiments were carried out in 250 mL Erlenmeyer flasks containing the optimum pulp density and 100 mL of bacterial culture medium without bacterial inoculation. The pH of the medium was adjusted to 2 by concentrated H2SO4. As in the bioleaching tests, the Erlenmeyer flasks were placed in a shaker at 140 rpm and 30 °C. At the end of the chemical leaching experiment, the leached liquor was filtered through a 0.22 μm filter and the concentration of metals was analyzed by ICP-OES. The obtained results were compared with bioleaching results.

2.4. Two-step bioleaching experiment

2.7. Statistical analysis

In bioleaching, different approaches have been applied. In the approach of one-step bioleaching, the bacteria were inoculated to the culture medium containing SCCs powder. Since no cell growth was observed in one-step bioleaching of SCCs powder (even by applying the adaptation process), the approach of two-step bioleaching was

All experiments were also performed in three replications due to the heterogeneous nature of the devices and the results expressed as mean ± standard deviation (SD) values. The statistical significance 359

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3.3. Two-step bioleaching of SCCs

Table 2 Metals content of SCCs. Component

Mn

Li

Mg

Co

Fe

Al

Zn

Content (mg kg−1 powder)

526580

35850

910

532

420

195

20

As mentioned before, in contrary with two-step bioleaching, no cell growth was observed in one-step bioleaching of SCCs powder even by applying the adaptation process. It was reported that production of microbial metabolites is higher in two-step bioleaching maybe because the pre-culture of microbes in the absence of waste is conducive for the higher growth of microbes (Qu et al., 2013). Also, the metabolites excretion prior to addition of solid powder to the medium decreases the heavy metal ions toxicity through complexation (Asghari et al., 2013). It's worth noting that the toxicity limits the optimal applied pulp density and thus, this two-step process is applied to reduce the toxic effects of waste on microorganisms (Shah et al., 2015). Furthermore, it was proposed that a two-step approach for an industrial application can be appropriate due to enhanced bioleaching efficiency and faster removal of heavy metals caused by acidic solution generated by microorganism before the addition of solid powder to the medium (Mishra and Rhee, 2014). Based on the results of section 3.2, for the approach of two-step bioleaching, the 10th day was selected for adding the SCCs powder to the medium due to the entrance of A. thiooxidans to the logarithmic phase of growth. Fig. 1 shows the growth characteristics of A. thiooxidans (changes in pH, sulfate concentration and cell count) in the presence of SCCs powder. The time of adding the powder to the bacterial culture medium was considered as a zero time in Fig. 1. Fig. 1(a) shows the cell count of A. thiooxidans at different pulp densities versus bioleaching time. In the first days, the cell numbers sharply decreased may be due to the bacterial cells adsorption onto the surface of SCCs powder, the toxicity of environment and sudden incremental changes in pH of the medium (Arshadi and Mousavi, 2014). As can be seen, the reduction in cell numbers is more severe in higher pulp densities. It may be due to the metals accumulation beyond the tolerance of bacteria which disrupt the membrane integrity of bacteria and reduce the bacterial population (Dopson et al., 2003). In addition, the O2 and CO2 dissolution and their transfer to the bacteria were lower in higher pulp densities which resulted in lower viability and activity of bacteria (Lee et al., 2015). In the following days, the bacterial counts remain nearly constant for several days and then began to decrease until the bacteria died. The pH variation for different pulp densities of SCCs powder during the bioleaching process are shown in Fig. 1(b). After adding the SCCs powder to the culture medium, the pH increased in all pulp densities except for pulp density of 10 g L−1. In the following days of bioleaching, the pH initially decreased slightly which means the production of sulfate in the culture medium and then began to rise due to a decrease in bacterial population and lack of proton production. Generally, if the consumption of H+ was higher than its generation, a net increase occurred in pH values (Zeng et al., 2013). Thus, because of higher metal content and presence of more acid consuming material in higher pulp densities, an increment of pH was more severe in the bioleaching process at higher pulp densities. Lithium is one of the acid consuming materials which uses protons of medium and produces OH− according to Eq. (3) and thus, increases the pH of culture medium (Li et al., 1994).

was determined at a probability level of P < 0.05. 3. Results and discussion 3.1. Characterization of the SCCs powder Table 2 shows the metals content of SCCs. Also, the crystalline phases of LiMn2O4 and Mn3O4 were detected in the SCCs powder by using XRD analysis. In addition, the initial pH of the solution was found to be close to 10. It indicates the alkaline nature of the SCCs powder which may be due to the presence of the Li compounds. Lithium belongs to the alkali metals group that reacts strongly with water and forms strongly alkaline hydroxides. The composition and thermal/chemical stability TGA analysis are depicted in Fig. S2. It shows the changes in mass with respect to time. Nine distinct loss were observed in the TGA curve for the heating process from 25 °C to 1200 °C: i) 25–113 °C (1.6% weight loss), ii) 113–190 °C (2.1% weight loss), iii) 190–262 °C (2% weight loss), iv) 262–321 °C (3.2% weight loss), v) 321–414 °C (5.3% weight loss), vi) 414–555 °C (3.1% weight loss), vii) 555–707 °C (4.3% weight loss), viii) 707–951 °C (4% weight loss), and ix) 951–1190 °C (4.66% weight loss). The total weight loss of 30.5% is attributed to the evaporation of oxygen from the battery powder. Accordingly, the small weight loss in the range of 25–113 °C can be related to the loss of water. After that, a weight loss of nearly 29% can be observed upon heating, due to the instability of battery powder. At relatively low temperatures, from 113 to 600 °C, a decomposition process occurred for LiMnxCoyO2 into Li2O, CoO, and MnO (Huang et al., 2018). Furthermore, a weight loss from 320 to 610 °C is due to the burning of acetylene black and the pyrolysis of PVdF. Next, by increasing the temperature (up to 900 °C), due to the carbon decomposition to carbon dioxide or carbon monoxide, a reducing process took place for CoO. On the other words, CoO was easily reduced into Co in the presence of carbon monoxide at elevated temperatures. By further increasing the temperature, up to 1200 °C, a weight loss of 4% is distinguished due to loss of Li (Li et al., 2017). 3.2. The growth of A. thiooxidans The changes in pH, sulfate concentration and cell count during the growth of A. thiooxidans are shown in Fig. S3. After 10 days of incubation and after a sharp increase in bacterial population, a maximum cell count (5.5 × 108 cells mL−1) was obtained. With regards to the growth characteristics of A. thiooxidans, it can be concluded that the logarithmic phase of growth occurred after 10 days of incubation. In addition, after 10 days of bacterial incubation, the pH (the indicator of H+ in the medium) decreased from 2 to 1.4 owing to the bacterial activity and production of acid. During growth, A. thiooxidans gains its energy from converting the elemental sulfur to sulfate ions according to Eq. (2) (Liu et al., 2004):

S0 (s) + 1.5 O2 (aq) + H2 O(aq)

2H+ (aq) + + SO24 (aq)

4Li + 2H2 O+ O2

4Li+ + 4OH

(3)

Another reason for more severe changes in pH values at higher pulp densities could be related to the toxicity of environment for bacteria and as a result lower bacterial population and lower sulfuric acid production at higher pulp densities. Fig. 1(c) shows the changes in sulfate concentration.

(2)

3.3.1. Extraction of metals The recovery of metals at different pulp densities is shown in Fig. 2. The metal ions concentration in bioleaching solution was measured daily and the maximum metals recovery was observed after 11 days. In

As can be seen in Fig. S3, an increase in sulfate concentration was accompanied by a decrease in the pH of culture medium. 360

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Fig. 2. Recovery of metals at different pulp densities of SCCs powder.

from the solid mass surface (Gerayeli et al., 2013). Also according to Eq. (5), Mn3O4 can be oxidized and produce MnO2 (Xin et al., 2012).

2LiMn2 O4 + 4H+

Mn3O4 + O2

2Li+ + 3MnO2 + Mn2+ + 2H2 O

(4) (5)

MnO2

In addition, MnO2 can react with sulfur of culture medium and produce Mn2+ (Eq. (6)) (Thamdrup et al., 1993).

3MnO2 + S0 + 2H2 O

SO24 + 3Mn2 + + 4OH

(6)

Insoluble MnO2 reduces the leaching recovery of Mn. Therefore, as can be seen in Fig. 2, the recovery of Mn is low. In addition, for cobalt leaching, Co3+ convert to Co2+ by a reducing agent (Xin et al., 2009). The reduction of Co3+ to Co2+ occurs by unknown intermediate reduction compounds, which may have resulted from sulfur metabolism (Niu et al., 2014). As can be seen in Fig. 2, with increasing the pulp density, the metals recovery decreases. At higher pulp densities, the bioleaching agents concentration is not sufficient for reacting with metals which are resulted from the lower growth of bacteria due to the solution viscosity, limited air transfer and environmental toxicity (Liang et al., 2013; Rastegar et al., 2015a,b). From an industrial point of view, higher pulp densities are more preferable. By comparing all recovery results, the pulp density of 30 g L−1 was chosen as an optimum pulp density that had higher leaching recovery than pulp densities of 40 and 50 g L−1. At pulp density of 30 g L−1, 99% Li, 60% Co, and 20% Mn were leached after 11 days. Fig. S4 depicts the metals leaching recovery versus bioleaching time at a pulp density of 30 g L−1. Over time, the metals recovery has risen and reached its highest level on the 11th day. 3.4. Structural analysis Different structural analyzes such as XRD, EDX, SEM, FTIR were performed on SSCs powder before and after bioleaching at an optimum pulp density of 30 g L−1 to study the progress of the bioleaching process.

Fig. 1. Changes in (a) cell count, (b) pH, and (c) sulfate concentration during two-step bioleaching by A. thiooxidans at different pulp densities (g L−1).

the following days of bioleaching, the recovery of metals was decreased due to a reduction in sulfuric acid production. As can be seen in Fig. 2, the recovery of Li is higher than Co and Mn in all pulp densities due to its high reactivity in the aqueous medium. In the SCCs, Mn is in the form of Mn3O4 and LiMn2O4. As said before, A. thiooxidans produces sulfuric acid according to Eq. (2). The protons attack LiMn2O4 according to Eq. (4) and produce Li+, Mn2+, and insoluble MnO2 (Liu et al., 2015). In fact, because of readily protonation of atoms of oxygen that cover metal compounds, metals can detach

3.4.1. FTIR analysis In FTIR analyzer, the energy sent to the sample is processed by an interferometer. By plotting the absorption intensity versus the wave number, the relative position and size of all peaks can be specified. The key point in FTIR analysis is that every molecule structure and the functional group has a unique spectrum that makes it possible to determine the identification, quality, and consistency of a powder sample (Malmberg, 2016). Fig. 3 shows FTIR spectrums of original powder and 361

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Fig. 3. FTIR analysis for SCCs powder (a) before and (b) after bioleaching.

bioleached residue. The FTIR peaks showed the structural changes in SCCs powder through leaching by A. thiooxidans. The comparison between different spectrums of Fig. 3(a) and (b) showed that some peaks become less intensive in bioleached residue which indicated the leaching of metals and their transfer to the solution. The peaks at 500-600 cm−1 may be related to M-O bonds (M corresponds to the metal ions of Co, Mn, and Li) (Bahaloo-Horeh et al., 2016) and the peak around 1083 cm−1 is related to the C-O-C bridge vibration (Rasoulnia et al., 2016) that the bands transmittance has decreased after bioleaching. The peaks around 3162 cm− 1 indicate the strong OH stretching group (Liu et al., 2011) and the peak around 1500 cm−1 is related to the graphite structure of SCCs powder (Heydarian et al., 2018). In addition, some new peaks appeared in the spectrum of bioleached residue that may be due to the adsorbed bacteria on solid surface or culture medium components (Chen et al., 2008). The peak at 1706 cm−1 could be ascribed to amide bands from bacterial cells or nitrogen of the medium which is sediment in the form of N-H (Moen et al., 2009). The peak at 967 cm− 1 could be related to the sulfate vibrations (Panda et al., 2013).

3.4.2. XRD analysis of SCCs powder Fig. 4 shows the XRD analysis of SCCs powder before and after bioleaching. The phases of LiMn2O4 and Mn3O4 were observed in the XRD pattern. Although the ICP analysis showed the presence of Co in SCCs powder, there was no visible peak of Co in XRD pattern of powder before and after bioleaching Usually, 44°, 51°, and 75° are corresponding to (111), (200) and (220) lattice planes of metallic Co (JCPDS no. 15–0806). In Fig. 4, the peaks between 40 and 50 are sideways, indicating peaks (∼44°) are hidden in them (Li et al., 2019). Furthermore, the diffraction of the amorphous material was not detectable due to their low amplitude atomic order (Jowkar et al., 2018); thus, maybe some phases had amorphous states and were not detected in XRD pattern. After bioleaching, the formation of a sulfur layer was also observed. 3.4.3. SEM analysis of SCCs powder Surface morphology analysis is another important test for investigating the bioleaching progress. Fig. S5 shows the SEM photomicrographs of original powder and bioleached residue at 5000× and 10000× magnification. The photomicrographs show that there is a significant difference between the surface morphology of the SCCs 362

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can be used for understanding the bioleaching kinetics and evaluating the rate controlling step. Bioleaching of metals from solid mass comprises four sequential steps: (1) diffusion of the leaching agents through the liquid film; (2) diffusion of the leaching agents through the shell; (3) surface chemical reaction; and (4) the transfer of the generated substances to the bulk solution (Amiri et al., 2012). Due to the vigorous shaking required for the bioleaching process, it can be assumed that the first and last steps are not the rate controlling steps (Jowkar et al., 2018). If the heterogeneous reaction rate is controlled by the diffusion, the following equation can be applied based on shrinking core model theory (Gerayeli et al., 2013):

kt = 1

2/3X

(1

(7)

X )2/3

where k is the parabolic rate constant, t is the time of bioleaching process, X is the leaching recovery of metals from SCCs powder. If the heterogeneous reaction rate is controlled by the surface chemical reaction, the following equation can be applied based on shrinking core model theory:

kt = 1

(8)

X )1/3

(1

Generally, in kinetics studies of the bioleaching process, one of the assumptions is that the leaching agent concentration is constant. The bacteria of A. thiooxidans oxidize elemental sulfur and convert it to sulfate ion, and then the generated sulfuric acid causes the metals solubilization (Jowkar et al., 2018). Since the sulfate ions concentration (as a leaching agent) varies due to the presence of A. thiooxidans and its activity, this assumption may cause inaccurate simulation of the SCCs bioleaching using conventional kinetic models (Haghshenas et al., 2009). This means that k cannot be assumed constant, and these changes should be applied to the shrinking core model. Therefore, the modified shrinking core models can be considered for the variation of sulfate concentration as the following equations for the diffusion and chemical reaction, respectively (Chen et al., 2015; Mishra et al., 2008):

Fig. 4. XRD analysis of SCCs powder (a) before and (b) after bioleaching.

powder before and after bioleaching. It was observed that the surface of the powder was nearly smooth before bioleaching. In bioleached residue photomicrographs, the porous surface and smaller particles were observed. The oxidation-reduction reactions, the bacterial metabolites and the acidic condition of culture medium caused porosity and erosion in the powder (Rasoulnia et al., 2016). The corrosive chemical action caused that more reactive and fresh surfaces be accessible and thus the metal mobilization occurred (Bahaloo-Horeh et al., 2016).

P (X ) = 1

2/3X (t )

(1

t

2bDe 2 (1 R x

X (t ))2/3 =

)

Csulfate dt = F (t ) 0

(9)

G (X ) = 1

(1

X (t ))1/3 =

t

bk R x (1

)

Csulfate dt = £ F (t ) 0

(10)

where

3.4.4. EDX analysis of SCCs powder Fig. 5 shows the EDX and mapping of original powder and bioleached residue. The results indicated the bioleaching effectiveness. In bioleached residue, high proportions of Mn were detected by EDX analysis which indicates the low recovery of Mn. Also, the negligible amount of Co and Li were observed in bioleached residue which indicates the high leaching recovery of Co and Li from SCCs powder. The EDX analyses of the bioleaching residue also revealed the sulfur layer formation over the SCCs matrix. This elemental sulfur layer may act as a porous or impervious layer. It was reported that as the elemental sulfur layer was growing in thickness, the flow of oxidants and electrons to and from the solid surface was hindered (Lotfalian et al., 2015). The EDX analysis confirmed the data of FTIR and XRD which indicates the presence of sulfur components in the bioleached residue.

2bDe 2 x R (1

bk R x (1

) )

=

(11)

=£

(12)

where De is the diffusion coefficient of the sulfate ion concentration; ρx is the molar density of metals in SCCs powder, R is the particle radius, ε is the porosity of the SCCs particle, Csulfate is the sulfate ion concentration, £ is the chemical reaction rate constant and λ is the diffusion rate constant. The zero time in term of

t

0

CSulfate dt refers to the

moment that the waste is added to the bacterial culture medium. In Fig. 6, the conventional and modified kinetic models (G(X) and P (X)) were plotted for two cases of

3.5. Evaluation of the rate controlling step

t

0

CSulfate dt (time-dependent sulfate

variations) and t (time-independent sulfate variations) for metals of Li, Co and Mn by using the results of optimum pulp density of 30 g L−1. In order to better comparison of results, the values of R2 in both cases are summarized in Table 3.

Although most of the available models for investigating the metal extraction kinetics are related to hydrometallurgical studies, its basis

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Fig. 5. EDX and mapping analysis of SCCs powder (a) before and (b) after bioleaching.

As can be seen, the chemical reaction model (higher R2) fits better with the results than the diffusion model. Also, in the chemical reaction model, the value of R2 for the case of ignoring the variation in sulfate concentration is higher than the case of regarding the sulfate concentration variations. The results indicate that the chemical reaction is a rate-limiting step in SCCs bioleaching process by A. thiooxidans, even though the formation of sulfur was also observed. It means that the layer of elemental sulfur has a porous characteristic. This result has also been reported by Gomez et al. (1999).

compounds, amino acids, polypeptides, phosphatidylinositol, etc. which can act as a wetting agent, increase the oxidation of elemental sulfur and affect the efficiency of bioleaching (Fazzini et al., 2011). 3.7. Toxicity characteristic of SCCs powder before and after bioleaching Table 5 shows the results of the TCLP test on SCCs powder before and after bioleaching and a comparison of results with the identification standard for hazardous wastes. It can be seen that before bioleaching, the Mn concentration was found to exceed the regulatory level, thus the waste requires treatment before disposal. After bioleaching, the Mn concentration was reduced to below acceptable levels, thus the bioleached residue of SCCs can be disposed of safely. Furthermore, there was a significant difference between the values of the TCLP test before and after bioleaching for lithium, but no regulatory level was found for it.

3.6. Chemical leaching of SCCs powder The chemical leaching test was performed in order to determine the success of the bioleaching process. Table 4 compares the metals recovery at an optimum pulp density of 30 g L−1 for chemical leaching and bioleaching method. As can be seen in Table 4, no Co and Mn were leached by chemical leaching. Relatively high recovery of lithium through chemical leaching was due to the high reactivity of lithium with the aqueous medium. The comparative results confirmed that A. thiooxidans can enhance the leaching of metals. This may be due to the fact that in addition to sulfuric acid, bacteria can produce other metabolites such as organic

4. Conclusion In the present study, a bioleaching process was developed as a sustainable method of metals recovery from SCCs using A. thiooxidans. The growth curve of A. thiooxidans showed that the bacteria entered the logarithmic phase on the 10th day. The 10th day was chosen for adding

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Fig. 6. Comparison between measurements and correlations expressing diffusion and chemical reaction controlled mechanisms for (a) Li conventional model, (b) Li modified model, (c) Co conventional model, (d) Co modified model, (e) Mn conventional model, and (f) Mn modified model. Table 3 Comparison of correlation coefficient values for kinetic models. Metal

Li Co Mn

Table 5 Results of toxicity characteristic of SCCs powder before and after bioleaching.

R2

Metals

Time-independent sulfate variations

Time-dependent sulfate variations

Diffusion P(X)

Chemical reaction G(X)

Diffusion P(X)

Chemical reaction G(X)

0.91 0.94 0.93

0.92 0.97 0.99

0.50 0.42 0.38

0.62 0.63 0.54

Li Mn Co

Li Co Mn

Chemical leaching

99 60 20

76 0 0

After

TCLP limit (mg L−1)

1305 492 3

96 1 0

n.s. 50a 80b

the powder in two-step bioleaching process. The results show that the highest recovery of Li, Co and Mn were achieved at a pulp density of 30 g L−1, in values of 99%, 60%, and 20%, respectively. The EDX, SEM, XRD and FTIR analysis of SCCs powder before and after bioleaching confirmed the effectiveness of A. thiooxidans activity on metals mobilization. The shrinking core model showed that the chemical reaction is the rate controlling step of the process. In addition, in comparison with chemical leaching, Acidithiobacillus thiooxidans can enhance the

Recovery (%) Bioleaching

Before

n.s.: not stated. a Regulatory level based on Victorian EPA Industrial Waste Strategy Management Paper WMI/86. b Metal constituents and California regulatory threshold limits.

Table 4 Comparing metals recovery between chemical leaching and bioleaching. Metals

TCLP (mg L−1)

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leaching of metals. The results show that bioleaching can act as an effective way to recover metals from SCCs. Toxicity assessment tests of the SCCs powder demonstrate that the bioleached residue of SCCs meets environmental limitations and can be disposed of safely.

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