Bioleaching of copper from waste printed circuit boards by bacteria-free cultural supernatant of iron–sulfur-oxidizing bacteria
© The Author(s) 2018
Received: 6 December 2017
Accepted: 19 February 2018
Published: 22 February 2018
The toxicity of waste printed circuit boards (PCBs) to bacteria was considered as the major limitation in bioleaching of copper from PCBs. To reduce the toxicity of PCBs, copper extraction from PCBs was investigated using bacteria-free cultural supernatant from some metallurgical microbial consortium, whose predominant organisms were Leptospirillum ferriphilum and Sulfobacillus thermosulfidooxidans.
About 100% copper was recovered in 2 h from 5 g/L PCBs by bacteria-free cultural supernatant. The result indicated that the indirect non-contact mechanism was the predominant mechanism in bioleaching of copper from PCBs. It was not necessary for bacteria to exist in copper extraction. In addition, the role of bacteria was most likely to regenerate Fe3+ as an oxidant. Furthermore, the biooxidation of Fe2+ to Fe3+ was determined as the rate-limited step in bioleaching of copper from PCBs. In addition, the biooxidation activity of bacteria would be strongly inhibited by the toxicity of PCBs.
With the rapid development of electronic and electrical industries, more and more new electronic products are produced. When these electronic products reach their service life, a large number of e-wastes will be generated. It was estimated that about 20–25 million tons of e-waste were produced every year in the world (Robinson 2009). Therefore, it is urgent to dispose these e-wastes. As the basic part of electronic equipment, PCBs have been increasing sharply with the increment of e-wastes. PCBs contained varieties of hazardous organic and inorganic substances which required special treatment to avoid environmental contamination (Robinson 2009). In addition, PCBs contained several valuable metals and precious metals with quantities higher than those in some ores (Ilyas and Lee 2014). Therefore, the recovery of valuable metals from PCBs is profitable. Various processes, such as mechanical (Meng et al. 2017), pyrometallurgical (Jung et al. 2017), hydrometallurgical (Pant et al. 2012). and biometallurgical (Mrážiková et al. 2016; Priya and Hait 2017) process, have been employed for the recovery of metals from PCBs.
The biometallurgical process is usually referred as bioleaching. Bioleaching is a promising technology which utilizes microorganisms to recover metals from low-grade ores and e-waste (Hong and Valix 2014). Benefiting from lower operational cost and energy requirements in metal recovery, bioleaching has drawn more and more attention. Chemolithoautotrophs bacteria are commonly used for metal recovery from e-waste, such as Acidithiobacillus ferrooxidans, Leptospirillum ferrooxidans, Acidithiobacillus thiooxidans, and so on (Erüst et al. 2013). Those bacteria which use CO2 as carbon source and inorganic compounds (Fe2+ and reduced S) as energy source utilize their ability to facilitate metal dissolution through a series of biooxidants and bioleaching reactions.
The direct and indirect biooxidation are the two mechanism of bioleaching of ore. Usually, indirect biooxidation mechanism has been accepted by most researchers (Liu et al. 2017). The indirect biooxidation mechanism includes contact and non-contact biooxidation mechanisms (Jadhav and Hocheng 2013). In contact mechanism, bacteria would adhere to ore and form a biofilm between bacteria and ore. Inside this biofilm, Fe2+ is oxidized by bacteria to Fe3+ and the ore is dissolved by Fe3+ (Liu et al. 2017). It has been proved that the formation of biofilm is important in bioleaching of ore (More et al. 2014). The concentration of ferric iron and H+ in biofilm is much higher than that in solution, which could greatly increase the dissolution rate of ores (Coram and Rawlings 2002). In non-contact mechanism, the bacteria are no need to adhere to the ore. In addition, the Fe3+ which is produced by bacteria plays key role in the dissolution of ore.
In this process, the dissolution of copper from PCBs can be divided into two phases. In the first phase, the ferrous ions are oxidized by bacteria to generate ferric ions. In the second phase, copper is mobilized from the PCBs by the ferric ions, and the ferric ions are reduced to ferrous ions. Therefore, a cycle between Fe3+ and Fe2+ is formed and copper is leached out (Yang et al. 2009).
Many researchers have studied the process of bioleaching of copper from PCBs (Arshadi and Mousavi 2015; Mrážiková et al. 2016). However, few process of bioleaching of PCBs was applied commercially for the reasons of long leaching time and low leaching efficiency.
The toxicity of the PCBs which can affect the growth of bacteria has been thought to be the major reason of low-efficient leaching (Yang et al. 2014). The activity of bacteria could be inhibited immediately by addition of elemental metal ions (Cu2+, Cr3+, Ni+, Sn2+, and Zn2+) (Bryan et al. 2015). The presence of non-metallic components in PCBs showed the bacterial toxicity in the bioleaching process (Zhu et al. 2011).
Bioleaching of metals from PCBs
Recovery and conditions
Characterization of microorganisms
Arshadi and Mousavi (2015)
100% Cu and Ni in 20 days at 8.5 g/L pulp density
Isildar et al. (2016)
Acidithiobacillus ferrivorans and Acidithiobacillus thiooxidans
98.4% Cu in 7 days at 10 g/L pulp density
Ilyas et al. (2013)
Sulfobacillus thermosulfidooxidans and Thermoplasma acidophilum
74% Zn, 68% Al, 85% Cu, 78% Ni in 165 days at 100 g/L pulp density
Moderately thermophilic bacteria
Rodrigues et al. (2015)
85% Cu in 8 days at 25 g/L pulp density
Moderately thermophilic bacteria
Zhu et al. (2011)
Mixed culture of acidophilic bacteria
96.8% Cu in 45 h, 88.2% Al and 91.6% Zn in 98 h at 12 g/L pulp density
Vestola et al. (2010)
Acidithiobacillus sp. and Leptospirillum sp.
100% Cu and Ni in 42 days at 10 g/L pulp density
93.4% Cu in 9 days at 100 g/L pulp density
Moderately thermophilic bacteria
Furthermore, two-step process was used to mitigate the toxic effect of PCBs (Arshadi and Mousavi 2015; Xiang et al. 2010). In addition, response surface methodology (RSM) was used to optimize the parameters of bioleaching of PCBs (Arshadi and Mousavi 2015). However, the activity of bacteria is inevitably affected by the contact of PCBs. Due to the toxicity of PCBs, the indirect non-contact mechanism may be the better mechanism for bioleaching of copper from PCBs. To the best of our knowledge, few studies have reported the bioleaching of copper from PCBs using bacteria-free cultural supernatant.
The purpose of the present study is to prove that if it is feasible to achieve the bioleaching of copper from PCBs using bacteria-free cultural supernatant. In addition, the biooxidation process and chemical-leaching process during the whole bioleaching process of PCBs were investigated and compared to confirm the role of bacteria in bioleaching of PCBs. Besides, the toxic effect of PCBs on bacteria was investigated. Finally, a continuous biooxidation–leaching–separation cycle with high leaching efficiency was designed to mitigate the toxic effect of PCBs on bacteria.
Waste printed circuit boards and pyrite samples
The waste printed circuit boards were obtained from a local electronics company in Shanghai, China. The scraps of PCBs were first cut into small pieces manually, then crushed by the high-speed universal pulverizer for 2 min, and finally sieved. The power with the size below 40 mesh was collected and subjected to hydraulic sorting so as to remove the non-metallic components from PCBs’ powder. The left part then was air-dried.
The PCB concentrates was digested with aqua regia, cooled, and then diluted to appropriate concentration range using deionized water. The metal content of digestion solution was determined using inductively coupled plasma-optical emission spectrometry (ICP-OES, Agilent 725ES). The metal content of PCB concentrates was found to be copper (65.0%), aluminum (0.85%), iron (0.23%), nickel (< 0.01%), lead (0.02%), and zinc (< 0.01%). The experiments were conducted in triplicates. All data presented in this study were obtained from triplicate experiments with a standard error of ≤ ± 0.05.
The pyrite samples were kindly supplied by one gold mine Co. Ltd., P. R. China, which containing 30 ± 0.5% Fe, 28 ± 0.3% S, and 3 ± 0.1% As. The sample was sieved to obtain a particle size distribution between 63 and 90 μm.
Bacteria and growth media
Copper extraction from PCBs using bacteria-free cultural supernatant
The adjusted 9K medium (15 g/L Fe2+) was added into 250 mL Erlenmeyer flask with 10% inoculum, cultivated at the initial pH of 0.9, 42 °C and 200 rpm for several hours until the ferrous ion was totally oxidized to ferric, then filtered to remove precipitation and sterilized by filtration using 0.22 µm membrane (Merck Millipore Ltd). 5, 10, and 15 g/L PCBs were placed into the filtrate, respectively. In addition, 15 g/L ferric sulfate solution, pure water, and pure medium without FeSO4·7H2O were set as control. The experiments were carried out at the initial pH of 1.2, 55 °C, and 200 rpm. All experiments were done in orbital shaker incubators. Samples were collected intervals to analyze pH, the concentrations of ferrous and copper ions. The experiments were conducted in triplicate.
The effect of PCBs on bacterial oxidation activity
Different amounts of PCBs were added into the adjusted 9K medium with 10% inoculum to obtain the initial concentrations of PCBs at 0, 5, 10, and 15 g/L. The culture was cultivated at the initial pH of 0.9, 32 °C, and 180 rpm. Samples were collected intervals to analyze pH, Eh, and the concentrations of ferrous ions. The experiments were conducted in triplicate.
The role of pyrite on bacterial oxidation of ferrous ions
For the purpose of immobilization of bacteria, pyrite was introduced into the process of bacterial oxidation of ferrous ions. Five grams pyrite was added into 90 mL adjusted 9K medium with 10% inoculum. The culture was cultivated at 42 °C and 180 rpm. After the ferrous ion in the solution was exhausted, the solution was stood and filtered to remove the supernatant. Then, 100 ml fresh adjusted 9K medium was injected into the precipitation for the bacterial culture. Once the ferrous ion was exhausted, the solution was stood, filtered. In addition, the fresh medium was injected again. Samples of bioleaching solution were collected to analyze pH, Eh, and the concentrations of Fe2+ and Fe3+. The experiments were conducted in triplicate.
The biooxidation–leaching–separation cycle
A new biooxidation–leaching–separation cycle was designed to bioleaching of PCBs. The details of the cycle were as follows: in the Biooxidation process, it consisted of three parts: adjusted 9k medium, the mixed bacterial culture, and pyrite. The bacteria were absorbed on pyrite. In addition, Fe2+ in the medium was oxidized to Fe3+ by bacteria. After Fe2+ was exhausted, the solution was left to stand. The supernatant which contained high concentration of Fe3+ was used to the Leaching process. In addition, the precipitate which was pyrite and bacteria was used to oxidize Fe2+ again. In the leaching process, the supernatant from biooxidation process was used to leaching PCBs for the recovery of copper. After the reaction finished, the solution contained copper ion was filtered to be used to the Separation process. In the separation process, the copper ion in the solution was recovered by iron power. In addition, the solution, which obtained Fe2+, was returned to the biooxidation process again.
To prove the feasibility of the cycle, several experiments were designed. 100 mL of adjusted 9K medium was oxidized by bacteria first. And then, the supernatant was used to leaching 15 g/L PCBs. After the leaching process was accomplished, the solution was filtered. Then, Cu2+ in the solution was separated by displacement of iron power. Finally, the solution was diluted to the concentration of 15 g/L Fe2+ for the bacterial oxidation again. A control which fresh adjusted 9K medium (15 g/L Fe2+) was added was set. The cultures were cultivated at the initial pH of 0.9, 32 °C, and 180 rpm. Samples were collected every 6 h to analyze pH, Eh, and the concentrations of Fe2+ and Fe3+. The experiments were conducted in triplicate.
The bacterial oxidation activity might be affected by some metals such as Ni, Al, and Zn which were mobilized from PCBs. Therefore, the effect of the copper (0, 1, 3, 5, and 10 g/L), Ni (0, 1, 5, 10, and 20 g/L), Al (0, 1, 5, 10, and 20 g/L), and Zn (0, 1, 5, 10, and 20 g/L) on bacterial oxidation of 15 g/L Fe2+ was test. Samples were collected every 6 h to analyze pH, Eh, and the concentrations of Fe2+ and Fe3+. The experiments were conducted in triplicate.
The effect of increase of cycles on bacterial oxidation of Fe2+ was studied. 100 mL of adjusted 9K medium was oxidized by bacteria firstly. And then, the supernatant was used to leaching PCBs. The solution was filtered after the bioleaching process was accomplished. Cu2+ in the leachate was separated by displacement of iron power. Finally, the solution was diluted to the concentration of 15 g/L Fe2+ for the bacterial oxidation again. Totally, 100 g/L of PCBs were disposed with nine times of cycles. The tactic was as follows: the addition of PCBs was 15 g/L at the first 4 cycles and 10 g/L at the next 4 cycles, and 0 g/L PCBs at the last cycle for completely reaction. Samples were collected to analyze pH, Eh, and the concentrations of Fe2+, Fe3+, and Cu2+.
The pH and redox potential was measured by a pH meter and Eh meter (Mettler model FE20). The concentration of ferrous iron was determined by titration with potassium dichromate in the presence of the indicator N-phenylanthranilic acid. Copper ion concentration was determined by atomic absorption spectrometer (Analytic Jena AG, Germany). The concentration of Fe3+ was determined by the titration of EDTA at pH 2 in the presence of sulphosalicylic acid as an indicator. All experiments were done in orbital shaker incubators.
Results and discussion
Copper extraction from PCBs using bacteria-free cultural supernatant
Range of metal tolerance of different kinds of bacteria
The maximum metal concentration whereby metabolic activity still occurs
Tian et al. (2007)
Ni2+(30–40 mM), Zn2+(20–30 mM), Co2+ (5–10 mM), Cu2+ (< 5 mM) and Cd2+ (< 5 mM)
Dopson et al. (2003)
6 mM Cu2+, 43 mM Zn2+, and 5 mM Ni2+
Hallmann et al. (1992)
Al3+ (278 mM), Co2+ (17.0 mM), Cu2+ (391 mM), Mn2+ (546 mM), Ni2+ (127 mM), and Zn2+ (461 mM)
Al3+ (1049 mM), Zn2+ (1046 mM), Ni2+ (681 mM) and Cu2+ (781 mM)
The toxic effect of PCBs on bacterial oxidation activity
Biooxidation rate of Fe2+ on different amounts of PCBs
Biooxidation rate of Fe2+ (g/L h)
In bioleaching of sulfide ores, the chemical dissolution rate of sulfide ores by ferric ions was very slow. Therefore, bacteria were required to form biofilm between bacteria and sulfide ore to accelerate the dissolution of sulfide ores. While in bioleaching of PCBs, the copper was easily chemically leached by Fe3+, and the addition of bacteria might not significantly increase the dissolution rate of copper. Instead, the rate of biooxidation was inhibited because of the toxicity of PCBs. Therefore, the strategy which separated the process of bacterial oxidation from bioleaching of PCBs might be a good choice.
The role of pyrite in bacterial oxidation of ferrous ions
The biooxidation–leaching–separation cycle
In this biooxidation–leaching–separation cycle, copper in the solution would be recovered in separation process. While other metals, such as Al, Zn, and Ni, would be accumulated in the solution with the increase of the cycles. When the metals in the solution accumulated to a line, the activity of the bacteria would be inhibited. Therefore, an important reference for determination of the numbers of the cycle could be provided by studying the effect of metal ions on the activity of bacteria.
Comparison of leaching efficiency, conditions and capacity in bioleaching of copper from PCBs
Leaching efficiency (%)
Capacity (gCu/L h)
Zhu et al. (2011)
12 g/L PCBs concentrates with 83.8% copper in 45 h
Yang et al. (2009)
15 g/L PCBs with 25.06% copper in 24 h
Nie et al. (2015)
12 g/L PCBs concentrates with 63.37% copper in 7 days
Xiang et al. (2010)
20 g/L PCBs with 23.10% copper in 5 days
Rodrigues et al. (2015)
25 g/L PCBs with 28.50% copper in 8 days
Wang et al. (2009)
7.8 g/L PCBs with 37.10% copper in 9 days
100 g/L PCBs concentrates with 65.0% copper in 9 days
Various methods were used to reduce the toxicity of PCB to bacterial activity, such as the pretreatment of PCBs (Zhu et al. 2011), the use of adapted bacteria (Arshadi and Mousavi 2015), and the application of two-step process (Bryan et al. 2015). The two-step process was the most commonly used technology to reduce the toxic effect of PCBs (Isildar et al. 2016; Shah et al. 2015; Xiang et al. 2010). In the two-step process, bacteria were first cultivated for a period of time under its optimized conditions to obtain high activity; then, PCBs were added into the culture. The two-step process could improve the leaching efficiency and reduce the leaching time (Xiang et al. 2010; Zhu et al. 2011). As the bacteria in the two-step process had been cultured for a period of time without PCBs, there was high concentration of ferric ion in the solution before the addition of PCBs. This was consistent with the idea of using bacterial culture supernatant to leach PCBs in this paper. However, the oxidation activity of bacteria was inevitably affected after the addition of PCBs with the leaching efficiency reduced finally. Probably, the isolation of bacteria from the PCBs was the optimal way to avoid the toxicity of the PCBs. The results of this study also showed that the rate of copper extraction from PCBs increased significantly.
In the present study, the copper extraction from PCBs was investigated using bacteria-free cultural supernatant. It was demonstrated that about 100% copper was recovered in 2 h from 5 g/L PCBs. The result indicated that the indirect non-contact mechanism was the predominant mechanism in bioleaching of copper from PCBs. Furthermore, the activity of bacteria was strongly inhibited by the toxicity of PCBs. In addition, the isolation of bacteria from the PCBs probably was the optimal way to avoid the negative effect. A biooxidation–leaching–separation cycle was designed to extract copper from PCBs. In addition, a total of 93.4% of copper was recovered from 100 g/L PCB concentrates in 9 days. Our findings represent a novel type of metal solubilization technique, which may be implemented to develop a three-stage recycle reactor system. Such systems may provide more efficient and cleaner industrial application for the recovery of copper from waste printed circuit boards.
WT and XZ conceived and designed the experiments. WW and XL performed the experiments and analyzed the data. WW wrote the paper. XZ and MZ revised the manuscript. All authors read and approved the final manuscript.
The authors declare that they have no competing interests.
Availability of data and materials
All data generated or analyzed during this study are included in the main manuscript file.
Consent for publication
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Ethics approval and consent to participate
This study was supported by the Open Project Funding of the State Key Laboratory of Bioreactor Engineering of China and the National High Technology Research and Development Program of China (Nos. 2007AA060904 and 2012AA061503).
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