Waste Management 34 (2014) 901–907

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Waste Management
journal homepage: www.elsevier.com/locate/wasman

A new strain for recovering precious metals from waste

printed circuit boards
Ruan Jujun, Zhu Xingjiong, Qian Yiming, Hu Jian ⇑
Jiangsu Key Laboratory of Environmental Material and Environmental Engineering, School of Environmental Science and Engineering,
Yangzhou University, 196 Huayang Road, Yangzhou 225000, China

a r t i c l e i n f o a b s t r a c t

Article history: A new strain, Pseudomonas Chlororaphis (PC), was found for dissolving gold, silver, and copper from the
Received 8 October 2013 metallic particles of crushed waste printed circuit boards (PCBs). The optimized conditions that greatly
Accepted 18 February 2014 improved the ability of producing CN (for dissolving metals) were obtained. Dissolving experiments
Available online 11 March 2014
of pure gold, silver, and copper showed that the metals could be changed into Au+, Ag+, and Cu2+. PC cells
and their secreta would adsorb metallic ions. Meanwhile, metallic ions destroyed the growth of PC. Dis-
Keywords: solving experiments of metallic particles from crushed waste PCBs were performed by PC. The results
Precious metals
indicated that 8.2% of the gold, 12.1% silver, and 52.3% copper were dissolved into solution. This paper
Waste PCBs
Recovering
contributed significance information to recovering precious metals from waste PCBs by bioleaching.
Ó 2014 Elsevier Ltd. All rights reserved.

1. Introduction separation by physical methods (Li and Xu, 2010). Precious metals
were lost in physical recovering process.
China has been one of the largest e-waste dumping grounds in Therefore, developing new technology for recovering precious
the world. About 2.5 million tons of e-waste (both self-generated metals is urgently demanded for improving added value of waste
and imported from developed countries) appeared in Chinese PCBs recovery.
mainland (Ongondo et al., 2011) every year. Among which, waste Bioleaching is widely used in mineral processing (Watling, 2006).
printed circuit boards (PCBs), the core component of electronics It has the advantages of environment-friendly and low-cost. How-
products, were also produced. Waste PCB contains nearly 28% ever, its application for recovering waste PCBs is still in its infant.
metals and the purities of metals are more than 10 times higher Currently, Xiang et al. (2010) reported the application of bioleaching
than that of rich-content minerals (Li et al., 2007.). Therefore, for recovering copper from waste PCBs. Chromobacterium Violaceum
recovering waste PCBs has now become increasingly important, (CV) was the most used microbe in the bioleaching process for recov-
which is mostly done by small backyards workshop using crude ering precious metals from waste PCBs (Pant et al., 2012). Precious
technologies (such as acid-washing or open incineration). metals were dissolved into solution by CN emitted from CV. Chem-
However, serious pollution has been generated in the recovering ical equation of the dissolution process could be presented as:
process such as exposure of polybrominated diphenyl ethers, poly-
chlorinated dibenzo-pdioxins and dibenzofurans (Duan et al.,
2011), and heavy metals (Leung and Wong, 2008; Ilgin and Gupta, 4Au þ 8CN þ O2 þ 2H2 O ¼ 4AuðCNÞ2 þ 4OH ð1Þ
2010). Therefore, environment-friendly technology is a pressing 
demand for treating waste PCBs. Although CV has great ability to produce CN , it is not conve-
Physical methods are preferred for recovering waste PCBs (Ruan nient to be employed in industrial application. CV mainly appears
and Xu, 2012a,2012b; Ruan et al., 2013; Veit and Bernardes, 2006). in tropical and subtropical regions. The special demand on living
However, physical treatments are insufficient in recovering pre- condition restrains the scope of its industrial application in recov-
cious metals. Abundant precious metals (such as gold and silver) ering precious metals from waste PCBs. Therefore, it will be of
were contained in waste PCBs (Li et al., 2012). Small proportion great significance to search suitable strain for the industrial biole-
and inertial characteristics of precious metals cause difficulties in aching process of recovering precious metals from waste PCBs.
Pseudomonas strains also have the ability to produce CN
though the ability is not as strong as CV. However, pseudomonas
⇑ Corresponding author. Tel./fax: +86 514 87979480. strains have an important advantage of being employed in the
E-mail addresses: [email protected], [email protected] (J. Hu). industrial application for recovering precious metals from waste

http://dx.doi.org/10.1016/j.wasman.2014.02.014
0956-053X/Ó 2014 Elsevier Ltd. All rights reserved.
902 J. Ruan et al. / Waste Management 34 (2014) 901–907

PCBs. They are easy to be found in rhizosphere microbial commu- (in 1 L culture bottle). Then, 3 ml strain was inoculated into nutri-
nities, and have strong ability of acclimation. ent solution. After cultivation, concentrations of metals in the
In this study, a new strain of pseudomonas was found, which supernatant of nutrient solution were monitored. Concentration
could produce CN to recover precious metals from waste PCBs. of Au+ in nutrient solution was detected by the method of Induc-
Its category was distinguished by the method of DNA phylogenetic tively Coupled Plasma Optical Emission Spectrometer (ICP–OES).
tree. Factors influencing the new strain for producing CN (PH, Concentrations of Ag+ and Cu2+ were monitored by the method
temperature, additive, rotation) were investigated. Then, bioleach- of Atomic Absorption Spectrometry (AAS).
ing process of copper, silver, and gold from crushed waste PCBs by
the new strain was observed. This strain can be employed for 2.5. Percentage analysis of Au, Ag, and Cu in the mixed metals from
recovering precious metals from waste PCBs. The goal of this paper crushed waste PCBs and the bioleaching process
is to search a suitable strain for the industrial bioleaching process
of recovering precious metals from waste PCBs and will contribute Mixed metallic particles were obtained from corona-electro-
a lot to the development of new technology for recovering precious static separation of crushed waste PCBs. The process of gaining
metals and a value-added e-waste recovery. the mixed metallic particles was given in Fig. 1. Waste PCBs of mo-
bile phone were crushed into mixed particles (size 0.6 mm) of met-
2. Materials and methods als and nonmetals. Then the mixed particles were sorted into
metallic particles and nonmetallic particles by corona-electrostatic
2.1. Screening of pseudomonas separation. Separation rate of corona-electrostatic separation was
greater than 95%. The mixed metallic particles mainly contained
Soil for screening pseudomonas was obtained from reed root at copper and zinc as well as some precious metals of gold and silver.
mining region. Then, 0.2 ml soil extract (1 g soil dissolved in The nonmetallic particles mainly contained epoxy and fiberglass.
10 ml sterile water) was inoculated to NB medium (comprised of 4 g of mixed metallic particles (contained little nonmetallic parti-
beef extract, peptone, NaCl, and agar), which contained sterile pen- cles) were dissolved by aqua regia and diluted to 100 ml by dis-
icillin, novobiocin, and cycloheximide. After 72 h of cultivation, tilled water in a 100 ml volumetric flask. Then the concentration
various strains of Pseudomonas were selected and purified. of Au+ in the volumetric flask was detected by the method of
ICP–OES and the concentrations of Ag+ and Cu2+ were monitored
2.2. Monitoring of CN-producing ability of pseudomonas by the methods of AAS.
Mass percentage of Au, Ag, and Cu in the mixed metallic parti-
Color reaction was adopted to identify which strains could pro- cles could be calculated by Eq. (3):
duce CN. The strain which produced CN would turn the yellow c  0:1
test paper (dipped in the solution of 0.5% picric acid and 2% sodium g¼  100% ð3Þ
4
carbonate) to red. Turning time and color grade showed the CN-
producing ability. where g is the mass percentage of metal in the mixed metallic par-
For investigating the ability of producing CN, 1 ml Pseudomonas ticles, c is the concentration of metal in volumetric flask (g/L).
solution was cultured for 6 h, 12 h, 24 h, 36 h, 72 h, 120 h, and 196 h Bioleaching experiments of mixed metallic particles were per-
in nutrient solution (pH = 7; 25 °C) respectively. Concentrations of formed in lab. 4 g mixed metallic particles collected from crushed
CN produced by the strain in nutrient solutions were measured waste PCBs were fed into 250 ml of nutrient solution and the strain
by titration of silver nitrate (National standard of China, 2009). was inoculated into the nutrient solution. Under the optimized
[Ag(CN)2] will be generated when CN meets AgNO3. The excess conditions of producing CN, ten times of bioleaching were per-
Ag+ will gather indicator and turn the solution from yellow to or- formed to dissolve the 4 g of mixed metallic particles and each
ange red. The concentrations of CN can be computed by: time lasted 72 h in 250 ml of nutrient solution. Then, the concen-
trations of Au+, Ag+, and Cu2+ in the supernatant fluid of nutrient
cðV a  V 0 Þ  52:04  V 1  1000 solution were detected and the mass of dissolved Au+, Ag+, and
q¼ ð2Þ
V Cu2+ could be computed by multiplying metal concentration to
where c is the concentrations of silver nitrate, mol/L; Va, the the volume of nutrient solution.
volume of silver nitrate solution, ml; V0, the volume of silver
nitrate solution for blank control, ml; V, the total volume of sample,
3. Results and discussion
ml; and V1, the volume of the tested sample, ml.
3.1. Screening of pseudomonas strains and the phylogenetic tree
2.3. 16S rDNA sequence determination of the pseudomonas
According to color reaction, eleven strains (marked as 1#, 2#, 3#,
DNAs of Pseudomonas strains were extracted by the method of 4 , 5#, 6#, 7#, 8#, 9#, 10#, and 11# respectively), which were found
#

freeze–thaw. Then, DNAs were amplified under the primers of to have the ability of producing CN, were selected from the soil
27F(50 -AGAGTTTGATCCTGGCTCAG-30 ) and 1492R(50 -GGTTACCTT extract and presented as Fig. 2. The Figure showed that strain 6#
GTTACGACTT-30 ), and the sequences of DNAs were detected. had the greatest ability to produce CN.
According to the gene sequences, homology analyses of the strains After DNA extraction, PCR amplification, and sequences deter-
were performed by comparing to GenBank data via software of mination, phylogenetic tree of the strains were constructed by
DNAMAN (McMahan et al., 2012). Then, phylogenetic tree of the comparing the gene sequence to GenBank and presented as shown
strains were constructed by MEGA 5. in Fig. S1. According to phylogenetic tree, the genetic relationship
of the eleven strains was determined as shown in Table 1.
2.4. Investigation of precious-metal-leaching ability The threshold of homology judgment of strains by 16SrDNA se-
quences is 98%. That is, if the similarity is less than they are not the
Leaching ability of the strains to precious metals can be indi- same species. Thus, 1#, 4#, and 6# strains belonged to Pseudomonas
cated by the concentrations of dissolved metallic ions in nutrient Mosselii, Pseudomonas Aeruginosa, and Pseudomonas Chlororaphis
solution. Metallic particles were fed into 750 ml nutrient solution respectively (sequences of strain 6# were placed in supporting
 J. Ruan et al. / Waste Management 34 (2014) 901–907 903

Fig. 1. Mixed metals obtained from the crushed waste PCBs for bioleaching process.

Fig. 2. The selected eleven strains of pseudomonas which having the ability to
produce CN.

Table 1
Genetic relationships of the strains.

Strains of pseudomonas in GenBank Selected strains (similarity)

Pseudomonas Aeruginosa 4# (100%)
Pseudomonas chlororaphis 6# (100%)
Pseudomonas Putida 3# (99%), 5# (99%), 10# (99%), 7# (99%)
Pseudomonas Mosselii 1# (100%)
Pseudomonas Fluorescens 2# (99%)
Pseudomonas Sp. 8# (99%), 9# (99%), 11# (99%)

information). 3#, 5#, 10#, and 7# strains had close genetic relation-
ships to Pseudomonas Putida. 8#, 9#, and 11# strains were close to
Pseudomonas sp. And 2# strain was close to Pseudomonas
Fluorescens.

3.2. CN-producing ability of the selected strains

Concentrations of CN in nutrient solution of the mixed strains

were investigated. The results had been placed in Fig. 3(a). It could
be found that concentrations of CN increased with culture time.
Fig. 3. (a) Dynamic changes of the concentrations of CN in the culturing process of
And then, after cultured 24 h, concentrations of CN decreased to
the selected strains; and (b) the abilities of producing CN of the different selected
0.93 mg/L at the culture time of 196 h. The highest concentration strains.
of CN was 8.71 mg/L at the culture time of 24 h. The reason for
the decrease in CN concentrations was not found. However, this
phenomenon offered a good chance to treat residual CN. The Although color reaction showed that Pseudomonas Chlororaphis
residual CN would bring harm to the application of Pseudomonas (PC) had the greatest CN-producing ability, experiments for
for recovering waste PCBs. detecting the concentrations of CN produced by the selected
904 J. Ruan et al. / Waste Management 34 (2014) 901–907

eleven Pseudomonas strains were still performed. The strains were of 24 h. The highest concentration of CN at the culture condition
cultured for 24 h at the temperature of 25 °C. Then, concentrations of pH10 appeared at the culture time of 24 h and was 6.88 mg/L.
of CN were tested. The results were given in Fig. 3(b). It showed The two highest concentrations were not markedly different. It
that PC had the greatest ability of producing CN, and the concen- meant that pH (ranging from 7 to 10) exerted less influence on
tration of CN reached 7.11 mg/L. This ability was greater than CV the ability of producing CN.
in other published information.
3.3.2. Influencing of temperature on the ability of producing CN
3.3. Influences of the culture conditions to the ability of producing CN The published information showed the suitable temperature
ranged for CV producing CN was from 25 °C to 30 °C (Zoidakis
Various culture conditions were designed with different pH et al., 2005). The selected temperatures for the experiments were
(pH = 7, pH = 10), temperatures (15 °C, 25 °C, 35 °C), rotation 15 °C, 25 °C, and 35 °C respectively. The results were presented in
speeds of culture bottles (60 r/min, 120 r/min, 180 r/mim), and Fig. 4(b). The highest concentration of CN, 7.56 mg/L, appeared
additives (glycine, methionine, glycine + methionine). Because of at 25 °C.
having the greatest CN-producing ability, PC was chosen in the
experiments of investigating the influences of different culture
3.3.3. Influence of the additive on CN-producing ability
conditions.
According to the reports, glycine and methionine brought posi-
tive influence on the ability of producing CN of CV (Fairbrother
3.3.1. The influence of pH on the CN-producing ability et al., 2009). Thus, glycine and methionine were added to the cul-
The published information showed the CN-producing ability of ture medium in the experiment of investigating their influences on
CV increased with pH value, ranging from 7 to 9 (Chi et al., 2011). the ability of producing CN. The mediums were set as NB (N),
When pH was greater than 9, the ability would descend. Thus, the NB + 4.4 g/L glycine (N + G), NB + 2 g/L methionine (N + M), and
range of pH selected in the experiments was from 7 to 10. The re- NB + 4.4 g/L glycine + 2 g/L methionine (N + G + M). Then, the con-
sults were given in Fig. 4(a). Concentrations of CN in the culture centrations of CN were detected and the results were placed in
condition of pH7 were greater than pH10. It reached the maximum Fig. 4(c). The maximum CN concentration was improved to
of 7.1 mg/L at the culture condition of pH7 and at the culture time 15.52 mg/L by adding (N + G + M) when cultured for 72 h.

Fig. 4. The influences of PH, temperature, additive, and rotation on the ability of producing CN.
 J. Ruan et al. / Waste Management 34 (2014) 901–907 905

Meanwhile, the concentrations of CN in the medium added with presented in Table 2. The percentages of metals were similar to
methionine were greater than the medium which added glycine. their composition in waste PCBs of mobile phone.
This phenomenon showed that methionine could exert positive The results of dissolving experiments of samples I, II, and III
influence to the ability and glycine boosted this positive influence. were presented as Fig. 5(a) and (b).
Result of copper dissolution showed that the concentration of
3.3.4. Influence of rotation on the ability of producing CN Cu2+ in nutrient solution was increased as the culture time increas-
The purpose of rotation was to improve the dissolved oxygen in ing. The concentration reached 2.9 g/L when cultured for 120 h and
the culture solution. However, high rotation speed would destroy little copper particle was found in the nutrient solution.
the growth of Pseudomonas strain (Mohammad and Helmut, The result of silver dissolution indicated that little silver was
2008). Thus, rotation speed was chosen to replace dissolved oxy- dissolved within the culture time of 12 h. However, at the culture
gen for investigating the influence on the ability of producing time of 72 h, the concentration of Ag+ in the solution reached the
CN. Rotation speeds were set at 60 r/min, 120 r/min, and 180 highest levels of 2.5 mg/L and then decreased after 72 h. The rea-
r/min respectively. The results were given in Fig. 4(d). The maxi- son for the above change was that cells of the strain and the secreta
mum concentration reached 9.26 mg/L when the rotation speed adsorbed Ag+. It was proved by SEM picture (see Fig. S1) of strain
was 60 r/min. cell. Some particles were adsorbed in the secreta of the cell. The
Results of Fig. 4 showed that the optimized conditions of bring- dissolution process of gold was similar to silver. Little gold was dis-
ing the greatest ability of producing CN were at pH 7, 25 °C, with solved until it was cultured for 12 h. Concentration of Au+ in nutri-
glycine (4.4 g/L) + methionine (2 g/L) added, for 72 h of culture, and ent solution reached the highest level of 0.54 mg/L when cultured
at the rotation speed of 60 r/min. for 72 h. After that, concentrations of Au+ went down. The reason
was similar to that of silver. Results of dissolution experiments of
3.4. Dissolving ability of PC to copper, silver, and gold sole metals indicated that dissolution ability of PC for gold was
lower than copper and silver.
By employing the optimized conditions of bringing the greatest Results of the dissolution experiment of sample IV were pre-
ability of producing CN, PC was used to dissolve pure metals sented in Fig. 5(c) and (d). The maximum concentration of Cu2+
in solution was 2.6 g/L when cultured for 72 h. Meanwhile, the
Table 2 concentrations of Ag+ and Au+ also reached the highest levels.
Samples of precious metals for dissolve.
However, the levels of Ag+ (0.39 mg/L) and Au+ (0.22 mg/L) were
Sample I Sample II Sample III Sample IV lower than the sole dissolution process of silver and gold. The rea-
Metals Au Ag Cu Au + Ag + Cu son was that copper is more active than silver and gold. Copper
Mass (g) 0.1 0.5 3 0.1 + 0.5 + 3 was dissolved first. This competition between copper, silver, and

Fig. 5. Dissolving of the metal samples by PC.

906 J. Ruan et al. / Waste Management 34 (2014) 901–907

Fig. 6. SEM pictures and energy spectrum analysis of the cells dissolving copper, silver, and gold after 72 h.

gold kept the concentrations of Ag+ and Au+ low in the nutrient in the sole metal dissolution experiments. The reason was that
solution. Additionally, after being cultured for 72 h, the concentra- copper had more activity than silver and gold. This competition be-
tions of Cu2+, Ag+, and Au+ began to decrease. The adsorption of tween copper, silver, and gold kept the concentrations of Ag+ and
cells caused this phenomenon. SEM pictures and energy spectrum Au+ low in the solution. Dissolved metallic ions could be adsorbed
analysis of the cells gave the explanation. Fig. 6 showed that Cu2+, in cells, and Au+ was easier to be adsorbed than Cu2+ and Ag+. Addi-
Ag+, and Au+ were adsorbed in the cells. The mass fractions of Cu2+, tionally, after being cultured for 72 h, cells of the strain were de-
Ag+, and Au+ in cells were 4.5 wt%, 2.13 wt%, and 70.55 wt% respec- stroyed by the metallic ions.
tively. Besides Al (background), the atom percentage of gold
(27.66%) in the cells was considerably higher than silver (1.52%)
and copper (5.47%). The exact reasons for this phenomenon needed 3.5. Recovering Ag and Au from waste PCBs by PC
further research. However, one reason might be that the density of
gold was much higher than that of silver and copper, which made it 3.5.1. Percentage analysis of Au, Ag, and Cu in the metals from crushed
much easier for the adsorbed Cu2+ and Ag+ to escape than Au+ from waste PCBs
cell tissue. Thus, the atom percentage of gold was higher than that The Percentage of Au, Ag, and Cu in 4 g mixed metallic particles
of silver and copper. from waste PCBs was analyzed and the results were placed in Ta-
The increase of metal ions in solution destroyed the growth of ble 3. The mass of Au, Ag, and Cu in the 4 g of mixed metallic par-
PC, and damaged the dissolving process. Fig. S2 showed the expla- ticles were 0.0002 g, 0.0038 g, and 3.617 g respectively and their
nation. Metals destroyed cells of PC in the dissolving process of mass percentage was 0.005%, 0.095%, and 90.425% respectively.
copper, silver, and gold. Without metals, PC grew well when cul- The residual mass (0.379 g) of metallic particles might consist of
tured for 72 h. Thus, the increase of Cu2+, Ag+, and Au+ in nutrient zinc and lead, which were not monitored in the experiments.
solution accelerated the death of cells.
Copper, silver, and gold could be dissolved by CN produced by 3.5.2. Dissolving process of the metallic particles from crushed waste
PC respectively. In mixed metal dissolution experiments, the dis- PCBs by PC
solving ability of PC for copper was greater than that for silver The dissolution experiments were performed under the condi-
and gold. Meanwhile, the levels of Ag+ and Au+ were lower than tions that PC had the greatest ability of producing CN. The disso-
lution process was presented in Fig. 7. 4 g of mixed metallic
particles were dissolved ten times by PC, and each lasted for
Table 3
Contents of gold, silver, and copper in the 4 g mixed metallic particle from crushed
72 h. The results of the dissolution experiments were given in
waste PCBs. Table 4.
The dissolved masses of gold, silver, and copper were
Metals Au+ Ag+ Cu2+
0.0000164 g, 0.00046 g, and 1.892 g respectively. The comparison
Concentration (g/L) 0.002 0.038 36.17 between Tables 3 and 4 showed that 8.2% gold, 12.1% silver, and
Mass (g) 0.0002 0.0038 3.617
Mass percents (%) 0.005 0.095 90.425
52.3% copper in the metallic particles from crushed waste PCBs
were dissolved into solution. The dissolved metals (Au+, Ag+, and

Fig. 7. Dissolving process of Au, Ag, and Cu in the metallic particles from crushed waste PCBs by PC.
 J. Ruan et al. / Waste Management 34 (2014) 901–907 907

Table 4 Acknowledgments
Dissolving of Au, Ag, and Cu in the mixed metallic particle from crushed waste PCBs
by PC.
This work was supported by the National Natural Science Foun-
Metals Au+ Ag+ Cu2+ dation of China (51308488), the Natural Science Foundation of
Concentration (g/L) 0.0000656 0.00184 7.568 Jiangsu province (BK20130449), the Science and Technology Coop-
Mass (g) 0.0000164 0.00046 1.892 eration Fund Program of Yangzhou City and Yangzhou University
Dissolving rate (%) 8.2 12.1 52.3
(2012038-15), the Scientific Research Project of Environmental
fund of Yangzhou city (YHK1307). The authors are grateful to the
reviewers who help us improve the paper by many pertinent com-
Cu2+) can be recovered by the replacement reaction of more active ments and suggestions.
metal in sequence.
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Supporting information

Phylogenetic tree and Gene sequences of PC, Fig. S1, Fig. S2 were
placed in supporting information. This information is available free
of charge via the internet at http://www.elsevier.com.