Metal recovery from printed circuit boards by magnetotactic bacteria

Hydrometallurgy 187 (2019) 113–124

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Metal recovery from printed circuit boards by magnetotactic bacteria Sumana Sannigrahi, Suthindhiran K.

⁎

T

Marine Biotechnology and Bioproducts Laboratory, School of Bio Sciences and Technology, Vellore Institute of Technology, Vellore 632014, Tamil Nadu, India

A R T I C LE I N FO

A B S T R A C T

Keywords: Electronic waste Printed circuit boards Bioleaching Biorecovery Magnetotactic bacteria

Dumping of used printed circuit boards (PCB's) (diode and resistor) into the environment has been a major threat and its degradation methods are inadequate and time-consuming. Therefore development of novel strategies for the recovery of metals is the need of the hour. The current study was focused on biodegradation of waste printed circuit boards (diode and resistors) with five strains Magnetospirillum sp. RJS2 (KJ570852), Magnetospirillum sp. RJS5 (KM289194), Magnetospirillum sp. RJS6 (KT266803), Magnetospirillum sp. RJS7 (KT693285) and Magnetospirillum gryphiswaldense (MSR-1). The circuit boards were milled for size reduction and the samples were analysed using particle size analyser and X-ray powder diffraction (XRD). Heavy metals such as cadmium, copper, nickel, lead and zinc were detected in diode from PCB's, whereas arsenic, chromium, copper, lead, silicon, aluminium, silver and zinc were observed in resistors. The samples were treated with the bacterial strains (RJS2, RJS5, RJS6, RJS7 and MSR-1) individually and in consortia for 12 days. Atomic absorption spectroscopy (AAS) analysis revealed the isolate RJS2, MSR-1 and RJS6 showed maximum recovery of cadmium (97%), lead (100%) and nickel (99%) from diode respectively. Similarly from resistor the maximum recovery was observed with RJS2 (copper - 89%) and RJS6 (zinc - 88%). The overall average recovery of cadmium (80%) and lead (66%) was more from treated diode. Similarly, copper (45%) and lead (40%) were recovered from resistors. It was also observed that the isolate RJS2 was effective in metal recovery (52%) from diode and strain RJS6 (66%) for the resistor. Two groups of consortia were developed MAG1 (RJS2, RJS5 and MSR-1) and MAG2 (RJS6 and RJS7) based on their growth requirements, where MAG1 exhibited better recovery of metals such as nickel (100%), zinc (75%) from diode and cadmium (90%), nickel (22%) and zinc (47%) from resistor as compared to individual strains. MAG2 also exhibited better recovery of lead (57%) from diode and nickel (22%) from resistor. Scanning electron microscope Energy-dispersive X-ray spectroscopy (SEM-EDS) and X-ray fluorescence (XRF) analysis confirmed RJS2 and RJS6 were dominant strains in metal recovery. The study showed the efficacy of Magnetospirillum bacteria in enhanced metal recovery from PCB's, highlighting its possible role in the management of E-waste.

1. Introduction E-waste consists of appliances that use an electric power supply which has reached its expiry and are discarded by the user (Wath et al., 2011). The dumping of E-waste in the form of circuit boards is increasing worldwide due to the rapid upgradation of electronic goods such as computers, televisions, audio equipment and printers etc. (Cui and Forssberg, 2003). Treatment of used PCB's is a challenge owing to its complex equipmentation (Huang et al., 2009). Printed circuit boards (PCB's) consists of polymers, ceramics and metals such as copper: 10–20%, lead: 1–5% and nickel: 1–3% (Hoffmann, 1992; Ludwig et al., 2012). These E-wastes are considered to be hazardous when the metals like lead, mercury, arsenic, cadmium, selenium, hexavalent chromium and flame retardants are present beyond permissible limits (CPCB,

⁎

2007; Pant et al., 2012). The environmental protection agency has set permissible limits for heavy metals such as cadmium (10 μg/ml), copper (1.3 mg/L), lead (15 μg/L), nickel (0.1 mg/L) and zinc (5 mg/L) (American Public Health Association (APHA), 1999; EPA, 2000). Lead is one of the main components in PCB's and the toxic nature of lead poses various problems in recovery studies (Lo et al., 1999; Ramachandra and Saira, 2004). Furthermore, the PCB's release considerable amount of toxic substances, such as the flame-retarding “synergist” antimony trioxide, which can percolate the soil and reach into the groundwater and enter the food chain leading to biomagnification (E-Waste Fact Sheet, Clean Up, 2009; Veit et al., 2005). Several reports have shown that recycling of PCB's can lead to the recovery of precious metals such as copper, gold, silver, palladium etc. (Bleiwas and Kelly, 2001; Das et al., 2009; Goosey and Kellner, 2003;

Corresponding author. E-mail address: [email protected] (K. Suthindhiran).

https://doi.org/10.1016/j.hydromet.2019.05.007 Received 7 July 2018; Received in revised form 5 April 2019; Accepted 11 May 2019 Available online 13 May 2019 0304-386X/ © 2019 Elsevier B.V. All rights reserved.

Hydrometallurgy 187 (2019) 113–124

S. Sannigrahi and K. Suthindhiran

SCIENTIFIC SZ-100, Japan) and the presence of heavy metals was analysed through X-ray powder diffraction (XRD, BRUKER, Germany). One gram of powdered sample was treated with few drops of HNO3 and the volume was made up to 100 ml with double distilled water. The prepared samples were filtered (< 100 μM) and subsequently used for metal recovery batch experiment (Adhapure et al., 2013).

Yang et al., 2009; Yazici and Deveci, 2013). However, the existing practice for recycling PCB's by pyrometallurgical methods consumes energy and leads to atmospheric pollution through the release of dioxins and furans (Akcil et al., 2015; Tsydenova and Bengtsson, 2011). Hydrometallurgical process, on the other hand, causes exposure to acids and cleaning solvents (Bernardes et al., 2004). Likewise, the thermal process releases heat to the environment; electrochemical process are fast but consumes electricity and chemical processes are not cost effective (Mecucci and Scott, 2002; Ordoñez et al., 2016). Therefore, a eco-friendly, efficient and low-cost processing technology for E-waste recycling and metal recovery are required. Magnetotactic bacteria (MTB) are Gram-negative, motile prokaryotes that align themselves along the geomagnetic field (Bazylinski and Williams, 2006). The MTB's have great potential to be used for magnetic separation, magnetic domains analysis, heavy metals and radionuclide recovery (Bazylinski and Schübbe, 2007). Previously, recovery of metals from wastewater using magnetotactic bacteria was established (Bahaj et al., 1998). Cadmium uptake was successfully demonstrated by Sulfate-Reducing Magnetotactic Bacterium, Desulfovibrio magneticus RS-1 using magnetic separation technique (Arakaki et al., 2002). Also, uptake of metals like zinc and cobalt by Magnetospirillum magnetotacticum MS-1 was reported by Tu et al. (2014). MTB have a unique ability to reduce iron molecules along with oxygen or sulphate to form intracellular magnetite and greigite through the process of compartmentalization (Bazylinski et al., 1995; Komeili, 2012; Matsunaga et al., 1991). In certain cases, copper is taken up from the environment to form magnetosome (Bazylinski et al., 1993). There are other sulphate reducing bacteria which poses the ability to uptake heavy metals (Karwowska et al., 2014; Sitte et al., 2010). Our earlier reports have shown that calcium chloride coated magnetosomes effectively removes chromium and nickel from tannery effluent (Jacob et al., 2018a, 2018b). This research was hypothesized that magnetotactic bacteria can be used as bioabsorbents in the recovery of selected metals from E-waste. In the current study metals were recovered from PCB's (diode and resistor) using MTB strains individually and in consortia. Scanning electron microscope Energy-dispersive X-ray spectroscopy (SEM-EDS) and X-ray fluorescence (XRF) analysis was performed to understand the biosorption potential.

2.3. Metal recovery batch experiment The PCB samples were supplemented to MSGM and OSGM (1:10) in sterile serum bottles. The microaerophilic condition was maintained by sparging nitrogen gas and the pH were adjusted to 6.7 and 7 in MSGM and OSGM respectively to achieve maximum growth of isolates. Additionally, sterile vitamin and the ferric quinate solution were added to MSGM and sterile cysteine HCl, vitamin solution and ferric citrate solution were added to OSGM to enhance the growth of strains. One ml of 10 days incubated MTB culture (RJS2, RJS5 and MSR-1 in MSGM and RJS6 and RJS7 in OSGM) was inoculated to each setup except for two sets of control. The first control was maintained without the PCB's (media + culture) whereas uninoculated media with PCB's (media + PCB's) served as another control. The inoculated bottles were kept in shaking condition (120 rpm) for 12 days at 28 ± 2 °C (Fig. 1). Growth of the culture was determined at regular intervals of 12 h. The initial and the final metal concentration was analysed using Atomic Atomic absorption spectroscopy (AAS, VARIAN SPECTRAA240, Australia). 2.4. Preparation of consortium and biodegradation batch experiment Two sets of consortium (MAG1 and MAG2) were developed based on the growth requirements of strains. MAG1 consisting of RJS2, RJS5 and MSR-1 were cultivated in MSGM. The second set was cultured in OSGM containing RJS6 and RJS7 (MAG2). The metals were recovered as described above (Fig. 1). 2.5. Sample preparation The metal concentration in the experimental broth was determined using AAS. For plotting the calibration curve, stock solutions (1000 ppm) of metals such as cadmium, copper, nickel, lead and zinc were prepared and standard procedures for the analysis of heavy metals were followed (Franson, 1995). Standard working solutions of 100, 200 and 300 ppm were prepared by diluting the stock solution in deionized water (AOAC, 1971). Instrumental setup and calibration were carried out according to the guidelines given in the manual provided by the manufacturer (Acmas technologies (P) Ltd., India). The treated PCB samples were centrifuged (Refrigerated Centrifuge LI-HRC-16 K, Lark Innovative Fine Teknowledge, India) (10,000 rpm for 10 min); bacteria were separated and sequentially analysed for metals using AAS as per the given Eq. (1).

2. Materials and methods 2.1. Microorganisms and growth medium The chemicals were procured from Himedia Laboratories, India. Magnetospirullium RJS2 (KJ570852), Magnetospirillum RJS5 (KM289194), Magnetospirillum RJS6 (KT266803) and Magnetospirillum RJS7 (KT693285) were isolated from marine sediments and are maintained in Marine Biotechnology and Bioproducts laboratory, VIT, Vellore, India (Jacob et al., 2016). The molecular and phylogenetic characterization of the strains RJS2, RJS5, RJS6 and RJS7 were reported earlier by Jacob et al. (2016, 2018a, 2018b). The strain Magnetospirullium gryphiswaldense (MSR-1) was obtained from Deutsche Sammlung von Mikroorganismen und Zellkulturen (DSMZ) Germany. Strains RJS2, RJS5 and MSR-1 were cultured in Magnetospirillum growth medium (MSGM) (Blakemore et al., 1979) and strains RJS6 and RJS7 were cultured in oxygen-sulfide gradient medium (OSGM) (Schüler et al., 1999). Hungate anaerobic technique (Hungate, 1950) was used for the culturing of all strains.

%Metal recovery = [(Abscontrol − Abstest)/Abscontrol] × 100

(1)

Abscontrol: Absorbance in control sample; Abstest: Absorbance in test sample. The pellet containing the MTB strains were collected and fixed with 0.25% glutaraldehyde for overnight incubation. The cells were dehydrated with ethanol and mounted over a glass slide to analyse through SEM-EDS (Tescan VEGA 3SBH with BrukerEasy EDS, Czech Republic working at 25 kV high vacuum mode). Further, the pellet was re-suspended in Tris-HCl buffer and subjected to sonication for 120 min (30 W). SDS (1%) was added to the pellet and incubated in a water bath (90 °C) for 5 h. The samples were collected through centrifugation (10,000 rpm, 10 min) and lyophilized (Lark, Penguin Classic Plus, India). The powdered samples were analysed through XRF (XGT-5200, HORIBA, Japan) to determine the metal content.

2.2. Preparation of PCB sample The waste PCB (2,000,802,731 CXI HXI SXI) was collected from the local market in Vellore, Tamilnadu. The parts such as diode and resistor were detached carefully from the circuit boards and were hammermilled to reduce the particle size. The particle sizes of both diode and resistor were analysed using particle size analyser (HORIBA 114

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Fig. 1. Diagrammatic representation showing methodology of metal recovery from PCB's using batch experiment.

3. Results

3.4. The percentage recovery of metals from diode with individual strains

3.1. Particle size analysis of diode and resistor from waste PCB's

AAS analysis was performed to determine the percentage recovery of metal from diode after bacterial treatment. All the strains were capable of recovering the tested five metals from the treated diode. The strain MSR-1 recovered cadmium (82.6%), copper (42%), nickel (7.8%), lead (100%) and zinc (2.5%) (Fig. 4a). The strain RJS2 displayed a better percentage recovery of metals as compared to MSR-1. It sequestered cadmium (97%), copper (8.3%), nickel (41%), lead (100%) and zinc (13%) from diode (Fig. 4b). The strain RJS5 exhibited lower metal recovery compared to MSR-1, but recovery of zinc was relatively higher (28%). Additionally, it recovered 80.6% of cadmium, 2% of copper, 7% of nickel and 77% of lead (Fig. 4c). The strain RJS6 exhibited a better uptake of metals as compared to the other strains (MSR1 and RJS5). It recovered 70% of cadmium, 9% of copper, 99% of nickel, 4% of lead, and 29.5% of zinc (Fig. 4d). RJS7 demonstrated relatively lower uptake of metals from diode as compared to other strains. However, sequestration of zinc (36%) was maximum when RJS7 was used. It also recovered cadmium (72.5%), copper (2.4%), nickel (8.7%) and lead (50%) from diode (Fig. 4e).

The average size of particles present in the diode and resistor were found to be 1232.8 nm and 2305.4 nm (Fig. 2a, Fig. 2b).

3.2. The presence of metals in diode and resistor from waste PCB's The XRD analysis revealed the presence of copper, nickel, lead, strontium and yttrium in the form of bushmakinite in the diode of waste PCB's (Fig. 3a). The XRD analysis of resistors depicted the presence of metals in various forms. Arsenic, chromium, copper and lead were present in the form of iranite. Chromium, lead and silicon were present as fornacite. Further, vauquelinite contained metals such as chromium, copper and aluminium. Chromium and copper were predominantly present in hemihedrite phase (Fig. 3b).

3.3. Treatment, colour change and adaptation

3.5. The percentage recovery of metals from resistor with individual strains

There was a significant difference in the growth pattern of Magnetospirillum strains in the media supplemented with and without PCB's. Further, the media amended with resistor showed a change in colour from violet to pink. Similarly, the colour was changed to green in the media supplemented with diode. The change in colour in the media was possibly due to the change in pH. Initially the pH of the medium was 6.7 in MSGM and 7 in OSGM. Upon the addition of PCB's the pH reduced to 5.8 in MSGM and 6 in OSGM. Nevertheless, to achieve the maximum growth of the isolates, the pH of the media was readjusted to 6.7 and 7 in MSGM and OSGM respectively. The isolate MSR-1 showed magnetic moment which reduced upon treatment with PCB's when analysed by placing the culture bottles on a magnetic stirrer and by observing the strength scattering of light. It might be due to the inability of few bacterial cells to adapt in the presence of PCB's.

Recovery of metal from resistor of PCB's was found to be efficient by all the strains. The strains RJS2, RJS5, RJS6 and RJS7 effectively sequestered all five metals from the resistor. The strain MSR-1 recovered metals such as cadmium (9.8%), copper (6.4%), nickel (4.3%) and zinc (6.7%) from the resistor (Fig. 5a). The strain MSR-1 was inefficient in lead recovery from the resistor, however, the strains RJS2, RJS5, RJS6 and RJS7 exhibited increased recovery of lead. The strain RJS2 solubilized cadmium (23.4%), copper (89%), nickel (13%), lead (37%) and zinc (13.3%) (Fig. 5b). The strain RJS5 exhibit recovery of cadmium (7.4%), copper (51.6%), nickel (1.4%), lead (33.3%) and zinc (15%) (Fig. 5c). Both RJS2 and RJS5 exhibit a good recovery of copper and lead. However, the strain RJS6 displayed higher recovery of all the five 115

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Fig. 2. a) Particle size analysis of diode from waste PCB's. b) Particle size analysis of resistor from waste PCB's.

strains. The consortium effectively grew in presence of resistor and effectively recovered all the five metals. MAG1 consortium recovered cadmium (90.1%), copper (40.5%), nickel (22.3%) lead (2.8%) and zinc (47.4%) (Fig. 7a). Excess recovery of cadmium, copper and zinc were obtained in MAG1 consortium. Further, in comparison with individual strains, MAG1 consortium exhibited higher recovery of cadmium, nickel and zinc. It was also observed that the magnetosome production was suppressed in MAG1 consortium treated with resistor. MAG2 (RJS6, RJS7) consortium also showed moderate recovery of metals from the resistor. MAG2 displayed recovery of metals such as cadmium (5.7%), copper (14.5%), nickel (22.8%), lead (13.9%) and zinc (9.7%) (Fig. 7b). The MAG2 consortium exhibited a maximum recovery of nickel from the resistor. Further, in comparison with the individual strains, recovery of nickel was enhanced by 3%. However, recovery of other metals in individual strain was comparatively higher.

metals such as cadmium (85%), copper (78%), nickel (30%), lead (50%) and zinc (88%) (Fig. 5d). The strain RJS7 exhibit good recovery of lead (83%), cadmium (40.5%) and zinc (36.7%) while low recovery of copper (1%) and nickel (9.5%) (Fig. 5e). 3.6. Metal recovery from diode using MAG1 and MAG2 consortium The metal recovery analysis was further analysed using Magnetospirillum consortia. MAG1 (RJS2, RJS5, MSR-1) consortium displayed improved metal recovery from diode of PCB's. Among the five metals, cadmium (51%), nickel (100%) and zinc (75%) were recovered largely from the diode. The recovery of other metal such as lead (26%) was found to be poor (Fig. 6a). Recovery of copper was negligible from diode using MAG-1. The recovery of metal from diode was also detected using MAG2 consortium. MAG2 consortium recovered four metals cadmium (18%), nickel (38.9), lead (57%) and zinc (18%) from diode. Lead and nickel were recovered in higher concentration, though there was no recovery of copper. Further, in comparison with the individual strains, MAG2 consortium elevated the quantity of recovery (30%) of lead (Fig. 6b). Recoveries of other metals were low in the presence of MAG2 consortium from the diode of PCB's as compared to MAG1.

3.8. SEM-EDS analysis The SEM-EDS analysis was performed for four strains (RJS2, RJS5, RJS6 and RJS7) based on their performance of metal recovery in AAS. The strain RJS2 showed better recovery of metals like copper, nickel, zinc, iron, cadmium, manganese and lead from diode (Fig. 8a). The amount of manganese was dominant, followed by zinc, iron, lead and cadmium. Uptake of copper and nickel was negligible. Similarly, RJS5 showed better ability of uptake from diode for metals like zinc, manganese, iron, lead and cadmium (Fig. 8b). Copper and nickel uptake was less prominent in RJS5 from diode. The strains RJS6 and RJS7 exhibited

3.7. Metal recovery from resistor using MAG1 and MAG2 consortium The percentage recovery of metals using MAG1 (RJS2, RJS5, MSR1) consortium showed a remarkable difference than the individual 116

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Fig. 3. a) XRD analysis of diode from waste PCB's shows the presence of copper, lead, nickel, strontium and yttrium. b) XRD analysis of resistor from waste PCB's shows the presence of arsenic, chromium, copper, lead, silica and aluminium.

3.9. XRF analysis

better metal recovery from resistors in AAS studies. Hence, the SEMEDS analysis of RJS6 from resistor was conducted which revealed high uptake of metals like zinc, lead, iron, manganese, cadmium and copper while low uptake of nickel (Fig. 8c). RJS7 also showed uptake of metals like zinc, manganese, lead and iron from resisitor. However, uptake of other metals such as copper, cadmium and nickel was insignificant (Fig. 8d).

The XRF analysis was carried out to determine the recovery of metal by the MTB strains from diode and resistor of PCB's (Table 1). Treatment of diode by MTB strains showed effective recovery of metals like copper, zinc, manganese and iron. The performance of the MTB strain was determined through average recovery of each metal. It was evident that, RJS2 and RJS5 could recover majority of the metals at a larger rate compared to other MTB's. Sequestration of zinc in strains RJS5, RJS6 and RJS7 was evident from diode. 117

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0.25

0.1

Concentration mg/L

Concentration mg/L

0.12

0.08 0.06

control test

0.04

0.2 0.15 control

0.1

test

0.05

0.02 0 Cd

Cu

Ni

Pb

0

Zn

Cd

Cu

Ni Metals

Metals

Pb

Zn

c

Concentration mg/L

0.12 0.1 0.08 0.06

control test

0.04 0.02 0 Cd

d

Cu

Ni Metals

Pb

Zn

Concentration mg/L

0.14 0.12 0.1 0.08 control

0.06

test

0.04 0.02 0 Cd

Cu

Ni Metals

Pb

Zn

e 0.14 Concentration mg/L

0.12 0.1 0.08 control

0.06

test

0.04 0.02 0 Cd

Cu

Ni Metals

Pb

Zn

Fig. 4. a) AAS analysis of diode from waste PCB's treated with the strain MSR-1. The figure shows significant recovery in the quantity of cadmium, copper, nickel and lead after treatment. Lead is efficiently recovered after the treatment but low recovery of zinc is obtained. b) AAS analysis of diode from waste PCB's treated with the strain RJS2. The figure shows significant recovery of cadmium, nickel and lead but low recovery of copper and zinc. c) AAS analysis of diode from waste PCB's with the strain RJS5 strain. The figure shows considerable recovery of cadmium, lead and zinc. Low recovery of copper and nickel was obtained in the diode after being treated. d) AAS analysis of diode from waste PCB's treated with the strain RJS6. The figure shows a considerable reduction in the quantity of cadmium, nickel and zinc. Low recovery of copper and lead was estimated in diode after treatment with RJS6 strain. e) AAS analysis of diode from waste PCB's treated with the strain RJS7. The figure shows a considerable recovery of cadmium, lead and zinc in the diode of circuit boards. Low recovery of copper and nickel was obtained in the diode. 118

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a

0.1 0.09

Concentration mg/L

0.08 0.07 0.06 0.05

control

0.04

test

0.03 0.02 0.01 0 Cd

Cu

Ni Metals

Pb

Zn

b 0.1

Concentration mg/L

0.09 0.08 0.07 0.06 0.05

control

0.04

test

0.03 0.02 0.01 0 Cd

c

Cu

Ni Metals

Pb

Zn

0.1

Concentration mg/L

0.09 0.08 0.07 0.06 0.05

control

0.04

test

0.03 0.02 0.01 0 Cd

Cu

Ni Metals

Pb

Zn

Fig. 5. a) AAS analysis of resistor from waste PCB's treated with the strain MSR-1. There was the low recovery of metals in the resistor. Cadmium, copper, nickel and zinc recovery was < 10% while no recovery of lead was obtained. b) AAS analysis of resistor from waste PCB's treated with the strain RJS2. The amount of cadmium, copper and lead were effectively recovered while low recovery of nickel and zinc was obtained. c) AAS analysis of resistor from waste PCB's with the strain RJS5. The amount of copper and lead was effectively recovered while cadmium, nickel and zinc were recovered in low quantity. d) AAS analysis of resistor from waste PCB's treated with the strain RJS6. The metals namely cadmium, copper, nickel, lead, and zinc were efficiently recovered from the resistor. e) AAS analysis of resistor from waste PCB's treated with the strain RJS7. Efficient quantity of cadmium, lead and zinc were recovered. The amount of copper and nickel recovery was low in the resistor.

4. Discussion

Metal recovery from resistor using MTB strains showed conclusive results. Metals such as copper, manganese and zinc displayed effective recovery. Among the five isolates, RJS6 showed prominent recovery of three metals copper, zinc and manganese with a higher recovery rate. Sequestration of zinc by RJS6 and RJS7 was also confirmed through XRF analysis.

PCB's consists of various metals such as copper, tin, lead, iron, nickel, cadmium, chromium, manganese, palladium, platinum etc., which poses serious threat to ecosystem (Yang et al., 2011). Although biodegradation of PCB's have been reported (Eswaraiah et al., 2008; 119

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d 0.7

Concentration mg/L

0.6 0.5 0.4

control

0.3 test 0.2 0.1 0 Cd

e

Cu

Ni Metals

Pb

Zn

0.7

Concentration mg/L

0.6 0.5 0.4

control

0.3 test

0.2 0.1 0 Cd

Cu

Ni Metals

Pb

Zn

Fig. 5. (continued)

which corresponded to metals such as copper, nickel, lead, strontium, yttrium, arsenic, chromium, aluminium and silica. Similar studies have been carried out by Xue et al. (2011) where metal like chromium, copper, cadmium and lead has been detected. Addition of PCB's to the MTB containing media showed colour change from violet to pink due to the reduction of inactive resazurin to resorufin (Bazylinski et al., 2013). However, previous reports have shown that the redox indicator also changes colour and intensity with change in pH (Tashyrev and Prekrasna, 2014). Initially, there was a reduction in the growth of MTB in broth supplemented with diode and

Pradhan and Kumar, 2012), studies on the recovery and reuse of metals from PCB's are meagre. This research was attempted to exploit the bioleaching property of Magnetospirillum strains for E-waste management from substrates like diode and resistor (PCB's). The diode and resistor were powdered and the sizes of those particles were found to be < 2500 nm which makes it suitable for bacteria mediated metal recovery experiments. It should be noted that leaching studies dealing with PCB's mostly involves milling of PCB's into powder with a particle size of < 0.5 mm (Alam et al., 2007; Yang et al., 2009). XRD analysis of powdered PCB's revealed the presence of structures

a.

b. 0.45

0.6

0.4 0.3

control test

0.2

Concentration mg/L

Concentration mg/L

0.4 0.5

0.35 0.3 0.25 control

0.2

test

0.15 0.1

0.1

0.05

0 Cd

Cu

Ni Metals

Pb

0

Zn

Cd

Cu

Ni Metals

Pb

Zn

Fig. 6. a) AAS analysis of diode from waste PCB's treated with MAG1 consortium. Efficient recovery of cadmium, nickel, lead and zinc was obtained from the diode. However, there was no recovery of copper in the diode. b) AAS analysis of diode from waste PCB's treated with MAG2 consortium. Efficient recovery of nickel and lead was obtained in the diode. Low recovery of cadmium and zinc was obtained after treatment while no recovery of copper was observed. 120

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b 0.9

1 0.9

0.8 0.7 0.6 0.5 0.4

control

0.3

test

Concentration mg/L

Concentration mg/L

a

0.8 0.7 0.6 0.5

control

0.4

test

0.3

0.2

0.2

0.1

0.1 0

0 Cd

Cu

Ni Metals

Pb

Cd

Zn

Cu

Ni Metals

Pb

Zn

Fig. 7. a) AAS analysis of resistor from waste circuit boards treated with MAG1 consortium. Among the five metals, cadmium, copper, nickel and zinc were effectively recovered from the resistor but the low recovery of lead was obtained from the resistor. b) AAS analysis of resistor from waste circuit boards treated with MAG2 consortium. Among the five metals, only effective recovery of nickel was obtained from the resistor. Recovery of cadmium, copper, lead and zinc were low in the resistor.

diode and resistor. Hence maximum recovery of metals was achieved as compared to previous studies. Further, AAS analysis was carried out to estimate the concentration of metal ion in the broth upon treatment with the test organisms. In diode, it was evident that strains RJS2 and RJS6 were capable of

resistor which could be due to the acclimatization of the strains. There are studies showing the reduction in growth of bacteria when treated with E-waste (Ilyas et al., 2007) and toxic effect of electronic scrap was observed on A. ferrooxidans (Brandl et al., 2001). All the isolates were highly effective and were capable of solubilizing metals present in

Fig. 8. SEM-EDS analysis. (a): RJS2 from diode, (b): RJS5 from diode, (c): RJS6 from resistor, (d): RJS7 from resistor. 121

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Table 1 XRF analysis of metal recovery in MTB strains from diode and resistor (PCB's). Diode %

RJS2 RJS5 RJS6 RJS7 MSR-1

Resistor %

Cd

Cu

Ni

Pb

Zn

Mn

Fe

Cd

Cu

Ni

Pb

Zn

Mn

Fe

0 0.001 0 0 0.002

22 1.1 0.9 0.04 20.6

0.007 0.04 0.04 0 0

0.03 0.06 0.04 0.12 0.006

0.3 24 23 20.3 0.9

16.4 13.5 14 15 19

2.3 3.7 4 5.4 –

0.02 0 0 0 –

15.5 8.1 23.4 1.01 21

0 0 0.01 0.04 0

0.23 0.05 0.01 0.01 0.005

0.05 0.01 39.8 19.1 0.95

18.4 12.6 15.3 13.8 18

– – – 3.5 0.5

Note: (−) = Not determined.

metals from PCB's as compared to MAG1. Among the consortia, MAG1 was better in metal recovery from PCB's. The conventional microorganism such as autotrophic acidophilic bacteria was reported to be ineffective in metal recovery by bioleaching process as compared to Magnetospirillum species (Brandl et al., 2001). It is also observed that application of heterotrophic bacteria and fungi like Bacillus sp., Penicillium simplicissimum, Aspergillus niger, Saccharomyces cerevisiae and Yarrowia lipolytica have proven to recover lead, copper and tin from PCB's (Brandl et al., 2001; Hahn et al., 1993; Keong, 2003). Further, SEM-EDS analysis determined the surface elemental composition in the MTB strains. The strains RJS2, RJS5, RJS6 and RJS7 displayed good uptake of zinc and manganese. The reason could be the presence of excessive iron content in the media supplement which ultimately triggered the uptake of zinc in MTB's (Deveci et al., 2004). Manganese on the other hand is one of the essential trace elements which serve a vital role in bacterial growth during a stress condition (Jakubovics and Jenkinson, 2001). Exposing the MTB's to PCB's might result in a nutrient imbalance resulting in uptake of high manganese during the whole process. The XRF analysis of the lyophilized MTB strains collected after the bioleaching process confirmed the intracellular metal uptake. Results were definitive to SEM-EDS analysis with prominent metals being manganese and zinc. Furthermore, copper was also recovered by MTB's in immense quantity. The recovery of copper from resistor was considerable higher than the zinc recovery in MTB strains. The free copper ion is highly toxic to bacterial cells which cause difficulty in copper uptake (Rademacher and Masepohl, 2012). However, MTB's especially MV-1 strain contains ChpA (copper handling proteins) which are directly involved with iron accumulation and magnetosome formation (Dubbels et al., 2004). The direct exposure to copper present in PCB's can also accelerate the process of magnetosome formation in MTB's (Schüler, 2008). The current study is the first of its kind, where Magnetospirillum has been employed as a promising candidate for the solubilisation and recovery of metals such as manganese, cadmium, lead, copper, nickel and zinc from PCB's. Further, the strains RJS2 and RJS6 were capable of recovering cadmium, manganese, lead and copper in significant concentrations from PCB's. The strains RJS2 and RJS6 along with MAG1 consortium could be further implemented for large scale recovery of noble metals in a cost-effective and eco-friendly methodology.

recovering metals at higher concentration as compared to MSR-1 strain. All the five strains recovered cadmium and lead at significantly higher concentration. An average of 80.5% cadmium and 66% of lead was recovered from diode. The strain RJS6 exhibited better recovery of cadmium and nickel with low recovery of lead. Recovery of zinc and copper from diode was comparatively less in all strains. However, the percentage recovery of metals such as copper and lead were maximum from resistor. The strains RJS2, RJS5 and RJS6 showed increased recovery of copper and RJS7 exhibited maximum recovery of lead from resistor. Notable recovery of cadmium was observed in RJS2, RJS6 and RJS7. Comparatively, MSR-1 showed low recovery of heavy metals from resistor. The current study has shown enhanced recovery of lead, one of the major toxic heavy metal from both the parts of PCB's. The Ranitovic et al. (2016) reported 98% leaching of lead using hydrometallurgical process at 80 °C from waste PCB's. But, treating metals such as lead, copper and cadmium with high temperature is highly hazardous due to the low melting point of these metals (Tsydenova and Bengtsson, 2011). Similarly, Castro and Martins (2009) have shown 93% recovery of copper from PCB's using leaching and precipitation methods. However, the use of acids during leaching process leads to toxic effects to the ecosystem when discharged. In the current study a simple and cost effective bioprocess technology with maximum recovery of lead using strains RJS2 and MSR-1 has been employed. Past studies mostly emphasise on lead and copper recovery from PCB's (Li et al., 2007; Oishi et al., 2007; Veit et al., 2006; Willner and Fornalczyk, 2013). Our study also proved better recovery of metals like cadmium, nickel and zinc in addition to lead and copper. Promising recovery of metals was achieved when RJS2 and RJS6 were augmented. Similarly, Harikrushnan et al. (2016) used a combination of hydrometallurgy and biological process to achieve better recovery of copper, nickel and zinc. The strain RJS2 marked promising recovery of cadmium (97%), nickel (41%) and lead (100%) from diode while copper (89%) and lead (37%) from the resistor. However, the strain RJS6 displayed remarkable recovery of cadmium (70%) and nickel (99%) from diode while cadmium (85%), copper (78%), lead (50%) and zinc (88%) from the resistor. The strain RJS7 exhibit a good recovery of cadmium, lead and zinc from both parts of PCB's. The strain RJS5 recovered lead in moderate quantity from both the parts of PCB's while it recovered 80% of cadmium from the diode and 51% of copper from the resistor. MSR-1 exhibits a high recovery of cadmium (82%) and lead (100%) from the diode. Further, development of consortium such as MAG1 (RJS2, RJS5 and MSR-1) and MAG2 (RJS6 and RJS7) resulted in the enhanced solubilisation of metals from PCB's thereby increasing the recovery of metals as compared to individual strains. In diode, the recovery of nickel and zinc was enhanced by 81.4% and 60% respectively by MAG1. Nevertheless, the production of magnetosome in MAG1 consortium was found to be reduced in the presence of diode. In resistor, the recovery of cadmium, nickel and zinc were enhanced by approximately 76.5%, 16% and 35.8% respectively by MAG1. Although, recovery of copper and lead was low in MAG1 consortium, overall recovery of all the metal was enhanced by 20%. However, MAG2 showed reduced recovery of

5. Conclusion The present study demonstrates the ability of Magnetospirillum strains in metal recovery from diode and resistors of PCB's. The strains RJS2 and RJS6 have shown maximum recovery of metals such as lead, cadmium, manganese and copper. Furthermore, the MTB consortia exhibits better recovery compared to individual strains. The MAG1 consortium recovers the metals such as nickel, cadmium and zinc. Our results indicate that MTB could be exploited for E-waste management as cost-effective and eco-friendly process. Further, the MTB can be separated using external magnetic field and intracellular metals can be 122

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easily separated and recovered from cells through simple precipitation process. Furthermore, it is envisaged that recovery of metals such as silver and gold from E-waste using Magnetospirillum strains and their consortium could be inexpensive and efficient technology.

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