Waste Management xxx (2015) xxx–xxx

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Waste Management

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Bioleaching of spent Zn–Mn or Ni–Cd batteries by Aspergillus species

http://dx.doi.org/10.1016/j.wasman.2015.11.0010956-053X/� 2015 Elsevier Ltd. All rights reserved.

⇑ Corresponding author.E-mail addresses: kimmj@korea.ac.kr (M.-J. Kim), jyseo@korea.ac.kr (J.-Y. Seo),

choikfri@korea.kr (Y.-S. Choi), lovewood@korea.ac.kr (G.-H. Kim).

Please cite this article in press as: Kim, M.-J., et al. Bioleaching of spent Zn–Mn or Ni–Cd batteries by Aspergillus species. Waste Management (2015)dx.doi.org/10.1016/j.wasman.2015.11.001

Min-Ji Kim a, Ja-Yeon Seo b, Yong-Seok Choi c, Gyu-Hyeok Kim b,⇑aBK21 Plus Eco-Leader Education Center, Korea University, Seoul 136-713, Republic of KoreabDivision of Environmental Science & Ecological Engineering, College of Life Sciences & Biotechnology, Korea University, 5-1 Anam-dong, Seongbuk-gu, Seoul 136-701, Republicof KoreacDivision of Wood Engineering, Department of Forest Products, Korea Forest Research Institute, 57, Hoegiro, Dongdaemun-gu, Seoul 130-712, Republic of Korea

a r t i c l e i n f o

Article history:Received 12 August 2015Revised 29 October 2015Accepted 1 November 2015Available online xxxx

Keywords:AspergillusBioleachingHeavy metalNi–Cd batteryZn–Mn battery

a b s t r a c t

This research explores the recovery of metals from spent Zn–Mn or Ni–Cd batteries by a bioleaching usingsix Aspergillus species. Two different nutrients, malt extract and sucrose, were used to produce differenttypes of organic acids. Oxalic acid and citric acid were shown to be the dominant organic acid in maltextract and sucrose media, respectively. In the bioleaching, the metal removal was higher in sucrosemedia than malt extract. All species, except A. niger KUC5254, showed more than 90% removal of metalsfrom Zn–Mn battery. For Ni–Cd battery, more than 95% of metals was extracted by A. niger KUC5254 andA. tubingensis KUC5037. As a result, A. tubingensis KUC5037 which is a non-ochratoxigenic fungus wasconsidered to have the greatest potential for improving the safety and efficiency of the bioleaching.

� 2015 Elsevier Ltd. All rights reserved.

1. Introduction

The production and consumption of batteries has increased inrecent years due to huge demands from both industrial activitiesand consumer usage (De souza et al., 2001; Patricio et al., 2015).There are two types of batteries, non-rechargeable primary batter-ies and rechargeable secondary batteries. Primary batteries, whichproduce an electric current by means of an irreversible chemicalreaction, are composed of Zn–Mn blends, C–Zn blends, primary-lithium or mercury batteries. Among these, the Zn–Mn battery,developed after the C–Zn battery, is the most frequently usedand accounts for nearly 80% of the spent batteries generated inKorea (Shin et al., 2007). Rechargeable batteries such as Ni–Cd,Ni–metal hybrid (Ni–MH) and lithium-ion batteries are used inmany industrial applications, especially in portable electronicproducts. For example, Ni–Cd batteries are most frequently usedin wireless communication and wireless computing devices. Allof these batteries are a rich repository of valuable metals includingZn, Mn, Ni, Cd, Co, and Al (Vassura et el., 2009). However, disposalof spent batteries generates serious environmental problems, espe-cially due to the presence of hazardous heavy metals and a lack oflicensed landfills for their disposal (Sayilgan et al., 2009). For these

reasons, development of an effective recycling program is criticallyimportant.

Pyrometallurgy and hydrometallurgy are conventional tech-niques used by many industries to extract metals from solid waste.The pyrometallurgical process is fast and efficient, but producespolluting emissions and involves high operation costs. Thehydrometallurgical process consumes less energy, but is dangerousdue to its use of large amounts of strong acids. Both of theseconventional methods require extreme conditions such as hightemperature, high pressure, and a dangerous chemical environ-ment. In contrast, biological processes operate under mild condi-tions. The bioleaching can reduce the demand of ores, energy,and landfill space and it costs only one-third to one-half of conven-tional methods (Krebs et al., 1997; Lee and Pandey, 2012). Thus,bioleaching is considered a promising technology for the extractionof metals from spent batteries (Willner et al., 2015).

In the bioleaching, heterotrophic bacteria and autotrophic fungihave been used to solubilize various metals. By using the metabolicproducts and biomass of certain microorganisms, leaching is flexi-ble, selective, and environmentally friendly (Lundgren et al., 1986).Several studies have been reported on bioleaching of spent batter-ies using microorganisms, but most of these are restricted to use afew well-known bacteria (Velgosova et al., 2013; Xin et al., 2012).Because constant supply of nutrients for fungal growth, handling offungi in turnover and long processing time were magnified.However, fungal bioleaching has several advantages over bacterialbioleaching. Burgstaller and Schinner (1993) stated that fungi have

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the ability to grow at high pH, which makes them more effectivefor bioleaching of alkaline materials. They can also leach metalsrapidly with a short lag phase and excrete organic acids that causea chelating reaction with metal ions. Despite such advantages,there is still insufficient information regarding metal removal fromspent batteries using fungi. Therefore, species from the genusAspergillus, known for its ability to secrete large amounts of organicacids, was selected for use in this study. Organic acids are able tochelate metal ions that facilitate the dissolution of metals. In thispaper, organic acids produced by six Aspergillus species under dif-ferent nutrient sources and the bioleaching efficiency of spent Zn–Mn or Ni–Cd batteries using fungal produced organic acids wereinvestigated to evaluate the bioleaching capability of Aspergillus.

2. Materials and methods

2.1. Fungal isolates and organic acid production

A total of six isolates of Aspergillus species, A. fumigatusKUC1520, A. flavipes KUC5033, A. japonicus KUC5035, A. tubingensisKUC5037, A. versicolor KUC5201, and A. niger KUC5254, wereobtained from the Korea University Culture collection (KUC).Investigation of organic acid production by each of these sixAspergillus species was performed in 250 mL Erlenmeyer flaskscontaining 100 mL of sterilized culture medium. Malt extract(ME) and sucrose media were used as the two different nutrientsources. The ME medium was composed of 20 g/L malt extract.The sucrose medium was composed of 100 g/L sucrose, 1.5 g/LNaNO3, 0.5 g/L KH2PO4, 0.025 g/L MgSO4�7H2O, 0.025 g/L KCl and1.6 g/L yeast extract. Spores of the six different Aspergillus specieswere collected from 10-day-old cultures using a surfactant(0.02% Tween� 80). One milliliter of each spore suspension(107 spores/mL) was inoculated into each flask containing a culturemedium and agitated for 14 days at 150 rpm on a rotary shaker at27 �C. After this fermentation period, samples were taken for mea-suring pH and organic acid concentration. From the filtrateobtained after rotary agitation, the metabolites from each of thesix Aspergillus species were measured using high performanceliquid chromatography (HPLC) (Waters, USA) equipped with aRepro-Gel H+ column (DR. A. Maisch, Germany) and a photodiodearray detector at 210 nm. Each culture filtrate was analyzed byinjecting a 10-lL sample into the column. The column’s mobilephase was composed of 9 mM sulfuric acid passed at a flow rateof 1 mL/min at ambient temperature. An external standard methodwas used to quantify the amount of organic acid in the samples.

2.2. Bioleaching of metals from spent batteries

2.2.1. Preparation of spent batteriesThe spent Zn–Mn and Ni–Cd batteries were supplied by the

Korea Battery Recycling Association (Ansung, Korea). The batterieswere manually dismantled. All dismantled materials were col-lected and safely discarded except for the electrode powder mate-rials. The powder was mixed, dried, ground by milling, and sievedto obtain a mesh size of less than 200 lm (Mishra et al., 2008). Todetermine the metal content, the powder was dissolved using theUSEPA method 3050B (USEPA, 1986). Analysis was done using aninductively coupled plasma-optical emission spectrometer(ICP-OES) (Agilent, USA). The total metal content of Zn–Mn andNi–Cd batteries is shown in Table 1.

2.2.2. BioleachingBioleaching of metals from spent batteries was performed using

a modified method described by Kartal et al. (2004). In this study,sterilized 0.1% w/v spent battery powder was placed in a 250 mL

Please cite this article in press as: Kim, M.-J., et al. Bioleaching of spent Zn–Mn odx.doi.org/10.1016/j.wasman.2015.11.001

flask containing 100 mL of fermentation broth obtained by pre-culturing each strain for 14 days in ME and sucrose media asdescribed in Section 2.1. Fungal mycelia were removed from thefermentation broth prior to placing the powder into the culturesolution. The flasks were incubated at 27 �C for 8 days with rotaryshaking (150 rpm). Samples were then harvested every 2 days formeasuring pH and percent of metal. ME and sucrose media withoutfungal inoculation were served as controls.

2.2.3. Metal elements analysisEach supernatant sample collected at each reaction time was

filtered and diluted using 2% nitric acid. From Zn–Mn batteries,residual Zn and Mn ions were analyzed using ICP-OES. Analysisof residual Ni, Cd, Co and Zn ions for Ni–Cd batteries was also per-formed. Based on results, the percent metal removed was calcu-lated using Eq. (1);

Percentage of metal removal ¼ Cs=Cb � 100 ð1Þwhere Cb (mg/L) is the initial metal concentration of the batteries,and Cs (mg/L) is the metal concentration leached from the batteryin fermentation broth.

3. Results and discussion

3.1. Organic acid production by Aspergillus species

Organic acids secreted by six Aspergillus species grown on twodifferent culture mediums were examined. Tables 2 and 3 illustratethe amount of oxalic acid and citric acid produced in ME andsucrose media as a function of pH, respectively. It was noted thatA. fumigatus KUC1520 and A. flavipes KUC5033 did not produceboth oxalic acid and citric acid. As predicted, the nutrient typehad a large influence on dissolution biochemistry organic acid pro-duction. Oxalic acid and citric acid were the dominant organic acidpresent in ME and sucrose media, respectively.

Table 2 illustrates the amount of oxalic acid and citric acidproduced in the ME medium. In this case, oxalic acid was the dom-inant organic acid by most Aspergillus species. A. versicolorKUC5201 produced the highest amounts of oxalic acid (85.9 mM)with the largest decrease in pH (from 5.05 to 1.34). Followingthe A. versicolor KUC5201, the concentration of oxalic acid wererepresented in the order of A. tubingensis KUC5037 (53.4 mM) > A.japonicus KUC5035 (10.3 mM) > A. niger KUC5254 (4.4 mM). A.fumigatus KUC1520 and A. flavipes KUC5033 secreted only a smallamount of organic acid as indicated by a slight decrease in pH,however, neither oxalic acid nor citric acid were detected after fer-mentation. Citric acid was produced by only three species, A. tubin-gensis KUC5037, A. versicolor KUC5201 and A. niger KUC5254, andthe amount of citric acid produced was low (less than 8.3 mM).

The amount of organic acid produced in the sucrose medium isshown in Table 3. Citric acid was the major organic acid producedin sucrose media whereas oxalic acid was dominant in ME media.A. versicolor KUC5201, however, showed the greatest organic acidproduction ability and had the lowest pH (2.08) in both sucroseand ME media. Of the six species, A. versicolor KUC5201, A. nigerKUC5254 and A. tubingensis KUC5037 secreted the highest amountof citric acid (136.3, 118.8 and 96.3 mM, respectively). The produc-tion of citric acid by A. fumigatus KUC1250 and A. flavipes KUC5033was not detectable and the pH of their culture media actuallyincreased. Slightly lower amounts of oxalic acid (less than17.3 mM) were produced by A. tubingensis KUC5037, A. versicolorKUC5201 and A. niger KUC5254.

According to previous studies on bioleaching by fungal gener-ated organic acids, oxalic acid and citric acid are expected to beeffective leaching agents for recovery of metals from spent

r Ni–Cd batteries by Aspergillus species. Waste Management (2015), http://

Table 1Metal concentrations of spent Zn–Mn and Ni–Cd batteries.

Battery type Metal concentration (mg/g)

Al Cd Co Cu Fe Li Mn Ni Pb Zn

Zn–Mn battery 0.042 0.679 0.065 0.041 4.948 0.004 511.775 0.222 2.548 13.128Ni–Cd battery 0.491 230.520 68.944 0.077 0.361 1.038 0.270 697.925 0.174 26.608

Table 2Amount of organic acid produced by Aspergillus in ME media.

Fungal species IsolateNo.

pH Organic acid production(mM)a

Oxalic acid Citric acid

Uninoculatedmedium

– 5.05 – – – –

A. fumigatus KUC1520 3.37 ± 0.44 NDb Ec ND CA. flavipes KUC5033 4.57 ± 0.01 ND E ND CA. japonicus KUC5035 2.38 ± 0.07 10.3 ± 0.4 C ND CA. tubingensis KUC5037 1.50 ± 0.04 53.4 ± 1.1 B 1.4 ± 0.1 BA. versicolor KUC5201 1.34 ± 0.03 85.9 ± 5.4 A 8.3 ± 1.0 AA. niger KUC5254 2.54 ± 0.11 4.4 ± 0.8 D 1.0 ± 0.2 B

a Values represent the average of three replicates with standard deviationsincluded.

b Not detected.c Means with the same letter in each column are not significantly different

(a = 0.05) according to the Duncan’s method.

M.-J. Kim et al. /Waste Management xxx (2015) xxx–xxx 3

materials (Deng et al., 2013; Hassan et al., 2013). The amount ofoxalic acid and citric acid produced was different between MEand sucrose media. This result implied that the metabolic pathwayof genus Aspergillus can change depending on the nutrients avail-able. Biosynthesis of oxalic acid from glucose occurs when oxaloac-etate is hydrolyzed to oxalate and acetate catalyzed by cytosolicoxaloacetase, whereas citric acid is produced as an intermediatein the tricarboxylic acid cycle involving a polysaccharide such assucrose (Gadd, 1999). Thus, it is clear that the choice of the nutri-ent source will impact the results.

3.2. Bioleaching of metals from spent battery materials

3.2.1. Zn–Mn batteryThe amount of metal removed from a spent Zn–Mn battery via

bioleaching using both ME and sucrose media was analyzed over8 days. After six days, the highest concentration of soluble Znwas obtained from A. niger KUC5254 in the ME medium (96% Znremoval), which had the lowest oxalic acid content (4.4 mM).The next highest was A. japonicus KUC5035, then A. versicolorKUC5201 and A. Tubingensis KUC5037 (Fig. 1). These data indicate

Table 3Amount of organic acid produced in sucrose medium by Aspergillus.

Fungal species IsolateNo.

pH Organic acid production (mM)a

Oxalic acid Citric acid

Uninoculatedmedium

– 5.60 – – – –

A. fumigatus KUC1520 7.47 ± 0.05 NDb Cc ND DA. flavipes KUC5033 7.59 ± 0.05 ND C ND DA. japonicus KUC5035 4.31 ± 0.13 ND C 9.6 ± 0.7 DA. tubingensis KUC5037 2.31 ± 0.44 1.7 ± 0.2 B 96.3 ± 9.8 CA. versicolor KUC5201 2.08 ± 0.10 17.3 ± 1.2 A 136.3 ± 3.0 AA. niger KUC5254 2.47 ± 0.06 0.8 ± 0.2 BC 118.8 ± 8.2 B

a Values represent the average of three replicates with standard deviationsincluded.

b Not detected.c Means with the same letter in each column are not significantly different

(a = 0.05) according to the Duncan’s method.

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that Zn was efficiently extracted when low amounts of oxalic acidwere produced by an Aspergillus species. This result was consistentwith previous studies (Sayer and Gadd, 1997; Sayilgan et al., 2010)that reported Zn formed an insoluble oxalate in the presence ofoxalic acid via an intermediate solubilization process. The percentof manganese removed from spent Zn–Mn battery materials in MEmedia was more than 90% after 6 days by all species without anymetal precipitation.

In sucrose media, a larger amount of both Zn and Mn wereextracted than in ME media. This means that citric acid, whichwas the dominant organic acid in sucrose media, played a key rolein Zn recovery. The amount of Zn extracted after 8 days byAspergillus species was in the order of A. tubingensis KUC5037(100%) > A. versicolor KUC5201 (90%) > japonicus KUC5035 (85%)(Fig. 2). In addition, more than 92% of Mn was removed by thesethree Aspergillus species after 8 days. It is interesting to note thatA. japonicus KUC5035, which produced a noticeably low amountof citric acid (9.6 mM), showed a similar percentage of Zn andMn removal while the other species produced more than96.3 mM of citric acid. Only small amounts of citric acid, therefore,were needed to recover metals from spent Zn–Mn batteries, whichcould have economic implications.

3.2.2. Ni–Cd batteryThe percentage of metal removal from spent Ni–Cd batteries

using ME and sucrose media is represented in Figs. 3 and 4.Ni–Cd batteries contain Ni, Cd, Co and Zn. In ME media, thebioleaching efficiency for all metals appeared to be very low forall Aspergillus species. Although A. niger KUC5254 was the best atmetal removal, it only extracted 32, 33, 13 and 1% of Ni, Cd, Coand Zn, respectively. Similar results were obtained for Zn–Mn bat-teries. It seemed that larger quantities of oxalic acid inhibited thedissolution of metals due to a precipitation reaction between Ni,Cd, Co, Zn, and oxalic acid (Biswas et al. 2013). Consequently, A.niger KUC5254, which showed the lowest oxalic acid production(4.4 mM), produced the highest percentage of metal removal.

Extracted amounts of Ni, Cd, Co and Zn were definitely higher insucrose media than in ME media. It is interesting to note that A.versicolor KUC5201 showed the lowest metal removal rate despitehaving the highest production of organic acid (136 mM of citricacid and 17 mM of oxalic acid). As suggested in the previous para-graph, the most plausible explanation is that higher amounts ofoxalic acid acts as an inhibitor for the reaction between citric acidand metals by forming a metal-oxalate precipitate (Biswas et al.2013). In the case of A. niger KUC5254 and A. tubingensisKUC5037, more than 90% of Ni, Cd, and Zn was removed after4 days, and the maximum amount of Co was extracted after just2 days. Although A. japonicus KUC5035 produced much loweramounts of citric acid (9.6 mM), about 80% of Ni, Cd, and Zn, and90% of Co were extracted by this species after 8 days. As a result,citric acid, which is produced in large quantities in sucrose media,was the best leaching agent in this study. Hence, the Aspergillusspecies, which generates citric acid, might be an alternative tocommercial leaching agents (Nogueira and Delmas, 1999; Reddyet al., 2005).

Among the four metals present in Ni–Cd batteries, Cd is awell-known toxic heavy metal that is harmful to humans and the

r Ni–Cd batteries by Aspergillus species. Waste Management (2015), http://

Fig. 1. Metal leaching efficiency of Aspergillus cultured in malt extract from spent Zn–Mn batteries: (a) Zn and (b) Mn.

Fig. 2. Metal leaching efficiency of Aspergillus cultured in sucrose from spent Zn–Mn batteries: (a) Zn and (b) Mn.

4 M.-J. Kim et al. /Waste Management xxx (2015) xxx–xxx

Please cite this article in press as: Kim, M.-J., et al. Bioleaching of spent Zn–Mn or Ni–Cd batteries by Aspergillus species. Waste Management (2015), http://dx.doi.org/10.1016/j.wasman.2015.11.001

Fig. 3. Metal leaching efficiency of Aspergillus cultured in malt extract from spent Ni–Cd batteries: (a) Ni, (b) Cd, (c) Co, and (d) Zn.

Fig. 4. Metal leaching efficiency of Aspergillus cultured in sucrose from spent Ni–Cd batteries: (a) Ni, (b) Cd, (c) Co, and (d) Zn.

M.-J. Kim et al. /Waste Management xxx (2015) xxx–xxx 5

environment. Ni and Co, however, are classified as valuable metalsbecause reserves are decreasing and trading prices are increasing.Therefore, metal recovery from spent Ni–Cd batteries is veryimportant for environmental and economic reasons. To reuse met-als extracted by leaching, it is necessary to recover metals ionizedin the extraction solution. There have been numerous attempts toextract metals from various spent materials (Deng et al., 2013;Hassan et al., 2013), though studies on selective metal recoveryare still limited. In view of these facts, Machado et al. (2011) con-ducted research on selective recovery of metals using a combinedelectrochemical and chemical process. With this process, Cr (95%),Cu (98%), Ni (88%) and Zn (83%) were successfully recovered.

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Considering the potential for reusability of resources and environ-mental impact issues, more research is needed for development ofthese concepts.

3.3. Selection of useful fungal species

In the present study, we confirmed that citric acid, produced insucrose media, is a suitable extracting agent for bioleaching ofZn–Mn or Ni–Cd batteries. Using fungal generated citric acid, A.tubingensis KUC 5037 demonstrated the highest bioleaching effi-ciency for Zn–Mn batteries. A. niger KUC5254 and A. tubingensisKUC5037 showed the highest percentage of metal removal from

r Ni–Cd batteries by Aspergillus species. Waste Management (2015), http://

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Ni–Cd batteries. Among the Aspergillus species, section Nigri,including A. niger, A. tubingensis, and A. japonicus, are consideredindustrially important fungal taxa for producing useful metabolitesbut, unfortunately, also mycotoxins. Mycotoxins can limit the prac-tical use of these fungi for toxicology reasons (Varga et al., 2003).All Aspergillus species used in this study are also known to secreteseveral toxic metabolites. One of the renowned mycotoxin,Ochratoxin A, is known to have nephrotoxic, nephrocarcinogenic,teratogenic and immunosuppressive effects (Serra et al., 2003).Some results have been recently published showing that theAspergillus species produces ochratoxins. Storari et al. (2012), how-ever, re-examined these claims and found that A. tubingensis didnot produce ochratoxin A when grown on synthetic media. In thisrespect, finding from this study revealed that a non-ochratoxigenicspecies, A. tubingensis KUC5037, can remove similar quantities ofmetal as A. niger KUC5254. Thus, the discovery of the outstandingability of A. tubingensis is of great significance for future work.

4. Conclusions

Oxalic acid and citric acid were found to be the dominantorganic acids produced by 4 Aspergillus species via ME and sucrosemedia, respectively. Because the fungal metabolic pathway wasinfluenced by the type of media used, choosing the proper nutrientsource is an essential consideration for metal recovery viabioleaching. The citric acid is a more suitable agent for metalextraction from both spent Zn–Mn or Ni–Cd batteries since oxalicacid tends to form insoluble metal oxalates. Finally, A. tunbingensisKUC5037 might be a useful fungus for bioleaching industrybecause of its non-ochratoxigenic characteristics and great metalextraction. To improve the efficiency of metallurgical process usingfungi, operation technologies such as immobilization and biofilmand optimal treatment conditions should be developed. It wouldovercome the limitations that most people think in fungalbioleaching.

Acknowledgement

This research was supported by a Korea University Grant(K1421041).

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