ArticlePDF AvailableLiterature Review

Biotechnological strategies for the recovery of valuable and critical raw materials from waste electrical and electronic equipment (WEEE) – A review

Abstract and Figures

Critical raw materials (CRMs) are essential in the development of novel high-tech applications. They are essential in sustainable materials and green technologies, including renewable energy, emissionfree electric vehicles and energy-efficient lighting. However, the sustainable supply of CRMs is a major concern. Recycling end-of-life devices is an integral element of the CRMs supply policy of many countries. Waste electrical and electronic equipment (WEEE) is an important secondary source of CRMs. Currently, pyrometallurgical processes are used to recycle metals from WEEE. These processes are deemed imperfect, energy-intensive and non-selective towards CRMs. Biotechnologies are a promising alternative to the current industrial best available technologies (BAT). In this review, we present the current frontiers in CRMs recovery from WEEE using biotechnology, the biochemical fundamentals of these bio-based technologies and discuss recent research and development (R&D) activities. These technologies encompass biologically induced leaching (bioleaching) from various matrices,biomass-induced sorption (biosorption), and bioelectrochemical systems (BES).
Content may be subject to copyright.
Contents lists available at ScienceDirect
Journal of Hazardous Materials
journal homepage:
Biotechnological strategies for the recovery of valuable and critical raw
materials from waste electrical and electronic equipment (WEEE) A review
Arda Işıldar
, Eric D. van Hullebusch
, Markus Lenz
, Gijs Du Laing
, Alessandra Marra
Alessandra Cesaro
, Sandeep Panda
, Ata Akcil
, Mehmet Ali Kucuker
, Kerstin Kuchta
IHE Delft Institute for Water Education, Delft, The Netherlands
Université Paris-Est, Laboratoire Geomatériaux et Environnement (LGE), EA 4508, UPEM, 77454 Marne-la-Vallée, France
Institut de Physique du Globe de Paris, Sorbonne Paris Cité, Universitè Paris Diderot, UMR 7154, CNRS, F-75005 Paris, France
Fachhochschule Nordwestschweiz, University of Applied Sciences and Arts Northwestern Switzerland, Brugg, Switzerland
Sub-Department of Environmental Technology, Wageningen University, 6700 AA Wageningen, The Netherlands
Department of Applied Analytical and Physical Chemistry, Ghent University, Belgium
Sanitary Environmental Engineering Division (SEED), Department of Civil Engineering, University of Salerno, Italy
Mineral-Metal Recovery and Recycling Research Group, Mineral Processing Division, Department of Mining Engineering, Suleyman Demirel University, TR32260 Isparta,
Hamburg University of Technology (TUHH), Institute of Environmental Technology and Energy Economics, Waste Resources Management, Harburger Schloßstr. 36,
21079 Hamburg, Germany
Critical metals
Electronic waste
Critical raw materials (CRMs) are essential in the development of novel high-tech applications. They are es-
sential in sustainable materials and green technologies, including renewable energy, emissionfree electric ve-
hicles and energy-ecient lighting. However, the sustainable supply of CRMs is a major concern. Recycling end-
of-life devices is an integral element of the CRMs supply policy of many countries. Waste electrical and electronic
equipment (WEEE) is an important secondary source of CRMs. Currently, pyrometallurgical processes are used to
recycle metals from WEEE. These processes are deemed imperfect, energy-intensive and non-selective towards
CRMs. Biotechnologies are a promising alternative to the current industrial best available technologies (BAT). In
this review, we present the current frontiers in CRMs recovery from WEEE using biotechnology, the biochemical
fundamentals of these bio-based technologies and discuss recent research and development (R&D) activities.
These technologies encompass biologically induced leaching (bioleaching) from various matrices,biomass-in-
duced sorption (biosorption), and bioelectrochemical systems (BES).
1. Introduction
Electronic waste, E-waste or waste electrical and electronic equip-
ment (WEEE) refers to discarded devices that are at the end of their
economic use and cannot be utilized by consumers anymore. The pro-
duct spectrum of electrical and electronic equipment (EEE) expanded
rapidly, coupled to an increase in consumer demand for electronics and
aordability. This resulted in an unprecedented global WEEE genera-
tion. WEEE constitutes the largest and fastest growing fraction of mu-
nicipal waste [1], and reached a global total of 41.8 million tons per
annum in 2014 [2]. The EU-28 plus Norway, Iceland, Liechtenstein,
Switzerland, and Turkey are the largest WEEE generators with a total of
9.8 M tons and 20.4 kg/person/year in average, along with the United
States (7.1 M tons and 22.3 kg/person) and China (6 M tons, 4.4 kg/
person) [2,3]. WEEE generation is directly correlated with gross do-
mestic product (GDP) [4], and the per capita generation increased
particularly in the developing countries [5].
Improper management of WEEE is an alarming global environ-
mental problem due to the presence of a large variety of toxic sub-
stances embedded in the devices [6]. Despite preventive legislation,
most WEEE is still poorly managed, either landlled, or transferred to
developing countries either through legal or unregistered routes [7]. In
Europe approximately 35% of WEEE is recycled, and the rest is land-
lled, exported or lost [4,8]. According to the current EU directive
regarding WEEE [203], approximately 45% of WEEE should be col-
lected in 2016, and the minimum collection rate annually shall be 65%
in 2019 (European Commission, 2012). Nevertheless, collection rate in
EU-28 countries are higher than those of other high GDP countries.
Received 17 January 2018; Received in revised form 14 August 2018; Accepted 16 August 2018
Corresponding author at: IHE Delft Institute for Water Education, Delft, The Netherlands.
E-mail address: (A. Işıldar).
Journal of Hazardous Materials 362 (2019) 467–481
Available online 17 August 2018
0304-3894/ © 2018 The Authors. Published by Elsevier B.V. This is an open access article under the CC BY-NC-ND license
Whereas transboundary movement of WEEE from developed to devel-
oping countries had become the norm in 2000s, the situation is now
changing due to an increasing public interest under the umbrella of the
Basel Convention and the regional precautionary measures taken by the
WEEE is an important secondary source of valuable and critical
metals. Perpetual innovation of consumer EEE resulted in highly vari-
able material properties and shape of the products, with an increasing
complexity [9]. Thus, the elemental composition of the discarded de-
vices is also highly variable and complex [10]. A modern smartphone
includes up to 58 elements at various concentrations and chemical
composition [11]. Thus, novel recycling strategies should consider se-
lectivity for metal recovery from these complex materials. The proper
implementation of novel resource recovery-oriented recycling strate-
gies may contribute to controlling the environmental risks associated
with improperly managed WEEE. In the recent years, considerable re-
search eorts have been carried out to develop environmentally
friendly biotechnological processes. Selectivity towards individual
metals, cost-eectiveness and eco-innovation are the potential ad-
vantages of biotechnological processes [12]. They are foreseen to play a
considerate role in sustainable development, particularly for the me-
tallurgical, chemical and waste processing sectors [13].
Currently, high-grade WEEE is treated in high temperature pyr-
ometallurgical facilities, to recover the valuable metallic fraction of the
end-of-life devices (Ebin and Isik [196]). Several investigations on hy-
drometallurgical metal recovery from WEEE have also proven suc-
cessful and nancially feasible at various technology readiness levels
[14,15]. Biotechnologies may oer promising alternatives to pyr-
ometallurgical technology in metal recovery from post-consumer waste.
Biohydrometallurgy is already an established route to process primary
ores of many metals [16,17] and may play an important role in the
urban mining of critical raw materials in the future. Selectivity towards
critical and valuable metals may be a major advantage of biotechnol-
ogies over conventional chemical recovery methods [18]. Further, they
may oer advantages in cost-eectiveness and lower environmental
impact [19]. This review presents the latest developments in global
WEEE generation and critical metals contained therein and focusses on
the use of biotechnologies to recover both critical and conventional
metals from these waste streams. Specically, this review focusses on
recent developments in bioprocessing by such diverse biotechnological
strategies as autotrophic and heterotrophic bioleaching, biosorption,
bioprecipitation and bioelectrochemical recovery.
2. Global WEEE management
2.1. WEEE classication, hazards, and global generation
WEEE encompasses a wide range of discarded devices, and is clas-
sied per product type and legislative relevancy. WEEE is grouped into
10 primary categories according to the WEEE Directive by the European
Commission (2012/19/EU), i.e. (i) large household appliances, (ii)
small household appliances, (iii) information technology and commu-
nication (ITC) equipment, (iv) consumer electronics, (v) lighting, (vi)
electrical and electronic tools, (vii) toys, (viii) leisure and sports
equipment, (ix) medical devices, and (x) automatic dispensers. These
collection categories also exist in actual WEEE collection and man-
agement practice [20]. These ten major product categories are further
grouped into 58 sub-categories, representing approximately 920 pro-
Due to the nature of minerals, energy and chemicals used for pro-
duction, the energy usage during use, and materials landlled at the
end of life, WEEE is a rapidly growing global environmental problem. A
considerate share of WEEE generated is landlled or shipped to de-
veloping countries where it possesses a signicant hazard to the en-
vironment and local communities [21]. The hazards are associated with
the presence of heavy metals, brominated ame retardants (BFRs),
polybrominated diphenyl ethers (PBDEs), dioxins and other potentially
harmful substances either contained in or formed during waste pro-
cessing [10]. In addition, about 50% of personal computer components
contain hazardous arsenic (As), hexavalent chromium (Cr(VI)) and
mercury (Hg) [3].
The quantication of WEEE volumes is a prerequisite for the de-
velopment of sustainable solutions. Challenges include the lack of re-
liable data, sensitivity-related issues, the dynamic nature of the ows
and their constituents (Schluep et al. [187]). This task is particularly
unwieldy in developing countries as informal waste management sys-
tems are poorly documented and data quality is an issue [22,23]. In
addition, lack of quantitative understanding of the amounts involved in
transboundary WEEE movement is prevalent [24]. An overview of the
total WEEE generation in 2013 and its forecast for 2020 is shown in
Fig. 1 [19,2426]. Generation of WEEE has exponentially increased due
to rapid technological innovations in the electronics sector, coupled
with demand growth for electronics in developing countries. In addi-
tion, decreasing economic lifespan of electronic devices [27,28] lack of
international legislative consensus on WEEE management [29] and
aordability played a major role in increasing the generation of WEEE.
Lifespan of the electronic decreased to an average of 10 to 2 years and
24 to 9 months for large EEE and mobile phones, respectively
[27,3032]. These issues, coupled with ever-increasing spectrum of
devices make WEEE the fastest growing post-consumer waste stream. In
2014, 41.8 million tons of WEEE was generated, and the value is ex-
pected to increase to over 50 million tons in 2018 [2]. WEEE occupies
an increasing fraction of municipal waste, up to 8% of total municipal
waste in developed economies, with saturated EEE markets [33]. Re-
portedly, a substantial increase in WEEE generation is also expected in
developing countries, as a result of the forecasted economic growth
[34]. Consequently, regions with large populations and rapid economic
growth are expected to become large WEEE producers in the coming
Discarded devices are particularly concentrated in urban areas
where population density is very high [35]. This leads to an emerging
eld of research termed as urban mining, in which many waste mate-
rials are re-used as a secondary source of materials [36]. Analogous to
primary ores, urban mines are distinct with regard to their metal
composition and content [32]. Usually, in WEEE derived from urban
minesmetals are found in complex alloys and in their metallic ele-
mental form [37]. This requires a novel approach to sustainably and
selectively recover metals from WEEE. Conventional mechanical, pyr-
ometallurgical, hydrometallurgical and bio-hydrometallurgical
Fig. 1. Annual electronic waste generation in 2013 and future prediction in
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
processes, and often a combination of these are proposed for metal
recovery from WEEE [3840]. Biotechnologies might nd a niche in
this area with their lower waste production, emissions, and carbon
2.2. Critical metal content of WEEE
Primary sources of critical metals, such as rare earth elements (REE)
and platinum group metals (PGM), are neither ubiquitously available
nor equally distributed in the world. For instance, China produces 87%,
95%, and 95% of Sb, heavy REE (HREE) and light REE (LREE), re-
spectively. Brazil supplies 90% of niobium (Nb), and the USA 90% of
beryllium (Be) [41]. Chinese export restrictions on REE in 2009 trig-
gered a raw materials supply issue, and gave momentum to several
national and international initiatives (European Commission [204];
[42]; USNRC [205]). The drivers of resource scarcity are associated
with (1) the demand of a growing world population striving for a high
standard of living, and (2) geopolitical scenarios such as, export re-
strictions and/or political instability of major producing and reserve-
hosting nations, rather than exhaustion of the primary ores. The Eur-
opean Commission (EC) ranked the raw materials in terms of their
criticality according to the risks of supply shortage and their economic
importance for the rst time in 2011 and updates this list regularly
[41]. The list currently includes 27 CRM and a number of them are
essential for the EEE, in particular emerging green technologies. EEE
contain many critical metals including the light and the heavy rare
earth elements (LREE, HREE), cobalt (Co), antimony (Sb), tungsten
(W), gallium (Ga), germanium (Ge), indium (In), tantalum (Ta), and
platinum group metals (PGM), and near-critical elements such as tin
(Sn), chromium (Cr), lithium (Li), and silver (Ag). They are essential
components of EEE and have an increasing importance in the transition
to a green, low-carbon economy. Examples of critical elements and
their abundance in respective WEEE units is given in Table 1.
Critical materials (such as Co, HREE, In, Li, LREE, Ni, PGM, and Sb)
are essential to the functionality of EEE and can often not be replaced.
In turn, printed circuit boards, permanent magnets, lithium-ion, nickel
metal hybrid (NiMH) and nickel cadmium (NiCd) batteries, lamp
phosphors, liquid crystal displays (LCDs), light emitting diodes (LED),
and hard disc drives (HDD) are thus important secondary sources of
critical metals (Binnemans et al. [188]; Ueberschaar and Rotter
[175],18]). The risk for insucient supply and scarcity of raw materials
is now perceived by many leading companies from dierent manu-
facturing industries, particularly, renewable energy, electric vehicles,
and consumer electronics. This underlines the importance of developing
novel (bio)technologies for recovery of critical raw materials from
WEEE, which has been identied as a strategic research direction in the
3. Bioprocessing of WEEE for metal recovery
Biotechnology is an established route for extraction of Au, Ag, As,
Co, Cu, Mn, Mo, Ni, U, V, and W, Zn from primary ores (Morin et al.,
2006, [17]). Around 15% of copper (Cu) and 5% of gold (Au), and
lower amounts of nickel (Ni) and zinc (Zn), are produced using mi-
croorganisms (Johnson [206][12]). Bioleaching was proven to be an
applicable technology for processing of primary, in particular the low
grade ores. There is an increasing academic and commercial interest in
bioprocessing of waste for metal recovery, which can be attributed to its
(1) potentially better environmental prole, (2) ease and practicality of
operation, (3) better cost-eectiveness, and (4) potential for future
development. Moreover bio-based technologies could be more selective
towards metals, which gives them an additional advantage. The bio-
chemical mechanisms involved in biomining of primary minerals are
well understood and explained in detail e.g. by Mahmoud et al. [12].
Brierley and Brierley [45] and Rohwerder et al. [46]. Waste materials,
i.e. post-consumer anthropogenic discarded materials, on the other
hand, show dissimilarities to primary ores, as most metals are found in
their zero valence elemental state in WEEE, often alloyed with other
metals [11,32].
3.1. Bioleaching of critical metals from WEEE
Bioleaching of metals is carried out by a largely diverse group of
microorganisms, mainly including three groups of microorganisms,
namely (i) chemolithotrophic prokaryotes, (ii) heterotrophic bacteria
and (iii) fungi [47]. In nature, a large variety of chemolithotrophic and
organotrophic microorganisms are involved in bioleaching of ores [48]
(Panda et al. [189]). Current state-of-the-art research on metal recovery
from WEEE via biotechnology involves both autotrophic (i.e. sulfur-and
iron-oxidizers) [49,50] and heterotrophic (e.g. cyanide-producing
telluric microorganisms) [51,52]. The fundamentally dierent chem-
istry of metals contained in primary (suldic) ores in contrast to WEEE
implies that dierent leaching mechanisms underlie. Fig. 2 gives an
overview of conventional autotrophic bioleaching of primary ores and
heterotrophic and autotrophic bioleaching of secondary raw materials.
3.1.1. Chemolithotrophic autotrophic bioleaching
Chemolithotrophic organisms utilize atmospheric carbon dioxide
) as carbon source, and inorganic compounds such as ferrous iron
), elemental sulfur (S°) and/or reduced sulfur compounds as en-
ergy source [53,54]. In biomining, they are the most widely studied
group of microorganisms, and the subject of a considerable amount of
fundamental and applied research [5557]. Most chemolithoautotrophs
have a high tolerance for heavy metals toxicity [58], which makes them
the most widely used group of microorganisms to process also other
Table 1
Examples of critical metal content of WEEE components.
WEEE component Metals
(%, w/w) Concentration (ppm) Number. of critical and valuable metals References
Main boards
Printed circuit boards Au,Pd,Ge,Ga 1100 4 Ghosh et al. [39]; Hadi et al. [10]
Fe, Al, Ag, Ni, Zn 100 10,000
Cu > 10,000
Li-Ion batteries Co, Li 1100 2 Lee and Pandey [43], Bigum [213], Kim et al. [44]
NiMH batteries Co,La, Ni 100 - 10,000 2
Memory drives
HDD magnets Nd, Pr, Dy > 10,000 3 [175], Cucchiella et al. [183]
Solid state drives (SDD) Cu, Ag, Au,Pd 1100 4
Liquid crystal displays (LCD) Y,In, Sr 1 100 2 Zhang et al. (2015); Cucchiella et al. [183]
Light emitting diodes (LED) Au, Ag, In,Sn 1100 3
Only metals with concentration over 1 ppm are given.
Critical metals are highlighted in bold letters.
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
polymetallic sources such as WEEE (after addition of reduced Fe/S
minerals, see Fig. 2). Acidithiobacillus ferrooxidans, Acidithiobacillus
thiooxidans and Leptospirillum ferrooxidans are the most extensively
studied mesophilic microorganisms in bioleaching communities [59].
On the other hand, thermophilic processes involve microorganisms
such as Acidianus brierleyi,Sulfobacillus thermosuldooxidans and Me-
tallosphaera sedula [60]. These acidophiles thrive on iron-and sulfur-
containing ores such as pyrite, pentlandite [(Fe,Ni)
] and chalco-
pyrite (CuFeS
) at temperatures between 45 and 75 °C.
3.1.2. Autotrophic bioleaching of secondary sources
Autotrophic bioleaching of secondary sources may be misleading
from the point that autotrophs cannot grow directly on oxidation /
dissolution of the WEEE matrix. However, when mixed to the WEEE
substrate, suldic minerals such a pyrite [61] can provide energy for
autotrophic growth. As in conventionalautotrophic leaching, mi-
crobial oxidation of suldic minerals will then result in production of
acidity and ferric ions, which can in turn solubilize metals from WEEE.
Whereas autotrophic bioleaching of suldic ores will ultimately lead to
a dissolution of (most of) the matrix, the non-metallic fraction of WEEE
will not be dissolved, which is an important dierence for processing
schemes (Fig. 2). The application of biomining for REE recovery from
other secondary sources faces similar challenges due to the particular
matrix in which the REEs are embedded. REEs are typically extracted as
phosphates (monazite and xenotime) or carbonates (bastnäsite) in the
primary ores exploited.
Early studies from between 1980 and 1990 revealed the ability of A.
ferrooxidans and Acetobacter strains in mobilizing REEs from minerals;
however, the mechanism of interaction of microbes with rare earths is
still not well-known [62]. A limited number of studies on REE bio-
leaching is currently available; these are mainly focused on the ex-
traction of rare earths from native minerals [6366]. The only record of
a REE bio-heap leaching project is carried out by DNI Metals in Alberta
Canada. Economically viable quantities of Sc, i.e. 5 g/ton was ex-
plored in polymetallic suldes [18].
Research work on chemolithotrophic autotrophic mesophilic bio-
leaching of metals from WEEE using acids produced by iron- and sulfur-
oxidizers is limited. It focused mainly on recovery of transition metals
[50,67] and also REEs to a smaller extent [68]. Investigations on au-
totrophic bioprocessing of WEEE were carried out using moderate
thermophiles [69], although recent reports have shown the feasibility
of bioprocessing WEEE at ambient temperatures [70,71].
3.1.3. Heterotrophic bioleaching
The development of several biotechnological systems for metal re-
covery from secondary raw materials, such as REE-bearing waste as red
mud, slags, coal ashes and uorescent powders, was recently initiated
([72]; Potysz et al. [190][73,74]). As REE-containing waste does not
contain metal suldes, bioleaching via heterotrophic microorganism
appears as a promising approach [74]. Moreover, heterotrophic mi-
croorganism can tolerate high pH conditions as well as complexed
metals in solution [75].
Bacteria, archaea and fungi are typically involved in heterotrophic
bioleaching of metals [53]. Compared to acidophiles, heterotrophs
tolerate a wider range of pH and are employed for treating moderately
alkaline wastes [76]. Research on heterotrophic bioleaching of critical
metals from WEEE has been focused on cyanide- and organic acid-
generating microorganisms. Cyanogenic bioleaching targets precious
metals and the platinum group metals (PGM), i.e. Au, Ag, Pt, Pd, Rh,
and Ru which are often not leachable by mineral acids. Critical metals,
such as Co, Ga, Ge, Li, Sb, and W, are typically leached from secondary
sources using chelation. Heterotrophic bacteria and fungi contribute to
bioleaching through biosynthesis of organic acids solubilizing metals
(Bosecker [207]; Gadd, 2000). Organic acids; namely acetic acid, lactic
acid, formic acid, oxalic acid, citric acid, succinic acid, and gluconic
acid can mediate complexolysis (Brandl [209]). To the best of our
knowledge, no industrial heterotrophic bioleaching project has been
implemented yet. Due to the need for a high supply of carbon and
energy that are needed for the metabolic activities of the heterotrophic
microorganisms, full-scale application has been implemented yet [18]. Heterotrophic bacterial bioleaching of metals. Several
Pseudomonas strains such as P. aeruginosa,Puorescens, and P. putida,
are involved in bioleaching of valuable metals. They are microbes that
are found ubiquitously, typically in soils, and solubilize metals owing to
various metabolic products. Biogenically produced cyanide is excreted
during growth limitation phase, and provides the cyanide-tolerant
microbe a selective advantage [77]. Cyanide excretion occurs in soils
with top layers rich in organic matter, where a symbiotic relationship
between the plants and the cyanogenic microorganisms occurs [78].
Bioleaching of Cu, Au, Ag, Pt, and Zn by various Pseudomonas species
from primary ores [79,80], metallurgical slags (Cheng et al. [191];
Potysz et al. [190]), and crushed WEEE [81] has been reported.
Complexolysis reactions with cyanide leading to gold solubilization
are not only the basis for bioleaching [71,82], but also for conventional
gold mining (Akcil et al. [192]).
Chi et al. [83] investigated bioleaching of Au with Chromobacterium
violaceum from high-grade cell phone PCB. He reached 10.8%
(0.46 ppm) Au removal in 8 days with an increase in pH. Ruan et al.
[52] identied a new Pseudomonas species from a mining region based
on 16S rDNA analysis. The new species Pseudomonas chlororaphis (PC)
removed 8%, 12%, and 52% of the Au, Ag, and Cu from discarded PCB
at the optimal conditions of pH at 7, room temperature (25 °C), in 72 h,
with the addition of 4.4 g/L glycine as precursor and 2 g/L methionine
as catalyzer.
Cu is predominantly found in discarded PCB, and also other types of
electronic waste. It competes with the other metals, i.e. Au and Ag, for
biorecovery of precious metals, due to preferential complexation and
leaching. Işıldar et al. [71] developed and applied a two-step auto-
trophic/heterotrophic biorecovery strategy to selectively remove Cu
and Au. Cu was bioleached by a mixture of autotrophic iron- and sulfur
oxidizer Acidithiobacillus ferrivorans and Acidithiobacillus thiooxidans in
the rst step with 98.4% removal. In the second step, Au was removed
by Pseudomonas putida with 44.0% removal at ambient temperature
Fig. 2. Conventional autotrophic bioleaching of primary ores and heterotrophic
and autotrophic bioleaching of secondary raw materials.
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
(25 °C). The relatively low gold removal was related to low cyanide
generation of the Pseudomonas cultures and a cyanide concentration of
21.4 mg/L did not allow complete gold removal from the waste mate-
Several strategies were elaborated to increase the biogenic cyanide
production, including sequential nutrient addition [51], medium
modication [84], and genetic modication [85]. Ting and Pham [86]
investigated the adaptation of cyanogenic bacteria to pH values above
9.5 so as to promote the bioleaching ecacy. Chromobacterium viola-
ceum, the most widely studied cyanogenic heterotroph was found to
adapt to pH values up to 9.5 [87]. Adapted cells of the cyanogenic
microorganism bioleached 18%, 22.5% and 19% of Au at pH 9, 9.5 and
10, respectively, while non-adapted bacteria bioleached only 11% at pH
7. Natarajan and Ting [84] further investigated Au bioleaching ecacy
of genetically modied strains, showing highest biogenic cyanide ac-
tivity (bioleaching of 30% of Au).
Heterotrophic bioleaching of REE from waste materials by biogenic
gluconic acid has recently been demonstrated. Three microbial isolates,
two bacterial strains identied as Acinetobacter and Pseudomonas spe-
cies and a fungal one related to Penicillum and Talaromyces, were se-
lected along with the industrially known bacterium of Gluconobacter
oxydans for leaching phosphor powders and spent uid catalytic
cracking catalysts. For phosphor powders, the REE leaching eciency
reached a maximum of 2%, while 49% of total REE was leached out
from the uid catalytic cracking catalyst using cell-free culture super-
natants of G. oxydans [74]. Heterotrophic bacterial leaching of REE
from primary ores and thorium-uranium concentrates (monatize mi-
nerals) was investigated. Pseudomonas aeruginosa exhibited REE
leaching eciencies of up to 63.5% under optimum conditions [88]
while Acetobacter aceti showed low extraction eciency (0.13%) [89],
Marra et al. [90] investigated the recovery of base metals, precious
metals and rare earth elements from WEEE dusts. In the rst step, base
metals were almost completely leached from the dust in 8 days by
Acidithiobacillus thiooxidans at acidic conditions. During this step,
cerium, europium and neodymium were recovered at high percentages
(> 99%), along with La and Y with a yield of 80%. In the second step,
cyanide-producing Pseudomonas putida recovered 48% of Au within 3 h
from by A. thiooxidans. Fungal bioleaching. Fungal bioleaching mechanisms involve
leaching of metals by organically excreted acids (acidolysis and
complexolysis) and change in the oxidation potential of the medium
(redoxolysis), or a combination of the three [9193]. In contrast to
acidophilic bacterial leaching, fungal redoxolysis bioleaching takes
place at a relatively higher pH, i.e. near-neural or alkaline values (Xu
and Ting [197]). Aspergillus niger and Penicillium simplicissimum are
among the most studies microbes in fungal bioleaching of metals from
waste material [43]. In a rst attempt to mobilize metals from
electronic waste Brandl et al. [94] used the latter species to extract
Cu and Sn with 65% eciency, and Al, Ni, Pb, and Zn by more than
95%. After a prolonged adaptation time of 6 weeks, the microorganisms
were able to adapt to higher pulp densities of up to 10% (w/v). The
authors recommended a separate process where the cells are grown in
absence of waste material due it is inhibitory eect on growth.
Bioleaching of Al, Cd, Cu, Co, Fe, Li, Mn, Ni, Pb, Zn from incinerator
ash [95,96]byAspergillus niger and Cd, Co, Mn, Ni, Zn from spent Zn-
Mn or Ni-Cd batteries by six Aspergillus species [44] were investigated.
The authors noted the dierence in metal removal eciency when
dierent carbon sources were used, which is related to the conversion
of the given carbon source and the excreted organic acid.
Fungal bioleaching of the critical REE by Aspergillus cuum from
primary sources has been investigated as well by Hassanien et al. [88].
In this study, under optimum conditions, 75.4% and 63.8% of REEs
were directly bioleached from monazite and a thorium-uranium con-
centrate, respectively. Aspergillus cuum was subject to another study by
Desouky et al. [64], who removed 20% of lanthanum, 33% of cerium
and 2.5% of yttrium at pH 3.0 in 24 h by this fungal strain from
thorium-uranium concentrates. Brisson et al. [63] used the fungal
strains of Aspergillus niger ATCC 1015, Aspergillus terreus ML3-1 and
Paecilomyces spp for solubilizing REE using monazite as a phosphate
source. Comparison with abiotic leaching experiments indicated the
benecial eect of microorganism presence.
Fungal bioleaching of REE was investigated by Qu and Lian [73],
who focused their work on waste red mud material, i.e. the main by-
product in bauxite processing for alumina production. Leaching ex-
periments were performed using Penicillium tricolor under three dif-
ferent pulp densities (2%, 5%, 10%) and three dierent bioleaching
processes: (1) one step bioleaching, involving microorganism cultiva-
tion in presence of red mud; (2) two step bioleaching with a fungal pre-
growth in absence of red mud followed by its addition; (3) cell-free
spent medium. The maximum leaching extraction of REEs was achieved
by the one step leaching method at 2% pulp density, whereas a two-step
leaching process exhibited the highest eciency at 10% pulp density.
3.1.4. Biochemical mechanisms of bioleaching reactions
The exact mechanism of biological metal extraction from waste
material has been long debated. The bioleaching mechanism of Cu from
printed circuit boards by A. ferrooxidans is speculated to be similar to
that of metal suldes [97] in terms of involving indirect leaching
mediated by the biogenic sulfuric acid. The role of the microorganisms
in this process is to oxidize elemental sulfur (S°) to sulfuric acid (H
as shown in Eq. (1). S° is not typically found in discarded PCB and
added externally to the leaching medium. Ferrous iron (Fe
) is also
added externally to the leaching medium, and plays the role of an
electron donor. It is subsequently oxidized to ferric iron (Fe
bacteria (Eq. (2)).
SO Microbial
1.5O H O 2H ( )
022 4
++ → +
Fe O 2H 4Fe 2OH (
In the bioleaching reaction, Fe
plays the role of an oxidizing
agent for enhancing the leaching reaction as shown in Eq. (3). Biogenic
ferric iron and sulfuric acid mobilizes copper from the waste material as
shown in Eqs. (3) and (4), respectively. This translates into a combined
acidolysis redoxolysis bioleaching mechanism for metal dissolution
from waste material.
++ +
u2Fe Cu 2Fe(
03 2 2 (3)
u H SO 0.5O Cu SO H O ( )
024 2 24
The bioleaching rate primarily depends on the initial pH, initial
ferrous iron (Fe
) concentration and oxidation rate of ferrous (Fe
to ferric ions (Fe
)[98]. Biogenic Fe
concentration is directly
correlated with leaching rate (mg metal leached as a function of time)
and the total extraction eciency [28]. On the other hand, a involve-
ment of a contact mechanism is discussed as well. A. ferrooxidans cells
do not attach randomly to the solid surface (though chemotaxis may be
involved in the preferential attachment of bacteria [46]). The interac-
tion between A. ferrooxidans cells and crushed PCB particles was sus-
pected favorable only if the van der Waals attractive force is greater
than the electrostatic repulsive force, which would occur at high ionic
strength of the solution only [99]. Indeed, Silva et al. [99] showed less
copper being mobilized (25%) when contact was avoided. For this,
ground PCB sample (particle size 5001000 μm) were placed inside a
semi-permeable membrane. Ultimately, the results for bacterial adhe-
sion tests were found consistent with DerjaguinLandauVerweyO-
verbeek theory [99].
Cyanide is the general term for chemicals which contain a cyano-
group with the chemical formula CN
. Trace amounts of thiocyanide
(SCN) is found in human saliva, urine, and gastric juices [100]. Cyanide
is suspected to be produced by bacteria under certain conditions to
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
create a competitive advantage for the producer microorganism and as
bio-control mechanism suppressing diseases on plant roots [101,102].
Biogenic cyanide is a secondary metabolite formed by oxidative dec-
arboxylation of glycine, as shown below in Eq. (5):
22 2
Methionine enhances the cyanide production yield but will not
substitute glycine [103]. Cyanide is formed during the early stationary
phase. Induction of hcn genes which are involved in cyanide production
is initiated under conditions in which oxygen is limited, however some
species can produce reasonable amounts of cyanide under normal
conditions as well [104]. Biogenic cyanide production depends on
several parameters, i.e., glycine concentration, initial pH, temperature,
solid to liquid ratio, oxygen concentration [80,82]. Though glycine is
essential for biogenic cyanide production, high concentrations have
been reported to be inhibitory for growth [103,105]. Likewise, cyanide
remains dissolved in solution at high pH, and gold cyanidation is re-
ported to be most ecient in the range of 10.511. For some micro-
organisms, such high pH however, has been reported inhibitory for cell
growth [106].
Microbe-REE-interactions are not yet fully understood, and bio-
leaching process are discussed under the terms of acidolysis, re-
doxolysis and complexolysis [62]. Organic acids (e.g. malic, oxalic, and
citric acid) have chelating properties with some REE, donating H
form metal-ligand complexes.
3.1.5. Scale-up of bioleaching applications in WEEE processing
A list of bioleaching studies involving the autotrophs and hetero-
trophs for critical and valuable metal recovery from WEEE is given in
Table 2. Several authors investigated leaching of metals from WEEE in
scaled up setups with technology readiness levels higher than 4, which
translates into tests carried out in semi-pilot level. Reported metal
bioleaching eciencies were typically between 50% and 99% and be-
tween 37 days at solid to liquid ratio between 110% (w/v). Several
studies have demonstrated improved bioleaching eciency in sulfur-
and ferrous iron-supplemented media [70,97,107]. Bottlenecks for
scaling up was certainly metal bioleaching ecacy generally decreasing
with increasing pulp density. Some discarded WEEE materials had an
alkaline nature, and was therefore acid-consuming [94] to allow for
growth of acidophiles. The non-metallic fraction, i.e. epoxy-coated
substrate, organic fraction etc., of the material may be toxic to bacteria
[28,108]. Further, inhibition upon direct contact of the cells with the
metal-rich waste materials is a bottleneck in scaling biotechnologies
[107](Xu and Ting [198]).
Ilyas et al. [69] studied bioleaching of, Al, Cu, Ni Zn from ground
printed circuit boards with a moderately thermophilic acidophilic,
chemolithotrophic and a heterotrophic consortium that was isolated
from a local site. 64%, 86%, 74%, and 80% of Al, Cu, Ni, and Zn, re-
spectively, was removed after a 27-day pre-leaching period followed by
280-day bioleaching period. Follow-up bioleaching studies by Ilyas
et al. [97] in a reactor setup using an adapted moderately thermophilic
pure culture of chemolithotrophic Sulfobacillus thermosuldooxidans
reached almost complete removal of Al, Cu, Zn, and Ni, at of 10% (w/v)
pulp density. The bioleaching medium was supplemented with 25% O
+ 0.03% CO
, and 2.5% (w/v) biogenic S°, and kept at 45 °C. An in-
teresting nding was the faster oxidation rate of biogenic sulfur over
technical sulfur, which can be attributed to the higher bioavailability
and hydrophilicity of biogenic S [112].
Mäkinen et al. (2015) studied the bioleaching of discarded printed
circuit board (PCB) froth, using pretreatment (separation of hydrophilic
/ hydrophobic fractions), pre-inoculation (to favor the dominance of
sulfur-oxidizers over iron oxidizers) and ultimately CSTR operation
ultimately achieving copper solubilization of 99% (maximal copper
concentration of 6.8 g/L).
Chen et al. [70] investigated bioleaching of copper from ground PCB
using Acidithiobacillus ferrooxidans.Copper recovery was relatively high,
(94.8% after 28 days) however, the study indicated that the rate of
copper dissolution was limited by diusion due to secondary mineral
precipitation (Jarosite, iron oxyhydroxides) covering the surface of the
leaching material. The formation of such jarosite precipitates may be
prevented by maintaining acidic conditions (dilute sulfuric acid addi-
tion) of the leaching medium.
Compared to bioprocessing for base metal recovery, bioleaching
applications related to rare earth elements are less common. Studies
demonstrated the ability of selected microorganisms in bioleaching of
rare earth elements (REE) from primary and secondary raw materials.
Some patents on microbial REE bioleaching have been developed as
well [62]. Recent studies on REE extraction through bioleaching pro-
cesses are outlined in Table 3, both for primary sources and for sec-
ondary ones including electronic waste.
Ibrahim and El-Sheikh [65] investigated bioleaching of REE, Al, U,
and Zn, from uraniferous gibbsite ore by Acidithiobacillus ferrooxidans
in column setup, achieving 67.6% eciency for REE (30 cycles, 0.5%
elemental sulfur addition). Muravyov et al. [72] investigated REE bio-
leaching from metal-bearing coal ashslag in airlift percolators,
leaching Sc, Y, and La at 52%, 52.6%, and 59.5%, resp. (10 days of
operation at 45 °C, 10% pulp density; 10:1 ashslag to elemental
sulfur). As mentioned above, DNI Metals operated a REE bio-heap
leaching project as full scale bioleaching application [18]. Apart, to the
best of our knowledge, applications at a greater technology readiness
level than 6, i.e. industrial scale, involving heterotrophic microorgan-
isms have not been reported yet.
3.2. Biosorption, bioelectrochemical and bioprecipitation processes for
selective metal recovery from leachates
In the last decades, signicant research eorts in the eld of en-
vironmental technology were focused on the removal of toxic metals
from contaminated ground waters, polluted soils and (industrial and
domestic) wastewaters. These strategies include bio-based technologies,
e.g. biosorption and bioprecipitation. Recently, this research focus is
shifting partly towards the recovery of valuable metals from (industrial)
wastewaters and polluted soils, leachates and solid wastes, including
WEEE. This paradigm shift can be ascribed to the fact that bio-based
technologies are considered a cost-eective option to concentrate ele-
ments from diluted wastewaters and leachates as part of these recovery
strategies, and recovery of valuable elements may help to reduce the
cost of waste treatment. Bio-based strategies can not only work with
those dilute waste streams, but also may require a low energy input.
Therefore, bioelectrochemical systems, bioprecipitation and biosorp-
tion techniques are now also being integrated into novel hydro-, bio-
and hybrid-metallurgical systems.
3.2.1. Biosorption The biosorption process. Biosorption is a physico-chemical and
metabolically-independent process that includes absorption,
adsorption, ion exchange, micro precipitation, surface complexation
mechanisms on material of biologic origin (Volesky, 2003; [115]).
Consequently, a number of materials have been studied in the frame of
biosorption: living or inactive biomass of bacterial [116]; Vargas et al.,
2004), fungal (Wang, and Chen [201]; Sağ[211]; Niu, and Volesky,
2007) or plant origin (Romera et al. [193]; Mack et al. [194]; Vilar et al.
[195]); agricultural residues, waste crustacean biomass, etc. (Volesky
[212]; Wang and Chen [199]). New members of biosorbent family are
waste materials or biomass by-products from large scale fermentation
processes (Kapoor and Viraraghaven [200]; Wang and Chen, 2006).
Fig. 3 displays a schematic classication of the biosorption mechanisms
The eciency of metal biosorption is aected by the structure of the
biosorbent, especially cell surface and the cell wall (Volesky [212];
Wang and Chen, [199]; 186,118]). Several functional groups are in-
volved, such as carboxyl, imidazole, sulfhydryl, amino, phosphate,
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
Table 2
Recent studies on biotechnological strategies for valuable metal recovery from WEEE, operational conditions and metal yields.
Microorganisms Operational parameters Bioleaching mechanism Leached metals %
(mg/g PCB)
T(°C) pH Pulp density
Technology readiness level < 4 (batch reactors)
Autotrophic bioleaching
Sulfobacillus thermosuldooxidans, acidophilic isolate 45 °C 2.0 10:1000 Acidolysis (H
), Redoxolysis (Fe
) Cu 89% (76 mg/g), Ni 81% (16.2 mg/g), Zn 83%
(66.4 mg/g)
Acidithiobacillus sp., Gallionella sp., Leptospirillum sp. 30 °C 1.5 - 2.5 20:1000 Redoxolysis (Fe
) Cu 95% (219 mg/g) [98]
At. ferrooxidans, At. thiooxidans 28 °C 1.5 - 3.5 30:1000 Acidolysis (H
), redoxolysis (Fe
)Cu (94%), Ni (89%), Zn (90%) [107]
Acidophilic consortium (genera Acidithiobacillus and Gallionella) 30 °C 2.0 12:1000 Redoxolysis (Fe
) Cu 97% (626 mg/g), Al 88% (34 mg/g), Zn 92%
(28 mg/g)
At. ferrooxidans, Leptospirillum ferrooxidans, At. thiooxidans 25 °C 1.7 10:1000 Acidolysis (H
), redoxolysis (Fe
) Cu 95% (106 mg/g) [61]
Acidithiobacillus thiooxidans 30 °C 0.5 10:1000 Acidolysis (H
) Cu 98% (132 mg/g) [ 67]
At. caldus, Le. ferriphilum, Sulfobacillus benefaciens, Ferroplasma acidiphilum 37 °C 1.7 10:1000 Acidolysis (H
), redoxolysis (Fe
) Cu 99% (29 mg/g) [109]
Heterotrophic leaching
Aspergillus niger, Penicillium simplicissimum 30 °C 3.5 10:1000 Acidolysis (organic acids) Cu 65% (52 mg/g), Al 95% (225 mg/g), Ni 95%
(14 mg/g), Zn 95% (25 mg/g)
Chromobacterium violaceum, Pseudomonas uorescens, Pseudomonas plecoglossicida 30 °C 7.2 - 9.2 various Complexolysis (CN
) Au 69% (not specied) [51]
Chromobacterium violaceum (metabolically engineered) 30 °C Neutral 5:1000 Complexolysis (CN
)Au 31% (0.04 mg/g) [110]
Ps. chlororaphis 25 °C 7.0 19:1000 Complexolysis (CN
) Au (8%), Ag (12%), Cu (52%) [52]
At. ferrooxidans, At. thiooxidans, Thiobacillus denitricans, Thiobacillus
thioparus, Bacillus subtilis, Bacillus cereus
22 - 37 °C 5.0 - 7.0 10:1000 Acidolysis (H
), redoxolysis (Fe
complexolysis (surfactants)
Cu 53% (22 mg/g), Ni 48.5% (6.4 mg/g), Zn
48% (6 mg/g)
Ps. putida (two-step) 30 °C 8.0 - 9.2 10:1000 Complexolysis (CN
) Cu 98% (164 mg/g), Au 44% (0.1 mg/g) [71]
Technology readiness level >4 (column and tank reactors)
Autotrophic bioleaching
Sb. thermosuldooxidans, Thermoplasma acidophilum 45 °C, 1.5-2.7, n/a (10 kg) Acidolysis (H
), redoxolysis (Fe
) Cu 86% (76 mg/g), Zn 80% (71 mg/g), Ni 74%
(15 mg/g), Al 64% (6.5 mg/g)
Sb. thermosuldooxidans 45 °C, 2.0, 1.5-3.5% Acidolysis (H
), redoxolysis (Fe
) Cu 95% (105 mg/g), Al 91% (19 mg/g), Zn 96%
(18 mg/g), Ni 94% (18 mg/g)
At. ferrooxidans 30 °C, 2.0, 1.5% Acidolysis (H
), redoxolysis (Fe
) Cu 97% (247 mg/g), Zn 84% (52 mg/g), Al 75%
(47 mg/g)
At. ferrooxidans, At. thiooxidans 28 °C, 1.1-1.6, 1% Acidolysis (H
), redoxolysis (Fe
) Cu 99% (151 mg/g) [114]
At. ferrooxidans 30 °C, 2.0, 1% Acidolysis (H
), redoxolysis (Fe
) Cu 95% (203 mg/g) [70]
S/L: Solid to liquid ratio.
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
sulfate, thioether, phenol, carbonyl, amide and hydroxyl moieties are
involved in the sorption processes (Wang and Chen [199]; Volesky,
2007). It has been proven that a higher sorption capacity can be
achieved by functionalizing non-living biomaterials with chelating
agents, or by other chemical (e.g., alteration of functional groups or use
of crosslinking agents) or physical (e.g., heat treatment, ultrasonic
treatment) modication of the materials (Fig. 3). For instance, Ru
loading (from 86 to 145 mg/g dry cells) and selectivity over Ni and Zn
were improved by the acid pretreatment of Rhodopseudomonas palustris
cells, whereas the Ru loading capacity of the biomass was increased by
6.9-fold using chitosan and surface modication with Polyethyleimine
(PEI) [119,120]. Recently, some novel chemically modied biosorbents
have been developed that show excellent selectivity to recover valuable
metals from industrial wastewaters and leachates of industrial residues,
generating pure metal solutions (e.g., Roosen and Binnemans [202];
Roosen et al., 2016). However, functionalization / pretreatment often
increase the cost and environmental impact of the technology con-
siderably [81,115].
Further, the eciency of biosorption is related to the surface area of
the biomass [118], with cellular microorganisms exhibiting the highest
biosorption potential. Ecacy of the (de)sorption processes is aected
by (1) the form in which metals are present, i.e. their speciation [73],
and (2) operational parameters (e.g., temperature, biosorbent dosage
and pH) and (3) the type of sorbent used [118,121,122].
Table 3
Recent studies on biotechnological strategies for REE extraction from solid matrices.
Microorganism(s) Matrix Operational parameters Bioleaching
Leached metals (%) References
T(°C) pH S/L
(%, w/v)
Technology readiness level < 4 (batch reactors)
Autotrophic bioleaching
Acidithiobacillus ferrooxidans,
Acidithiobacillus thiooxidans,
Leptospirillum ferrooxidans
CRT uorescent
30 °C n/a 10% Acidolysis (H
redoxolysis (Fe3
Y 70% [68]
Heterotrophic leaching
Aspergillus cuum Monazite mineral 30 °C 3 0.6% Acidolysis (organic
acids), Complexolysis
Total REEs 75.4% [88]
Pseudomonas aeruginosa Monazite mineral 35 °C 6 0.6% Acidolysis (organic acids) Total REEs 63.5% [88]
Penicillium tricolor red mud 30 °C 2-2.5 2% Acidolysis (organic acids) La, Ce, Pr, Nd, Sm, Eu, Gd, Tb,
Dy, Ho, Er, Tm, Yb, Lu, Y, Sc 36
Acetobacter aceti Monazite mineral 30 °C 3-5 16.6% Acidolysis (organic
acids), Complexolysis
Ce 0.13%, La 0.11% [89]
Aspergillus cuum thorium-uranium
25 °C 3 0.75 % Acidolysis (organic acids) La 20%, Ce 33%, Y 2.5% [64]
Aspergillus niger, Aspergillus terreus,
Monazite mineral 2528°C 2-2.8 1% Acidolysis (organic acids) Ce, La, Nd, Pr 3-5% [63]
Gluconobacter oxydans uorescent lamp
phosphor powder
30 °C n/a 1.5% Acidolysis (organic acids) Total REEs (Y, La, Ce, Pr, Nd,
Sm, Eu, Gd, Tb, Ho, Dy, Er, Tm,
Yb, Lu, Th) 2%
Technology readiness level >4 (column and tank reactors)
Autotrophic bioleaching
Acidithiobacillus ferrooxidans Gibbsite mineral 25 °C 2 1kg/500mL Acidolysis (H
) REEs 67.6% [65]
Acidophilic chemolithotrophs Coal ashes 45 °C 0.9- 2 10% Acidolysis (H
) Sc 52%, Y 52.6%, La 59.5% [72]
S/L: Solid to liquid ratio.
Fig. 3. Schematic explanation of metal biosorption mechanisms (Redrawn after [117]).
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
To summarize, biosorption has the following advantages: (1) the
elements can be absorbed selectively even at very low concentrations,
(2) the process is energy ecient, (3) the process conditions are mild in
terms of e.g. pH and temperature, (4) the elements can be harvested
easily, and (5) some biosorbents can be regenerated if needed (Kücüker
et al. [186]). Despite the research eorts since 1990s, there has been
limited exploitation of biosorption in an industrial context [81]in
general, and of biosorption-based recovery of metals from WEEE lea-
chate solutions in particular. The lack of commercial success is attrib-
uted by Fomina and Gadd [115] still poor understanding of the me-
chanisms, kinetics and thermodynamics of the processes, as well as the
wide range of competing technologies that are available. In addition,
further drawbacks for biosorption particular relating to WEEE are (1)
lack of data allowing to assess their selectivity for complex, highly
acidic / multi metal rich waste streams dierent from the original
tested solutions, (2) that chemical modications of the materials are
often needed to increase their selectivity, and (3) the need to initially
dissolve metal ions from a complex solid matrix (Fig. 4). Recovery of metals by biosorption.Table 4 gives a list of studies
on biosorption of REEs and PGMs (Wang and Chen [199]; [74];
Kücüker et al. [186]). These studies mainly focused on the
application of biosorption processes to recover metals from WEEE
leachates. Studies on recovery from wastewaters generated by WEEE
industries are still scarce. For instance, Bhat et al. [117] have proposed
an integrated model for the recovery of Au and Ag from WEEE using a
combination of hydrometallurgical and biometallurgical processes.
They concluded that Eicchornia root biomass and waste tea powder
were ecient biosorbents for recovery of leached silver-cyanide from
electronic scrap, and the concentrated silver-cyanide recovered in the
biosorption process could further be used as an input material for
electroplating industry. Côrtes et al. [33] studied biosorption of gold
alone and in combination with precipitation from discarded computer
microprocessor (DCM) thiourea leachates using chitin as a biosorbent.
Ultimately, about 80% of the gold were recovered at 20 g/L of chitin
within 4 h.
Kücüker et al. [80] studied Nd removal from neodymium magnet
leachates in batch and continuous sorption systems by using dried green
microalgae (Chlorella vulgaris). The maximum Nd uptake
(q = 157.21 mg/g sorbent) was determined at pH 5 with a biosorbent
dosage of 500 mg/L and an initial neodymium concentration in the
mixed leachate solution of 250 mg/L at 35 °C. Though Chlorella vulgaris
was considered a potent biosorbent, substantial pH adaptation was
needed prior to biosorption, which may be a bottleneck. Due to the
above mentioned bottlenecks, most biosorption processes are still at the
laboratory scale. Still, biosorption may nd applications in the recovery
of valuable metals. Furthermore, the use of hybrid technologies for
selective metal recovery and the potential of the technology to directly
produce valuable products, including e.g. micronutrient-enriched feed
supplements and fertilizers, from waste streams should also be explored
Most of the previous studies on metal biosorption focused on bio-
sorption for pollutant removal and, therefore, recovery of loaded metals
from the waste streams was not even considered. In particular selective
desorption from the biosorbent may proof a challenge [81,115], in
particular since most previous studies focused on metal sorption in lab-
scale using synthetic solutions.
3.2.2. Bioprecipitation and bioelectrochemical systems (BES) Bioprecipitation and bioreduction. Bioprecipitation processes to
Fig. 4. Biosorbent pre-treatment and modication methods to improve the uptake capacity (redrawn after [115]).
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
remove metals from (industrial) waste streams typically have focused
on the use of sulphate reducing bacteria, forming insoluble metal
sulphidic precipitates, as illustrated in the review published by Hussain
et al. [89]. Sulphate reduction processes have mainly been used in
mining and metal recycling industries. Furthermore, metabolizing
bacteria can release other compounds which can be used in
precipitation processes (e.g., phosphates) and/or induce changes of
the aqueous environment, such as pH changes, which may promote
precipitation [121]. Janyasuthiwong et al. [26] successfully applied
sulphate reducing bacteria to precipitate Cu from PCB leachates (1.0 M
) in a continuous system, yielding more than 90% Cu recovery.
Furthermore, direct bioreduction of precious metals to metallic
nanoparticles also has received attention in recent years. Production of
nanomaterials from waste materials using microorganisms is particu-
larly promising because (1) the produced nanomaterials can be directly
valorized in catalytic/industrial processes, (2) the microorganisms are
considered as inexpensive catalysts and synthesis is conducted at am-
bient temperature and pressure. Several researchers have focused on
studying Pd bioreduction in the form of biomass-associated nano-
palladium (Pd(0) or bio-Pd) [127]. The microbial activity seems par-
ticularly useful for in situ generation of reducing agents, such as hy-
drogen, for Pd(II) reduction as well as for the subsequent catalytic
reactions [15,110,128,129]. For instance, microbial reduction of Pd(II)
to bio-Pd was used to recover the element from industrial automotive
catalyst, and from the leachates of catalytic transformation of chemicals
and pollutants applications [86]. A three-stage biobased process using
native and palladized D. desulfuricans was also already developed for
selective sequential recovery of Au and PGMs from e-waste leachates
Formation of other biogenic metallic (nano)particles was also pre-
viously investigated and shown to have potential to generate products
from waste streams which can be directly valorized. For example,
Deplanche et al. [37] focused on biorecovery of gold from jewellery
wastes by Escherichia coli and biomanufacture of catalytically active Au-
nanomaterials for the oxidation of glycerol. Work of [22,23] ex-
emplied the fabrication of novel gold nanostructures and stable bio-Au
nanocomposites with excellent optical properties by combining micro-
organisms and a surfactant. De Gusseme et al. [179,180] illustrated the
potential use of biogenic Ce and Ag(0) particles for virus disinfection,
whereas [170,171] have prepared membranes containing biogenic Ag
(0) precipitates having antifouling properties. The bio-Ag-0/PES com-
posite membranes, even with the lowest content of biogenic silver
(140 mg bio-Ag(0) m
), not only exhibited excellent anti-bacterial ac-
tivity, but also prevented bacterial attachment to the membrane surface
and decreased the biolm formation. De Corte et al. [93] have devel-
oped biosupported bimetallic Pd-Au nanocatalysts which can be used
for dechlorination of environmental contaminants. Although all of this
work is very promising, many of these studies still used synthetic media
to prepare the biogenic particles and illustrate their potential for re-
moval and recovery of valuable metals from waste. Therefore, there is
Table 4
Recovery of critical metals from aqueous sources through biosorption.
Cation Biosorbent Biosorption capacity (mg/g) References
Chemically modied chitosan resin 413.62 Donia et al. [184]
Bacillus cereus 91.75 Li et al. [14]
Saccharomyces cerevisiae 135.91 Chen et al. [46]
Klebsiella sp.3S1 141.1 Muñoz et al. [18]
Magnetospirillum gryphiswaldense 13.5 Wang et al. [123]
Fucus vesiculosus 68.94 Mata et al. (2009)
Rice husk carbon 1496.90 Chand et al. (2009)
Chemically modied chitosan 669.66 Donia et al. [184]
Crosslinked chitosan resin 70.34 Fujiwara et al. (2007)
Silk and chitosan 0.20 Chen et al. (2010)
Thiourea modied alginate 1668.25 Gao et al. [52]
Racomitrium lanuginosum 37.2 Sari and Mustafa et al. [185]
Bayberry tannin 33.4 Ma et al. [124]
NaOH modied Pleurotus ostreatus 45.45 Hussein et al. [28]
Fish scales 250.00 Das and Varshini [176]
Pleurotus ostreatus basidiocarps 54.54 Hussien [214]
Chlamydomonas reinhardtii 142.86 Birungi and Chirwa [25]
Sargassum sp. 91.68 Oliveira and Garcia [125]
Chlorella vulgaris 74.60 Birungi and Chirwa [25]
Grapefruit peel 159.30 Torab et al. (2015)
Prawn carapace 1000.00 Varshini and Das [176]
Fish scales 200.00 Varshini and Das [176]
Corn style 250.00 Varshini and Das [176]
Platanus orientalis 32.05 Sert et al. [126]
Green seaweed (Ulva lactuca) 69.75 Vijayaraghavan [215]
Free Turbinaria conoides (brown seaweed) 146.4 Vijayaraghavan and Jegan [177]
Polysulfone immobilized Turbinaria conoides 119.5 Vijayaraghavan and Jegan [177]
Crab shell 66.60 Varshini and Das (2015b)
Sargassum sp. 98.63 Oliveria et al. (2011)
Chlorella vulgaris 157.21 Kücüker et al. [186]
Physcomitrella patens 106.73 Heilmann et al. [126]
Calothrix brevissima 69.23 Heilmann et al. [126]
Tetraselmis chuii 51.92 Heilmann et al. [126]
Sargassum sp. 100.96 Oliveira and Garcia [125]
Activated biochars from cactus bres (pH = 3.0) 90.00 Hadjittoti et al. (2016)
Activated biochars from cactus bres (pH = 6.5) 350.00 Hadjittoti et al. (2016)
Sargassum sp. 105.25 Oliveria et al. (2011)
Activated carbon 86.00 Anagnostopoulos and Asaymeopoulos (2013)
Modied cactus bres (MnO2-coated)) 0.46 Prodromou and Pashalidis [178]
Sargassum polycystum Ca-loaded biomass 62.30 Diniz and Volesky [79]
Sargassum polycystum Ca-loaded biomass 62.30 Oliveira and Garcia [125]
Yb Sargassum polycystum Ca-loaded biomass 48.45 Diniz and Volesky [79]
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
currently a clear need for setting up experiments focused on the gen-
eration of biogenic particles from real waste streams, including WEEE,
and upscaling of the technologies to pilot-scale. Bioelectrochemical systems (BES). Bioelectrochemical systems
(BES) link electrochemical systems with the microbial metabolism.
Microorganisms can respire on electrodes, harvesting electrons from
waste streams containing organic matter. This can be used to generate
electricity (in microbial fuel cells - MFCs), treat contaminants and/or
produce chemical products, such as methane, ethanol, or hydrogen
peroxide (in microbial electrolysis cells - MECs) (Fig. 5). However, the
electrons removed may also be used to recover metals from solution at
the cathode. Metals can be reduced at the cathode with a net positive
cell potential and power generation if the potential generated at the
bioanode is lower than the redox potential of the half-cell reaction at
the cathode, which is often the case. In other cases, supply of voltage is
needed. Recovery of several base metals (e.g., Cu, Ni, Cd, Zn) as well as
of a few precious and scarce metal(loid)s (e.g., Ag, Au, Co, and Se) have
recently been demonstrated in BESs (e.g., [78,130,59]). Most
researchers worked with synthetic solutions, delivering a proof-of-
principle. However, Peiravi et al. [54] and Pozo et al. [131] recently
designed bioelectrochemical systems for treatment of real mine
drainage. Pozo et al. [131] produced a solid metal sludge which was
twice less voluminous and 9 times more readily settleable than metal-
sludge precipitated using NaOH. Concomitant precipitation of rare
earth elements, among other high-value metals, occurred, which could
be used to oset the treatment costs. Additional studies are still needed
to investigate the possibility to recover metals from other real waste
streams and leachates, e.g. those generated by WEEE processing, using
BES and to scale up the technology. Furthermore, the potential
application of the BES platform for recovery of a range of other
precious and technology-critical metals, such as metals occurring in
WEEE, can still be further explored.
4. Perspectives and future developments
Global waste electrical and electronic equipment (WEEE) genera-
tion will increase in the next years, particularly in the developing
countries. WEEE is an important secondary source of critical raw ma-
terials. These metals play a central role particularly in the transition to
a green society. Their secure supply is under risk, therefore alternative
supply sources, for instance metal-rich post-consumer waste materials,
are of importance. However, the potential economic benets from cri-
tical material recovery should not be perceived as the sole driver to
develop these technologies. Improper disposal / handling of WEEE and
many other toxic metal-bearing secondary sources, is a risk for the
environment and public health. Admittedly, it is challenging to assign
an economic value to a risk that has been mitigated. Environmental
sustainability accounting tools, e.g. Life Cycle Assessment (LCA) and
Life Cycle Costing (LCC) might prove useful to map the environmental
hotspots and to communicate this to the public and the decision ma-
kers. Biotechnology is highlighted to play a signicant role in the
treatment and resource recovery from metal-containing waste materials
[13,20,43]. Bioprocessing of waste for metal recovery attracts interest
to meet two objectives: resource recovery and pollution mitigation.
Biotechnology will provide a number of technological innovations
supplementing conventional technologies in recovery and re-use of
critical metals from secondary sources in the transition to a sustainable
management of WEEE.
Biotechnologies have a historical niche area in processing of low-
grade ores. WEEE is distinct compared to primary ores in terms of its
chemical composition, abundance of the metals and their complexity.
WEEE typically include high concentrations of conventional metals and
a lower concentration of critical metals in various mixtures. Current
WEEE recycling practices are inadequate to target the critical metals,
which are typically found in low concentrations [22]. It is important to
note that conventional (established) bioleaching operations make use of
autotrophic microorganisms that can conserve energy from solubilizing
Fig. 5. Removal and recovery of heavy metals in (a) microbial fuel cells, (b) microbial electrolysis cells, (c) microbial fuel cell with bipolar membrane (modied and
redrawn after ter Heijne et al. [182] and (d) microbial fuel cells and microbial electrochemical cells with biocathodes.
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
(oxidizing) suldic ores. WEEE, on the other hand, include metals in
their native metallic form. Thus, it is required to supplement the mi-
crobes with additional energy source. This specic challenge requires
novel strategies for critical metal recovery from WEEE.
There is need to perform more fundamental research on WEEE
bioprocessing as some of the main leaching mechanisms are not fully
understood. As for metals present in other forms (carbonates, oxides or
silicates), the principles / experiences using autotrophic bioleaching
cannot simply be transferred to WEEE bioleaching due to the funda-
mentally dierent underlying chemistry (i.e. WEEE not containing
metals in form of suldes). Further investigations are required in order
to advance further into full-scale applications, including optimization of
the operational conditions and assessment of environmental impacts is
needed. In addition, including scale-up studies with techno-economic
assessment and environmental sustainability analysis considerations
are important considerations in biotechnological strategies for metal
The authors would like to acknowledge networking support by the
COST Action ES1407 funded by the European Commission (EC). Ata
Akcil acknowledges the Scientic and Technological Research Council
of Turkey for the INTENC Project (113Y011) during 2014-2018.
[1] F.O. Ongondo, I.D. Williams, T.J. Cherrett, How are WEEE doing? A global review
of the management of electrical and electronic wastes, Waste Manag. 31 (2011)
[2] C.P. Baldé, F. Wang, R. Kuehr, J. Huisman, The Global E-Waste Monitor 2014,
United Nations University, IAS SCYCLE, Bonn, Germany, 2015.
[3] European Commission, Report on critical raw materials for the EU, Report of the
Ad Hoc Working Group on Dening Critical Raw Materials, (2014).
[4] J. Huisman, WEEE Recast: from 4 Kg to 65%: the Compliance Consequences, UNU
Expert Opinion on the EU European Parliament Draft Report on the WEEE
Directive With Updates of the 2007 WEEE Review Study. Bonn, (2010).
[5] Y. Gu, Y. Wu, M. Xu, X. Mu, T. Zuo, Waste electrical and electronic equipment
(WEEE) recycling for a sustainable resource supply in the electronics industry in
China, J. Clean. Prod. 127 (2016) 331338,
[6] P. Kiddee, R. Naidu, M.H. Wong, Electronic waste management approaches: an
overview, Waste Manag. 33 (2013) 12371250,
[7] F. Cucchiella, I. DAdamo, S.C. Lenny Koh, P. Rosa, Recycling of WEEEs: an eco-
nomic assessment of present and future e-waste streams, Renew. Sustain. Energy
Rev. 51 (2015) 263272,
[8] Eurostat, Recycling Rate of WEEE, Retrieved from (2018) , accessed on 1 June
[9] P. Chancerel, S. Rotter, Recycling-oriented characterization of small waste elec-
trical and electronic equipment, Waste Manag. 29 (2009) 23362352, https://doi.
[10] P. Hadi, M. Xu, C.S.K. Lin, C.W. Hui, G. McKay, Waste printed circuit board re-
cycling techniques and product utilization, J. Hazard. Mater. 283 (2015) 234243,
[11] A. Bloodworth, Track ows to manage technology-metal supply, Nature 505
(2014) 910,
[12] A. Mahmoud, P. Cézac, F.A.H. Hoadley, F. Contamine, P. DHugues, A review of
sulde minerals microbially assisted leaching in stirred tank reactors, Int.
Biodeterior. Biodegrad. 119 (2017) 118149,
[13] A. Arundel, D. Sawaya, The Bioeconomy to 2030: Designing a Policy Agenda,
OECD Publishing, 2009,
[14] L. Li, Q. Hu, J.H. Zang, H.Y. Qi, G.Q. Zhuang, Resistance and biosorption me-
chanism of silver ions by Bacillus cereus biomass, J. Environ. Sci. 23 (1) (2011)
[15] E. Suja, Y.V. Nancharaiah, V.P. Venugopalan, Biogenic nanopalladium production
by self-immobilized granular biomass: application for contaminant remediation,
Water Res. 65 (2014) 395401.
[16] D. Morin, A. Lips, T. Pinches, J. Huisman, C. Frias, A. Norberg, E. Forssberg,
BioMinE - integrated project for the development of biotechnology for metal-
bearing materials in Europe, Hydrometallurgy 83 (2006) 6976,
[17] R. Jain, D. Dominic, N. Jordan, E.R. Rene, S. Weiss, E.D. van Hullebusch,
R. Hubner, P.N.L. Lens, Preferential adsorption of Cu in a multi-metal mixture onto
biogenic elemental selenium nanoparticles, Chem. Eng. J. 284 (2016) 917925.
[18] A.J. Muñoz, F. Espínola, E. Ruiz, Biosorption of Ag (I) from aqueous solutions by
Klebsiella sp. 3S1, J. Hazard. Mater. 329 (2017) 166177.
[19] S. Ilyas, J. Lee, Biometallurgical recovery of metals from waste electrical and
electronic equipment: a review, ChemBioEng Rev. 1 (2014) 148169, https://doi.
[20] X. Dominguez-Benetton, J.C. Varia, G. Pozo, O. Modin, A. Ter Heijne, J. Fransaer,
K. Rabaey, Metal recovery by microbial electro-metallurgy, Prog. Mater Sci. 94
(2018) 435461,
[21] N.J. Creamer, V.S. Baxter-Plant, J. Henderson, M. Potter, L.E. Macaskie, Palladium
and gold removal and recovery from precious metal solutions and electronic scrap
leachates by Desulfovibrio desulfuricans, Biotechnol. Lett 28 (2006) 14751484.
[22] S. Ilyas, M. Kim, J. Lee, A. Jabeen, H.N. Bhatti, Bio-Reclamation of Strategic and
Energy Critical Metals from Secondary Resources 117, (2017),
[23] S.T. Akar, A. Gorgulu, Z. Kaynak, B. Anilan, T. Akar, Biosorption of reactive Blue
49 dye under batch and continuous mode using a mixed biosorbent of macro-
fungus Agaricus bisporus and Thuja orientalis cones, Chem. Eng. J. (2008) 2634.
[24] K. Breivik, J.M. Armitage, F. Wania, K.C. Jones, Tracking the global generation
and exports of e-waste. Do existing estimates add up? Environ. Sci. Technol. 48
(2014) 87358743,
[25] Z.S. Birungi, E.M.N. Chirwa, The kinetics of uptake and recovery of lanthanum
using freshwater algae as biosorbents: comparative analysis, Bioresour. Technol.
160 (2014) 4351.
[26] S. Janyasuthiwong, R. Ugas, E.R. Rene,, A. Carucci, G. Esposito, P.N.L. Lens, Eect
of operational parameters on the leaching eciency and recovery of heavy metals
from computer printed circuit boards, J. Chem. Technol. Biotechnol. 91 (2016)
[27] B. De Gusseme, G. Du Laing, T. Hennebel, P. Renard, D. Chidambaram, J.P. Fitts,
E. Bruneel, I. Van Driessche, K. Verbeken, N. Boon, W. Verstraete, Virus removal
by biogenic cerium, Environ. Sci. Technol. 44 (2010) 63506356.
[28] H. Hussein, S.F. Ibrahim, K. Kandeel, H. Moawad, Biosorption of heavy metals
from waste water using Pseudomonas sp, Electron. J. Biotechnol. 7 (2004) 3846.
[29] H. Friege, Review of material recovery from used electric and electronic equip-
ment-alternative options for resource conservation, Waste Manag. Res. 30 (2012)
[30] B. De Gusseme, T. Hennebel, E. Christiaens, H. Saveyn, K. Verbeken, J.P. Fitts,
N. Boon, W. Verstraete, Virus disinfection in water by biogenic silver immobilized
in polyvinylidene uoride membranes, Water Res. 45 (2011) 18561864.
[31] A.C. Kasper, G.B.T. Berselli, B.D. Freitas, J.A.S. Tenório, A.M. Bernardes,
H.M. Veit, Printed wiring boards for mobile phones: characterization and recycling
of copper, Waste Manag. 31 (2011) 25362545,
[32] F.O. Ongondo, I.D. Williams, G. Whitlock, Distinct urban mines: exploiting sec-
ondary resources in unique anthropogenic spaces, Waste Manag. 45 (2015) 49,
[33] L.N. Côrtes, E.H. Tanabe, D.A. Bertuol, G.L. Dotto, Biosorption of gold from
computer microprocessor leachate solutions using chitin, Waste Manage. 45
(2015) 272279.
[34] L.H. Yamane, V.T. de Moraes, D.C.R. Espinosa, J.A.S. Tenório, Recycling of WEEE:
characterization of spent printed circuit boards from mobile phones and compu-
ters, Waste Manag. 31 (2011) 25532558,
[35] S.R. Zimmerley, D.G. Wilson, J.D. Prater, Cyclic Leaching Process Employing Iron
Oxidising Bacteria, 282996 (1958).
[36] R. Cossu, I.D. Williams, Urban mining: concepts, terminology, challenges, Waste
Manag. 45 (2015) 13,
[37] K. Deplanche, G.A. Attard, L.E. Macaskie, Biorecovery of gold from jewellery
wastes by Escherichia coli and biomanufacture of active Au-nanomaterial, Adv.
Mater. Res. 2021 (2007) 647650.
[38] J. Cui, L. Zhang, Metallurgical recovery of metals from electronic waste: a review,
J. Hazard. Mater. 158 (2008) 228256,
[39] B. Ghosh, M.K. Ghosh, P. Parhi, P.S. Mukherjee, B.K. Mishra, Waste printed circuit
boards recycling: an extensive assessment of current status, J. Clean. Prod. 94
(2015) 519,
[40] S. Ilyas, J. Lee, L. Crystal, Hybrid leaching: an emerging trend in bioprocessing of
secondary resources, Microbiol. Miner. Met. Mater. Environ. (2015) 359382.
[41] European Commission, European Commission 2017. COM/2017/0490, (2017).
[42] H. Kawamoto, Japans policies to be adopted on rare metal resources, Sci. Technol.
Trends 27 (2008) 5776.
[43] J. Lee, B. Pandey, Bio-processing of solid wastes and secondary resources for metal
extractiona review, Waste Manag. 32 (2012) 318,
[44] M.J. Kim, J.Y. Seo, Y.S. Choi, G.H. Kim, Bioleaching of spent Zn-Mn or Ni-Cd
batteries by Aspergillus species, Waste Manag. 51 (2016) 168173,
[45] C.L. Brierley, J.A. Brierley, Progress in bioleaching: part B: applications of mi-
crobial processes by the minerals industries, Appl. Microbiol. Biotechnol. 97
(2013) 75437552,
[46] C. Chen, D. Wen, J. Wang, Cellular surface characteristics of Saccharomyces cere-
visiae before and after Ag (I) biosorption, Bioresour. Technol. 156 (2014) 380383.
[47] D.B. Johnson, C.A. Du Plessis, Biomining in reverse gear: using bacteria to extract
metals from oxidised ores, Miner. Eng. 75 (2015) 25,
[48] A. Bharadwaj, Y. Ting, From biomining of mineral ores to bio urban mining of
industrial waste, Environ. Technol. Manag. Conf. 4th ETMC, (2011).
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481
[49] T. Hennebel, N. Boon, S. Maes, M. Lenz, Biotechnologies for critical raw material
recovery from primary and secondary sources: R&D priorities and future per-
spectives, N. Biotechnol. 32 (2015) 121127,
[50] F. Bakhtiari, H. Atashi, M. Zivdar, S.A.S. Bagheri, Continuous copper recovery
from a smelters dust in stirred tank reactors, Int. J. Miner. Process. 86 (2008)
[51] H. Brandl, S. Lehmann, M.A. Faramarzi, D. Martinelli, Biomobilization of silver,
gold, and platinum from solid waste materials by HCN-forming microorganisms,
Hydrometallurgy 94 (2008) 1417,
[52] X. Gao, Y. Zhang, Y. Zhao, Biosorption and reduction of Au (III) to gold nano-
particles by thiourea modied alginate, Carbohydr. Polym. 159 (2017) 108115.
[53] E.R. Donati, W. Sand, Microbial processing of metal suldes, Microbial Processing
of Metal Suldes, Springer, 2007,
[54] M. Peiravi, S.R. Mote, M.K. Mohanty, J. Liu, Bioelectrochemical treatment of acid
mine drainage (AMD) from an abandoned coal mine under aerobic condition, J.
Hazard. Mater. 333 (2017) 329338.
[55] S. Hedrich, M. Schlömann, D. Barrie Johnson, The iron-oxidizing proteobacteria,
Microbiology 157 (2011) 15511564,
[56] D.E. Rawlings, D.B. Johnson, The microbiology of biomining: development and
optimization of mineral-oxidizing microbial consortia, Microbiology 153 (2007)
[57] W. Sand, T. Gehrke, P.G. Jozsa, A. Schippers, (Bio)chemistry of bacterial leaching -
direct vs. indirect bioleaching, Hydrometallurgy 59 (2001) 159175, https://doi.
[58] A. Orell, C.A. Navarro, R. Arancibia, J.C. Mobarec, C.A. Jerez, Life in blue: copper
resistance mechanisms of bacteria and Archaea used in industrial biomining of
minerals, Biotechnol. Adv. 28 (2010) 839848,
[59] O. Modin, N. Fuad, S. Rauch, Microbial electrochemical recovery of zinc,
Electrochim. Acta 248 (2017) 5863.
[60] C.A. Du Plessis, J.D. Batty, D.W. Dew, Commercial applications of thermophile
bioleaching, Biomining (2007) 5780,
[61] A.D. Bas, H. Deveci, E.Y. Yazici, Bioleaching of copper from low grade scrap TV
circuit boards using mesophilic bacteria, Hydrometallurgy 138 (2013) 6570,
[62] F. Barmettler, C. Castelberg, C. Fabbri, H. Brandl, Microbial mobilization of rare
earth elements (REE) from mineral solidsa mini review, AIMS Microbiol. 2
(2016) 190204,
[63] V.L. Brisson, W.-Q. Zhuang, L. Alvarez-Cohen, Bioleaching of rare earth elements
from monazite sand, Biotechnol. Bioeng. 113 (2016) 339348,
[64] O.A. Desouky, A.A. El-Mougith, W.A. Hassanien, G.S. Awadalla, S.S. Hussien,
Extraction of some strategic elements from thoriumuranium concentrate using
bioproducts of Aspergillus cuum and Pseudomonas aeruginosa, Arab. J. Chem. 9
(2016) S795S805,
[65] H.A. Ibrahim, E.M. El-Sheikh, Bioleaching treatment of Abu Zeneima uraniferous
gibbsite ore material for recovering U, REEs, Al and Zn, Res. J. Chem. Sci. 1
(2011) 55.
[66] D. Shin, J. Kim, B. Kim, J. Jeong, J. Lee, Use of phosphate solubilizing bacteria to
leach rare earth elements from monazite-bearing ore, Minerals 5 (2015) 189202,
[67] Y. Hong, M. Valix, Bioleaching of electronic waste using acidophilic sulfur oxi-
dising bacteria, J. Clean. Prod. 65 (2014) 465472,
[68] F. Beolchini, V. Fonti, A. DellAnno, L. Rocchetti, F. Vegliò, Assessment of bio-
technological strategies for the valorization of metal bearing wastes, Waste
Manag. 32 (2012) 949956,
[69] S. Ilyas, M.A. Anwar, S.B. Niazi, M. Afzal Ghauri, Bioleaching of metals from
electronic scrap by moderately thermophilic acidophilic bacteria,
Hydrometallurgy 88 (2007) 180188,
[70] S. Chen, Y. Yang, C. Liu, F. Dong, B. Liu, Column bioleaching copper and its ki-
netics of waste printed circuit boards (WPCBs) by Acidithiobacillus ferrooxidans,
Chemosphere 141 (2015) 162168,
[71] A. Işıldar, J. van de Vossenberg, E.R. Rene, E.D. van Hullebusch, P.N.L. Lens, Two-
step bioleaching of copper and gold from discarded printed circuit boards (PCB),
Waste Manag. 57 (2016) 149157,
[72] M.I. Muravyov, A.G. Bulaev, V.S. Melamud, T.F. Kondrateva, Leaching of rare
earth elements from coal ashes using acidophilic chemolithotrophic microbial
communities, Microbiology 84 (2015) 194201,
[73] M.D. Machado, E.V. Soares, M.V.M. Helena, H.M.V.M. Soares, Removal of heavy
metals using a brewers yeast strain of Saccharomyces cerevisiae: chemical specia-
tion as a tool in the prediction and improving of treatment efciency of real
electroplating efuents, J. Hazard. Mater. 180 (2010) 347353.
[74] N. Das, D. Das, Recovery of rare earth metals through biosorption: an overview, J.
Rare Earths 31 (2013) 933943.
[75] W. Burgstaller, F. Schinner, Leaching of metals with fungi, J. Biotechnol. 27
(1993) 91116.
[76] G. Natarajan, T. Ramanathan, A. Bharadwaj, Bioleaching of metals from major
hazardous solid wastes, Microbiol. Miner. Met. Mater. Environ. 2025 (2015)
[77] A.H. Kaksonen, B.M. Mudunuru, R. Hackl, The role of microorganisms in gold
processing and recoverya review, Hydrometallurgy 142 (2014) 7083, https://
[78] Y.V. Nancharaiah, S. Venkata Mohan, P.N.L. Lens, Biological and bioelec-
trochemical recovery of critical and scarce metals, Trends Biotechnol. 34 (2016)
[79] V. Diniz, B. Volesky, Biosorption of La, Eu and Yb using sargassum biomass, Water
Res. 39 (2005) 239247.
[80] M.A. Kücüker, J.B. Nadal, K. Kuchta, Comparison between batch and continuous
reactor systems for biosorption of Neodymium (Nd) using microalgae, Int. J. Plant
Anim. Environ. Sci. 6 (2016) XX.
[81] G. Gadd, Biosorption: critical review of scientic rationale, environmental im-
portance and signicance for pollution treatment, J. Chem. Technol. Biotechnol.
84 (2009) 1328.
[82] L. Fairbrother, J. Shapter, J. Brugger, G. Southam, A. Pring, F. Reith, Eect of the
cyanide-producing bacterium Chromobacterium violaceum on ultraat Au surfaces,
Chem. Geol. 265 (2009) 313320,
[83] T. Chi, J. Lee, B.D. Pandey, K. Yoo, J. Jeong, Bioleaching of gold and copper from
waste mobile phone PCBs by using a cyanogenic bacterium, Miner. Eng. 24 (2011)
[84] G. Natarajan, Y.-P. Ting, Gold biorecovery from e-waste: an improved strategy
through spent medium leaching with pH modication, Chemosphere 136 (2015)
[85] G. Natarajan, S.B. Tay, W.S. Yew, Y.P. Ting, Engineered strains enhance gold
biorecovery from electronic scrap, Miner. Eng. 75 (2015) 3237,
[86] K. Deplanche, J.A. Bennett, I.P. Mikheenko, J. Omajali, A.S. Wells, R.E. Meadows,
J. Wood, Catalytic activity of biomass-supported Pd nanoparticles: inuence of the
biological component in catalytic ecacy and potential application in green
synthesis of ne chemicals and pharmaceuticals, Appl. Catal. B: Environ. 147
(2014) 651665.
[87] G. Natarajan, Y.-P. Ting, Pretreatment of e-waste and mutation of alkali-tolerant
cyanogenic bacteria promote gold biorecovery, Bioresour. Technol. 152 (2014)
[88] W.A. Hassanien, O.A. Desouky, A.A. El-Mougith, G.S. Awadalla, S.S. Hussien,
Biosorption of some bioleached rare earth elements from Egyptian monazite using
pretreated Aspergillus cuum and Pseudomonas aeruginosa, J. Bot. 40 (2011)
[89] A. Hussain, A. Hasan, A. Javid, J.I. Qazi, Exploited application of sulfate-reducing
bacteria for concomitant treatment of metallic and non-metallic wastes: a mini
review, 3Biotech 6 (2016) 119.
[90] A. Marra, A. Cesaro, E.R. Rene, V. Belgiorno, P.N.L. Lens, Bioleaching of metals
from WEEE shredding dust, J. Environ. Manag. 210 (2018) 180190, https://doi.
[91] X. Deng, L. Chai, Z. Yang, C. Tang, Y. Wang, Y. Shi, Bioleaching mechanism of
heavy metals in the mixture of contaminated soil and slag by using indigenous
Penicillium chrysogenum strain F1, J. Hazard. Mater. 248249 (2013) 107114,
[92] G.M. Gadd, Metals, minerals and microbes: geomicrobiology and bioremediation,
Microbiology 156 (2010) 609643,
[93] S. De Corte, T. Hennebel, J.P. Fitts, T. Sabbe, V. Biznuk, S. Verschuere, D. van der
Lelie, W. Verstraete, N. Boon, Biosupported bimetallic Pd-Au nanocatalysts for
dechlorination of environmental contaminants, Environ. Sci. Technol. 45 (2011)
[94] H. Brandl, R. Bosshard, M. Wegmann, Computer-munching microbes: metal
leaching from electronic scrap by bacteria and fungi, Hydrometallurgy 59 (2001)
[95] K.A. Natarajan, Biomineralisation and microbially induced beneciation,
Microbiol. Miner. Met. Mater. Environ. (2015) 134.
[96] A.V. Pethkar, S.K. Kulkarni, K.M. Paknikar, Comparative studies on metal bio-
sorption by two strains of Cladosporium cladosporioides, Bioresour. Technol. 80 (3)
(2001) 211215.
[97] S. Ilyas, C. Ruan, H.N. Bhatti, M.A. Ghauri, M.A. Anwar, Column bioleaching of
metals from electronic scrap, Hydrometallurgy 101 (2010) 135140, https://doi.
[98] M. Oguchi, H. Sakanakura, A. Terazono, H. Takigami, Fate of metals contained in
waste electrical and electronic equipment in a municipal waste treatment process,
Waste Manag. 32 (2012) 96103,
[99] T. Pumpel, L.E. Macaskie, J.A. Finlay, L. Diels, M. Tsezos, Nickel removal from
nickel plating waste water using a biologically active moving-bed sand lter,
Biometals 16 (2003) 567581.
[100] S.A. Waksman, J.S. Joe, Microörganisms concerned in the oxidation of sulfur in
the soil, J. Bacteriol. 7 (1922) 239256,
[101] P.A.H.M. Bakker, C.M.J. Pieterse, L.C. van Loon, Induced systemic resistance by
uorescent Pseudomonas spp, Phytopathology 97 (2007) 239243, https://doi.
[102] C.J. Knowles, Microorganisms and cyanide, Bacteriol. Rev. 40 (1976) 652680.
[103] P.A. Castric, Glycine metabolism by Pseudomonas aeruginosa: hydrogen cyanide
biosynthesis, J. Bacteriol. 130 (1977) 826831.
[104] C. Blumer, D. Haas, Mechanism, regulation, and ecological role of bacterial cya-
nide biosynthesis, Arch. Microbiol. 173 (2000) 170177,
A. Işıldar et al. Journal of Hazardous Materials 362 (2019) 467–481