Review

Received: 6 May 2013 Revised: 24 June 2013 Accepted article published: 1 July 2013 Published online in Wiley Online Library: 31 July 2013

(wileyonlinelibrary.com) DOI 10.1002/jctb.4164

Biohydrometallurgy of secondary metal

resources: a potential alternative approach for
metal recovery
Ceren Erüst,a Ata Akcil,a∗ Chandra Sekhar Gahan,a Aysenur Tuncuka and
Haci Devecib
Abstract
Research on biohydrometallurgy of secondary metal resources is primarily focused on the leaching of valuable metals.
For secondary metal resources biological processing can be an economically more effective and environmentally friendlier
alternative to traditional hydrometallurgical and pyrometallurgical processes. Therefore, biohydrometallurgy is a rapidly
evolving biotechnology that has already provided revolutionary solutions to old problems associated with recovery of metals
by conventional pyrometallurgy and chemical metallurgy. This review evaluates various processes of recovery of metals from
waste materials and commercial applications are discussed. Case studies and future technology directions are reviewed.

c 2013 Society of Chemical Industry

Keywords: biohydrometallurgy; metal recovery; recycling; secondary metal resources

INTRODUCTION biobeneficiation.24 Recycling of secondary raw materials is critical

Rapid increase in the generation of waste materials together
with the rising global population and expansion of industrial
applications with improved technologies has motivated research
and development to focus on waste recycling. The main thrust
has been an evaluation of waste materials for the recovery of
their metal values together with stabilization of toxic elements
present in them by proper waste management strategies for
environmental safety. Several options have been tested until now
with regards to the scope of waste management. In recent years,
novel approaches to the recovery of metal values from municipal
and industrial wastes have shown promise.1 – 16 Microorganisms
are well known to solubilize mineral matrices by lixiviant
generation (e.g. Fe3+ and/or H+ ).8,17 – 22 Biohydrometallurgy
encompasses two related microbial processes that are useful
in extractive metallurgy such as bioleaching and biooxidation.23
Bioleaching is microbial mediated leaching of the metal of interest
either from its respective ores or concentrates or wastes; in contrast
biooxidation processes do not leach the metal of interest but
pretreats the feed material by oxidizing the mineral matrix and
liberates the metals of interest, making them amenable to leaching
easily in a further step of chemical leaching. In the bioleaching
process, microorganisms play a role in converting insoluble
metal sulphides (zinc, copper, nickel, cobalt) or oxides (uranium)
into water-soluble metal sulphates, whereas in the biooxidation
process, mostly applied on refractory gold concentrates, the role
of the microorganisms is to oxidize the pyrite and arsenopyrite
mineral matrix exposing the entrapped gold for further cyanide
leaching. Furthermore, microbial desulphurization of coal also
comes under the process of biooxidation, where pyrite in coal
is oxidized to form soluble ferric ion and sulphate ion into
solution thereby cleaning the coal from gangue minerals (iron
not only to supplement the secured supply of metals and materials
thereby reducing the demand on the limited natural/mineral
resources, but also to reduce the environmental degradation due
to disposal. With the success of bio-hydrometallurgical processes
for copper, gold, nickel and uranium on large scale by heap/dump
and bioreactor (STR/CSTR) leaching, extraction of valuable metals
from the secondary resources with the aid of microbial action
has gained attention in the past few decades. Considerable
efforts have been made to develop processes for bioleaching
of wastes and by-products generated from metallurgical and
industrial processes and manmade resources. As the metal content
in many of these solid wastes is in the form of inorganic
sulphides/oxides or pure metals and sometimes as organic metallic
complexes, where the metal of interest can be solubilized either
by autoptrophic or heterotrophic microorganisms provided with
a suitable energy source.25 Autotrophic microorganisms such as
bacteria (e.g. Acidithiobacilli sp.) and Archaea (e.g. Ferroplasma sp.);
heterotrophic microorganism such as bacteria (e.g. Pseudomonas
sp., Bacillus sp.) and fungi (e.g. Aspergillus sp., Penicillium spp.)
are the major groups of microbes involved in bioleaching of
metals.26 The ability of these microbes to solubilize metals from
∗
Correspondence to: A. Akcil, Department of Mining Engineering, Mineral
Processing Division (Mineral-Metal Recovery and Recycling Research
Group), Suleyman Demirel University, TR32260, Isparta, Turkey. Email:
ataakcil@sdu.edu.tr
a Department of Mining Engineering, Mineral Processing Division (Mineral-
Metal Recovery and Recycling Research Group), Suleyman Demirel University,
TR32260, Isparta, Turkey
b Mineral Processing Division, Department of Mining Engineering, Karadeniz
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and inorganic sulphur) and the complete process is called as Technical University, TR61080, Trabzon, Turkey

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secondary raw materials especially in extremely acidic metal-rich
environments, has accelerated the growth of biohydrometallurgy.
Metals that are present in different types of waste streams,
including mine drainage, industrial waste sludge and filter dust,
marine sediments, medical waste, electronic scraps and fly ashes
are also available for recovery and utilization.
BIOHYDROMETALLURGICAL PROCESSES
Biohydrometallurgical processes which utilize microorganisms
for the extraction of metals from ores/concentrates/wastes are
regarded as one of the most promising and revolutionary
biotechnological breakthrough with regards to mineral processing
and metallurgy. The products of such processes are dissolved
metal ion species in aqueous solution which are more
amenable to containment, treatment and recovery. Additionally,
biohydrometallurgy can be conducted under mild conditions,
usually without the use of any toxic chemicals.27 Chemical leaching
is a rapid and efficient process but can create environmental
problems. Biological leaching on the other hand is a cost effective
technique by comparison, but slow.28 Biohydrometallurgy is
sometimes utilized together with pyro and hydrometallurgical
procedures of metal recovery. Biohydrometallurgical methods
for mineral extraction and processing together with biologically
mediated remediation require less energy and have the advantage
of being environmentally benign owing to less or no emission of
toxic gases and chemicals.27,29 – 33 Bioleaching is a microbiological
dissolution process in which microorganisms mobilize metals from
a solid material such as a mineral, an ore, or a solid waste.8,18,34 – 36
A generalized reaction can be used to describe the biological
oxidation of a mineral involved in leaching:
MS + 2O2 → M2+ + SO2−
4
where M is the bivalent metal that is solubilized from the mineral
by the action of microbial metabolites. Until now, a widely studied
bioleaching process has been the microbial solubilization of metal
sulphides.37
Autotrophic bioleaching processes facilitating mineral bio-
oxidation and bioleaching are defined in terms of the contact
mechanism, the non-contact mechanism and the cooperative
mechanism. In the contact mechanism, the bacterial cells attach
with the aid of extracellular polymeric substances (EPS) layer
to the mineral surfaces, resulting in dissolution of the sulphide
minerals at the interface by an electrochemical process involving
bacterial catalysis (redox enzymes at the cell surface) gaining
energy from ferrous and sulphur oxidation process. In the
non-contact mechanism the ferric iron, produced through bio-
oxidation of ferrous iron comes in contact with the mineral
surfaces, oxidize the sulphide mineral and releases ferrous
iron back into the cycle. While, in the cooperative mechanism
planktonic iron and sulphur oxidizers oxidizes colloidal sulphur,
other sulphur intermediates and ferrous iron in the leaching
solution, releasing protons and ferric iron which are then used
in non-contact leaching.38 Biohydrometallurgical operations use
microorganisms to accelerate the dissolution of metals from
oxidic and sulphidic mineral ores/concentrates.24 Microorganisms
require energy to sustain their growth. The energy required for
their metabolic functions is obtained from either the metabolism
of organic compounds or the oxidation of inorganic compounds
and/or elements depending on the type of microorganisms.
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When acidiophilic, autotrophic bacteria are involved, ferrous iron,
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C Erüst et al.
reduced sulphur compounds, or mineral sulphides can serve as
energy sources.39 The metal solubilization by chemolithotrophic
acidophiles from sulphidic/oxidic minerals is assisted by ferric
ion generated from microbial ferrous iron oxidation and partly
by sulphuric acid produced due to microbial sulphur oxidation.
Several chemical reactions pathways controlling the microbially
mediated leaching of sulphide minerals are as follows:
O2 /CO2 (g) → O2 /CO2 (aq) (2)
Fe2+ + 1/4 O2 + H+ → Fe3+ + 1/2 H2 O (3)
S0 + 1.5O2 + H2 O → 2H+ + SO2−
4 (4)
MeS + Fe3+ → Me2+ + Fe2+ + S0 (5)
+
FeS2 + 6Fe3+ + 3H2 O → 7Fe2+ + S2 O2−
3 + 6H (6)
3 + 8Fe
S2 O2− 3+
+ 5 H2 O → 2SO2−
4 + 8Fe
2+
+ 10H+ (7)
+
FeS2 + 7O2 + H2 O → Fe2+ + 2SO2−
4 + 2H (8)
Equation (2) describes the absorption of atmospheric O2 and CO2
by the aqueous phase. This is important because all the reactions
involved in bioleaching occur in the aqueous phase. Equations (3)
(1) and (4) show the microbial oxidation of ferrous iron and sulphur
species respectively, while Equation (5) shows the oxidative
dissolution of the metal sulphide by biologically produced ferric
iron (Equation (3)). The series of chemical reactions given in
Equations (6)–(8) explains the oxidation pathway of pyrite mineral
by ferric iron resulting with thiosulphate and ferrous iron as
intermediates (Equation (6)). The ferrous iron produced is further
oxidized by microbes (Equation (3)), while the thiosulphate is
oxidized to sulphates by the ferric iron (Equation (7)). This thio-
sulphate can also be oxidized into sulphate by sulphur oxidizing
microorganisms and finally the overall reaction based on the
primary oxidant (O2 ) could be as stated in Equation (8). Dissolution
of the metal sulphides is controlled by two different reaction
pathways, i.e. the thiosulphate pathway and the polysulphide
pathway. The thiosulphate pathway applies only to the acid
insoluble metal sulphides such as pyrite (FeS2 ), molybdenite
(MoS2 ) and tungstenite (WS2 ). The thiosulphate pathway that
occurs in the bioleaching of pyrite is described by Equations (6)
and (7), which are combined in the following overall equation:
FeS2 + 14Fe3+ + 8H2 O → 2SO2−
4 + 15Fe
2+
+ 16H+ (9)
The main role of the microorganisms in this mechanism is
to catalyse the regeneration of the consumed ferric iron by
oxidizing the ferrous iron in the presence of oxygen (O2 ) and
proton (H+ ) as shown in Equation (3). The overall reaction based
on the primary oxidant oxygen as shown in Equation (8). The
polysulphide pathway is applicable to the oxidation of acid-soluble
sulphides like galena (PbS), sphalerite (ZnS), arsenopyrite (FeAsS)
and chalcopyrite (CuFeS2 ). The polysulphide pathway followed
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Biohydrometallurgy of secondary metal resources
during zinc sulphide bioleaching is represented by Equations (10)
and (11).
8ZnS + 14Fe3+ + 2H+ → 8Zn2+ + 14 Fe2+ + H2 S8 (10)
H2 S8 + 2Fe3+ → S8 + 2Fe2+ + 2H+ (11)
The role of the microorganisms in this reaction consists of two
steps. The first step catalyses the regeneration of the ferric ions
(Equation (3)) to oxidize intermediate hydrogen sulphide into
elemental sulphur forming polysulphides (Equation (11)) followed
by second step, where catalysis of sulphuric acid generation
(Equation (12)) occurs to meet the proton requirement to dissolve
the metal sulphides. Additional reactions that occur are as follows:
+ thermoferrooxidans
S8 + 12O2 + 8H2 O → 8SO2−
4 + 16H (12)
The overall reaction derived based on the primary oxidant oxygen
is pH neutral as shown in Equation (14).
ZnS + 2O2 → Zn2+ + SO2− (14)
4
However, it should be noted that the maintenance of efficient
bioleaching of sulphide minerals requires elevated or high rate
ferrous oxidation.40,11,41 Investigations by Torma42,43 have shown
that the following non-iron metal sulfides can be oxidized by
microorganisms in the absence of soluble iron, albeit at a
remarkably slow rate: covellite (CuS), chalcocite (Cu2 S), sphalerite
(ZnS), galena (PbS), molybdenite (MoS2 ), stibnite (Sb2 S3 ), cobaltite
(CoS), millerite (NiS). These microbial oxidations are easily
demonstrated, but the microbial metabolism and growth can
be negatively affected by dissolved metal ions which then limit
the bioleaching process efficiency.27,44 – 47
Heterotrophic microorganisms (bacteria and fungi) are also
known to mobilize metals from minerals, ores, and some solid
wastes, in this instance with the help of organic acids produced as
end-products of their energy metabolism. The organic acids may
originate from the oxidation of glucose or other carbohydrates,
under aerobic or anaerobic conditions, depending on the
microorganism. These organic acids are well known for metal
dissolution by the protonation and complexation/chelation of the
minerals into soluble organo-metallic complexes.48 Microbially
produced ligands comprising of 2-ketogluconic acid, gluconic acid,
citric acid, oxalic, humic acid, etc. are well known for their potential
to dissolve silicates and oxides from the mineral matrix.49 – 58 A few
heterotrophic microbes are also well known to dissolve alumino-
silicate minerals, in which the silicon is surrounded by four oxygen
atoms in tetrahedral fashion59 and aluminium with oxygen in
tetrahedral/octahedral fashion, depending upon the mineral.60 In
the alumino-silicate minerals, these units are arranged in bi- or
tri-layers separated by water layers of variable thickness, through
which polar molecules, including organic acids attack on the Si–O
bonds of silloxanes linkages (Si–O–Si) and as the aluminosilicates
are very strong with weaker Al–O bonds. Therefore, Si–O
bonds are relatively resistant to acid hydrolysis,61 unlike Al–O
bonds. Some bacteria and fungi are known to solubilize silicates
with the help of exo-polysaccharides together with organic
acids.62,58 Heterotrophic bioleaching processes operating with the
generation of organic and inorganic acids by fungal and bacterial
strains may be carried out in two stages in an industrial process.
In the first stage, the microorganisms are allowed to grow in an
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Table 1. Different types of microorganisms actively involved in
bioleaching
Moderate
Mesophiles thermophiles Thermophiles
Acidithiobacillus Acidimicrobium Sulfolobus metallicus
ferrooxidans ferroxidans
Acidithiobacillus Acidithiobacillus Sulphobacillus sp.
thiooxidans caldus
Acidithiobacillus Sulphobacillus ther- Metallosphaera
caldus mosulphooxidans sedula
Leptospirillum
ferrooxidans
Leptospirillum
ferrodiazotrophum
Leptospirillum
Leptospirillum
ferriphilum
adequate growth medium under appropriate cultural conditions
to produce primary and secondary metabolites, which include
the chemical agents that have the ability to promote leaching of
minerals. In the second stage, spent culture medium from the first
stage is brought in contact with the mineral in the absence of the
microorganisms from the first stage for the purpose of leaching
the mineral. This process results in enhanced metal recovery.
Operation of the leaching process in two stages with an absence
in the second stage of the organisms that generate the leaching
agent is often advantageous over leaching in the presence of the
organism in a single stage. The reason for use of fungal metabolites
without fungus is as follows: first, as there is no energy source in
the ore unlike autotrophic organism there is no point trying to
leach in the presence of organisms; second, the growth of fungus
with the residual carbohydrate present in the growth medium
would allow growth of mycelia mat in the ore; third, there would
be another step to be added to remove the mycelia from the ore
which complicates the process; fourth, there would be no benefit
using live organisms growing in an ore.63,47
Microorganisms
The mineral sulphide oxidizing microorganisms are acidophilic
prokaryotes. Their growth is optimal in the pH range 1.5–2.5.
They are autotrophic in nature as they use inorganic carbon (CO2 )
as carbon source. They are strictly chemolithotrophic, i.e. derive
energy for growth and other metabolic functions from oxidation
of ferrous iron, reduced sulphur compounds, metal sulphides and
some species also derive energy from the oxidation of hydrogen
sulfide. They are classified into three groups such as mesophiles
(20–40◦ C), moderate thermophiles (40–60◦ C), and thermophiles
(60–80◦ C), based on the temperature requirements for optimal
growth (Table 1).
In a stirred tank reactor the acidophilic species vary from one type
of concentrate to another depending upon the species tolerant
in the specific ore/concentrate (data reported from commercial
application), for details see Table 2.
The most widely reported mesophilic iron oxidizer dominating in
continuous stirred tank reactors is L. ferrooxidans but in some cases,
Leptospirillum ferriphilum dominates.65,64,67 The cause for the dom-
inance of L. ferriphilum over L. ferrooxidans is due to its faster iron
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oxidation ability and tolerance of slightly elevated temperatures.68
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Table 2. Acidophiles in mineral sulphide concentrate processing at different temperatures64

Mineral
concentrate Temperature (◦ C) Major types in populations

Pyrite/arsenopyritea 40 Leptospirillum ferrooxidans Acidithiobacillus thiooxidans At. ferrooxidans (10-17%)

(48-57%) /At. caldus (26-34%)
Mixed sulphidesb 45 At. caldus (65%) L. ferrooxidans (29%) Sulfobacillus sp. (6%)
Nickel concentratec 49 At. caldus (63%) Acidimicrobium sp. (32%) Sulfobacillus sp. (6%)
55 Sulfobacillus sp. (93%) At. caldus (5%) Acidimicrobium sp. (2%)
Chalcopyrited 75-78 ‘‘Sulfolobus’’ sp. (59%) Metallosphaera sp. (1) (34%) Metallosphaera sp. (2) (5%)
a Fairview and São Bento industrial plants.65
b Mintek pilot plant.66
c
Warwick University laboratory scale (Cleaver and Norris unpublished data).
d
Warwick University laboratory scale, HIOX culture (Norris unpublished data).
(The estimated proportions of species refer to continuous cultures and to primary reactors where several were in series).

The mesophiles actively involved in biooxidation and bioleaching Acidithiobacillus caldus

are Acidithiobacillus ferrooxidans, Acidithiobacillus thiooxidans and
Acidithiobacillus caldus, Leptospirillum ferrooxidans, Leptospirillum
ferrodiazotrophum, Leptospirillum thermoferrooxidans and Lep-
tospirillum ferriphilum, the moderately thermophiles are Acidimi-
crobium ferroxidans, Acidithiobacillus caldus and Sulphobacillus
thermosulphooxidans, while the thermophiles are Sulfolobus metal-
licus, Sulphobacillus sp. and Metallosphaera sedula. Characteristics
features of some of the important microorganisms are given below.
Genus Acidithiobacillus
This genus is representative of the γ -subdivision of proteobacteria
and the type species is Acidithiobacillus thiooxidans (formerly
Thiobacillus thiooxidans). They are gram negative, rod shaped
bacteria with a size of approximately 0.4 × 2 µm. They are motile
having one or more flagella as the locomotory organelle. Some
of the species are mesophilic having optimum growth at a
temperature 30–35◦ C, while some are moderately thermophilic
having optimum growth at a temperature of 45◦ C. The G + C
content of the DNA is 52–64 mol%. The most important
species of the genus Acidithiobacillus involved in bioleaching
and biooxidation processes are Acidithiobacillus ferrooxidans,
Acidithiobacillus thiooxidans and Acidithiobacillus caldus.69
Acidithiobacillus ferrooxidans
Acidithiobacillus ferrooxidans is a gram negative rod shaped
bacterium, acidophilic by nature and obligately chemolithotrophic
for nutrition. It grows with ferrous iron as the sole energy substrate
by oxidation of the ferrous iron. The optimum pH for growth is 2.5
and the optimum temperature range for growth is 30–35◦ C. The
G + C content of the DNA is 58–59 mol%.70
Acidithiobacillus thiooxidans
Acidithiobacillus thiooxidans is motile and has a polar flagellum
as the locomotory organelle. It derives energy solely through
oxidation of reduced sulphur compounds, cannot oxidize iron or
pyrite but has been able to grow on sulphur from pyrite in co-
culture with Leptospirillum ferrooxidans, which is an iron oxidizing
bacterium. They are gram negative rod shaped bacteria acidophilic
by nature and obligately chemolithotrophic for nutrition. The
optimal pH for growth is 2–3 and the temperature range for
optimal growth is between 28 and 30◦ C. The G + C content of the
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Acidithiobacillus caldus is a gram negative, motile bacterium,
having a pH optimum for growth of 2–2.5 and an optimum growth
temperature of 45◦ C. It is classified as moderate thermophile. It
is chemolithotrophic and grows on reduced sulphur substrates.
It can also use molecular hydrogen as electron donor. The G + C
content of this species is 63.1–63.9 mol%.72
Genus Leptospirillum
It is gram negative, aerobic and motile by means of a single
polar flagellum. Cells are vibrioid to spirilla shaped and sometimes
they can form into cocci or pseudococci shapes. These bacterial
cells measure 0.2–0.6 by 0.9–3.5 µm and have optimum growth
at a pH of 1.3–4.0. Some of the species of Leptospirillum are
either mesophilic or moderately thermophilic and their maximum
temperature ranges up to 55◦ C. It is chemoautotrophic and grows
on iron substrate, but cannot oxidize sulphur or thiosulphate. The
G + C content of the DNA is 50–57 mol%.73 The different types
of species of Leptospirillum involved in metal sulphide oxidation
are Leptospirillum ferrooxidans, Leptospirillum ferrodiazotrophum,
Leptospirillum thermoferrooxidans and Leptospirillum ferriphilum.74
Leptospirillum ferrooxidans
Leptospirillum ferrooxidans is a gram negative, acidophilic, aerobic,
small curved rod shaped bacteria of size 0.3–0.6 by 1.0–3.3 µm.
They are motile by means of a single polar flagellum. The pH range
for their ambient growth ranges from 2.5–3.0. It can only oxidize
ferrous iron to derive energy for their growth. The G + C content
of the DNA is 51.7 mol%.74
Leptospirillum thermoferrooxidans
Leptospirillum thermoferrooxidans is a moderately thermophilic
species with an optimum growth temperature of 45 to 50◦ C
(maximum, 55 to 60◦ C). The G + C content of the DNA is 56% and
has 27% similarity with the DNA of the mesophiles.75
Bioleaching by mesophilic bacteria
The bioleaching mesophiles belong to the genus Acidithiobacillus,
which includes the iron and sulphur oxidizing At. ferrooxidans,
the sulphur oxidizing At. thiooxidans and the iron-oxidizing
L. ferrooxidans and L. ferriphilum.76 These bacteria are usually
regarded as mesophilic with their ability to grow at 40◦ C or less.

DNA is 52 mol%.71 At. ferrooxidans is endowed with a remarkably broad metabolic

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capacity. These species thrive on the oxidation of reduced sulphur
compounds and, in addition, are able to oxidize iron(II) ions.
Anaerobic growth is possible by oxidation of sulphur compounds
or hydrogen sulphide coupled with iron(III) reduction.77 – 79,38
Bioleaching by moderately thermophilic bacteria
Moderately thermophilic microoganisms consist of the genera
Acidimicrobium, Ferromicrobium, and Sulfobacillus.80 Ferromicro-
bium acidophilus is an obligatory mixotrophic iron(II)-oxidizing
bacterium.81 Sulfobacillus spp. show poor chemolithotrophic
growth, as is the case with many thermophilic Sulfolobales.80
A mixed culture of moderate thermophiles has been found to
be successful in biomining. Microbial species of Acidimicrobium
and Sulfobacillus have always appeared to be the principal iron
oxidizing microorgansim, while the Acidithiobacillus caldus has
been the principal sulphur oxidizing microbe. Optimum growth
appears to occur at an operating temperature of 50◦ C but effective
bioleaching has been achieved at temperatures up to 55◦ C.82
Bioleaching by extremely thermophilic bacteria
Archaea that leach metals have been known for many years. All
belong to the Sulfolobales, a group of extremely thermophilic
sulphur and iron oxidizers including genera such as Sulfolobus,
Acidianus, Metallosphaera and Sulfurisphaera.83 Extremely ther-
mophilic bacteria growing at temperatures above 60◦ C were
first isolated by Brierley and Brierley,84 Karavaiko et al.61 Acidi-
anus brierleyi, formerly associated with the genus Sulfolobus,85
is a chemolithoautotrophic, facultatively aerobic, extremely aci-
dophilic Archaeon growing on ferrous iron, elemental sulphur and
metal sulfides. Under anaerobic conditions elemental sulphur is
used as an electron acceptor and is reduced to H2 S.18 The ther-
mophiles adapted to sulphide mineral leaching are Sulfolobus-like
archaea. Two cultures have been successfully adapted to copper
and nickel sulphide mineral leaching, a 68◦ C culture, operating in
the range 65◦ C–70◦ C, and a 78◦ C culture, operating in the range
75◦ C–85◦ C. The 68◦ C culture, isolated by Billiton Process Research,
is most probably of the type Sulfolobus metallicus. The 78◦ C culture
has not been fully characterized. It was provided by by Paul Norris,
University of Warwick, UK.82 Members of the genus Sulfolobus
are aerobic, facultatively chemolithotrophic bacteria oxidizing
ferrous iron, elemental sulphur and sulfide minerals. The same
compounds are used as energy source by Sulfobacillus thermosul-
fidooxidans, a spore-forming facultatively autotrophic bacterium.
Growth, however, will only occur in the presence of yeast extract.18
Bioleaching of metals by fungi
Some species of heterotrophic microorganisms, such as Aspergillus
and Penicillium, have shown potential for metal bioleaching. Metal
leaching by heterotrophic microorganisms generally involves
an indirect process with microbial production of amino acids,
other organic acids, and other metabolites. These metabolites
dissolve metals from minerals by displacement of metal ion from
the ore or soil matrix by hydrogen ions, or by the formation
of soluble metal complexes and chelates. The most important
species of fungi capable of bioleaching are Aspergillus niger (A.
niger) and Penicillium simplicissimum because of their ability to
excrete abundant amounts of organic acids.86 A. niger is one of
the most widely used fungi in bioleaching. The fungus has been
used commercially in the production of organic acids, such as
citric acid,87 oxalic acid88 and gluconic acid.89 These acids are well
known lixiviants for the leaching of heavy metals from ore materials
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and solid wastes,90 and may reduce the cost of commercial heavy
metal decontamination and decrease any environmental impacts
resulting from metal contamination.91,63 A. niger has been found
to overproduce organic acids that can serve as leaching agents
for the solubilization of Al, Fe, Mn, Ni, Pb, Cd, Cu, and Zn from
secondary raw materials.92
SECONDARY RAW MATERIALS
Bacterial leaching can be an economical alternative in metal recov-
ery from ores in place of conventional treatments used by the min-
ing industry. Microorganisms can also be exploited in the recovery
of metals from mine drainage, industrial effluents, solid waste incin-
eration (MSWI) fly ash, spent catalysts, waste sludge, contaminated
sediments, medical waste and electronic scrap, etc.30,93
E-waste
Demand for electrical–electronic equipments (EEE) has rapidly
increased in recent years resulting in large-scale production
and consumption. The annual sales of mobile phones were
estimated to be 1.2 billion in 2009, while the sales of computers
have tended to increase annually by ∼10%.94 The rapid
advancement in the technology of electronic devices with lucrative
benefits has resulted in a decrease in the life-span of most
electrical–electronic equipments including mobile phones and
PCBs. End-of-life equipments/materials including those broken
or obsolete (computers, televisions, printed circuit boards etc.)
become waste for disposal. These wastes of electrical–electronic
devices are collectively known as ‘E-waste (WEEE)’. Annually 20 to
50 million metric tonnes of WEEE were estimated to be discarded
in the world.95 WEEE is also one of the most rapidly growing
waste streams in Europe. Up to 25–30 kg of end-of-life WEEE
per household was estimated to be generated annually in Europe
where end-of-life electronics constitute about 5% of the total waste
stream.96 Tonnage of electronic waste generation has increased
2 to 3 times faster than other wastes.97,98 Only a small fraction
of electronic waste is recycled and the remaining fraction is
disposed of at landfills without any pretreatment.99,100 The data on
e-waste generation amassed by the United States Environmental
Protection Agency (US-EPA) indicates that approximately 500
million computers were discarded annually between the years
2000 and 2007. Two million tons of them ended up among the
trash in landfills, whereas only 400 thousand tons were recycled
successfully.98 The Natural Resources Defense Council estimated
that 0.13 million computers were discarded with 1 million cell
phones in the year 2006.101 Turkey, which has a population of 73
million people, is one of the largest consumers of EEE in Europe.
Based on the GDP data, in Turkey, the generation of WEEE per
person is estimated to be 4 kg, which is expected to increase
with the economic growth of the country. Currently, WEEE is not
properly managed in Turkey since the collection/recycling rate is
too low, i.e. only 1% of the total WEEE generation. Therefore, it
is imperative to develop recycling projects to increase the public
awareness and to increase the collection rates to manage an
ever-increasing stream of WEEE in Turkey.102 – 104
It has been well known that both the electronic and electrical
waste generated contains a lot of non-degradable materials
mostly hazardous by nature.105 – 107 Recycling of electronic scrap
is important for two reasons: (i) recovery of valuable metals
(i.e. precious metals, in particular); and (ii) protection of the
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environment from accumulation of toxic or heavy metals in
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the soil or earth crust.108 – 111 Wide utilization of electronic and
electrical products in education, communication, health care and
transportation has revolutionized modern science and technology
with innovations contributing social progress.112 Studies on
electrical and electronic wastes suggest rapid increase in this
particular waste.113 – 115 Most of the electronic scrap generated
from used electronic products derives from discarded television
sets, telephones, computers, etc.
Landfilling of electronic waste is reaching its limits resulting as
a temporary measure due to their non-degradable nature. Most
of the developed and developing countries around the world
have implemented strict legislation for landfills with respect to
non-degradable materials especially electronic wastes. Recycling
of electrical and electronic wastes is now an emerging research
area mostly for Japan, Korea, China and European countries.
Considering the fate of electronic wastes together with the
stricter legislations in place, land filling will no longer be an
option. End of life management of these products in a safe and
environmentally friendly manner would be the only alternative
that could be implemented. Recycling through pyro- and hydro-
processes have been successful in recovering valuable metals from
electronic waste. However, the recycling companies are still in
their developmental stage and do not have adequate technology,
processes, techniques and models to treat this huge volume of
electronic scrap produced. Recycling companies in cooperation
with manufacturing companies are continuously working on
the recycling and management of electronic wastes. However,
electronic scrap recycling is limited for its material heterogeneity
and requirement for complex processes and equipments.116
Among electronic wastes, printed circuit boards have quite
diverse composition, containing metals, ceramics and polymers.
The metal content in electronic scrap limits to 28–30% among
which major metals comprise of 10–20%, Cu; 1–5%, Pb; 1–3%, Ni
and 0.3–0.4%, Ag, Au and Pt. E-waste contains many organic and
inorganic substances with most of them being hazardous by nature
such as Hg, Pd, etc. (inorganic) and chlorinated/brominated flame
retardants (organic). Due to the toxic nature of these substances,
the disposal of electronic wastes together with municipal wastes
causes major environmental problems in a landfill. The main
source of heavy-metal pollution (Hg and Pb in particular) in
municipal landfills originates from the e-wastes. On the other
hand, electronic wastes can be regarded as a potential secondary
resource with respect to the content of base and precious metals
values present in them. Printed circuit board, which is an essential
part of electronic devices, contains high levels of metals. The
printed circuit (wiring) board of a PC contains about 20% Cu
(200 kg/ton) and 0.025% Au (250 g/ton), which are high, i.e.
25 to 250-fold for gold and 20 to 40-fold for copper when
compared with gold ores (∼1–10 g/ton Au) and copper ores
(∼0.5–1% Cu), respectively. However, the economic potential of
electronic wastes as a secondary resource is yet to be exploited.
The other materials present include 19% plastics, 4% Br, 4–9%
glass and ceramics. Several organic compounds like phenolic
resins, isocyanates, phosgene and acrylic are also found in circuit
boards.117 Printed circuits used in all kinds of electronic devices,
starting from simple transistor amplifiers to super computers are
of different shapes and sizes. Some of them are integrated circuits,
while some are bare and can be recycled by different methods.
Mechanical and pyrometallurgical processing of electronic waste
as a means of recycling has been widely investigated by several
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researchers,118 – 120 but as yet these processes are inefficient in
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precious metal recovery and are energy intensive and produce
toxic dioxins and furans.36,121
Considering the environmental and economic issues, the
European Commision (EC) has implemented a WEEE Directive,
which imposes some responsibilities on producers and local
authorities to manage E-waste by arranging collection centres
and recycling electrical-electronic devices. Recently, the Ministry
of Environment and Forestry of Turkey has prepared a directive in
compliance with WEEE Directive of the EC. The transfer of state-of-
art knowledge and experience from EU member states to Turkey
as a candidate country will aid the development and successful
implementation of WEEE regulations in these countries for the
management of WEEE streams. WEEE Directive of the EC sets a
collection target of at least 4 kg per inhabitant, while the real
estimate of collection ended up to be 6 kg per inhabitant, which is
easily achievable depending on public awareness. In Turkey, only
less than 1% of end-of-life WEEE is currently collected for recycling
and the balance ends up in disposal sites and landfills with
severe risk of associated environmental problems and ‘wastage’
of metal-rich resources.122 Turkey can benefit from knowledge
and experience of the EU to establish collection infrastructure and
facilities properly, to increase the public awareness and to achieve
high collection rates. This will serve to achieve the environmental
sustainability and efficient exploitation of secondary resources
within Europe.
Waste of electric and electronic equipment is non-
homogeneous and complex in terms of materials and components.
In order to develop a cost-effective and environmentally friendly
recycling system, it is important to identify and quantify
valuable materials and hazardous substances to understand the
physical characteristics of this waste stream. For the recycling of
valuable metals from e-scrap by biohydrometallurgical methods,
a mechanical pre-treatment step is required. The different
components and devices can be selectively dismantled and
separated into various fractions such as metals (iron, copper,
aluminum, magnesium, etc.), plastics, ceramics, paper, wood and
devices such as capacitors, batteries, picture tubes, LCDs, and
circuit boards. These components can be re-used or directed
to specific recycling process. In this process manual dismantling
would be used to separate/collect metal-bearing components
such as circuit boards. Thereafter, shredders and hammer mills
will be used to separate, fragment, grind, rip or tear the E-
waste. The extent of size reduction depends on the recovery
process targeted. In this regard, many studies reported that almost
complete liberation of copper from computer and circuit board
scrap could be achieved at a particle size of <2 mm and poor
liberation at coarser fractions, which is due to the association of
copper pins with plastics together with encapsulation of copper
wire within plastics. Milled samples can be thoroughly mixed to
achieve homogeneity at a size fraction less than 0.5 mm. A variety
of physical separation methods including magnetic separation,
optical sorting and gravity separation can be used to test the
valuable metal contents (i.e. Cu, precious metals and REMs in
particular) in the WEEE and reduce the bulk of the material for
further processing. This process would help to evaluate the losses
of valuable metals of practical importance. Figure 1 shows the
e-waste species occurring in the European Union in 2005.
Following the mechanical treatment, bioleaching process
can be used for the metal recovery from the high metal
content complex/heterogenous WEEE. Recovery of copper
and other base metals from e-waste can be achieved by
using acidophilic microorganisms to generate leaching lixiviant.
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Biohydrometallurgy of secondary metal resources
Figure 1. Distribution of electrical and electronic waste in EU in 2005.125
Biohydrometallurgical processes can be optimized by controlling
the important parameters such as pH, temperature, growth media
composition, oxygen and carbon dioxide content, etc. together
with other parameters like toxic elements present in the WEEE
and acid/base consumption. The details of the studies on rapidly
evolving technology to combat negative effects of e-waste are
summarized in Table 3.
SPENT BATTERIES
Utilization and management of spent batteries have also of been
growing environmental concern with regard to their disposal.
Considering the high cost for safe disposal of spent batteries and
limited storage capacity of landfills and/or dumpsites, strategies
need to be developed for reutilization and recycling of hazardous
waste such as spent batteries. If the feed materials for battery pro-
duction could be replaced by the recycled metal contents from the
spent batteries, the cost of battery production could be reduced
and made economical together with presevation of virgin raw
materials and protection from environmental hazards.227,144 – 148
The European Union (EU) Battery Directive Extended Impact
Assessment149 reported that each year, approximately 800 000
metric tonnes of automotive batteries, 190 000 metric tonnes of
industrial batteries and 160 000 metric tonnes of portable batteries
are placed on the community market. The total weight of portable
batteries sold in the East and West Europe in 2003 was about
164,000 metric tonnes, of which 50, 197 and 99, 138 metric tonnes
were zinc-carbon and alkaline batteries, respectively (30.5% and
60.3% of the total annual sales).150 The collection rate on average
is currently 13.6% for the EU, whereas the target was 25% in
2012.151 At present, the collection, treatment and recycling of
waste batteries in Europe is not carried out effectively as only six
of the 25 EU countries have collection systems for spent batteries.
Belgium collects 59% of all spent batteries, Sweden 55%, Austria
44%, Germany 39%, the Netherlands 32%, and France 16%. Almost
half of all portable batteries sold in the EU-15 Member States in
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2002 were eventually incinerated or disposed of in landfills.152 – 154
A total of 26 928 and 26 940 metric tonnes of alkaline, zinc-
carbon and zinc-air batteries were recycled in 2006 and 2007,
respectively, by European Battery Recycling Association (EBRA)
members.151 One of the aims of this review is to evaluate the
recovery studies and associated technologies for metals from
spent batteries. Special attention was paid to the recovery of Zn,
Mn, Li, Co, Ni and Cd from spent nickel–cadmium batteries, lithium
ion batteries, alkaline and zinc–carbon batteries.
In Turkey, the Directive for Controlling Spent Batteries and
Accumulators is compatible with the EU directive and is currently
effective in regulating the import, utilization, collection, disposal
and recycling of batteries and accumulators. Currently, there are
no major treatment facilities for recovery of contained values
from spent batteries in Turkey although a total of 13 companies
have already received accumulator recovery licences. In Turkey,
annually about 10 000 metric tonnes of portable batteries are
consumed. Given that there are over 30 million mobile phone
users with an average battery life of 2 years, approximately 900
metric tonnes of spent batteries of mobile phones accumulate in
the waste stream.155 However, the spent batteries are generally not
separately collected in Turkey; thus, they are landfilled in municipal
landfills with other solid waste (only about 2% of spent batteries
have been separately collected at source within collection points).
Spent batteries cannot be disposed of together with other solid
waste and need to be recycled by several existing methods. On the
other hand, recycling of precious metals by hydrometallurgical
and biohydrometallurgical methods has been very effective, as
shown in several reports (Table 4).
Hydrometallurgical methods are being applied to recover
valuable metals from waste spent batteries. Bioleaching of spent
batteries is also another alternative method for extraction of
metals in an economical and environmentally friendly process. Its
principle is the microbial production of ferric iron and sulfuric acid
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aiding the oxidation and leaching of metals.
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Table 3. R&D work on bioleaching of e-waste
Source of waste Microbe used
Waste PCB Acidithiobacillus ferrooxidans and
Acidithiobacillus thiooxidans
Aspergillus niger and Penicillium
simplicissimum
Acidithiobacillus ferrooxidans
Chromobacterium violaceum
Desulfovibrio desulphuricans
S. thermosulfidooxidans and Acidophilic
heterotroph
C.violaceum, Pseudomonas fluorescens and
Pseudomonas plecoglossicida
Acidithiobacillus ferrooxidans
Thiobacillus ferrooxidans and Thiobacillus
thiooxidans
Thiobacillus ferrooxidans and Thiobacillus
thiooxidans
Acidithiobacillus sp. and Leptospirillum sp.
S.thermosulfido-oxidans and Thermoplasma
acidophilum
Acidithiobacillus sp., Gallionella sp. and
Leptospirillum spp.
Acidithiobacillus ferrooxidans
Mixed culture of acidophilic bacteria
Chromobacterium violaceum
E-waste Chromobacterium violaceum, Pseudomonas
aeruginosa and Pseudomonas fluorescens
Printed wire boards Acidithiobacillus ferrooxidans,
Acidithiobacillus thiooxidans and mixed
culture
Acidithiobacillus ferrooxidans
Waste mobile phone PCBs Chromobacterium violaceum
Chromobacterium violaceum
Bioleaching has been characterized by efficient release of metals
from solid phase into aqueous solution under mild conditions of
room temperature and pressure by contact and/or non-contact
mechanisms in the presence of acidophilic sulphur-oxidizing
and/or iron-oxidizing bacteria.38 In recent years, utilization of
bioleaching for recovery of valuable metals Co, Li, Ni, Cd from
spent nickel–cadmium batteries and lithium ion batteries (LIBs)
has drawn growing attention.156 – 158,162 – 164 There have been a
few reports on bioleaching of spent Zn–Mn batteries for recovery
of valuable metals Zn and Mn.166 For practical application of
bioleaching, the pulp density, i.e. the ratio of the solid material to
bioleaching media, was a very important parameter which greatly
affected the operational cost and subsequent separation.167
The use of LIBs has rapidly increased because, they are widely
used as electrochemical power sources in mobile telephones,
personal computers, video-cameras and other modern-life
appliances.168,169 They not only dominate the cellular phones
and laptop computer areas, but also will be the first category of
dynamic batteries to be chosen for electric-powered automobiles
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in the future because of their characteristics of light weight,
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Recovery and conditions Reference
Al, Cu, Ni, Zn-90% at 0.5–10g L-1 pulp density, 7 126
and 10 d
Metal recovery-%100 at 100 g L-1 pulp density by 126
gluconic acid
Cu-%37 with 7 g L-1 Fe(II) and 80% citric acid 127
Au-14.9% in 7d at a low pulp density 128
High recovery of Au as powder and Pb-95% at 5 129
pH from nitrate liquor
Cu-89%, Ni-81%, Zn-83%, Al-79% at 10 g L-1 pulp 99
density in 18days
Au-68.5 in 7d 130
Cu-%98 in 24 h, 6.66 g L-1 Fe(III) at 1.5pH with 131
100% inocula: Cu-%72 without inocula
Cu-99.5% pH 2.5 and 200 mm bed height at flow 132
rate of 2 mL min-1 9 d in D401
Cu-97.45% after copper extraction was carried out 133
using 10% N902 diluted in kerosene at O/A ratio
of 1:1
Cu and Ni-100% in 42d at 10 g L-1 pulp density, 1.5 134
pH in 4.5 g L-1 Fe(II) + 10 g L-1 S0
Cu-86%, Ni-74%, Zn-80%, Al-64% in acid pre-leach 135
(27d) and for 280d in column rector
Cu-95% after 5 d in the presence of initial pH 1.5, 9 136
g L-1 of initial Fe2+, and 20 g L-1 pulp density
Cu-63%, a rotary shaker under the following fixed 137
conditions (185 rpm, 30◦ C)
Cu-96.8% in 45 h, Al-88.2% and Zn-91.6% in 98 h at 138
pH 2.00, 12 g L-1 initial Fe(II)
Au-11% in 8d at pH 11.0 in presence of 4.0 × 103 139
mol L-1 MgSO 4
more than Cu-83%, Au-73%, Zn-49%, Fe-13%, and 140
Ag-8% at pH 7.2 (150 rpm, 30◦ C)
Cu-99-99.9% with mixed culture at 7.8 g L-1 pulp 141
density in 9d; Cu, Pb and Zn-88.9% in 5d
Cu-96.36%, in 48 h 142
Au-13% and Cu-37% in 8d at 100g L-1 pulp density 143
Au-11.31% at pH 10, Cu-24.6% at pH 11.0 in 8d 143
high energy and good performance.170,171 LIBs are increasingly
replacing other batteries. In 2000, the worldwide production of
LIBs reached about 500 millions cells. From this consumption, LIB
waste is annually estimated at 200–500 MT, with a metal content
of 5–15 wt% Co and 2–7 wt% Li.172
Recycling of LIBs has become increasingly important because
their safe disposal may become a serious problem due to the pres-
ence of flammable and toxic elements or compounds even though
spent LIBs are not generally classified as dangerous waste.173,174
At the same time some economic benefit could be achieved from
recovery of major components of LIBs.175 Bioleaching methods
for the extraction of cobalt and lithium from spent LIBs containing
LiCoO2 were explored, employing acidophilic chemolithotrophic
Acidithiobacillus ferrooxidans, which uses elemental sulphur and
ferrous iron as energy sources, respectively, for the production
of sulfuric acid and ferric iron as leaching agents.162 Application
of such a bioleaching method in the treatment of LIBs yielded
favorable results. The bacteria were able to grow in medium
containing elemental sulphur and iron as energy sources. The
sulfuric acid they produced was able to leach the metals from
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Table 4. R&D work on bioleaching of spent batteries

Number of Stirring Temperature

Type Microbe used microbe used Time rate (rpm) (◦ C) pH Solid/liquid Recovery (%) Reference

Ni-Cd Acidithiobacillus 5.0 × 107 cells/mL 93d 180 30 2.0 1/100 Cd-100%, Ni-96.5%, 156
ferrooxidans Fe-95%
Acidithiobacillus 4.6 × 107 cells/mL 6d 200 30 2.0 1/5 Cu-96.1%, Zn-94.6%, 157
ferrooxidans and Cd-81.7%,
Acidithiobacillus Ni-71.6%,Cr-61.5%,
thiooxidans Pb-48.5%
Sulfobacillus sp. 50d 180 30 3.0 1/100 Cd-100%, Ni-75% 157
Acidithiobacillus sp. 40d 200 27-30 2.0 1/100 Ni-96%, Cd-90% 158
Acidithiobacillus 30d 150 30 2.0 1/5 Ni-100%, Co-100%, 159
ferrooxidans and Cd-99%
Acidithiobacillus
thiooxidans
Acidithiobacillus 28d 120 30 1.5 1/100 Cd-100% 160
ferrooxidans
NiMH Acidithiobacillus 20d 120 30 1.0 1/100 Ni-95.7%, Co-72.4%, 161
ferrooxidans and Li-10%
Acidithiobacillus
thiooxidans
Li-ion Acidithiobacillus 3.2 × 107 cells/ml 6d 200 30 2.5 1/100 Co-65% 162
ferrooxidans
Acidithiobacillus 5d 120 30 1.0 1/100 Co-90%, Li-80% 163
ferrooxidans and
Acidithiobacillus
thiooxidans
Alicyclobacillus sp.and 12d 120 30 5.5 1/20 Zn-96%, Mn-60% 164
Sulfobacillus sp.
Acidithiobacillus 2.1 × 106 cells/ml 6d 160 35 3 1/20 Co-99.9% 165
ferrooxidans
Zn-Mn Alicyclobacillus sp. and 12d 120 30 5.5 1/20 Zn-100%, Mn-94% 166
Sulfobacillus sp.
Alicyclobacillus sp.and Zn-1d, Mn-7d 120 30 5.5 1/20 Zn-96%, Mn-60% 167
Sulfobacillus sp.

LIBs. Cobalt was leached faster than lithium, demonstrated by
EDAX mapping. The Fe(II) in the medium used in the leaching
experiments was to aid the growth of At. ferrooxidans. The higher
the Fe(II) concentration, the slower the metal dissolution. The
Fe(III) ion formed during the course of the investigation was
found to precipitate with the metals in the leach residues. Higher
solid/liquid ratios prevented bacterial activity in the process as
higher metal concentrations are toxic to the organism.176
SPENT CATALYSTS
Among these wastes are spent hydro-processing catalysts
generated from oil refineries, which are a valuable source rich
in metals such as Al, V, Mo, Ni and Fe. Spent petroleum catalysts
constitute a significant amount of the solid waste generated
by chemical and petrochemical industries. The amount of spent
catalysts generated is 150.000–170.000 tons per year.177 Most of
the metals used as catalysts are in an oxide form, and in some
cases, they are reduced to active metals to catalyze the appropriate
reactions needed for the process. The catalysts normally become
inactive after multiple and extensive use due to the deposition of
organic materials, such as benzene, toluene and other impurities,
and are considered hazardous material by the US Environmental
Protection Agency because of the difficulty of disposal due to
the presence of Ni, Mo, V, Co, Pt, and Pd.178 The main causes of
transformation, which cannot be easily reactivated by replacement
of fresh catalysts.179 Chemical and petrochemical industries have
started to reuse huge amounts of solid catalysts instead of land
filling after several cycles of regeneration. Some of these spent
catalysts are also being classified as hazardous waste despite being
rich in metal content, because they contain significant amounts of
heavy metals, which are a possible environmental hazard if buried
in a landfill without prior treatment.
Recycling of the spent catalysts before land filling would prevent
mobilization of metals into the environment. Several methods
to treat spent catalysts are available.180 Bioleaching of spent
petroleum catalysts is one of the emerging research applications
in biohydrometallurgy, on which a great deal of research has been
done, but which has not yet been practically applied. Various
options to regenerate or dispose of spent catalysts may involve
decoking, and selective leaching of Ni, V, and Fe, which may require
different reagents. Leaching of all metals from the spent catalysts
may be achieved if disposal is required and it is economically
feasible. The solid wastes must be encapsulated or stabilized
before final disposal to meet environmental standards. The spent
catalysts used in oil refinery treatments are at times recycled using
porous materials, such as alumina and silica, through precipitation
or impregnation processes.181
Hydrometallurgical and pyrometallurgical techniques have
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the petroleum spent catalysts.182 – 184 Even though pyrometal-
lurgical techniques are considered an advantageous technology
overall, the reluctance to use pyrotechnology is because it is an
energy-intensive process with toxic gas emissions. Considering
the pitfalls of pyrometallurgical techniques, research on the spent
catalysts has examined various hydrometallurgical techniques,
but industries are reluctant to embrace pure chemical leaching
because of the use of strong acids.178,185 Industrial application of
bioleaching has dealt mainly with chemolithotrophic autotrophs,
particularly mesophiles and thermophiles.186 Several studies have
reported using mesophilic iron and sulphur oxidizers for the dis-
solution of spent catalysts with a high yield of metal values.187 – 193
The spent catalyst from manufacture of sulfuric acid production
with 3.5% V, 0.63% Ni, 7.9% Fe and 9.64% Si was used for extraction
of Ni and V by alkaline and acidic leaching. Statistical design of the
experiments and ANOVA (analysis of variance) were performed
in order to determine the main effects and interactions of the
factors such as roasting, leaching temperature, concentration of
the leaching reagent (H2 SO4 and NaOH). Acidic leaching resulted in
96% Ni and 59% V recovery, when the spent catalyst were roasted
at 400–600◦ C prior to leaching. However the V recovery could be
enhanced to 78% by alkali leaching of the roasted spent catalyst
using NaoH at 80◦ C in 2 h.194 Bioleaching of spent catalysts rich in
Ni, V and Mo using iron/sulphur oxidizing bacteria by addition of
both S0 and Fe(II), with studies of possible toxicity, revealed that
addition of Fe(II) ion resulted in higher recovery of 83%, 90% and
∼35% for Ni, V and Mo, respectively. The reason for low recovery of
Mo could be possibly due to less liberation of Mo from the organic
entrapment of the spent catalyst. Dissolution kinetics of nickel
and vanadium was often significantly faster than molybdenum
as molybdenum may have been encapsulated in the unliberated
mineral matrix.195 In another study of bioleaching of spent catalyst,
a two-stage process was used. The first stage involved the growing
of sulphur-oxidizing organisms (At. thiooxidans and At. caldus) in
an inorganic S0 medium to produce adequate amounts of sulfuric
acid. In the second stage, the acid produced in the first stage was
used to leach the spent catalyst. The variable parameters chosen
for study were the reaction time, pulp density, content of S0 and
temperature. The results obtained showed that at 50 g of spent
catalyst per L and 20 g elemental sulphur per L, the recoveries of Ni,
Mo and V were 88.3%, 46.3% and 94.8%, respectively, in a reaction
time of 7 days. The results obtained were compared with chemical
leaching using sulfuric acid. The leaching mechanism was found
to be diffusion controlled. It was assumed that low recovery of Mo
was due to precipitation of Mo as MoO3 confirmed by EDAX and
XRD analysis of the bioleach residue.163 Bioleaching of petroleum
catalyst using Acidithiobacillus ferrooxidans and Acidithiobacillus
thiooxidans showed that the dissolution kinetics of Mo was lower
than those of V and Ni. The lower dissolution kinetics may have
been due to the formation of a sulphur product layer or the
refractory nature of MoS2 or both.196 The influence of temperature
on the rate of bioleaching of the mineral values has been well
studied. The results show that the relationship of microbial activity
to temperature with respect to the oxidation by sulphur and
ferrous iron proceeds as defined by the Ratkowsky and Arrhenius
equations. The results obtained provided the definition of the
temperature operating windows, to a precision not observed in the
past, for the majority of species that are frequently encountered as
the biological catalysts in tank and heap bioleaching operations.197
Many studies carried out on bioleaching were conventional
treatment, in which catalysts (Ni/Mo/P/Al2 O3 ) were physically
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and chemically characterized. Biotic leaching with autotrophic
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Acidithiobacillus ferrooxidans and Acidithiobacillus thiooxidans
involves Fe(III) as the oxidant, and H ions. Biotic leaching by
Aspergillus niger and Penicillium simplicissimum involves organic
acids produced by these fungi as the leaching agents. To study
abiotic leaching, reagent-grade organic acids such as citric, oxalic,
and gluconic acids were used to compare with the results from
heterotrophic leaching. Reagent-grade sulfuric acid and ferric
chloride were used as leaching agents for a comparison with
autotrophic leaching. Results showed that the surface area of fresh
catalyst was 23% higher than the spent catalyst, but during the
bioleaching of spent catalyst by Acidithiobacillus thiooxidans and
Acidithiobacillus ferrooxidans the surface area increased by 17%
and 33%, respectively. Toxicity characteristic leaching procedure
(TCLP) tests were conducted on the residues obtained from
bioleaching and chemical leaching to determine if the residue
obeyed the toxic limit set by United States-Environmental Protec-
tion Agency (US-EPA). The tests conducted on spent catalyst (feed
material before bioleaching/chemical leaching) showed that the
Ni content exceeded environmental limit set by US-EPA, but was
found to be within the toxic limit after bioleaching. Autotrophic
bioleaching conducted with Acidithiobacillus thiooxidans was
found to be promising with highest recovery of 29.3% Al, 64.5%
Mo and 99.8% Ni. More importantly, bacterial leaching was much
faster (15–20 days) compared with fungal leaching (45–50 days).
Compared with abiotic controls, bioleaching was better in metal
extraction from the spent catalyst.198
An attempt to mobilize Al Co, Mo and Ni from the spent catalyst
obtained from an Iranian oil refinery in batch bioleaching using
Acidithiobacillus ferrooxidans showed that addition of Fe(II) source
into the growth medium at pH 1.8–2.0 resulted in maximum
extractions of 63% Al, 96% Co, 84% Mo and 99% Ni in 30 days.
On the other hand bioleaching carried out using Acidithiobacillus
thiooxidans with addition of sulphur source to the growth medium
at pH 3.9–4.4 resulted in maximum extractions of 2.4% Al, 83%
Co, 95% Mo and 16% Ni in 30 days.199 Some other studies also
support the bioleaching of Ni, V and Mo from spent catalyst to
an extent of 83%, 90% and 40%, respectively, using Fe/S-oxidizing
microorganisms in a Fe(II) supplemented growth medium.200,201
Special cases where bioleaching of spent catalyst was carried out
using only sulphur oxidizers in a two-stage process, in which the
first stage was used to produce the acid via sulphur oxidation
by growing the S-oxidizers in sulphur supplemented growth
medium. In the second stage, the acid medium generated in
the first stage was used for leaching the spent catalyst. The result
obtained suggests that leaching kinetics followed successively two
different rates, the first being rapid, and the second being slower
as equilibrium was approached over a period of 7 days. First-order
rate kinetics was followed. However, the rate determining step was
found to be diffusion controlled. Overall leaching of Ni and V was
greater compared with Mo due to the formation of an impervious
layer by elemental sulphur and its refractory nature.202
Some studies have evaluated the recovery of metals from
a coal liquefaction catalyst that contains NiMo/Al2 O3 using
At. ferrooxidans, Sulfolobus and thermophilic Archaeal species.
Studies on spent vanadium phosphorus catalyst and spent
petroleum catalyst with acidophilic iron and sulphur oxidizing
microorganisms to extract metal values, such as Ni, V and Mo
have been discussed in depth in previous articles.7 A few studies
also reported on the bioleaching of spent catalyst using fungal
strains, but the operation of such a process in commercial-scale
reactors would be very costly because of the need for sterilization
of medium and equipment to prevent growth of contaminant
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Biohydrometallurgy of secondary metal resources
fungi and bacteria. If sterilization is not done many other fungi and
bacteria would consume the sugar in the medium outcompeting
the original fungi used for bioleaching, preventing the production
of the lixiviant. Large quantities of solid catalysts are routinely used
in many chemical industries especially in petroleum refining and
petrochemical industries.
Solid catalysts contain metals, metal oxides or sulfides, and
require replacement after 2 or 3 years of operation. Therefore,
large quantities of spent catalysts are generated as solid wastes
every year. Because of their hazardous nature and toxic chem-
ical products, there are stringent environmental regulations for
discarded spent catalysts. The recovery of metals from these cat-
alysts is also an important economic aspect as most of these
catalysts are supported, usually on alumina/silica with different
percentages of metal. Biohydrometallurgical approaches are more
economical and environmentally friendly than physicochemical
metal-extraction processes from spent catalysts.203 Applied biohy-
drometallurgical methods and recovery rates are given in Table 5.
CONTAMINATED SEDIMENTS
Contaminated sediments constitute a reservoir of organic
contaminants derived from anthropogenic activity. The problem
of contaminated sediment is especially important in shipping
ports and harbours, where the sediment needs to be dredged
periodically to increase the water depth.215 Beolchini et al.216
recovered >90% Cu, Cd, Hg and Zn with Fe-reducing bacteria and
Fe/S oxidizing bacteria from contaminated dredged sediments.
However, heavy-metal extraction yields ranged from 40–50%
both in the bioleaching treatment based on the bioaugmentation
of Fe/S oxidizing strains alone, and Fe-reducing bacteria alone
(data not shown). These results suggest that the two strains could
cooperate through a mutual substrate supply. The presence of
Fe-reducing bacteria and Fe/S oxidizing bacteria could solve the
problem of sulphur availability.217
Efficient microbial dissolution of valuable metals such as Cu, Co,
Ni, Mn and Fe has been achieved from ocean manganese nodules in
the presence of pyrite and reducing agents. Heavy metal leaching
from anaerobic sludge using pyrite as energy source has also been
reported.218 It has been reported that iron and sulphur oxidizing
bacteria solubilized more than 90% of Zn, Ni, Cu, and Cr from
river sediments at an optimum temperature of 37◦ C.93 At high
temperature, pH changes would have prevented initiation of the
indirect mechanism. Some components of river sediments have
been found to play a significant role in the bioleaching of metals
from contaminated sediments. The quantity of solids determines
the size of the bioreactor and the duration of the reaction.219,220
In spite of extensive studies on the bioleaching of ocean
manganese nodules, the method has yet to be demonstrated
and commercialized on a pilot or industrial scale.
Diaz et al.221 evaluated nickel and cobalt recoveries from
tailings from the Caron process using sulphuric acid produced by
Acidithiobacillus thiooxidans cultures under different conditions.
They reported that high nickel and cobalt recoveries (about 60%
for cobalt and 85–100% for nickel) were reached after 13 days
when low pulp densities (1% and 2.5%) of laterite tailings were
used. However, they observed negligible metal recoveries when
higher pulp densities were used. Ndlovu et al. treated nickel
laterites with analytical grade H2 SO4 acid, citric acid and acidified
Fe2 (SO4 )3 on a preliminary study to investigate the possibilities
of chemolithotrophic acidophilic bioleaching. Results obtained
from the preliminary study showed that H2 SO4 acid performed
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c 2013 Society of Chemical Industry
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better, in terms of nickel recovery, than citric acid or acidified
Fe2 (SO4 )3 . Bioleaching of lateritic nickel using mixed culture of At.
ferrooxidans, At. caldus and L. ferrooxidans in the presence of S0
and FeS2 showed that the S0 substrate exhibited better effects for
bacterial growth, acidification and Ni recovery compared with FeS2
substrate. Using response surface methodology, a maximum Ni
recovery of 79.8% was obtained at theoretical optimum conditions
of initial pH 2.0, 63 µm particle size and 2.6% pulp density.222
Solid waste incineration (MSWI) fly ash
The municipal solid waste incineration (MSWI) fly ash is classified
as a kind of hazardous waste because of the high quantities
of leachable toxic heavy metals. Therefore, it is necessary to
remove the heavy metals from fly ash before entering controlled
landfills or reuse.223,131 A study of metal leaching from fly ash was
undertaken by Tateda et al.224 with a Thiobacillus sp. strain (TM-32).
The application of a mixed culture of sulphur- and iron-oxidizing
bacteria in the presence of 2–5 g sulphur per L showed almost
complete leaching (100%) of Cr and Cd , and high recovery of
Cu (67%) and Zn (78%) at 10 g L-1 pulp density. This process
could be utilized practically as the preliminary treatment before
landfilling. The application, as in situ landfill technology, could be
more attractive for the recovery of metals while reducing the risk
of environmental pollution. The results to date suggest that the
bioleaching process for MSWI fly ash is a promising technology.6
Another study has dealt with leaching by the thermophilic archeon
Acidianusbrieleyi of zinc from fly ash resulting from municipal waste
incineration. Konishi et al. determined that over 90% leaching of
zinc was achieved after 9 days at 65◦ C.225 Some studies on this
subject are listed in Table 6.
STRATEGIES AND FUTURE
RECOMMENDATIONS
Biohydrometallurgy has been gaining in importance among
the available mining technologies. It has proved to be a
promising technology with economic and environment friendly
advantages with enhanced recovery of base metals, precious
metals and rare earth elements (REEs) from secondary oxides,
sulphides as well as waste materials. Presently many large-
scale bioleaching operations have been operational in both
developed and developing countries. Biohydromellurgy can be
regarded as a rapidly evolving technology. It has revolutionized
metal extraction as an alternative method, which can overcome
problems associated with conventional pyrometallurgy and
chemical hydrometallurgy in the recovery of metal. The application
of biohydrometallurgy is mainly concentrated in a small number
of countries, but has vast potential in developing countries. For
the sake of sustainable mining practices and environmental
protection, there is a strong need for both developed and
developing countries to come forward and adopt emerging
biohydrometallurgy technology. This technology would enable
operating more sustainable mining operations with the focus
on enhanced and optimized metal recovery in combination with
minimized environmental impact.
SUMMARY
Rapid depletion of primary metal resources such as oxidic and
sulphidic minerals processed by conventional pyrometallurgi-
2125
cal/hydrometallurgical operations have created opportunities for
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Table 5. R&D work on bioleaching of spent catalysts

Number of Stirring Temp.

Type Microbe used microbe used Time rate (rpm) (0 C) pH Solid/ Liquid Conditions Recovery (%) Reference
7 −1
Spent refinery Aspergillus niger 1 × 10 spores mL 70d 120 30 3.0 1% MES Buffer (pH:6) Mo–82.3%, Ni–58.2%, 7
catalyst Al–54.5%
Aspergillus niger 1 × 107 spores mL−1 30d 120 30 2.8 1% MES Buffer (pH:6), Mo–82.3%, Ni–78.5%, 204
deionized water Al–65.2%
(pH:6.8), organic

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acid
Acidithiobacillus thiooxidans 6.1 × 109 cells mL−1 7d 180 32 ± 0.5 1.8–2 10 g L−1 S0 V–94.8%, Ni–88.3%, 188
Mo–46.3%
Mixed Acidophilic culture 7d 180 32 ± 1 2.0 10% V–92%, Ni–85%, Mo–26% 205
bacteria
Acidithiobacillus ferrooxidans 1 × 108 cells mL−1 40h 180 35 2.0 10% 2 g L−1 Fe(II) and 10 g V–48%, Ni–45%, Mo–10% 206
and Acidithiobacillus L−1 S0
thiooxidans
Mixed culture of three strains 21d 175 30 2.0 V–90%, Ni–83% 195
Fe/S oxidizing bacteria

Acidithiobacillus ferrooxidans 30d 150 30 2.5 200 g/L Particle size 150µm Ni–99%, Co–96%, Mo–84%, 207
Al–63%
Acidithiobacillus ferrooxidans 5d 180 35 2.5(IOB), 10% 2 g L−1 Fe(II) for IOB, V–90%, Ni–90%, Mo–43% 196
and Acidithiobacillus 2.0(SOB) 10 g/L S0
thiooxidans
Acidithiobacillus ferrooxidans 5.6 × 107 cells mL−1 30d 166 40 1.5 1.5 g L−1 Fe(II) Co–91%, Ni–90%, Mo–84%, 199
particle size 80µm Al–56%
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Aspergillus niger 30d 115 31 5.0 1–12% %12 inoculum Mo–69%, Co–71%, Ni–46% 208
Acidithiobacillus 4.5 × 108 cells mL−1 21d 175 30 2.0 1% 8.88 g/L Fe(II) and 5 g V–90%, Ni–83% and 201
ferrooxidans, L−1 S0 Mo–40%
Acidithiobacillus
thiooxidans and

c 2013 Society of Chemical Industry

Leptospirillum ferrooxidans
Aspergillus niger 1 × 107 spores mL−1 30d 110–160 30 7.0 3% particle size Mo–99.5 ± 0.4%, Ni–45.8 209
150–212µm, ±1.2%, Al–13.9 ± 0.1%
sucrose 93.8 g L−1
Acidithiobacillus ferrooxidans 1 × 108 cells mL−1 1h 35 2.0 10% Two step leaching Mo–99%, Ni–97%, V–97% 210
Spent Aspergillus niger 43d 120 30 3.0 1% Sb–64%, V–36%, Al–30%, 5
hydrocracking Fe–23%, Ni–9%
catalyst
Aspergillus niger 43d 120 30 2.5 1% Particle size 45µm Ni–88%, Mo–87%, 211
Al–17.2%
Penicillium simplicissimum 15d 120 30 ± 1 4–6 1–5% W–100%, Fe–100%, 212
Mo–92.7%, Ni–66.43%,
Al–25%
Penicillium simplicissimum 1 × 107 spores mL−1 5d 110–160 30 5–9 3.95% %10.9 inhibitor Mo–98.8 ± 0.9%, 213
Ni–46.5 ± 0.6%,
Al–13.7 ± 0.4
Acidianus brierleyi 24d 125 80 2.0 1% two-step leaching Ni–98.7%, Mo–98.4%, 214
Fe–90.3%

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Biohydrometallurgy of secondary metal resources
Table 6. Bio-processing of fly ash of municipal solid waste (MSW) incinerators
Source of waste Microbe used
Fly ash of MSW Mixed culture of At. thiooxidans
Thiobacillus sp. strain TM-32
A. thiooxidans, A. ferrooxidans, (mixed culture of S
and iron oxidizing bacterium)
Pseudomonas putida
Aspergillus niger
processing secondary metal resources such as secondary sul-
phides/oxides together with waste materials with cost effective
and eco-friendly processes. Huge demand for base metals, pre-
cious metals and rare earths mostly by developing countries
especially China, India and Brazil together with Europe has moti-
vated researchers to discover an alternative technology to recover
metal from waste materials. This effort is likely to result in large
commercial and environmental benefits for developing countries
when waste materials are included for metal production. The
recycling of waste materials starting with electrical and electronic
scrap together with spent batteries and spent catalyst using biohy-
drometallurgical techniques has so far been at the level of research
and development. It needs scale-up to the pilot plant state to prove
its potential for full-scale operation. Future mining will be mostly
dependent on waste materials for two important reasons; first
to protect the Earth from serious environmental pollution, and
second, to meet the demand for metals for infrastructure develop-
ment and other human pursuits. This review summarizes in some
detail recent biohydrometallurgical developments and suggests
possible routes via both proven technological developments and
full-scale operations for processing different solid waste mate-
rials such as WEEE, spent batteries, spent catalysts, sediments,
MSWI, etc. Several problems that have arisen in biohydrometallur-
gical operations are also highlighted with possible solutions for
improvement. Future processes need to be developed considering
both microbiology and hydrometallurgical engineering with suit-
able process parameters for more success in biohydrometallurgical
processing of secondary waste. This will generate many full-scale
operations for metal recovery from waste materials/secondary
metal resources using biohydrometallurgy. As a huge amount
of funding has been mobilized for research and development
in waste materials/secondary metal resources recycling by gov-
ernment agencies and industry, some realistic developments can
be expected in the near future. These developments will help
to meet the global metal demand by most developing countries
and developed countries. There are a number of problems associ-
ated with recycling of waste materials/secondary metal resources,
and solutions to a few of the problems have been well defined
and those remaining will be sorted out soon. Today, several
industries and government organizations have started various pro-
grammes to promote waste materials/secondary metal resources
recycling for environmental benefits and metal production. Bio-
hydrometallurgy can be one of the potential technologies for
recycling waste materials/secondary metal resources for future
extractive metallurgy. Technological advancement in waste mate-
rials/secondary metal resources recycling would help industries
meet their demand for raw material for metal extraction and
protect the environment from hazardous waste pollution.
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Leaching efficiency (%) and conditions References
Cu, Cd, Zn -80%, Al-60%, Ni, Fe-30% in 2–3 weeks 226
Cu-57–85%, Cd-53–68.5%, Zn-39–56.4%, 224
Pb-2–19.6%
Cu-67%, Zn-78%, Cr and Cd-100% at 10 g L-1 PD in 6
presence of 2–5 g L-1 S
Cd, Ni, Zn-60–80% in batch culture with 200 g L-1 36
pulp density
Cd-96%, Mn-91%, Pb-73%, Zn-68%, Cr-35%, 141
Fe-30% in 20 days
ACKNOWLEDGEMENTS
The authors express their sincere gratitude to the Research Projects
Coordination Unit of the Suleyman Demirel University (project
no: BAP 3604-YL2-13 and project no: BAP 3605-YL2-13). The
authors Ata Akcil and Chandra Sekhar Gahan also acknowledge the
financial support from ‘The Scientific and Technological Research
Council of Turkey (TUBITAK), Co-funded by Marie Curie Actions
under FP7’.
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