Journal of Environmental Management 211 (2018) 138e153

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Journal of Environmental Management

journal homepage: www.elsevier.com/locate/jenvman

Research article

Biotechnology in the management and resource recovery from metal

bearing solid wastes: Recent advances
Manivannan Sethurajan a, c, *, Eric D. van Hullebusch b, c, Yarlagadda V. Nancharaiah a, d
a
Biofouling and Biofilm Processes Section, Water and Steam Chemistry Division, Bhabha Atomic Research Centre, Kalpakkam 603102, India
b
Universit

e Paris-Est, Laboratoire G

eomat

eriaux et Environnement (LGE), EA 4508, UPEM, 77454 Marne-la-Vall

ee, France
c
Department of Environmental Engineering and Water Technology, IHE Delft Institute for Water Education, Westvest 7, 2611 AX Delft, The Netherlands
d
Homi Bhabha National Institute, Anushakti Nagar Complex, Mumbai, 400 094, India

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

Article history: Solid metalliferous wastes (sludges, dusts, residues, slags, red mud and tailing wastes) originating from
Received 6 September 2017 ferrous and non-ferrous metallurgical industries are a serious environmental threat, when waste man-
Received in revised form agement practices are not properly followed. Metalliferous wastes generated by metallurgical industries
7 January 2018
are promising resources for biotechnological extraction of metals. These wastes still contain significant
Accepted 10 January 2018
amounts of valuable non-ferrous metals, sometimes precious metals and also rare earth elements.
Elemental composition and mineralogy of the metallurgical wastes is dependent on the nature of mining
site and composition of primary ores mined. Most of the metalliferous wastes are oxidized in nature and
Keywords:
Metallurgical wastes
contain less/no reduced sulfidic minerals (which can be quite well processed by biohydrometallurgy).
Secondary resources However, application of biohydrometallurgy is more challenging while extracting metals from metal-
Bio-hydrometallurgy lurgical wastes that contain oxide minerals. In this review, origin, elemental composition and mineralogy
Metal recovery of the metallurgical solid wastes are presented. Various bio-hydrometallurgical processes that can be
Metal-microbe interactions considered for the extraction of non-ferrous metals from metal bearing solid wastes are reviewed.
© 2018 Elsevier Ltd. All rights reserved.

1. Introduction release of metals to the environment is a serious threat. There have

Of late, demand for non-ferrous metals such as Al, Cu and Zn has
been increasing significantly. The metals are produced by metal-
lurgical industries from naturally occurring primary ores. However,
the metallurgical industries generate considerable quantities of
different types of solid wastes at each and every step of metallur-
gical unit operation (Lottermoser, 2010). According to EU estimates,
the wastes generated from mining and quarrying industries play a
big contribution (>50%) to the total wastes generated in Europe
(European Union statistics, 2012).
These metal bearing wastes are either stock piled in specially
built storage dams or disposed in the environment without proper
containment (Fig. 1). Storage of metallurgical wastes in the storage
dams is a common practice. However, failure of the dams and
* Corresponding author. Department of Environmental Engineering and Water
Technology, IHE Delft Institute for Water Education, Westvest 7, 2611 AX Delft, The
Netherlands.
E-mail addresses: m.sethurajan@un-ihe.org, biotek_mani@yahoo.co.in
(M. Sethurajan).
been instances of leakage and accidental collapses of several dams
(Ajka (Hungary), 2010; Bento Rodrigues (Brazil), 2015) in the recent
past (Ruyters et al., 2011; Segura et al., 2016). Such release of metals
was linked to harmful adverse effects on the environment
(Clemente et al., 2003; Hilson and Monhemius, 2006) (Fig. 1). In the
environment, metals can be mobilized from wastes by biological
agents and by natural processes like erosion aided by wind and
water is referred as weathering. Natural weathering enhances the
release of toxic metals into the environment, thus can contaminate
the water resources (Keith et al., 2001; Giere
et al., 2003; Kachur
et al., 2003; Kierczak et al., 2009; Johnson, 2009) (Fig. 1). Gradual
depletion of high grade metal reserves is another important issue to
be addressed (Anjum et al., 2012). Designing economic and eco-
friendly ways to remediate, recover and recycle metals from
metal bearing wastes would not only help in environmental pro-
tection but also allow sustainable resource management. One way
to combat environmental pollution is to implement sustainable
resource management. Though, these are considered as wastes but
they still contain significant quantities of metals. Wastes that
contain significant metal concentration needs to be considered as
secondary resources. Green and environmental friendly processes

https://doi.org/10.1016/j.jenvman.2018.01.035
0301-4797/© 2018 Elsevier Ltd. All rights reserved.
 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153 139

Fig. 1. Overview of mining and metallurgical operations, generation of metallurgical wastes and the problems associated with the disposal of metallurgical wastes.

must be developed to recover metals from these solid wastes. This
approach not only decrease the amount of waste to be disposed of
but also prevent release of metals into the environment.
1.1. Metallurgical wastes as secondary resource for metals
High grade primary ores have been depleting significantly in the
last decades, which forces the metal industries to search for alter-
native feedstocks. There have been a handful of studies on the eco-
friendly recovery of valuable metals from low grade ores (Anjum
et al., 2012). Metal bearing wastes including solid wastes, slurry
wastes and liquid wastes (such as mine water, fly ashes, spent li-
quors, spent catalysts, spent batteries, slags, shales and sludges)
have been examined for extracting metals (Brombacher et al., 1997;
Sethurajan et al., 2017a). Often these metallurgical wastes cannot
be treated by commercial extractive metallurgy i.e. hydrometal-
lurgy, pyrometallurgy or electrometallurgy. Hydrometallurgy is
aimed at solubilisation of metals from their insoluble ores with the
help of solvents. While, heat and electricity are used in pyromet-
allurgy and electrometallurgy, respectively, for extracting metals.
Various hydro-metallurgical processes were proposed for the re-
covery of zinc from wastes both from ferrous and non-ferrous in-
dustries (Jha et al., 2001). Not only wastes from metallurgical
industries such as slags and sludges but also household wastes like
electronic waste (E-waste) could be seen as a secondary resource
for the pyro/hydrometallurgical recovery of metals (Akcil et al.,
2015; Tan et al., 2015; Lu and Xu, 2016).
Biohydrometallurgy can be defined as conversion of insoluble
metal forms (e.g. metal sulfides) to soluble metals with the help of
one or more microorganisms. Biohydrometallurgy could also be
140 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153
used for recovering metals from waste materials. Lee and Pandey
(2012) discussed the available methods (such as bioleaching,
biogenic sulfide precipitation and bioreduction) for the extraction
of various metals (Cu, Zn and Ni) from different industrial wastes by
microbial processes. Erüst et al. (2013) reviewed the possible ap-
plications of biohydrometallurgy to recover metals from spent
batteries and catalysts. Hennebel et al. (2015) pointed out that the
scarcity of resources and crucial demand of raw materials, even for
basic requirements such as energy and water. They overviewed
biological approaches for the utilization of secondary resources to
supply some of the critical materials, e.g. platinum group elements
and rare earth elements. Kaksonen et al. (2014) reviewed the ability
of different microorganisms to process and recover gold from
various sources. Johnson (2014) and Dunbar (2017) discussed about
biomining and the possible biotechnological applications to extract
metals from ores and waste materials. Nancharaiah et al. (2015,
2016) overviewed the biological and bio-electrochemical recovery
of critical and scarce metals. This article critically discussed, up-to-
date information on microbe mediated leaching and recovery of
metals from reduced metallurgical wastes (such as dusts and tail-
ings which contain reduced minerals like sulfides) and oxidized
metallurgical wastes (such as slags, sludges, residues and red mud
which contains oxidized minerals like iron oxides and/or also
metals that are entrapped in silicate matrix).
1.2. Environmental impacts of metal bearing wastes
Pure metals are the end products of both pyro and hydromet-
allurgical operations. However, various metal bearing wastes are
generated as unwanted by-products during mining and metallur-
gical operations and are stock piled. During bio-geochemical
weathering, toxic heavy metals can leach out from the wastes
which are stock piled in storage dams, thus contaminating the
surrounding soil, surface and sub-surface water bodies. Soil fertility
of the surrounding sites is usually highly impacted by the
contamination with toxic heavy metals (Giere
et al., 2003; Kierczak
et al., 2009) (Fig. 1). Stock piles and metallurgical waste storage
dams would in turn act as a potential reservoir of toxic heavy
metals and metalloids. The other major damage done by the
metallurgical wastes is the contamination of water bodies. These
contaminated water bodies consisting of drainage systems, lakes,
pits and rivers, are collectively referred to as mine impacted water
bodies (MIW) (Johnson, 2009). Both surface and subsurface water
could be heavily contaminated by the release of the toxic metals by
weathering (Fig. 1). Metals such as Cd, Pb and Zn are phytotoxic i.e.
these metals can be up-taken and accumulated by plants by
different processes. These toxic metals can be incorporated into
food chain as well (Greger, 2004; Nagajyoti et al., 2010) (Fig. 1). As a
result of phyto-contamination, blood levels of people in certain
parts of Russia were found to contain significant concentrations of
toxic metals (e.g. Pb) (Kachur et al., 2003). Formation of metal
hydrosulfates on the surface of waste stocks/piles (due to the
evaporation of surface water) could release the heavy metals into
the environment (Keith et al., 2001; Sa
nchez Espan ~ a et al., 2005;
Romero et al., 2006). The efflorescence could lower the natural
pH (to acidic pH) of the proximal water bodies and also increase the
toxic metals and metalloids concentration (Keith et al., 2001;
Hammarstrom et al., 2005). The accumulated metals can reach
higher trophic levels and ultimately human beings.
2. Biohydrometallurgy as an alternative strategy for metal
leaching
Biohydrometallurgy is an economical and cost-effective meth-
odology, which has been widely used for the extraction of base
metals from mineral ores. Furthermore, it is an eco-friendly process
when compared to conventional chemical leaching processes.
Biohydrometallurgy has many advantages over the conventional
chemical hydrometallurgy and pyrometallurgy that include (i)
lower cost, (ii) environmentally benign, (iii) in-situ leaching, (iv)
less hazardous waste/sludge, (v) does not involve toxic chemicals
and high energy and (vi) suitable for extracting metals from sec-
ondary resources (Olson et al., 2003; Walting, 2006; Johnson,
2013).
2.1. Mechanisms of bioleaching
On one hand, microbial leaching can be classified into two types
(based on the contact of microbes with the ores) such as (i) direct
(contact) leaching and (ii) indirect leaching. On the other hand,
bioleaching can be grouped into three types based on leaching
mechanism: (i) redoxolysis, (ii) acidolysis and (iii) complexolysis.
4Fe2þ þ O2 þ 4Hþ /4Fe3þ þ 2H2 O (1)
CuFeS2 þ 4Fe3þ /5Fe2þ þ Cu2þ þ 2S0 (2)
Redoxolysis achieves metal solubilisation by electron transfer
from the minerals to microbes (in case of direct leaching) and
oxidation of Fe2þ to Fe3þ (in case of indirect leaching) (Rawlings,
2005). An example for indirect bioleaching, is bioleaching of chal-
copyrite by Acidithiobacillus ferrooxidans. At. ferrooxidans first
catalyze the oxidation of ferrous to ferric ions (Eq. (1)) and then the
ferric ions in turn oxidizes the chalcopyrite (Eq. (2)) which results
in metal leaching. The ferrous ions formed in the leaching reaction
are oxidized by acidophilic bacteria as shown in Eq. (1).
Acidolysis can be defined as a proton mediated dissolution of
insoluble metal species to soluble species (Fig. 2). This process
happens when the microbes acidify their environment by
consuming the nutrients and produce acids. For instance, At. thio-
oxidans consume elemental sulfur and produce biogenic sulfuric
acid (that can bioleach Zn from Zn-metallurgical wastes)
(Sethurajan et al., 2017b). Organic acids and carbonic acid (as a
result of CO2 respiration) producing fungi could also bioleach
metals from insoluble metal species. Biohydrometallurgy by acid-
olysis mostly follow shrinking core kinetics (i.e. the leaching rate is
controlled either by chemical reaction at the surface or by diffusion
of reactants through liquid film layer/solid product ash layer)
(Sethurajan et al., 2017b).
Complexolysis is the chelation of microbial metabolites with
metal ions that form stable metal-chelating agent complex (Fig. 2).
For instance, Pseudomonas putida produce extra cellular cyanide
which chelate with gold and thus induces gold leaching from
electronic wastes (Işıldar et al., 2016). Under iron-starving condi-
tions, siderophore forming bacteria (e.g. Pseudomonas aeruginosa)
can enhance the release of heavy metals (e.g. Cu) from the metal-
lurgical wastes (Potysz et al., 2016a).
2.2. Factors influencing bioleaching
Selection of appropriate microorganisms is the first and primary
step in the biohydrometallurgical processes. Acidithiobacillus was
the first organism employed in the bioleaching process. But a wide
variety of microbes like Leptospirillum spp., Acidanus spp., Sulfoba-
cillus spp. and Sulfolobus spp. have been tested for metals bio-
leaching (Spolaore et al., 2009, 2011; Bryan et al., 2011; Wakeman
et al., 2011).
In many cases, indigenous thermophilic bacteria isolated from
the acid mine drainage, pond tailings and contaminated soils have
shown promising results. Various factors that can influence
 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153
Fig. 2. Mechanisms of bioleaching of metals from the oxidized and reduced secondary wastes. Me(aq): metal(oid)s in soluble form; MeS - metal(oid) sulfide (Nancharaiah et al., 2016).
bioleaching are pH, temperature, pulp density, redox potential,
bacterial species, particle size and mineralogy of the wastes and
also oxygen and iron concentration (Sandstro € m and Petersson,
1997; Fu et al., 2008; Plumb et al., 2008). In many instances,
these factors affect the bioleaching individually and in some cases
combined effects of one or two factors can influence the bio-
leaching efficiency. For example, Sethurajan et al. (2017b) found out
that sulfur concentration individually and interaction between
sulfur concentration and pulp density and also interaction between
pulp density and initial pH influence the bioleaching of Zn from Zn-
leaching residues (ZLRs). Fungi and heterotrophic bacteria were
also reported to leach metals from different waste materials
(Mulligan and Galvez-Cloutier, 2000; Castro et al., 2000; Mulligan
et al., 2004; Shabani et al., 2013) (Fig. 3).
According to a study, a fungal strain Phanerochaete chrys-
osporium has proven its ability to reduce the preg-robbing capacity
of anthracite-grade carbonaceous matter during bioleaching of
double refractory ores (Ofori-Sarpong et al., 2010). In an effort to
develop a microbial process for effective utilization in the mining
industries, the strain was also investigated for its ability to trans-
form sulfides. P. chrysosporium was shown to reduce 15e35% of the
sulfide compounds in pyrite and arsenopyrite ores (Ofori-Sarpong
et al., 2011).
3. Biohydrometallurgy of reduced secondary wastes
Bacterial mediated leaching of reduced minerals has been
applied successfully to the extraction of metals (e.g. Cu from chal-
cocite and chalcopyrite) at a number of operations worldwide
(Jonglertjunya, 2003). Biohydrometallurgy of reduced minerals are
generally followed by redoxolysis or oxidative dissolution mediated
by ferric iron (Fe3þ).
MeS þ 2Fe3þ /2Fe2þ þ Me2þ þ S
Cu2 S þ 1:6Fe3þ /1:6Fe2þ þ 0:8Cu2þ þ Cu1:2 S
141
Cu1:2 S þ 2:4Fe3þ /2:4Fe2þ þ 1:2Cu2þ þ S0 (5)
ZnS þ 2Fe3þ /Zn2þ þ 2Fe2þ þ S0 (6)
2ZnS þ O2 þ 4Hþ /2Zn2þ þ 2H2 O þ 2S0 (7)
PbS þ 2Fe3þ /Pb2þ þ 2Fe2þ þ S0 (8)
According to Baba et al. (2011), redoxolysis of sulfide minerals
follow a generalized Eq. (3). Oxidative dissolution of reduced
minerals such as chalcopyrite, chalcocite (Leahy et al., 2005),
sphalerite (Haghshenas et al., 2009) and anglesite (Baba et al., 2011)
are illustrated in Eq. (2) and Eqs. (4)e(8).
Acidolysis of reduced minerals is very unlikely, however
Rodriguez et al. (2003) reported that initial dissolution of sphalerite
used to mediate by protons followed by the attack of ferric ions.
Similarly, complexolysis mediated bioleaching is not likely to
dissolve metals from reduced sulfidic minerals. Bio-
hydrometallurgy of reduced metallurgical wastes such as dusts and
tailings is discussed in detail below.
3.1. Dusts
Fine and dust like particles are mostly collected at gas exhaust of
smelters or furnaces, while processing Cu, Zn and Pb ores. These
waste particles are called as flue dusts, which usually contain sig-
nificant concentration of metals. For instance, dusts generated from
copper smelters contain up to 20e40% (w/w) of Cu (Davenport
et al., 2002). These dusts are generally in reduced state. The min-
eral phases such as chalcocite (Cu2S), chalcopyrite (CuFeS2), bornite
(Cu5FeS4) and covellite (CuS) are the most common mineral phases
present in the copper flue dusts (Massianaie et al., 2006). There are
(3) also metallic dusts generated during heating and cooling of the
electric arc furnace (EAF) smelting processes. Zn-oxides and Fe-
oxides are common in the EAF dusts (Jha et al., 2001). Dusts from
(4)
electric arc furnaces of steel industries usually contains (w/w %)
19.4% Zn, 24.6% Fe, 4.5% Pb, 0.42% Cu, 0.1% Cd, 2.2% Mn, 1.2% Mg,
142 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153
Fig. 3. Various microorganisms utilized for the bioleaching of metals from primary resources.
0.4% Ca, 0.3% Cr, 1.4% Si and 6.8% Cl (Caravaca et al., 1994). Blast
furnace (BF) dusts are similar to EAF, generated during the wet
cleaning of the gases in blast furnace mediated steel production.
These dusts usually get agglomerated after long term exposure to
atmosphere because of its inherent moisture content. Elemental
analysis revealed that BF dusts are rich with iron and carbon in high
concentrations. Carbon (~30%), Fe2O3 (~51%), SiO2 (~7%), Al2O3
(~3%) and other metals such as Zn, Pb and Mn are the typical
constituents of BF dusts (Das et al., 2002).
Various pyrometallurgical and chemical leaching procedures
were proposed for the recovery of metals associated with the dust
wastes (Cole et al., 1987; Gabler and Jones, 1988). pH played a major
role on the metals leachability from Cu smelter dusts (Vítkov
a et al.,
2011). Since these dusts contain metals in reduced sulfidic mineral
phases, biohydrometallurgy would be a better alternative for
extraction (Rossi, 1990; Schnell, 1997; Oliazadeh et al., 2006)
(Table 1). Chemolithotrophs such as Acidithiobacillus and Lep-
tospirillum are the most commonly used genera for the biomining
of metals from dusts. Acidithiobacillus ferroxidans extracted up to
70% of Zn from Fe-Mn alloy industrial dust by oxidative bioleaching
(Solisio et al., 2002). In many instances, mixed consortia of Fe and S
oxidizing bacteria showed better leaching efficiency than the in-
dividual pure cultures of either sulfur oxidizing bacteria or iron
oxidizing bacteria. Bakhtiari et al. (2008a; 2008b; 2010) investi-
gated bioleaching by a mixed consortium containing At. ferroox-
idans, At. thiooxidans and L. ferrooxidans. The bioleaching results
could well be replicated when operated in higher volume bio-
reactors such as continuous stirred tank reactors (CSTR) and airlift
bioreactors (ALR). A maximum of 90% of Cu was leached within 2
days at lower solid to liquid phase ratio (2.7%) in ALR configura-
tions. Unlike flue dusts, there are no reports on the biological
leaching of metals from furnace dusts. Conventionally, furnace
dusts were treated by acidic medium (sulfuric acid). Acidic leaching
efficiency of metals from furnace dusts is highly influenced by the
iron/zinc ratio present in the dust (Havlik et al., 2004). Hence,
bioleaching by biogenic sulfuric acid produced by Acidithiobacillus
spp. and complexolysis mediated bioleaching by fungi could be a
better alternative for recovering metals from the furnace dusts
(Mulligan et al., 1999; Mulligan and Galvez-Cloutier, 2000;
Sethurajan et al., 2017b).
3.2. Tailings
Tailing wastes are one of the important waste by-products
generated during the mineral beneficiation processing of the pri-
mary ores. After various mineral processing operations (floatation,
coagulation and flocculation) of the crushed natural ores, huge
mass will end up as tailing wastes. For instance, approximately 99%
of the mined gold ores could be left over as tailings after the
mineral beneficiation processes (Lottermoser, 2010). These tailing
wastes can be in the form of solids and sometimes slurry as well.
Usually the tailings are stored in specially built tailing dams or
tailing storage facilities (TSF). There could be around 3500 tailing
storage dams available worldwide (Davies et al., 2000). Mineral-
ogical studies on the tailings frequently show the presence of
reduced minerals like pyrite, chalcopyrite, chalcocite, arsenopyrite
 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153 143

Table 1
Different biohydrometallurgical approaches proposed for the leaching of heavy metals from metallurgical dusts.

Dust type (metal content - %) Bioprocess Leaching yield Reference

EAF dust
Zn - 1.23% At. ferrooxidans A maximum of 35% Zn and 33% Bayat et al. (2009)
Fe - 54.73% Fe can be bioleached after 21
days (at pH 1.3, pulp density 1%
w/v, particle size 0.038 mm)
Fe-Mn alloy industrial dust
Zn - 5.5% Bioleaching by At. ferrooxidans Maximum of 76% of Zn leached, Solisio et al. (2002)
Cu - 0.052% when the conditions were: 1%
Pb - 0.29% pulp density, pH 2, 250 rpm and
temperature 30  C
Copper smelter flue dust
Zn - 1.67% Mixed mesophilic (At. Maximum 85.5% of Cu was Bakhtiari et al. (2010)
Cu - 22.2% ferrooxidans, At. thiooxidans and leached after 23 days at 2.7%
Fe - 5.9% L. ferrooxidans) bioleaching pulp density
Pb - 1.54%
Flue dust of the Sarcheshmeh copper smelter
Cu - 35.8% Mixed culture of At. Maximum 90% of Cu was Bakhtiari et al. (2008a)
Fe - 15.3% ferrooxidans, At. thiooxidans and leached at 4% pulp density after
L. ferrooxidans 4 days
Copper flue dust
Cu - 35.8% At. ferrooxidans, At. thiooxidans Maximum 90% of Cu was Bakhtiari et al. (2008b)
Fe - 15.3% and Leptospirillum mixed leached at 2% pulp density after
cultures 2.7 days
Copper mining flue dust
Cu - 29.15% Mixed culture of At. Cu leaching was 87% after 22 Massianaie et al. (2006)
Fe - 22.23% ferrooxidans and At. thiooxidans days in shake flask and 91% in
bioreactor after 6.5 days
Copper mining flue dust
Cu - 29.15% Mixed culture of At. Maximum 87% of Cu was Oliazadeh et al. (2006)
Fe - 22.23% ferrooxidans and At. thiooxidans leached after 22 days at 5% pulp
density

and sphalerite (Ahmadi et al., 2015; Nguyen and Lee, 2015; Ye et al.,
2017). Tailings are characteristically poly-metallic and mostly
contain significant concentrations of Fe (0.5e30%), Zn (0.1e3%), Cu
(0.1e1%), Pb (0.1e2%) and may also contain As (1e3%) and In
(0.001%) (Park et al., 2014; Nguyen et al., 2015; Lee et al., 2015;
Martin et al., 2015).
As the tailings mostly contain reduced mineral phases, various
biohydrometallurgical processes were proposed for the extraction
of metals from the tailings (Table 2). As discussed earlier, oxidative
biological dissolution of metals from reduced minerals are highly
successful by chemolithotrophs. Direct and indirect bioleaching of
metals from different tailings by pure cultures of At. thiooxidans
(Lee et al., 2015) and At. ferrooxidans (Park et al., 2014) and mixed
cultures of the At. thiooxidans and At. ferrooxidans (Nguyen et al.,
2015; Nguyen and Lee, 2015) were proposed. Indigenous sulfur
oxidizing bacteria were found to extract more than 95% of Zn and
Cu from Shuikoushan mine tailing, China (Liu et al., 2008). Even
uncultured acidophilic ferrous iron-oxidizing and sulfur-oxidizing
consortia could bioleach more than 80% of Zn and In from David
Schacht tailings, Germany (Martin et al., 2015). Even though,
oxidative bioleaching of metals (like Cu, Zn, As and In) by chemo-
lithotrophs is efficient, Pb bioleaching from anglesite (PbSO4)
minerals is least effective as like any other oxidized minerals. To
overcome this problem, a sequential bioleaching was proposed by
Ye et al. (2017). More than 95% of Zn could be solubilized from
tailings by At. ferrooxidans in the first stage and in the second stage,
Pb (95% efficiency) could be leached chemically from the At. fer-
rooxidans-spent tailings (Ye et al., 2017).
4. Biohydrometallurgy of oxidized ores/resources/wastes
Even though bioleaching of reduced minerals is relatively well
established, biohydrometallurgy of the oxidized resources is still in
its initial stages. Because the oxidative dissolution mechanism by
acidophilic sulfur oxidizing bacteria and iron oxidizing bacteria
require reduced mineral phases (Johnson et al., 2013). Fungal bio-
leaching is one of the most investigated techniques for the
extraction of metals from the oxidized ores and secondary wastes
(Castro et al., 2000; Mulligan and Galvez-Cloutier, 2000). Organic
acids (citric, oxalic and maleic acids) produced by the fungi can
leach out the metals from the resources. Leaching by organic acid
producing heterotrophic bacteria (Shabani et al., 2013) was also
reported.
Recently a new approach was demonstrated for the extraction of
metals from oxidized lateritic ores/deposits (Hallberg et al., 2011;

Nancucheo et al., 2014; Schippers et al., 2013). The process is
termed as (anaerobic) reductive dissolution. Even though, Acid-
ithiobacilli spp. are aerobic bacteria, they can also survive under
anaerobic conditions by oxidizing sulfur and reducing soluble ferric

ions simultaneously (Nancucheo et al., 2014). There are few reports
on the extraction of Cu, Mn and Ni by chemolithotrophs from the
oxidized ores (Hallberg et al., 2011; Schippers et al., 2013;

Nancucheo et al., 2014). These approaches can be explored for
leaching of metals from other oxidized secondary resources. There
is a need for additional studies on reductive dissolution of metals
from secondary resources. Biological metal leaching from oxidized
metallurgical wastes, such as residues, red mud, slags and sludges is
discussed below.
4.1. Mineral sludges
Mineral sludges are by-products of various ferrous and non-
ferrous industries. There are different types of sludges (based on
their generation), such as (i) blast furnace sludges (BFS), (ii) electric
arc furnace sludges (EAFS), (iii) converter sludges, (iv) basic oxygen
furnace sludges (BOFS) from steel making industries, (v) sludges
from plating industries and (vi) sludges from metal producing in-
dustries. Ferrous industries are the major producers of sludge
144 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153

Table 2
Different biohydrometallurgical approaches proposed for the leaching of heavy metals from mine tailings.

Tailings (metal content - %) Bioprocessing microbes Leaching yield Reference

San Marcelino tailings,Philippine

Zn - 0.01% Pure and mixed consortia of More than 95% of Mn, 75% of Zn and 40% of Cu Nguyen et al. (2015);
Mn - 0.13% At. thiooxidans and At. ferrooxidans were solubilized by the mixed consortia within Nguyen and Lee (2015)
Cu - 0.13% 25 days (initial pH 2.0, pulp density 5% (w/v))
Fe - 3.61%
Shaoguan City tailings, China
Zn - 0.55% Bioleaching by At. ferrooxidans More than 95% of Zn was solubilized by At. Ye et al. (2017)
Pb - 0.44% (and followed by ferrooxidans within 50 days (pulp density 5% (w/
Fe - 20.94% chemical brine leaching) v), initial pH 2.0) (and followed by chemical
brine leaching which extracted more than 95%
of Pb from the bioleached residue)
Janggun Mine tailing, South Korea
As - 3.39% At. thiooxidans More than 50% of As, 35% of Zn and 16% of Cu Lee et al. (2015)
Zn - 2.89% were solubilized by At. thiooxidans within 25
Pb - 0.98% days (pulp density 0.5% (w/v), initial pH 1.8)
Cu - 0.27%
Fe - 13.31%
Janggun oxidized mine tailings, South Korea
Zn - 1.94% At. ferrooxidans More than 80% of As was bioleached by At. Park et al. (2014)
As - 2.61% thiooxidans within 15 days (pulp density 0.5%
Cu - 0.13% (w/v), initial pH  2.0)
Fe - 12.04%
Shuikoushan mine tailing, China
Zn - 0.12% Indigenous sulfur-oxidizing More than 95% of Zn and Cu and 44.34% Pb were Liu et al. (2008)
Cu - 0.13% bacteria (enriched consortia) solubilized by the consortia within 13 days
Pb - 0.02% (sulfur concentration 2% (w/v), pulp density 1%
Fe - 0.47% (w/v), initial pH 2.0)
David Schacht tailings, Germany
Pb - 0.468% Uncultured acidophilic ferrous More than 80% of Zn and In were solubilized by Martin et al. (2015)
Zn - 1.000% iron-oxidizing and the consortia within 10 days (pulp density 10%
In - 0.001% sulfur-oxidizing consortia (enriched) (w/v), initial pH 1.8)

wastes, for instance 1 ton of steel production generates approxi-
mately 2e4 tons of wastes (Das et al., 2006). The mineralogical and
elemental composition of the metallurgical sludge is dependent on
the nature of the ores. Magnetite (Fe3O4), hematite (Fe2O3) and
wuestite (FeO) are the major mineral phases present in the steel
industrial sludges. Apart from Fe, detectable amounts (mass
percent) of Zn (3%), Pb (1%), Cd (0.01%) and As (0.1%) are also found
in the ferrous sludges (Mansfeldt and Dohrmann, 2004). Pyritic
sludges from the metallurgical industries are also polymetallic,
containing significant mass percent of 44% of Fe, 28% of S, 0.38% of
As and 0.13% of Zn (Hita et al., 2006, 2008). The sludges typically
consist of approximately 2.5% of Zn and 61% of Fe (Trung et al.,
2011). Mansfeldt and Dohrmann (2004) studied the mineralogical
and chemical composition of the pig iron making sludges and found
that apart from iron mineral phases, they also contain primary and
secondary phases of metals Zn (3%), Pb (1%), Cd (0.01%) and As
(0.1%).
Several researchers in the past proposed different hydrometal-
lurgical approaches to process these sludges for the effective and
economic extraction of metals by optimizing various parameters.
Use of hydrometallurgical operations for the effective removal of Zn
and Pb from the BFS was reported by van Herck and Vandecasteele
(2000). These authors have focused on the effect of pH and redox
potential on leaching efficiency. Silva et al. (2005) investigated
various factors such as pulp density, stirring, concentration of
leachant and particle size on leaching of metals from galvanic
sludges and stated that 1M of H2SO4 can leach 88.6% Cu, 98.0% Ni
and 99.2% Zn at room temperature in 24 h. Trung et al. (2011) re-
ported that at high temperature (80  C), approximately 70% of Zn
can be leached within 15 min by using 1M H2SO4. Veres et al. (2012)
investigated the extraction of the Zn from the BFS by microwave
assisted procedure and revealed that the Zn leaching kinetics
follow shrinking core model and leaching rate was controlled by
the diffusion of reactants through the solid product layer. Bio-
leaching by oxidative dissolution might not be efficient for the
sludges because of the absence of reduced mineral phases. How-
ever, very few studies have been performed on the bio-
hydrometallurgy of the sludges (Table 3). There are only a few
instances where different bioleaching mechanisms were tried and
tested (Hita et al., 2008; Vestola et al., 2010). Bioleaching of the steel
plant sludge using Acidithiobacillus ferrooxidans was investigated by
Vestola et al. (2010). Metal leaching was achieved by biogenic
sulfuric acid attack and not by redox reactions. On the other hand,
industrial sludges containing sulfidic minerals can be treated by
oxidative dissolution. Hita et al. (2008) reported the possibility of
biological solubilisation of Fe, Zn and As from pyritic sludge
released due to the Aznalcollar dam failure.
4.2. Residues
Residues are typical metallurgical wastes of roasting-leaching-
electrowinning (RLE) hydrometallurgy. There are two types of
residues, namely (i) leach residues (filter cake formed after the
filtration of acid leached slurry) and (ii) purification residues
(generated after purification techniques like cementation, prior
sending the filtered slurry to electrowinning) (Sethurajan et al.,
2016a, 2016b). Huge amounts of residue wastes are co-generated
during metallurgical processes. For instance, approximately
910,000 metric tons of Zn plant residues (ZPR) are generated by a
single Zn-metallurgical industry located in the Republic of Congo
(during its 4 decades of operation) (Ngenda et al., 2009). Typically,
one ton of Zn production can co-generate 0.5e0.9 ton of Zn plant
residues (ZPR) (Creedy et al., 2013). Leach residues mainly contains
the metal of interest (e.g. high concentration of Zn present in the
leach residues generated from Zn-plant) along with Fe and impu-
rities. Purification residues mainly contain the impurities with
 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153 145

Table 3
Different biohydrometallurgical approaches proposed for the leaching of heavy metals from metallurgical sludges.

Sludge type (metal content - %) Bioprocessing microbes Leaching yield Reference

Copper converter sludge

Zn - 1.7% Mixed consortia (Acidithiobacillus spp. 36% of Zn can be bioleached after 79 days by Vestola et al. (2010)
Fe - 60.2% and Leptospirillum spp.) mixed consortia (pH 1.5, pulp density - 1% w/v,
S0 - 1%).

llar, Spain)
Pyritic sludge - (Aznalco
Zn - 0.13% Bioleaching with iron oxidizing Approximately 90% of total Zn was leached in Hita et al. (2008)
Fe - 44% bacteria (At. ferrooxidans, At. caldus) 10 days, pH 2, pulp density 2.5% (w/v),
and archaea (S. metallicus) temperature 65  C by S. metallicus

higher concentrations than the metals of interest and Fe
(Sethurajan et al., 2016b). The residues are typically found in the
zone of oxidation and found to contain highly stable spinel called
franklinite (ZnFe2O4), ZnSO4 and PbSO4 mineral phases. These are
secondary mineral phases formed as a result of desulfurization of
iron rich sphalerite and sulfuric acid leaching of the reduced min-
erals present in the natural ores.
There are various hydrometallurgical treatments proposed for
the extraction of Zn and other metals from the residues. Acid
leaching (mainly sulfuric acid) was proposed to extract maximum
metal values from ZPR. In many instances, the metal leaching from
ZPR follows shrinking core model (Safarzadeh et al., 2011). Sulfuric
acid concentration, particle size and temperature are the various
parameters that affect the metal leachability from the residues. In
some cases, addition of substances such as phenol could increase
manganese and cobalt leachability from ZPR. Thermal treatment
coupled with acidic leaching was also proposed for the extraction of
Zn from Kolwezi ZPR (Ngenda et al., 2009). Ammonium carbonate
leaching (Schnabel process) was also reported for the metal sol-
ubilisation from the leach residues (Harvey, 2006). Turan et al.
(2004) studied ZPR from carbonated ores of zinc-lead and pro-
posed a combination of pyrometallurgical (roasting) and hydro-
metallurgical processes (sulfuric acid, water and NaCl) for the
extraction of Zn and Pb from these residues. Ruşen et al. (2008)
reported similar hydrometallurgical extraction of Zn metals and
brine leaching for Pb. Sulfuric acid leaching followed by sphalerite
precipitation from leach residues and covellite precipitation from
purification residues were also reported (Sethurajan et al., 2016b,
2017c). There are many studies on the recovery of Pb from
different industrial residues (Turan et al., 2004; Ruşen et al., 2008;
Farahmand et al., 2009; Şahin and Erdem, 2015; Sethurajan, 2015).
Brine leaching was the most common technique used to leach Pb
from the PbSO4 bearing residues. The brine leaching of Pb from the
Pb-sulfates followed diffusion controlled first order kinetics
(Geidarov et al., 2009). The Pb leaching by brine solution is tem-
perature dependent, the activation required to leach maximum Pb
was ranging from 2.7 to 12.41 kJ/mol (Geidarov et al., 2009; Şahin
and Erdem, 2015). Şahin and Erdem (2015) proposed alkali leach-
ing of Pb from the ZLRs. Even though, the leaching efficiency was
high, this approach was not selective for recovering Pb as Zn was
also leached alongside Pb.
As like sludges, the metallurgical residues are also oxidized
wastes and hence conventional oxidative bioleaching will not be
suitable. However, there are few studies which investigated the
microbe mediated leachability of heavy metals from the oxidized
residues (Mulligan et al., 1999; Mulligan and Galvez-Cloutier, 2000;
Sethurajan et al., 2017b) (Table 4). Fungal bioleaching (using
A. niger) was proposed and proved efficient for the extraction of
copper from mining residues. A maximum of 60% of Cu was bio-
leached from copper residues containing 0.7% of Cu at 5% pulp
density. Gluconic acid (9673 mg L1) and citric acid (1244 mg L1)
were the highly produced organic acids by A. niger during the
bioleaching period and contributed to the bioleaching efficiency
(Mulligan et al., 1999; Mulligan and Galvez-Cloutier, 2000). The
bioleaching efficiency of Cu from mining residues could be well
improved from 60% to 80% by ultrasound pre-treatment (Mulligan
and Galvez-Cloutier, 2000). Similar to biogenic organic acids,
biogenic sulfuric acid also solubilise metals from the residues.
Sethurajan et al. (2017b) revealed that the biogenic sulfuric acid
produced by At. thiooxidans can leach more than 75% of Zn from ZPR
of oxidized Zn-plant leaching residues. Acidolysis mediated bio-
leaching could be left with some non-reacted solids called as spent-
residue. Mostly they are useless by-products. However, sometimes
the spent residue, were enriched with other heavy metals and
could be useful for the selective recovery of that particular metal.
For instance, Sethurajan et al. (2017b) investigated selective re-
covery of Zn from ZLRs using At. thiooxidans and after 45 days, more
than 70% of Zn and Fe could be leached from ZLRs. However, the
spent-ZLR was enriched with Pb (as Pb present in the ZLR was not
susceptible to H2SO4 leaching) and therefore the spent-ZLR can be
potential source for selective Pb recovery (Sethurajan, 2015).
4.3. Red mud
Red mud is a saline, alkaline secondary waste generated during
the Bayer processing (alkaline extraction of alumina) of bauxite ore.
55e65% of red mud (approximately 2 tons of red mud per ton of
aluminium) is generated with respect to the bauxite quality and
grade (Vachon et al., 1994; Uzun and Gülfen, 2007). Approximately
2.7 billion tons of red mud was available worldwide and increase

Table 4
Different biohydrometallurgical approaches proposed for the leaching of heavy metals from metallurgical residue.

Sludge type (metal content - %) Bioprocessing Leaching yield Reference

microbes

Copper mining residues, Canada

Cu - 0.72% A. niger 60% of total Cu was bioleached at 5% pulp density within 10 days Mulligan et al. (1999);
Fe - 2.64% from raw residue and a maximum of 80% of Cu was bioleached Mulligan and
Zn - 0.02% within 10 days from ultrasound pre-treated residue. Galvez-Cloutier (2000)
Zinc leach residue
Zn - 2.51% At. thiooxidans More than 70% of Zn bioleached within 45 days at 2.15% pulp Sethurajan et al. (2017b)
Fe - 11.5% density, 25.1 g L1 external sulfur concentration and initial pH
Pb - 2.35% 3.3.
146 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153
every year by 100e150 million tons per year (Power et al., 2011;
Klauber et al., 2011). Extreme alkalinity complicates the red mud
disposal into the environment (Vachon et al., 1994; Pyasi, 2014).
Despite its toxicity, red mud often finds applications in land fillings,
land reclamation, adsorbents, pH modifiers and building materials
construction (Uzun and Gülfen, 2007). Red mud is poly-metallic
and often consists of Al, Fe, Si and Ti bearing mineral phases such
as gibbsite, kaolinite, hematite, goethite, magnetite, anatase and
quartz mineral phases (Pyasi, 2014). In many instances, rare earth
elements (REE) were also observed in the red mud (Borra et al.,
2015, 2016; Davris et al., 2016; Onghena et al., 2017).
There are only a few studies reported on the bio-
hydrometallurgical extraction of Al from red mud (Table 5). Bio-
leaching of Al from red mud was investigated by Vachon et al.
(1994) using pure cultures of A. niger, P. notatum,
P. simplicissimum and Trichoderma viride and indigenous Acid-
ithiobacilli (enriched from sewage sludge). As the Acidithiobacilli
spp. are chemolithotrophic and acidophilic in nature, external
sulfur was supplied and H2SO4 was used to lower the pH initially to
adapt (Vachon et al., 1994). Adapted Acidithiobacilli (after repeated
sub-culturing in the presence of red mud at pH 9.0), was able to
leach 47% of Al from the red mud, while non-adapted Acid-
ithiobacilli leached only 10% of Al. T. thioporus and At. thiooxidans
were hypothesized to be the predominant species and responsible
for the bioleaching of Al by biogenic sulfuric acid production
(Vachon et al., 1994). On the other hand, complexolysis leaching of
Al from red mud (mediated by organic acids produced by fungi)
was better than the Acidithiobacilli leaching efficiency. A maximum
of 75% of Al could be bio-solubilized from the red mud by Penicil-
lium simplicissimum (Vachon et al., 1994). Three different method-
ologies such as (i) one-step bioleaching (inoculating fungi and
adding red mud at same time), (ii) two-step bioleaching (adding
the red mud to a well grown fungal culture where as inoculation of
the fungi being the first step) and (iii) bioleaching by cell-free spent
fungal culture supernatant was proposed for the fungal bioleaching
of metals from red mud (Qu et al., 2013; Vakilchap et al., 2016). The
results show that the bioleaching by the spent culture supernatant
was better than the one-step and two-step fungal bioleaching. A
maximum of 80% of Pb, 80% of Zn and 67% of Cu was bioleached by
A. niger within 30 days (Qu et al., 2013) and 69.8% of Al and 60% of Ti
was solubilized by A. niger within 40 days (Vakilchap et al., 2016).
Higher concentrations of the biogenic organic acids produced and
present in the cell-free culture supernatant compared to the one-
step and two-step cultures attributed to the better leaching effi-
ciency of the former.
4.4. Slags
Slags are one of the most studied waste by-products from
smelting operations. Huge amounts of slags are generated during
smelting operations (for example 1 ton of Cu production co-
generates ~2.2 tons of slags) (Gorai et al., 2003). These slags are
usually stock piled either in heaps or in tailing dams. Mineral phase
composition and bulk chemistry of the slags vary with respect to
Table 5
Different biohydrometallurgical approaches proposed for the leaching of heavy metals from red mud.
Red mud (metal content - %) Bioprocessing microbes
Zn - 0.07% A. niger
Pb - 0.03%
Cu - 0.02%
Fe - 8.42%
Al - 9.47% A. niger (PTCC 5210)
Ti - 2.94%
Fe - 13.74%
ores and metallurgical processing. Silicate minerals (e.g. fayalite
and diopside), sulfide minerals (e.g. sphalerite, chalcopyrite, pyr-
rhotite and bornite), oxide minerals (e.g. hercynite and secondary
metal sulfates) and sometimes pure metallic phases of Cu and Pb
are the frequently observed mineral phases in the slags (Potysz
et al., 2015). Typical metallurgical slags are always poly-metallic
in nature and often contains significant concentrations of heavy
metals such as Fe, Cu, Zn, Pb and Cd and metalloids like As.
Various pyro- and hydro-metallurgical processes such as acid
leaching (Tshiongo et al., 2010; Ahmed et al., 2012; Deng and Ling,
2007; Beşe, 2007), ferrous sulfate leaching (Carranza et al., 2009),
oxidative pressure leaching (Baghalha et al., 2007; Beşe, 2007),
chlorinated leaching (Herreros et al., 1998) and ammonium sulfate
leaching (Sukla et al., 1986) were proposed for recovering useful
metals from slags. However these processes employ one or more
environmentally hazardous substances for solubilisation of metals.
Bioleaching is proposed as a “green” alternative to the conventional
pyro/hydro-metallurgical processes in recovering metals from the
slags (Table 6). A. niger was the first microbe to be used to mobilise
metals from slags (Sukla et al., 1992, 1995). A. niger can solubilise
metals from the slags by producing organic acids, which act as
leaching agents. Oxidative bioleaching of Cu from the slags by pure
cultures of chemolithotrophs such as Acidithiobacillus spp. and
Leptospirillum spp. was also proposed (Mehta et al., 1999; Vestola
et al., 2010). Sulfuric acid produced by the sulfur oxidizing bacte-
ria and regeneration of Fe3þ/Fe2þ were responsible for this oxida-
tive bioleaching. Sulfur oxidizing bacteria utilize the sulfur moieties
present in the reduced mineral phases, thereby causes solubilisa-
tion of the particular metal (e.g. Zn from sphalerite phase). External
sulfur supplementation would enhance the initial bacterial growth
and aid metal solubilisation (Potysz et al., 2016b). Indigenous bac-
teria isolated from the contaminated sites and mixed cultures of
more than one bacterial culture were also proposed for the bio-
leaching of slags and reported to leach out more metals compared
to the individual cultures (Cheng et al., 2009; Kaksonen et al., 2011;
Wang et al., 2015). Biogenic sulfuric acid and Fe3þ ions present in
the cell-free spent culture medium of At. thiooxidans and At. fer-
rooxidans was reported to leach significant amounts of metals (Cu,
Zn and other metals). It was observed that 60% of Zn and 27% of Cu
were bioleached using 1 g L1 pulp density within 6 days from the
EAF slags (Hocheng et al., 2014). Bioleaching with indigenous
heterotrophic-thermophilic bacteria (Bacillus spp., Sporosarcina
spp. and Pseudomonas spp.) is another promising method to
improve leaching of metals from the slags (Cheng et al., 2009).
However, when mesophilic heterotrophs were used to recover
metals from slags, the leaching efficiency was found to be
comparatively lower (Potysz et al., 2016b). This is attributed by the
leaching efficiency of the low amounts of organic acids and/or li-
gands produced by the heterotrophs. Not only the organic acids
produced by the thermophilic bacteria react with the metallic
phase and form soluble complexes but also higher temperature
used to grow the thermophiles (compared to mesophiles) could be
the important factor for better bioleaching of metals by thermo-
philes. Bioleaching of metals from the slags has been scaled up-to
Leaching yield Reference
80% of Pb, 80% of Zn and 67% of Cu was solubilized by Qu et al. (2013)
A. niger spent medium within 40 days (pulp density 1% (w/
v), initial pH 2.5)
69.8%, 60% and 25.4% for Al, Ti and Fe were bioleached by Vakilchap et al. (2016)
A. niger spent medium within 30 days (pulp density 1% (w/
v), initial pH 2.5)
 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153 147

Table 6
Different (bio)hydrometallurgical approaches proposed for the leaching of heavy metals from metallurgical slags.

Slag type (metal content - %) Bioprocess Leaching yield Reference

Steel slag
Zn - 0.00007% Culture supernatant of At. thiooxidans A maximum of 60% Zn and 27% of Cu can be Hocheng et al. (2014)
Cu - 0.00007% 80191, At. ferrooxidans 13823 and A. niger leached after 4 repeated bioleaching cycles
Fe2O3 - 0.3% 34770 by At. thiooxidans culture supernatant
Copper slag
Zn - 1.7% Mixed consortia (Acidithiobacillus spp. and More than 60% of Zn and 95% of Cu can be Vestola et al. (2010)
Cu - 0.35% Leptospirillum spp.) bioleached after 79 days by mixed consortia
Fe - 40.7% (pH 1.5, pulp density - 1% w/v, S0 - 1%).
Copper slag
Cu - 4.03% A. niger A maximum of 47% Cu, 50% Co and 23% Ni Sukla et al. (1995)
Ni - 1.98% was leached after 3 days (2% w/v pulp
Co - 0.48% density, 120 rpm and 37 C)
Fe - 38.82%
Copper slag
Zn - 1.7% Mixed consortia (At. ferrooxidans, 62% Cu and 35% Zn was bioleached after 29 Kaksonen et al. (2011)
Cu - 0.35% At. thiooxidans, days (at pH 1.0, 5% w/v pulp density and 1%
Fe - 40.7% At. caldus, L. ferrooxidans and Sulfobacillus w/v of S0)
thermotolerans
Crystalline copper slag
Zn - 0.40% Pure cultures of At. thiooxidans and 79% Cu and 76% Zn was bioleached by At. Potysz et al. (2016b)
Cu - 0.57% P. fluorescens thiooxidans and 10% Cu and 4% Zn was
bioleached by P. fluorescens after 21 days
Amorphous copper slag
Zn - 0.78% Pure cultures of At. thiooxidans and 81% Cu and 79% Zn was bioleached by At. Potysz et al. (2016b)
Cu - 1.1% P. fluorescens thiooxidans and 4% Cu and 3% Zn was
bioleached by P. fluorescens after 21 days
Lead/zinc smelting slag
Zn - 2.83% Thermophilic mixed consortia 88% of Cu, 5% of Pb and 97% of Zn was Cheng et al. (2009)
Cu - 1.31% predominantly consists of Bacillus spp., bioleached after 6 days at 65 C, pH 1.5 and
Pb - 0.57% Sporosarcina spp. and Pseudomonas spp. 5% pulp density.
Copper smelting slag
Zn - 2.79% Mesophilic mixed consortia predominantly Approximately 70% of Cu and 7% of Zn were Kaksonen et al. (2016)
Cu - 0.38% consists of At. thiooxidans, At. ferrooxidans bioleached after 25 days (pH 2.1e2.2, 10%
Pb - 0.60% and L. ferriphilum w/v pulp density, 0.45% w/v of Fe2þ and 1%
w/v of S0)
Lead/zinc smelting slag
Zn - 14.12% Pure and mixed cultures of At. thiooxidans Approximately 90% of Zn, 86% Cd and 70% of Wang et al. (2015)
Cd - 0.88% and L. ferriphilum In were bioleached after 9 days (pH 1.0 and
Pb - 32.42% pulp density 10%)
In - 0.09%

lab scale reactors. Bioleaching of slags in bioreactor (CSTR) was also
tested and the results were comparable to the shake-flask studies
(Kaksonen et al., 2011). Approximately, 41% Fe, 62% Cu, 35% Zn and
44% Ni were leached in the CSTR after 29 days of bioleaching.
5. Biorecovery of metals from leachates and aqueous
solutions
Microbe-metal interactions have not only received special
attention in leaching metals from solid-minerals but also for the
selective recovery of soluble metal ions from the leachates and
aqueous solution (Nancharaiah et al., 2015, 2016). Microbial tech-
nologies are promising for the selective recovery of metal ions
because of low cost, technical feasibility for large scale applications
and no need for addition of toxic chemicals thereby avoids gener-
ation of toxic or hazardous sludge (Sethurajan et al., 2017a).
Various methods such as bioprecipitation, biosorption, bio-
reduction and bioaccumulation have been widely studied for the
removal of metal ions from the leachates and aqueous wastewater
(Ahemad and Malik, 2011; Kaksonen et al., 2014; Nancharaiah et al.,
2015; Sethurajan et al., 2017b). A pictorial representation of various
biorecovery methods is illustrated in Fig. 4.
5.1. Bioprecipitation
Precipitation is one of the conventional methodologies
developed for the removal and recovery of metals from the metal
bearing solutions. Precipitation of metals from the metal contam-
inated aqueous solutions (like acid mine drainage or industrial
wastewater) can be achieved in the form of (i) sulfides (ii) hy-
droxides and sometimes (iii) carbonates. Few metals like arsenic
can also be co-precipitated during flocculation with the salts of iron
and aluminium. Precipitation of metals occurs due to the change
the ionic equilibrium of the system with the addition of certain
chemicals/agents (precipitating agents) and this process is
distinctly different from coagulation and flocculation (Wang et al.,
2005). Removal efficiency of the metals by precipitation is highly
dependent on the concentrations of the metals in the solution and
also on the system pH. Precipitation of metals consists of various
critical stages like (i) nucleation, (ii) growth of nucleus and (iii)
aggregation and crystallization. The major disadvantages of these
processes are sludge generation and the high requirements of
chemicals to adjust the pH. Different metal precipitation strategies
were reported so far in which biogenic sulfide precipitation has
received special interest for industrial application.

2CH2 O þ SO2
4 /H2 S þ 2HCO3 (9)
Me2þ þ HS / MeSðYÞ þ Hþ (10)
(Me2þ - metal cation)
Sulfate reducing bacteria (SRB) are special group of
148 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153

Fig. 4. Mechanisms of biorecovery of metals from the leachates or aqueous solutions. Legends: Me(aq): metal(oid)s in soluble form; MeS - metal(oid) sulfide (Nancharaiah et al., 2016).

microorganisms (eubacteria and archaea) which utilize oxidized

sulfur compounds as electron acceptors while oxidizing organic
compounds for energy and produce sulfides. The biogenic sulfide
production can occur through two mechanisms namely, (i) assim-
ilatory sulfate reduction and (ii) dissimilatory sulfate reduction
(Thauer et al., 2007). The biogenic sulfide produced during sulfate
reduction can potentially precipitate and remove heavy metals
from the wastewater as explained in Eqs. (9) and (10).
Metal sulfide precipitation (MSP) by SRB occurs in two stages (1)
biological hydrogen sulfide production by SRB and (2) metal sulfide
precipitation by the biologically produced H2S. There are various
process parameters such as (i) electron donors, (ii) sulfate source,
(iii) effect of COD/SO24 ratio and (iv) pH that can influence the
production of biogenic sulfides (Sethurajan et al., 2017b). Similarly,
(i) metal to sulfide ratio and (ii) pH affect the MSP by biogenic
sulfides (Sethurajan et al., 2017b). MSP efficiency by biogenic sul-
fides could also be affected by SRB metabolites and medium com-
ponents such as EDTA and acetate (Esposito et al., 2006). MSP has
been reported for successfully removing metals from industrial
wastewater (Kosin
ska and Mi
skiewicz, 2012), synthetic bioleachate
(Cao et al., 2009), Cu-metallurgical slags (Kaksonen et al., 2011), Zn- Fig. 5. Flowchart showing selective recovery of heavy metals from polymetallic
leach residues bioleachate (Sethurajan et al., 2017b) and also leachate by bioprecipitation (adapted from Sethurajan et al., 2017b; 2017c).
various other sources (Lewis, 2010).
A major advantage of bioprecipitation is the possibility of se-
lective recovery of metals from multi metallic leachate. As metal polymetallic solution with high concentrations of Fe and Zn. Fe was
sulfide formation is dependent on the solution pH, metals can be firstly removed as Fe-oxide, followed by selective Zn recovery (as
selectively precipitated as metal sulfides by varying the system pH. sphalerite) using biogenic sulfides. The biorecovery of Zn from ZLRs
A flowchart depicting the strategy for selectively recovering metals by biogenic sulfide was comparable with that of chemical recovery
from polymetallic leachate is shown in Fig. 5. Kaksonen et al. (2011) by sodium sulfide addition (Sethurajan et al., 2017b). A major
investigated MSP from Cu-metallurgical slag bioleachates, using drawback of the bioprecipitation is sludge (by-products) formation.
biogenic sulfides. It was observed that over 98% of Cu could be Sludges (e.g. Fe-oxides) were co-generated during the bio-
precipitated at pH 2.8, more than 99% of Zn could be recovered at precipitation (Sethurajan et al., 2017b). Based on the leachate
pH 3.9 and approximately 60% of Ni recovered at pH 6.0e6.5. composition, the by-products (sludges) can also be precipitated as
However, selective recovery of metals was not attempted in this useful minerals like jarosite (Hu and Hu, 2012; Yazici et al., 2014a),
study. Sethurajan et al. (2017b) demonstrated efficient selective goethite (Yazici et al., 2014b) and paragoethite (Loan et al., 2006).
biorecovery of Zn from ZLRs. The ZLR bioleachate was a These Fe-oxides can be used in industries (e.g. cement industries
 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153
(Katsioti et al., 2005)). And another unavoidable by-product co-
generated during the bioprecipitation process is the spent-leachate.
Usually, the spent-leachate is depleted of heavy metals and also the
pH of the spent-leachate will also be increased to neutral - alkaline
range. Hence, this spent-leachate could be eco-friendly in nature
and can be disposed in the environment. However, more research is
needed prior to any practical applications.
5.2. Biosorption
Sorption is one of the widely used and relatively cost effective
technologies, which can be applied to heavy metals containing
aqueous solutions. The mechanism of sorption involves three
important phases (Das, 2010), (i) solid phase (which denotes the
sorbent used), (ii) liquid phase (water is normally used as the sol-
vent) and (iii) dissolved phase (refers to the dissolved metals ions).
Sorbents such as clay minerals, biological materials, carbon nano-
tubes, activated carbon, metal oxides and zeolites are mostly used
(Zhao et al., 2011) in the sorption of heavy metals. Ion-exchange
and expansion properties are important on the selection of suit-
able sorbent materials. Apart from low cost, sorption has other
advantages like low sludge production and regeneration of the
sorbent. The major limitation of this technique is the early satura-
tion of the sorbent (Alluri et al., 2007).
Biosorption is one of the emerging technologies developed for
the removal of heavy metals from wastewater. Microorganisms
such as bacteria and fungi can be used as sorbents and the process
is termed as biosorption. Microorganisms can sorb metals on their
cell wall either by their property or for a defence mechanism. Not
only microbes, even some plants would also be able to sorb metals.
They can uptake the metals either by active processes (at the
expense of energy) or passive processes (electrostatic attachment
to the cell wall). Different biosorbents have been reported for the
metal recovery from metal bearing waste streams (Petrisor et al.,
2002; Zouboulis et al., 2010). Petrisor et al. (2002) investigated
biosorption of metals from leachates generated at mine waste
disposal sites. Zouboulis et al. (2010) studied the biosorption effi-
ciency of Aeromonas caviae and Penicillium chrysogenum for the
removal of heavy metals from industrial wastewater. Biosorption is
also one of the fascinating alternative approaches to remove metals
from the heavy metal containing wastewater but still rigorous
laboratory trials are required.
5.3. Bioreduction
Bioreduction is a process that convert the soluble metal species
(especially precious metals like Au, Ag and Pd) to insoluble species.
This bioreduction is catalyzed various enzymatic or non-enzymatic
processes (Nangia et al., 2009; Sharma et al., 2009; Merza et al.,
2012). Bioreduction can be applied not only to precious metals
but also to toxic metal species. For instance, Cr(VI), Se(IV) and Se(VI)
and highly mobile Co(III) can be biologically reduced to non/less
toxic Cr(III) and Se(0) and less mobile Co(II) (Cheng and Li, 2009;
Sahinkaya et al., 2012; Nancharaiah and Lens, 2015; Reddy et al.,
2016). Bioreduction mediated biorecovery of Au, Ag and Pd from
the synthetic solutions have been reported in many instances but
there only a very few studies reported for the recovery of metals
from leachates (Kaksonen et al., 2014; Suja et al., 2014; Nancharaiah
et al., 2015, 2016). Zhou et al. (2016) investigated the bioreduction
mediated synthesis of Au nanoparticles from the synthetic E-waste
leachates. Bioreduction is a potential biorecovery strategy for the
recovery of precious metals from the leachate, however rigorous
lab-scale investigations are necessary prior to implementing it at
large-scale applications.
149
5.4. Bioaccumulation
Bioaccumulation is another potential biotechnological approach
for the removal of heavy metals from the wastewater. Heavy metals
uptake and transportation by living biomass is referred as bio-
accumulation (Jaafar et al., 2015). Bioaccumulation is distinctly
different from biosorption due to the fact that both living and dead
biomass can be used as biosorbents but only active biomass can be
used for bioaccumulation. Only living organisms can transport the
metals to the cell and accumulate the metals inside the cell

˛ tek and Krzywonos, 2014). Bioaccumulation is
(Zabochnicka-Swia
an active process (needs energy and respiration) unlike passive
biosorption (Dixit et al., 2015; Mosa et al., 2016). Bioaccumulation is
highly dependent on various factors such as structural properties,
physiological and genetic properties of the bacteria and speciation
and bioavailability of the heavy metals. Bacteria, under certain
conditions (such as increased metal exposure) produce metal-
binding proteins such as metallothioneins (MT) that can bind with
metals and transport them into the cell (Mosa et al., 2016). Few
reports were reported on the bacterial bioaccumulation of heavy
metals from synthetic solutions (Ahemad and Malik, 2011; El Baz
et al., 2015). However, very less or no studies that deals with the
bioaccumulation of heavy/precious metals from real industrial
wastes have been reported.
6. Future perspectives
On one hand, this review showed that the metal laden solid
wastes that are co-generated during mining and metallurgical
processes can be seen as a potential secondary resources for non-
ferrous metals. On the other hand, disposal of these solid wastes
is not only expensive but also adds remediation penalty due to
improper waste management practices. Hence, bioprocessing of
metal bearing solid wastes will introduce a new dimension to the
metallurgical industries in terms of sustainable resource utilization
and waste management. This way, the environmental impacts
associated with the storage and deposition of metal laden wastes
can be minimized. End products of a biohydrometallurgical pro-
cesses can be incorporated into an existing metallurgical unit op-
erations. For instance, bioleaching of Zn bearing metallurgical
waste that originate from Zn-sulfide primary ore, followed by
biogenic sulfide precipitation result in Zn-sulfide precipitates. This
Zn-sulfide can be seen as a potential alternative feed stock to
naturally occurring Zn-sulfide primary ore. Consequently, the
capital cost incurred in storing hazardous metallurgical wastes can
be reduced and the gradual depletion of the high grade mineral
resources can be addressed as well. Still, there is a room for
improvisation of metal recovery efficiency and commercialization
of this perspective. Recent innovations in biomining such as
reductive bioleaching of oxidized ores and urban biomining of
electronic wastes will also ensure opening of new doors in the
mineral and metal industries.
7. Conclusions
This review showcases that biotechnological management of
metallurgical wastes is attractive due to comparable efficiency with
pyro/hydrometallurgy and eco-friendly nature. Bio-
hydrometallurgy of metals from primary ores has been well
established and commercially viable. However, bio-
hydrometallurgy of low-grade ores and metallurgical wastes
remain challenging for commercial perspectives. Biological selec-
tive recovery of metals by bioprecipitation was proved to be an
alternative to chemical precipitation but its commercial perspec-
tive is yet to be proved. Selection of suitable microorganisms for
150 M. Sethurajan et al. / Journal of Environmental Management 211 (2018) 138e153
bioleaching and suitable biorecovery strategy, ensure maximum
recovery of metals from the metallurgical wastes.
Acknowledgements
The authors thank the financial support provided by Depart-
ment of Science and Technology (DST) - Science and Engineering
Research Board (SERB) under the frame of National Post-doctoral
fellowship (nPDF) no SERB-nPDF-000893 and the Experienced
Water Postdoc Fellowship COFUND Programme (FP7-PEOPLE-
2013-COFUND).
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