Hydrometallurgy 103 (2010) 1-157

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The fungal and chemolithotrophic leaching of nickel

laterites Challenges and opportunities
a
Geoffrey S. Simate Sehliselo Ndlovu a, Lubinda F. Walubita b
a
School of Chemical and Metallurgical Engineering, University of the Witwatersrand, Johannesburg, P/Bag 3, Wits 2050, South Africa b TTI,
Texas A&M University System, College Station, TX 77843, USA

A R T I C L E A B S T R A C
I N F O T
Article history: Nickel is an important metal in human life and in the industry. In recent years,
Received 22 August 2009 the world nickel demand has been driven by soaring steel production,
Received in revised form 11 March 2010 particularly in China. With the rapid growing demand for nickel coupled with
Accepted 16 March 2010 the depletion of high grade sulphide reserves, low-grade nickel ores, which
Available online 25 March 2010
cannot be economically processed by conventional metallurgical processes,
become increasingly important sources of nickel. Laterite ore, which is often
Keywords:
considered as a low-grade nickel ore, contains several kinds of metal elements
Microbial leaching
Nickel laterites
including nickel, cobalt, iron, silicon, aluminium, and chromium; and thus,
Chemoorganotrophic constitutes an alternative source of nickel. The nickel present in nickel
Fungal laterites is not usually present as discrete minerals, but as cations substituted
Chemolithotrophic within manganese oxides, goethite, and/or clays. Because of this, it is difficult
Microorganisms to upgrade the ore by beneficiation. As a result, nickel laterites are
traditionally processed using pyrometallurgical and hydrometallurgical
methods. In recent years, microbiological leaching has been found to be a
promising novel technology for recovering valuable minerals from traditionally
difficult-to- process ores. Microbial leaching of low-grade ores offers many
advantages over other conventional methods due to its relative simplicity,
requiring mild operating conditions, low capital costs, low energy input,
relatively unskilled labour requirements, and being environmentally friendly.
Because of the importance of microbial leaching, recent advances in microbial
assisted leaching of nickel laterites are discussed in this paper with emphasis
on fungal (chemoorganotrophic) and chemolithotrophic microorganisms.
2010 Elsevier B.V. All rights reserved.

Introduction
Though nickel laterites are in abundance contributing over 70% of land
based nickel reserves, it accounts for only approximately 40% of the world
annual nickel production (Moskalyk and Alfantazi, 2002;
Elias, 2002; Gleeson et al., 2003; Dalvi et al.,
2004; Watling, 2008). This is because the mineralogical
complexity of nickel laterites brings a lot of challenges in its processing.
Presently, most of the nickel comes from sulphide deposits. However,
worldwide reserves of this high grade nickel sulphide ores are diminishing
due to the rapid demand for the metal. The increasing cost of mining
sulphide resources underground and increasing environmental compliance
costs are also having a strong impact on the economics of mining these
deposits.
Interest in the microbial leaching of nickel laterites has increased over
the last decade. Microbiological leaching of low-grade ores offers many
advantages over other conventional methods due to its relative simplicity,
mild operating condition requirements, low capital costs, low energy
input, less skilled labour requirements, and beingenvironmentally friendly,
among others (Acevedo, 2000). The microorganisms which are
important in the biohydrometallurgical processes concerned with metal
extraction may be divided into two groups on the basis of nutritional
requirements, i.e., autotrophic and heterotrophic microorganisms. For
biological synthesis, the microorganisms require carbon, which they can
derive either from carbon dioxide or from organic substances.
Heterotrophic microorganisms make use of organic compounds as their
carbon sources; whereas autotrophic microorganisms make use of carbon
dioxide. In addition, chemoorganotrophic microorganisms obtain energy
through the oxidation of organic compounds, while chemolithotrophic
microorganisms make use of reduced inorganic compounds. Other micro-
organisms (i.e., facultative autotrophs), although they can metabolise
2 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157

organic compounds, have the additional capability to be

autotrophic depending upon their particular environment.
 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157
The most widely studied of these microorganisms in the
microbial assisted leaching of nickel laterites are those
which are fungal in nature. Fungi are heterotrophic and do
not perform photosynthesis (Glazer and Nikaido,
2007). These microorganisms secrete hydro- xycarboxylic
acids which dissolve nickel by lowering the pH, and
complexion/chelating into soluble organic-metallic
complexes (Tze- feris, 1992). On the other hand, the
use of chemolithotrophic microorganism has not been
explored much because of the lack ofreduced iron, and
inadequate sulphur in the nickel laterites. Reduced iron and
sulphur compounds can be used as energy suppliers for the
microorganisms. The biological oxidation of relevant
reduced sulphur moieties and the subsequent acid
generation is of great importance as it leads to the
liberation of nickel from the laterite ore. Furthermore, ferric
cations produced hydrolyse in the presence of water
generating acid, which can be consumed by nickel laterites;
thus further facilitating the leaching and nickel extraction
processes.
With the above background, the objective of this paper
is to review the current status, challenges and opportunities
arising from the microbial leaching of nickel laterites. As
regards to the scope and content, (1) the paper will briefly
look at the mineralogy of nickel laterites; (2) provide a
review of some of the conventional leaching methods for
nickel laterites; and (3) the research previously and
currently being undertaken on the microbial leaching of
nickel laterites using fungi and chemolithotrophic
microorganisms. The paper will then conclude by looking at
some of the challenges and opportunities in the biorecovery
of nickel from lateritic ores, and give an overview for future
prospects.
2. Mineralogy of nickel laterites
Nickel laterites are residual products of a prolonged
mechanical and chemical weathering of ultramafic bedrocks
at the surface of the earth (Golightly, 1981). The
mineralogy of nickel laterites is considered as being
complex (Alibhai et al., 1993). Commercially
viable nickel laterites generally do not contain discrete
nickel minerals, but ionic nickel is incorporated within, or
adsorbed by, a number of secondary oxides and silicate
minerals (Burger, 1996; Valix et al., 2001a).
On the basis of mineralogy, nickel laterites are classified as
oxide deposit, clay silicate deposit and hydrous silicate
deposit (Brand et al., 1998; Elias, 2002).
Nickeliferous limonite, (Fe,Ni)O (OH)-nH2O, is the oxide
deposit consisting mainly of goethite with mean grades of
1.0-1.6% nickel. The hydrous silicate deposit is dominated
by a mixed structure of hydrous magnesium-nickel silicates
and is informally known as garnierite, ((Ni,Mg)SiO 3-nH2O),
with the highest global nickel grades averaging 1.8-2.5%
(Brand et al., 1998; Gleeson et al.,
2003). The clay silicate deposit is nontronite (Camuti
and Riel, 1996) with mean grades averaging 1.0-1.5%
nickel (Brand et al., 1998).
3. Conventional methods of leaching nickel lateritic
ores
Several industrial methods are used to recover nickel
from low- grade laterites, and these have been extensively
documented elsewhere (Canterford, 1972;
3
Whittington and Muir, 2000; Moskalyk and
Alfantazi, 2002; Dalvi et al., 2004;
Simate, 2009). The difference in mineralogy is the
major factor controlling the choice of the treatment process;
thus all the three classes of nickel laterite ore discussed
above vary in processing requirements and economic value
(Gleeson et al., 2003). Table 1 gives an
estimate of the global resources for nickel laterites, from
the perspective of the processes employed to extract nickel
(hydrometallurgical or pyrometallurgical), in millions of
metric tonnes.
As shown in Table 1, there is almost twice as much
laterite resource that is amenable to hydrometallurgical
processing (e.g. limonite, nontronite/smectite) compared to
that amenable to pyro-
Table 1
Global resource for nickel laterites ( Dalvi et al., 2004).
Processing Resource Assay % Ni content Distribution
method Mt Ni Mt %
400
Pyrometallurgy 0 1.55 62 39
Hydrometallurgy 860 1.15 99 61
0
Total 12, 1.28
600 161 100
Mt = metric tonnes; Ni = nickel.
metallurgical processing (e.g. saprolite and garnierite)
(Elias, 2002; Dalvi et al., 2004). The higher
source of laterite ore with a low nickel content that is more
amenable to hydrometallurgical processing means that
future plants will have to focus more on cheaper and
environmental friendly hydro-processing routes (Simate,
2009).
Some of the industrial methods include reduction
roasting (Panda et al., 1980; Chander and
Sharma, 1981) followed by ammonia leaching (Caron
process), or high pressure leaching with sulphuric acid
(Georgiou and Papangelakis, 1998;
Rubisov and Papangelakis, 2000; Rubisov
et al., 2000; Kar et al., 2000; Moskalyk
and Alfantazi, 2002). The use of these methods,
however, is usually limited by the feed composition and
because of the worldwide trend of low nickel content in
ores, they are costly, especially the pyrometallurgical
treatment. In the case of serpentinic laterite, sulphuric acid
leaching or reduction roasting would be difficult to use
because of the high magnesium content (up to 20%) of the
laterite (Lee et al., 2005). Magnesium and
aluminium are strong acid consumers, and high levels of
aluminium can cause the formation of alunite ((H 3O)Al3
(SO4)2(OH)6) scale in the autoclave, which is undesired
(Georgiou and Papangelakis, 1998; Elias,
2002). Blending of ores to get some required grade is
recommended for different processes. Fig. 1 shows
generalised block flow diagrams for conventional nickel
laterite processes.
Xu et al. (2005) suggested the concentrated
sulphuric acid acidolysis and water leaching method.
Though this method is simple, effective and less energy
intensive, the sulphuric acid consumption of this method is
very high at 83 kg H2SO4/kg of valuable metals. A method
by Lee et al. (2005) extracts nickel through
electrochemical leaching. The electrochemical extraction of
nickel can be used for any type of laterite, regardless of the
magnesium and/or iron content. Despite some advantages,
there are some problems associated with this method.
 4 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157

Among these, is the low recovery of nickel, which was found

to be 50-75% of the initial nickel concentration and
dependent on the type of laterite and the iron content. It is
expected, however, that the recovery can be enhanced
through further developments of the technology. Since the
method is based on electrolysis, the selection of the
electrodes and the design of the cell will play an important
role in determining the efficiency of the extraction, as well
as the power consumption. Finally, this method causes
some environmental pollution from the emission of sulphur
dioxide during electrolysis.

Fig. 1. Generalised block flow diagram of conventional processes ( Dalvi et al., 2004).
 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157
Another pyrometallurgical method, segregation roasting
of laterites, may be considered for extracting nickel
(Wright, 1968). This method also has some
disadvantages in that flotation or magnetic separation is
required prior to ammonia leaching and, therefore, such
treatment would be more costly than the hydrometallurgical
processes.
Table 2 shows a summary of the advantages and
disadvantages of various processes as shown elsewhere in
literature (Acevedo, 2000; Rawlings, 2004;
Dalvi et al., 2004; Ndlovu, 2008).
4. Microbial assisted leaching of nickel laterites
In view of the several disadvantages of processing nickel
laterites by conventional methods, the interest in microbial
leaching has continued unabated. It has clear
environmental advantages, is economically competitive and
enables reductions in energy consumption as well as in
pollution and wastage generation. It is, therefore, of interest
to review a rapidly growing microbiologically based nickel
extraction.
4.1. Leaching using fungi
NiO + 2H+ ^Ni2+ + H2O(1)
MCO3 + 2H+ ^M2+ + H2O + CO2
where M is Fe, Mg, Mn, or Ca, etc.
Reduction
MnO2 + 2e- + 4H+ ^Mn2+ + 2H2O
Complexation/chelation
Ni2 + +C6H8O7^Ni(C6H5O7)- + 3H+
5
Microbial leaching of non-sulphide ores, especially oxides
and silicates, represents a new challenge. For these ores,
including laterites, chemoorganotrophic leaching using
fungi is necessary. This is because the organic acids
metabolically produced by fungi have a dual effect of
providing hydrogen ions for acidolysis of minerals and
complexing metals due to their chelating capacity
(Tzeferis, 1994; Gadd, 2001). Therefore, the
leaching of nickel laterites by fungi, which are heterotrophic
microorganisms has continued to be the main focus of
research in the recent past. In fact, several other
heterotrophic microorganisms, which include both bacteria
and fungi species are known for their leaching capabilities,
especially of oxidic, siliceous or carbonaceous material
(Willscher and Bosecker, 2003). These micro-
organisms, in direct contrast to autotrophs, ingest biomass
to obtain their energy and nutrition. The heterotrophs have
an absolute dependence on the biological products of
autotrophs. This is because they obtain their carbon for
growth solely by feeding on the carbonproduced by
autotrophs (e.g., dead plants and dead organic matter).
Aspergillus and Penicillium are the two widely studied
strains of fungi that can be used in the microbial leaching
(Bosecker, 1986, 1989, 1997; Franz et
al., 1991; Coto et al., 2001, 2003,
2005; Valix et al., 2001a,b,c).
Metal leaching by fungi generally involves an indirect
process with microbial production of organic acids, amino
acids, and other metabolites. Four mechanisms have been
identified: (i) acidolysis, (ii) complexolysis, (iii) redoxolysis
(Berthelin, 1983), and (iv) bioaccumulation (Weed
et al., 1969). The first three processes occur through
metabolites excreted by the fungus, while the fourth
process can be observed if the fungus accumulates the
metal ion from the solution and - by disturbing the
equilibrium between solid and dissolved metal - causes the
continuous solubilisation of the metal (Burgstaller
and Schinner, 1993).
The following are some of the possible reactions that
can take place to finally produce nickel ions (Tzeferis,
1992):
Proton attack
(2)
(3)
(4)
6 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157

In Eq. (1), the protons produced by organic acids

contribute to proton promoted mineral dissolution. As
mentioned in the Introduction, from a mineralogical
point of view, nickel laterite is considered as having a
complex mineralogy, i.e., few nickel atoms are spread in a
solid solution of atoms of other elements which appear in
large

Table 2
Advantages and disadvantages of various nickel recovery processes.

Smelting Caron process High pressure acid leaching Microbial leaching

Advantages Proven technology
Disadvantag Environmental concerns
es
Expensive to run
High temperature process
Effective only with specific
lateritic ore type with specific
grades (e.g., predominantly
Requires high technological
outlay
Proven technology
Environmental concerns
Expensive to run
Effective only with specific
lateritic ore type with specific
grades (e.g., limonite or mixture
of limonite and saprolite)
High temperature process
Requires various reagents
Requires high technological
outlay
Proven technology
Low temperature
process
Short residence time required Runs at atmospheric
pressure
Low degree of process
control
Can treat low-grade
nickel laterite ores
Cheaper to run
Requires simple
technological outlay
Environmental concerns Long residence time
required
Expensive to run Only been successful
at demonstration plant
scale
High temperature process
Runs at elevated pressures
Requires a higher degree of process control
An oxygen plant is required to supply the
necessary oxygen
Effective only with specific lateritic ore type
with specific grades (e.g., predominantly
limonite)
Requires high technological outlay
 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157 7

Table 3
PHIEP of laterite ore gangue ( Valix et al., 2001d). initial concentration of nickel.

Ore type PHIEP

Limonite 6.6
Nontronite 2.0
Saprolite 3.6
Weathered saprolite 3.8

quantities, such as Fe, Mg, Al, Mn, Ca, etc. As a result, acid
attack (Eq. (2)) of any carbonate material in the ore also
enhances nickel liberation. However, this reaction requires
the generation of excess acid. Furthermore, the reduction of
soluble manganese (Eq. (3)) can result in the equilibrium
pHIEP is the pH value that corresponds to isoelectric point of the
ore.

between solid-phase Mn4+ and soluble- phase Mn2+ being

shifted somewhat, accelerating the dissolution of the
mineral, thus liberating nickel. In Eq. (4), organic acids
complex with metal ions in solution, lowering metal activity,
thus increasing the apparent solubility of the mineral
(McKenzie et al., 1987).
The use of fungi in a quest to recover nickel from low-
grade nickel laterite ores has been studied by several
researchers (Bosecker, 1986; McKenzie et al.,
1987; Alibhai et al., 1993; Tzeferis,
1994; Valix et al., 2001a,b; Le et al.,
2006; Tang and Valix, 2006). However,
commercial application of these microorganisms has been
less successful due to process inefficiencies such as poor
metal recovery (Tang and Valix, 2006). This problem
is particularly prevalent in limonite ore, characterised by
high iron content in the form of goethite (FeOOH) and
nontronite, characterised by clay minerals consisting of
illite, kaolinite, and chlorite (Tang and Valix, 2006).
The effectiveness of these microorganisms was found to
depend on their ability to produce hydroxycarboxylic acids
(citric, lactic, gluconic, pyruvic and tartaric), and also other
metabolites, which are excreted in culture media
(Burgstaller and Schinner, 1993;
Tzeferis, 1994; Castro et al., 2000; Le
et al., 2006), and their resistant to heavy metals
(Burgstaller and Schinner, 1993; Le et
al., 2006). The results of these studies showed that
microbiological leaching is more effective compared to
chemical leaching. The more favourable results obtained in
the bioleaching process suggest that microbiological
activity, apart from bio-acid production is participating in
the leaching process (Valix et al., 2001a). It is
suggested, for example, that fungal hyphae physically
attach onto surfaces of minerals with possibility of high acid
concentration formed at hyphal tips reacting directly with
adjacent mineral surfaces without greatly affecting the pH
of the bulk medium (Alibhai et al., 1993).
Alibhai et al. (1993) examined different
samples of nickel laterites from different locations. The
chemical composition of these samples varied. Less
definitive information, such as effects observed with
different particle size fractions was employed because
direct linkage of mineralogical characteristics with leaching
efficiency was found difficult. The results of these
experiments showed that more leachable nickel-bearing
phases were generally more readily available in the larger
particles, even though the smaller particles carried a higher
8 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157

The studies by Tzeferis and Agatzini- suppressed metal dissolution. These results emphasises the
Leonardou (1994), Castro et al. (2000), importance of pH, ORP, and pulp density control during the
and Valix et al. (2001a) clearly showed bioleaching of nickel laterite ores.
differences in the leachability of different minerals (and/or Table 4 shows a summary of some of the studies
the metal present in it), i.e., the mineralogy of the ores had conducted, showing the types of ore or mineralogical
significant effects on the metal recovery and selectivity of makeup of nickel laterite, fungi species, types of acid
the leaching process. Extraction of nickel appeared more produced, and a range of recoveries obtained. It must be
effective from the silicate ores, the saprolite and weathered noted, however, that these studies were carried out for
saprolite, and least effective from limonite ores (Valix et different objectives, hence the experimental designs
al., 2001a,b). The nickel in the silicate ores, on the differed, e.g., the studies by Le et al. (2006) was
other hand, which are present in the brucite layer of the for fungal heavy metal
clay minerals, is weakly bound and, therefore, easily
dissolved (Valix et al., 2001b). Valix et al.
(2001b) further studied the effects of electrosorption,
physical properties and the mineralogy of the ores in an
attempt to establish the reasons for the difference in the
amenability of saprolite and limonite minerals toward
biological leaching. The results showed that leaching below
the isoelectric point increased the nickel and cobalt
recoveries for both the saprolite and limonite. This is
because the positively charged gangue inhibits the re-
adsorption of nickel and cobalt complexes on it. The
isoelectric point (i.e. point zero charge) of the various ores
is summarised in (Table 3). However, Beukes et
al. (2000) found that the ability of goethite and
hematite to adsorb nickel was also dependent on the
surface area, i.e., the larger the surface area, the higher the
adsorption per surface area of the mineral. It was also found
that high recovery of nickel and cobalt appears to be
associated with acid dehydration of the mineral phase in
which nickel and cobalt are associated. This phase change
was clearly seen with the saprolite ores where the
magnesium hydrosilicate mineral formed an amorphous
magnesium silicate phase, in which nickel became unstable
and was susceptible to acid attack. The acid was found to
be less effective in dehydrating goethite to haematite,
which resulted in poorer nickel and cobalt extraction. These
observations indicate that the choice of the suitable type of
nickel laterites is paramount in the development and
optimisation of such a process.
Apart from the effect of mineralogy, Tang and
Valix (2006) showed that nickel and cobalt
dissolution were also dependent on acid activity, oxygen
reduction potential, and pulp density. While previous studies
showed that various acids exhibit differences in
effectiveness in dissolving metals from laterites (Alibhai
et al., 1993; Burgstaller and Schinner,
1993; Tzeferis, 1994; Tzeferis and
Agatzini-Leonardou, 1994; Castro et al.,
2000), the results by Tang and Valix (2006)
suggested that the extent of metal dissolution is dependent
on the acid activity (hydronium ion concentration) rather
than the type of metabolic acids used. Other results by
Tang and Valix (2006) also suggested that highly
oxidizing conditions found at higher pulp densities
Table 4
Summary of the fungal leaching of nickel laterites.
Type of fungi or Ni recoveries (%
Ore/minerals strains Acid types wt) Reference
Saprolite, limonite, nontronite
Aspergillus,
X Up to 36
(2001a)
Garnierite, chlorite
Penicillum
Aspergillus, Citric, oxalic 50-60 al. (1993)
Limonite, garnierite, nontronite
Penicillum
Penicillum Citric Up to 72 (1986)
Greek nickeliferous Aspergillus, Citric, oxalic 55-60 (1994)
Calamine, garnierite
Penicillum
Aspergillus niger Citric, oxalic Up to 78
al. (2000)
Weathered saprolite Aspergillus foetidus X 28 (2006)
Saprolite, weathered saprolite, limonite, nontronite Aspergillus, X Up to 35 (2001d)
Chromite overburden Penicillum
Aspergillus Citric acid, oxalic, Up to 34 (2007)
gluconic
X' means not given.
G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157 9

Fig. 2. Schematic comparison of the thiosulfate (A) and polysulfide (B) mechanisms in (bio)leaching of
metal sulfides ( Schippers and Sand, 1999; Schippers et al.,
1996 ).

tolerance determinations, whereas that by Valix et

al. (2001d) was meant to study the electrosorption
properties of nickel on laterite gangue. It is also clear from
Table 4 that citric and oxalic acids were the two well
established products of fungal metabolism. Citric acid was
the most effective and oxalic acid was the least effective
leaching agent (Tzeferis, 1994). A possible
explanation for this could be that oxalic acid precipitates
the leached nickel as nickel oxalate, which is known to have
a very low solubility (Tzeferis, 1994).

4.2. Leaching using chemolithotrophic microorganisms

Until recently (Simate and Ndlovu, 2007;

Coto et al., 2008; Simate and Ndlovu,
2008; Simate, 2009; Simate et al.,
2009a,b; Ndlovu et al., 2009), literature on the
bacterial assisted leaching of nickel laterites using
chemolithotrophic microorganisms has been scarce. Chemo-
lithotrophic bacteria solubilise solid metal compounds by
two mechanisms: (i) in order to gain energy the leaching
material is solubilised by enzymically catalyzed reactions,
which imply a physical contact between the bacterium and
the leaching material and lead to the destruction of the
mineral, and (ii) the end products of these reactions,
namely sulphuric acid, supplying protons, and ferric iron,
supplying oxidizing capacity and protons, contribute also to
the solubilisation process. However, currently the two
postulated indirect mechanisms with no evidence for a
direct enzymatically mediated process have been used
widely. These are termed the thiosulphate mechanism and
the polysulphide mechanism (Schippers and Sand,
1999; Hanford and Vargas, 2001; Sand et
al., 2001), as shown in Fig. 2.
Because nickel laterites contain no energy source for the
growth of chemolithotrophic bacteria which depend on the
oxidation of sulphur or reduced iron and sulphur
10 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157

compounds, it becomes inevitable; therefore, that sulphur + +

or sulphur containing material is added. The primary NiO + 2H ^Ni2 + H2O

oxidations of sulphur containing minerals provide sulphuric

acid solutions (see also Fig. 2), which solubilises the (6)
metal content as shown below.
(where M is a metal).
bactem
The use of a mixed culture of chemolithotrophic
MSx + (2X-0.5)O2 + H2O ^ Mx+ + XSO24~ + microorganisms is also expected to promote the dissolution
2H+ (5)
of nickel laterites. This is because competition for oxygen
by iron oxidizing bacteria (Simate, 2009; Simate et
al., 2009b) could lead to reductive dissolution of ferric
iron in nickel laterites, thus destabilizing the structure of the
nickel laterites (Bridge and Johnson, 1998). As
indicated in the following equation (Bridge and
Johnson, 1998), the reduction of soluble ferric iron by
bacteria can result in the equilibrium between solid-phase
iron (III) and soluble-phase iron (III) being shifted somewhat,
accelerating the dissolution of the mineral:

2Fe H 2Fe H O 2F
soTidphase + 2" so"lublephase + 2 ^ ^
(7)

+ 'A O2 + 2H+(bybacterialreduction)

Using a mixed culture of chemolithotrophic

microorganisms (Acidithiobacillus ferrooxidans,
Acidithiobacillus caldus and Leptospirillum ferrooxidans),
Simate and Ndlovu (2007, 2008) statistically
determined the parameters that were effective in the
bacterial leaching of nickel laterites, whose mineralogy is
shown in Table 5. The

Table 5
Simate
Relative abundances of minerals in the nickel laterite ore sample (
and Ndlovu, 2008; Simate et al., 2009b).
Occurrenc
Mineral phase e
Nickeliferrous serpentine [(Mg, Fe, Ni)3Si4O5(OH)4] Minor
Goethite, hematite [(Fe,Ni)O(OH), Fe4O3H4O] Major
Titaniferrous pyrite [(Feji^] Trace
Nickeliferrous pyrite [(Fe,Ni) S2] Trace
Talc [Mg6Si8O20(OH)4] Trace
Saponite [Cao.45(Mg,Fe)3(Si,Al)4O'o(OH)4nH4O] Trace
Tremolite [Ca4Mg5Si8O44(OH)4] Trace
Quartz [SiO2] Predomina
nt
Predominant: >50% by mass; major: 20-50% by mass; minor: 5-10% mass; trace:
<5% by mass.
 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157
statistically significant factors included pH, particle size,
pulp density, and substrate type. Follow-up studies showed
that using elemental sulphur as an energy source
(compared to pyrite) was more effective in terms of
bacterial growth and acid production, hence higher nickel
recoveries (Simate, 2009; Simate et al.,
2009a). Under the optimisation experimental conditions
considered, the set of conditions that produced the
optimum nickel recovery (79.8%) were found to be a pH of
2.0, 63 pm particle size, and 2.6% pulp density (Simate,
2009; Simate et al., 2009b). These results can
constitute the basis to design a treatment process for
recovering even the rest of metals present in the nickel
laterites.
A recovery of nickel from a low-grade chromite
overburden was also attempted by employing mixed culture
of acidophiles in which A. ferrooxidans were predominant
(Mohapatra et al., 2007). In these studies,
increased nickel recoveries were observed with the higher
ferrous iron concentration in the culture medium. Here, two
possible mechanisms are likely to have promoted the
dissolution of nickel from lateritic ore. Firstly, the bacterial
oxidation of ferrous iron produces ferric iron. Subsequently,
ferric cations hydrolyse in the presence of water generating
acid, which can be consumed by nickel laterites; thus
facilitating the leaching and nickel extraction processes
(Simate, 2009). Secondly, it may be attributed to the
enhanced dissolution of goethite in acid media at lower
oxidation potential in the presence of ferrous ions (Lu and
Muir, 1988; Tindall and Muir, 1998).
In summary, the bioleaching of nickel laterites using
chemolitho- trophic microorganisms is affected by the lack
of sufficient amounts of reduced sulphur and the lack of
reduced form of iron in the lateritic ores.
5. Challenges and future prospects
5.1. Fungi
Although the amenability of nickel laterite mineral to
fungal leaching process has been successfully
demonstrated through this review, there still remains a
considerable amount of challenges before this process can
be applied commercially.
The successful growth and maintenance of the
organisms in an in-situ bioleaching environment amidst
abiotic stresses are key to the successful application of this
technology. Abiotic stresses from the immediate
environment of the organism, such as the heavy metals
which are dissolved by the organism, can initiate cellular
responses that can inhibit specific metabolic pathways
critical in maintaining bio-acid production and leaching of
minerals (Le et al., 2006). Heavy metals in small
concentrations can induce morphological changes and then
destroy the microorganism cell (Valix et al.,
2001c), while at relatively high concentrations the heavy
metals act as a general protoplasmic poison, inducing
denaturation of proteins and nucleic acid (Avakyan,
1994). However, it was observed that serial acclimatization
could lead to the organisms being tolerant to heavy metals
(Alibhai et al., 1993; Valix et al.,
2001c; Valix and Loon, 2003; Le et al.,
2006). It was also found that different organisms have
different tolerance levels for different types of heavy metals
(Alibhai et al., 1993; Valix et al.,
11
2001c), e.g., Penicillium funiculosum and Aspergillus
foetidus were the most tolerant to heavy metals. In general,
Penicillium simplicissimum exhibited the least tolerance
particularly for nickel and cobalt. The metal toxicity
increases with molecular weight (Avakyan, 1994), and
the presence of multimetals acts in synergy to impose a
greater toxicity in comparison to single metals alone ( Le
et al., 2006). The training of the organism (e.g., A.
foetidus) in the presence of multi-metals was found to
reduce the longer term acid production of the organism (Le
et al., 2006). However, despite the lower acid
production by the multi-tolerant organism, its ability to
dissolve nickel, cobalt, iron, and magnesium from the
weathered saprolite minerals, appeared to be enhanced by
its tolerance development.
The other challenge of using fungi is that they need a lot
of organic carbon source for growth and for the production
ofgreater amounts of leaching agents (Burgstaller
and Schinner, 1993). For successful implementation,
expensive nutrient requirements have to be replaced by
inexpensive carbon sources (e.g. molasses, lignocellulose
sugars, whey permeate) or organic waste products (e.g.
from sewage, paper, agricultural, food and beverage
industries) in order to reduce the overall cost ( Alibhai
et al., 1993; Burgstaller and Schinner,
1993; Tzeferis, 1994). The ability of fungi to grow
on such a wide variety of substrates is very important for
their future applications (Burgstaller and
Schinner, 1993). The other benefit is that the nature
of the leaching active metabolites excreted by these
microorganisms is strongly influenced by the medium
composition. This property may be advantageous if the
leaching agent has to have definite complexing properties
in order to improve the solubility of certain metal ions
(Burgstaller and Schinner, 1993).
Reaction kinetics of fungi was also found to be too slow
to be applicable to stirred tank technology. However, these
bioprocesses can be intensified under the influence of
ultrasound (Swamy et al., 2005). Ultrasound could
substantially improve the bioleaching of lateritic nickel ore
(Narayana et al., 1995; Sukla et al.,
1995) as enhanced growth of Aspergillus niger with
ultrasound was found (Swamy et al., 1993; Swamy
et al., 2005). It is hypothesized that ultrasound
increases the rate of transport of oxygen and nutrients to
the cells and increases the rate of transport of waste
products away from the cells, thus enhancing their growth
(Pitt and Ross, 2003). Furthermore, at certain
intensities, ultrasound has the potential for enhancing mass
transfer within the cell through intracellular streaming
(Bar, 1988) and a membrane permeation enhancing
effect (Swamy et al., 2005).
Depending on the conditions (e.g., pH), leached nickel is
also expected to be lost through electrosorption onto the
nickel gangue over time (Valix et al. 2001d).
However, this is irrespective of whether the process is
microbial leaching or direct chemical leaching. The surface
charge and type of minerals present in the ore gangue were
shown to have an important influence on the adsorption
capacity. Limonite and nontronite showed a higher
adsorption compared to silicate ores even at low pH. This
suggest that the lower recoveries achieved with limonite
and nontronite may be associated with both the difficulty in
leaching the nickel mineral from the goethite matrix, and
 12 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157
also by the higher affinity of nickel towards the gangue
matrix in these ores (Valix et al., 2001d). Table
3 shows the pH values that correspond to isoelectric points
of different nickel laterites ores. Higher pH (e.g., pH >8)
also promotes the precipitation of nickel ions as Ni(OH)2.
The optimisation of a microbial leaching should, therefore,
include adequate control of solution pH. Loss of nickel can
also be as a result of passive physicochemical adsorption
(biosorption) onto or bioaccumulation (active absorption)
within the biomass (Tzeferis, 1994). The two phases
are characterised by sharp differences in activation
energies and kinetics as follows (Rossi, 1990); (1)
activation energies for biosorption amount to 21 kJ mol-1
consistent with the physical nature of the process, whereas
they are of the order of 63 kJ mol-1 for bioaccumulation, as
required by the (bio) chemical nature of the process, (2)
passive adsorption is rapid and independent of the
presence of specific nutrients, whereas active absorption is
slow and nutrient dependent. It must be noted, however,
that the losses due to biosorption and bioaccumulation are
applicable to both the heterotrophic and chemolithotrophic
microorganisms. These losses as will be explained in the
subsequent text can be prevented by the use of a two-
phase process.
The other challenges are that heap or dump leach 5.3.
technology in which a nutrient feed is applied by spraying
onto the ore which has been previously seeded with a
proper fungus inoculum, will probably be confronted by
contamination problems from other organisms (indigenous
or from surrounding environment); by plugging problems
because of deposits of microbial origin which congregate
together and prevent solution flow; and by environmental
polluting problems because of severe biomass presence
(Tzeferis, 1994). To avoid the problem of
contamination, Tzeferis (1994) proposed to use a
two-step procedure in which the production of leachants
and the actual leaching of the nickel would be carried out as
separate processes. This two-phase process in which acid
metabolites are produced in a fermenter under controlled
conditions, followed by biomass-liquid separation and
application of the leaching solution to the ore (in heaps,
vats or in-situ) does not suffer from technical problems
since mycelial material would have been removed from the
fermentation fluid before leaching. Metal accumulation in
mycelial biomass and biosorption onto the microbial cells
can also be avoided using this technique. Tzeferis
(1994) further suggests that profitable application of the
two-step procedure is a matter of cost-benefit analysis
depending markedly on costs of substrates and the fermen-
tation process.
5.2. Chemolithotrophic microorganisms
Among the chemolithotrophic bacteria involved in
bacterial leaching, the acidophilic, iron- or sulphur-oxidizing
chemolitho- trophic microorganisms have been studied
most intensively and are the most important in commercial
operations to date (Rawlings, 2005). In addition, the
bacterial oxidation of sulphide minerals by Acidithiobacillus
bacteria is a well established phenomenon in the
commercial industry for the recovery of copper, uranium,
and in the biooxidation pretreatment of refractory sulphidic
gold ores before cyanidation (Acevedo, 2000;
Brierley and Brierley, 2001; Nestor et
al., 2001; Kodali et al., 2004; Ndlovu,
2008). These attributes make it easy for the application of
chemolithotrophic microorganisms in the microbial assisted
leaching of nickel laterites.
In regions where the nickel laterite ore body exist, the
sustainability of the process will depend on the supply of
sulphur containing material (commercial sulphur or metal
sulphide) for energy requirements of the bacteria. This is
likely to form the dominant operating cost component of the
bacterial leaching of nickel laterite ores using
chemolithotrophic microorganisms. Although elemental
sulphur substrate gave better results than pyrite in terms of
acid production and bacterial growth (Simate et al.,
2009a), it might be more cost effective to use pyrite
because it is the most widespread and represents the
highest composition of sulphur over the other types of
sulphide ores. In addition, this process is promising because
sulphuric acid is produced in-situ whereas in processes such
as high pressure acid leaching, sulphuric acid is produced in
external facilities. However, a two-step leaching process
where ferric sulphate and sulphuric acid are generated
externally by the microorganisms, and then later used in
the atmospheric nickel leach circuit may also be
appropriate.
Summary
Microbial leaching is considered as a simple and
effective technology for extracting valuable metals from
low-grade ores and mineral concentrates. Metal recovery
from sulphide minerals is based on the activity of
chemolithotrophic microorganisms, mainly A. ferrooxidans,
Acidothiobacillus thiooxidans and Leptospirilum ferroox-
idans, which convert insoluble metal sulphides into soluble
metal sulphates. Non-sulphide ores and minerals can be
treated by heterotrophic bacteria and fungi. In these cases,
metal extraction is due to the production of organic acids
and chelating and complexing compounds excreted into the
environment. In addition, metals may be solubilised or
immobilized by chemical or biochemical changes in
oxidations.
This review dealt with previous studies which were
concerned with the extraction of nickel from lateritic ore
through microbial leaching, i.e., the use of fungi and
chemolithotrophic microorganisms. The ability of a number
of fungi to solubilise great amounts of nickel from solid
materials may open up completely new prospects for the
application of fungi. However, there still remains a
considerable amount of challenges before this process can
be applied commercially. On the other hand, because nickel
laterite contains neither ferrous iron nor substantial amount
of reduced sulphur, it is not capable of participating in the
primary bacterial oxidation using chemolitho- trophic
microorganisms. However, its metal value can be recovered
by allowing the primary oxidation of pyrite, or similar
iron/sulphur minerals to provide sulphuric acid solutions,
which solubilise the metal content.
Disclaimer
The contents of this paper reflect the views of the
authors who are responsible for the facts and accuracy of
the data presented herein and do not necessarily reflect the
official views or policies of any agency or institute. This
paper does not constitute a standard, specification, nor is it
intended for design, construction, bidding, contracting, or
 G.S. Simate et al. / Hydrometallurgy 103 (2010) 150-157 13

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