Minerals Engineering 75 (2015) 25

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Minerals Engineering
jou r n a l hom ep ag e: www . el sevi er .co m /l ocat e / m i n
e ng

Biomining in reverse gear: Using bacteria to extract metals

from oxidised ores
D. Barrie Johnson a,, Chris A. du Plessis b

a
College of Natural Sciences, Bangor University, Deiniol Road, Bangor LL57 2UW, UK
b
Metalobus, Perth, Australia

a r t i c l e i n f o a b s t r a c t
Article history: Biomining, as traditionally practised, uses aerobic, acidophilic microorganisms to accelerate the oxidative
Received 5 August 2014
dissolution of sulfide minerals present in ores and concentrates, thereby either causing target metals to
Accepted 30 September 2014
be solubilised (e.g. copper) or made accessible to chemical extraction (e.g. gold). Many acidophiles are
Available online 6 November 2014
also able to catalyse the dissimilatory reduction of ferric iron in anoxic or oxygen-depleted environments,
and can accelerate the reductive dissolution of ferric iron minerals, such as goethite, under such
Keywords:
conditions. Recent work has demonstrated how this approach can be used to extract metals (nickel,
Acidophile
copper, cobalt and manganese) from oxidised ores, such as laterites deposits, at low ( 30 C)
Bioleaching
Copper temperatures. Reductive mineral dissolution has been trialled successfully with a variety of ores, pointing
Cobalt to a generic application of this approach.
Nickel 2014 Elsevier Ltd. All rights reserved.
Reduction

1. Introduction by an oxidative process, and are therefore routinely mostly

Biomining has, over the past 50 years, emerged as an important
area of biotechnology (Brierley and Brierley, 2013; Johnson, 2013;
Brierley, 2008). Within this time it has developed from minimally-
engineered dump leaching of run-of-mine copper ore to computer-
controlled bioreactors used mostly for pre-oxidising refractory
gold ores. However, commercial-scale bio-processing of minerals
is currently restricted to sulfidic ores where the target metals are
either contained in the sulfide minerals present (mostly base
metals), enshrouded with sulfides precluding direct chemical
extraction (as in the case of gold), or present in a reduced oxidation
state in a mineral that can be oxidised by microbially-generated
ferric iron (for example, uranium (IV) in uraninite). In all these
cases, mineral dissolution is mediated via a process of oxidative
dissolution in an extremely acidic lixiviant, in which the main
roles of the prokaryotic acidophiles present is to generate
both the chemical oxidant, ferric iron, and sulfuric acid (Vera et
al., 2013; Rawlings and Johnson, 2007).
Many metals of commercial importance are found in oxidised
as well as, or rather than, reduced ores, and these may represent
the major accessible mineral reserves for some metals, such as
nickel. Oxidised metal ores are obviously not amenable to bio-
processing
Corresponding author at: College of Natural Sciences, Brambell Building,
Deiniol
Road, Bangor LL57 2UW, UK. Tel.: +44 1248 382358; fax: +44 1248 370731.
E-mail address: d.b.johnson@bangor.ac.uk (D.B. Johnson).
processed using pyrometallurgy or hydrometallurgical pressure
leaching methods. However, an innovative biological approach
has, in recent years, been developed for extracting base metals
from oxidised ore bodies, such as laterites. The process of reductive
mineral dissolution is, like most conventional biomining opera-
tions, catalysed by chemolithotrophic bacteria in acidic liquors.
Since the main reaction (the dissimilatory reduction of ferric iron)
is essentially the opposite of that which drives in conventional
mineral processing, it has been referred to as biomining in reverse
gear. The current paper describes examples of successful demon-
strations of metal extraction from oxidised ores mediated by acido-
philic bacteria and suggests other metals and ores where this
approach may, or may not, be applied.
2. Reductive dissolution of nickel laterites
Although nickel sulfides currently account for the major
primary ores of this metal, they account for only 30% of nickel
reserves in the lithosphere, with the rest being oxide ores,
predominantly laterites (Dalvi et al., 2004). Nickel laterite
deposits comprise two distinct zones: (i) a limonitic zone,
generally containing 12% Ni, where most of the nickel is
associated with ferric iron minerals, such as goethite (FeO OH)
and (ii) a saprolite zone, which may contain 35% Ni, and which
is dominated by magnesium silicates. Nickel is recovered from
limonite using the Caron process (involving chemical
reduction of the dried ore at 750 C, and

http://dx.doi.org/10.1016/j.mineng.2014.09.024
0892-6875/ 2014 Elsevier Ltd. All rights reserved.
 D.B. Johnson, C.A. du Plessis / Minerals Engineering 75 (2015) 25 3

extraction of the metal from the calcine produced with
ammoniacal ammonium sulfate; Asselin, 2011) or by the PAL
process (a high pressure and temperature ( 250 C) process in
which nickel is solubilised and goethite transformed to
haematite; Taylor, 2013). While both processes have inherent
high energy costs, this is particularly the case with the Caron
process. Biological options for extracting nickel from limonites
have also been proposed. Bio- processing with species of fungi,
such as Aspergillus and Penicillium, that produce metal-chelating
metabolic by-products such as oxalic and citric acids, has been
demonstrated to solubilize nickel (Bosecker, 1986), but the low
yields of extraction coupled to the costs of substrates (e.g.
glucose) and production of large amounts of fungal biomass
means that this approach has not been consid- ered as a viable
option. Biological production of sulfuric acid (e.g. by
Acidithiobacillus spp.) to acid-leach laterites has also been
proposed (e.g. Simate and Ndlovu, 2008).
It has been known for some time that many species of acido-
philic prokaryotes can catalyse the dissimilatory reduction of
ferric iron to ferrous, usually in an energy-transducing process in
which ferric iron substitutes for molecular oxygen as an electron
acceptor in oxygen-limited environments. Autotrophic, and
facultatively and obligately heterotrophic, acidophiles can
reduce iron using either inorganic (e.g. sulfur or hydrogen) or
organic (e.g. glucose) electron donors (reviewed in Johnson and
Hallberg, 2009). Bridge and Johnson (2000) showed that the
heterotrophic acidophile Acidiphilium SJH could promote the
reductive dissolution of ferric iron minerals as well as reduce
soluble Fe3+, and that the rate at which the mineral was
solubilised correlated with its degree of crystallinity, suggesting
that the rate-limiting step in the process was the acid
dissolution of the ferric iron mineral rather than the reduction of
soluble ferric iron by the bacterium. On the basis of this
observation, Hallberg et al. (2011) screened four pure cultures of
acidophilic bacteria for their ability to catalyse the dissimilatory
reduction of a limonitic nickel ore. The chemolithotroph
Acidithiobacillus ferrooxidans, better known for its ability to oxidize
iron and sulfur, was chosen for bioreactor tests (Fig. 1), since: (i)
this acidophile can use elemental sulfur, which is a more cost-
effective electron donor for ferric iron reduction than organic com-
pounds such as glucose (which is used as both electron donors and
carbon sources by heterotrophic species), and (ii) the reductive
dis- solution of goethite coupled to the oxidation of elemental
sulfur is less consumptive of protons than when coupled to
glucose oxidation (Eqs. (1) and (2)), which means that less
(sulfuric) acid is consumed in a process that uses the inorganic
electron donor:
6FeO OH S0
10H ! SO24 8H2 O 1
2
6Fe
non-reductive acid dissolution. The solubilised nickel was retained
in solution due to the acidity of the leach liquor, and soluble iron
was present exclusively as ferrous iron; both factors would facili-
tate downstream recovery of the metal (Johnson, 2012). Other tests
carried out more recently with a lateritic ore obtained from a dif-
ferent geographical location have conrmed that reductive bio-
processing could be used generically to process nickel limonites
(I. N ancucheo, B.M. Grail and D.B. Johnson, unpublished
data).
3. The Ferredox process: an integrated concept for bio-
processing nickel laterites
Based on the report by Hallberg et al. (2011), du Plessis et al.
(2011) devised a modular process (Ferredox) that integrated the
reductive bio-processing of limonitic ores with the removal of tar-
get metals (nickel, etc.), bio-catalysed precipitation of iron as jaro-
site and the regeneration of acidic ferrous iron as leach lixiviant
(Fig. 3). The ferrous-based leach solution allows for the selective
removal of nickel over ferrous iron directly from the leach solution
using ion exchange resins, such as the DOW M4195 bis-picolyl-
amine, resin at low pH conditions (Hernandez et al., 2011). The
removal of nickel, and cobalt, ahead of iron removal within the
process circuit, overcomes the problem of metal loss due co-pre-
cipitation during ferric iron removal, as is common in conventional
hydrometallurgical process ow sheets (Willis, 2007). A further
advantage of generating a reduced leach solution (PLS) is that sub-
sequent iron removal from the circuit can be achieved via biocatal-
ysed ferrous iron oxidation and jarosite precipitation at low pH,
without the requirement for addition of neutralization agents
(Kaksonen et al., 2014a,b). The iron oxidation process within the
circuit also serves to generate large numbers of the facultative
anaerobe, At. ferrooxidans, which catalyses ferric iron reduction
and mineral dissolution elsewhere in the process. Residual soluble
ferric iron from the ferrous oxidation process, is used in a bio-cat-
alysed reductive acid-generating process in which ferric iron,
rather than oxygen, is used as the electron acceptor (Hedrich
et al., 2013) resulting in the generation of a ferrous iron-based
leach solution.
In contrast to the Caron and PAL processes, all components of
the Ferredox process operate at ambient pressure and temperature,
and in far less aggressive conditions (in terms of temperature, pres-
sure and acidity) requiring relatively inexpensive materials of con-
structing. The low intensity features of the process facilitate
modularization, similar to that used in the wastewater treatment

6FeO OH 0:25C6 H12 O6 12H
2
! 6Fe 1:5CO2 10:5H2 O: 2
Tests carried out in 2 L (working volume) bioreactors main-
tained at pH 1.8 and 30 C showed that >70% of the nickel in the
limonite could be extracted using bacterially-catalysed reductive
dissolution within 30 days (Fig. 2), compared with only 10% by
Fig. 1. Schematic representation of the reductive dissolution of a nickel limonite Fig. 2. Solubilisation of nickel and iron from a limonitic ore catalysed by bacterial
in which sulfur acts as the bacterial electron donor. reduction of ferric iron; inset, the PLS produced (Hallberg et al., 2011).
4 D.B. Johnson, C.A. du Plessis / Minerals Engineering 75 (2015) 25

Fig. 4. Changes in concentrations and speciation of copper and iron in a lateritic

material subjected to bacterially-accelerated reductive dissolution. The arrow
+
indicates the gas supply was switched from N2 to air. Key: , total copper; h, Cu ;
(reproduced from N ancucheo et al., 2014, with
2+
d, total iron; s, Fe
permission
from the publishers).

Fig. 3. Simplied schematic of the Ferredox process (du Plessis et al., 2011).
disso- lution of nickel and copper laterites suggested that other
industry, with the potential for reduced capital and technical risks minerals
for nickel limonite processing.

4. Reductive dissolution of copper laterite

Metals other than nickel can also be found in relatively high

concentrations in some lateritic deposits. In tropical regions, cop-
per-containing gossan caps can occur above deposits that have
undergone supergene enrichment. Again, goethite is commonly
the major ferric iron mineral in these surface lateritic deposits.
Since no cost-effective process has been available to extract copper
from this material, even though it may contain similar amounts of
copper to the underlying ore bodies, these lateritic materials are
generally not considered as ores.
An oxidised lateritic ore from a copper mine in South America
that contained 0.8% (by weight) copper was bioleached under
acidic reducing conditions with elemental sulfur as electron donor,
using similar conditions to those used for nickel limonite
(N ancucheo et al., 2014). Up to 78% of the copper present in
the
ore was extracted by this means, which was signicantly more
than in aerobic cultures or in sterile anoxic reactors maintained
at the same pH and temperature. The copper extracted included
that leached from acid-labile minerals (chiey copper silicates,
such as chrysocolla) as well as most of the fraction associated
with goethite. Soluble iron in the anoxic leach liquors was
present as ferrous iron (II) and copper as cuprous copper (copper
(I)), but both metals were rapidly oxidised (to ferric iron (III) and
cupric copper (II)) when the reactors were aerated (Fig. 4).
In the same study, N ancucheo et al. (2014) also looked at
a
number of factors that inuenced the efciency of copper dissolu-
tion from the laterite. Bacterial numbers, in particular, were noted
to have a critical role in dictating the rate and yield of iron, and to
a lesser extent of copper, solubilised from the ore (Fig. 5).
Bioleach- ing at pH 1.8 was also found to be more rapid and
copper yields signicantly greater than at pH 2.2. There was
only a marginal improvement in copper bioleaching at pH 1.5
compared to pH
1.8 but acid consumption was signicantly (2.4-times) greater,
making the economics of reductive bioleaching of the deposit far
less attractive at the lower pH value.

5. Prospects for reductive dissolution of other ores and

concentrates

Results obtained during tests carried out on the reductive

Fig. 5. Changes in concentrations of copper (grey symbols and lines) and iron
(black symbols and lines) in a lateritic material subjected to bacterially-
9 8
accelerated reductive dissolution, inoculated with 1.0 10 (j, j), 2.5 10 (N, N)
7
or 5.0 10
1
(., .) of At. ferrooxidans mL (reproduced from N ancucheo et al., 2014,
with
permission from the publishers).

could be processed and recovered using a similar approach

(Johnson et al., 2013). For example, concentrations of soluble man-
ganese, cobalt and chromium as well as nickel and iron, were
found to increase as bioleaching progressed in experiments carried
out with nickel limonite. The source of manganese and cobalt in
the deposit was predominantly the oxyhydroxide mineral
asbolane ((Ni,Co)xMn(O,OH)4 nH2O), and concentrations of
soluble manga- nese were highly correlated with those of cobalt
2
during dissolution of the nickel limonite (R = 0.93; Fig. 6). The
oxidation state of manganese in asbolane is +4 and, since Mn (IV)
is highly insoluble in pH 1.8 liquors, the implication was that
asbolane was also sub- jected to reductive dissolution. In order to
elucidate the mecha- nism of asbolane dissolution, limonite
samples were incubated in sterile acidic growth medium under
aerobic conditions, in the presence or absence of ferrous iron.
After seven days, concentra- tions of manganese and cobalt were
far greater in the liquors that contained ferrous iron (35.6 0.3
mg/L and 6.3 0.4 mg/L, respec- tively) than in the iron-free
controls (7.4 1.1 mg/L and
2.0 0.3 mg/L). These results suggested that At. ferrooxidans played
an indirect role in this case was indirect, mediating the reductive
dissolution of asbolane via its production of ferrous iron. Over
95% of the chromium in the limonite ore was also solubilised in
the same experiments. The source of this metal was the mineral
 D.B. Johnson, C.A. du Plessis / Minerals Engineering 75 (2015) 25
Manganese solubilised (mg L-1)
Cobalt solubilised (mg L-1)
Time (days)
Fig. 6. Concurrent solubilisation of manganese (d, s) and cobalt (N, 4) during the
bacterially-catalysed reductive dissolution of a nickel limonite ore (Johnson et al.,
2013). Solid symbols show data from reductive bioleaching, and hollow symbols
from oxidative (acid) bioleaching.
chromite (FeCr2O4) which was present at about 0.8%, by weight.
Both chromium and iron are present in reduced forms in chromite
(oxidation states of +3 and +2, respectively) and therefore dissolu-
tion of chromite was considered to have occurred by acid dissolu-
tion alone. However, bio-processing the limonite under reducing
conditions prevented the oxidation of the solubilised chromium
to its highly toxic +6 oxidation state, as in conventional processing.
Reductive mineral dissolution can also be used to remove sur-
face coverings of ferric iron minerals that encapsulate other
miner- als or metals of value, in a process analogous to the bio-
oxidation of refractory gold ores (Kaksonen et al., 2014c).
Preliminary work carried out in this area has yielded mixed
results, though experi- ments carried out with a sample in
which rare earth element (REE)-containing minerals were
occluded by hydrous iron oxides showing much greater
extraction of the REEs following a reductive pre-treatment (D.B.
Johnson et al., unpublished data).
Chalcopyrite is well-known to be recalcitrant to bioleaching,
except at elevated ( 80 C) temperatures and in some other
circumstances (e.g. in the presence of silver; Li et al., 2013). Two
of the component elements of this mineral are present in their
most reduced oxidation states (copper as +1, and sulfur as 2)
though the third element (iron) is present in its most oxidised
state (+3; Pierce et al., 2006). This suggests that chalcopyrite may
also be susceptible to reductive dissolution, though not one
mediated directly by ferrous iron. Tests carried out with a
chalcopyrite con- centrate, amended with elemental sulfur (as the
electron donor for ferric iron reduction) and bioleached with At.
ferrooxidans under anoxic conditions, failed to promote efcient
dissolution of the mineral, due to the rate-limiting step being
acid dissolution of the mineral rather than the bacterial
reduction of the ferric iron produced by this reaction (D.B.
Johnson and B.M. Grail, unpub- lished data). Reductive
bioprocessing of chalcopyrite is therefore unlikely to be a
feasible approach for extracting copper from this mineral,
though bioleaching at low redox potentials has been found to
be effective (e.g. Gericke et al., 2010; Falagan et al., 2014).
6. Conclusions
Bio-processing of metal ores using bacterially-catalysed reduc-
tive mineral dissolution has been demonstrated to be a feasible
alternative to current high energy-demanding processes. Reductive
bioleaching is an environmentally-benign and cost-effective way
to recover metals, such as nickel and copper, from oxidised
(lateritic) ores, and represents a potentially major innovation in
5
biomining technologies. Preliminary tests suggest that this
approach could have widespread application for processing oxi-
dised metal-containing ores and wastes. Pilot-scale and full-scale
operations are required in order to provide data on the robustness
and cost-effectiveness of this approach.
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