The Geomicrobiology of

Supergene Metal Deposits

Carla M. Zammit1, Jeremiah P. Shuster2, Emma J. Gagen3,

and Gordon Southam4
1811-5209/15/0011-0337$2.50 DOI: 10.2113/gselements.11.5.337

M
icrobe-catalyzed redistribution of metals in the Earth’s crust can
produce remarkable, and often economic, metal enrichments. The oxidation or reduction of
These catalytic processes rely on redox transformations to produce metals by microorganisms can
secondary-mineral assemblages. Classic supergene systems relate to copper, occur via direct and/or indirect
mechanisms – direct mecha-
where weathering is driven by microbial activity. Roll-front uranium deposits nisms involve microbial enzymes,
represent a similar, albeit lateral, evolution from aerobic weathering to whereas indirect mechanisms
anaerobic enrichment. Gold is generally resistant to oxidation but a remark- involve by-products of microbial
metabolism (e.g. acid, oxidising
able biogeochemical cycle can produce secondary gold. Finally, banded iron
agents and ligands). Rapid devel-
formations, which are microbially catalysed sedimentary deposits, can be opments in molecular biology
further weathered to form high-grade ore. Metals are as important to enzyme techniques have advanced our
catalysts as these catalysts are to metal enrichment. understanding of the role of micro-
organisms in metal solubility,
K EYWORDS : prokaryotes, mineral dissolution, mineral precipitation, mobility and precipitation. Here,
supergene processes, metal deposits we discuss the impact of the
biosphere on the evolution of
supergene copper, uranium, gold
INTRODUCTION and iron deposits, highlighting the often over looked role
Microorganisms interact with minerals in the Earth’s that microorganisms play in the formation of such deposits.
crust by catalysing weathering processes. This means
that minerals are often subjected to reduction–oxidation THE ROLE OF MICROORGANISMS
(redox) reactions that alter the chemical and physical state IN SUPERGENE COPPER DEPOSITS
of the metals they contain (Ehrlich and Newman 2008).
To promote cellular growth and sustain metabolic activity, An example of a supergene copper deposit that has been
all microorganisms require major and trace metal nutri- influenced/developed by microorganisms is that of the
ents, which can be acquired from metal-bearing minerals. Morenci copper mine (Arizona, USA). Here, oxidation and
Essential metals for metabolism include magnesium, enrichment processes have produced a classic example of
sodium, potassium, iron, cobalt, copper, molybdenum, a supergene profi le of an original copper porphyry system
nickel and zinc (Ehrlich and Newman 2008). Metals such (FIG. 1). This profi le is characterised by an increase in
as iron, arsenic, magnesium, vanadium, selenium and copper grade with depth (Enders et al. 2006). The profi le
uranium can also be used by microorganisms to generate contains a limonitic leached cap containing hematite that
energy (Ehrlich and Newman 2008). Some metals have no overlies an enriched ‘blanket’ of high-grade chalcocite
known function within a cell’s metabolic pathways and with occasional covellite as replacements and coatings on
just accumulate over time, leading to the biomineralisation primary pyrite and chalcopyrite. Weathering and alteration
of the cell membrane during fossilisation (Silver 2003). cycles of copper enrichment correspond to the lowering
From the perspective of an individual microorganism, of the local water table, which resulted in copper being
biogeochemical reactions occur on spatial and temporal leached from the cap, transported downward and fi nally
scales of micrometres and seconds, respectively. However, concentrated at depth (Enders et al. 2006).
when microbial populations ‘work’ over geological time The surfaces of metal sulphide minerals are ideal substrates
scales, biogeochemical processes can have profound local for the attachment of iron- and/or sulphur-oxidising micro-
to global effects, such as the oxygenation of Earth’s atmos- organisms that catalyse biogeochemical processes and
phere which promotes weathering and the formation of that have contributed to the formation of the Morenci
supergene metal deposits. We must never underestimate copper deposit. Acidithiobacillus ferrooxidans is a microor-
the importance of microorganisms. ganism capable of oxidising both iron and sulphur and
is associated with bioleaching operations and acid mine
drainage environments. A microorganism closely related
to A. ferrooxidans was recovered from samples of sulphide
1 School of Earth Sciences, The University of Queensland minerals at Morenci under near-neutral environmental pH
St Lucia, QLD 4072, Australia conditions. This microorganism forms microenvironments
E-mail: c.zammit1@[Link] on sulphide mineral surfaces (FIG. 2) and oxidises the iron
2 E-mail: [Link]@[Link] and/or sulphur in the rock, which results in acidification
(Mielke et al. 2003; Dockrey et al. 2014).
3 E-mail: [Link]@[Link]
4 E-mail: [Link]@[Link]

E LEMENTS , V OL . 11, PP. 337–342 337 O C TOBER 2015

 A B

(A) View of the Metcalf Pit, Morenci Copper Mine photo in B. (B) Jarosite (brown crystals) and chalcanthite (blue
FIGURE 1
(Arizona, USA) showing the weathering profile studied crystals), the latter being a very soluble copper mineral.
by Enders et al. (2006). Arrow indicates the position of close-up

In general, near-surface oxidation of metal sulphide

minerals is attributed to microorganisms (re)generating
ferric iron and acidity (reactions 1 and 2). As a result,
ferric iron acts as an oxidising agent that contributes to
the mobilisation of cupric ions from the dissolution of
metal sulphide minerals (reaction 3). Singer and Stumm
(1970) noted that although oxidation of metal sulphide
minerals can be perceived in abiotic mechanistic terms,
microorganisms catalyse sulphide mineral oxidation 105
times faster than the abiotic rate.

4Fe2+ + O2 + 4H + → 4Fe3+ + 2H2O (1)

S 0 (s) + 1½O2 + H2O → SO42− + 2H + (2)
CuFeS2(s) +16Fe3+ + 8H2O → Cu 2+ + 17Fe2+ +
(3)
2SO42− + 16H +
Copper enrichment in supergene deposits is generally
considered to occur through the abiotic replacement of
chalcopyrite with covellite (reaction 4)

Cu 2+ + CuFeS2(s) → 2CuS (s) + Fe2+ (4)

However, the activity of sulphate-reducing bacteria in
natural environments has been used to provide a model/
example of how metal sulphide ores are deposited (Labrenz
et al. 2000; Druschel et al. 2002). Sulphate-reducing
bacteria oxidise low-molecular-weight environmental
organic compounds. A by-product of their active metabo-
lism is the formation of hydrogen sulphide. This gas is then
released into the surrounding environment (Donald and FIGURE 2 Field emission scanning electron microscope
secondary electron micrograph of a bacterially
Southam 1999) and may contribute to metal enrichment colonized weathered pyrrhotite grain encased within secondary
(Southam and Saunders 2006). For example, Alpers and Fe(III) (oxy)hydroxysulphate precipitates at the sulphide–mineral
Brimhall (1989) proposed that sulphate-reducing bacteria surface. Image reproduced with permission from Dockrey et al.
activity might explain a thin zone of massive chalcocite at (2014).
the top of the enrichment blanket at La Escondida (Chile)
(reactions 5 and 6)

CH3COOH + SO42− → 2HCO3 − + H2 S (5) Contemporaneous biotic and abiotic factors contribute to
2Cu + + H2 S → Cu 2 S (s) + 2H + (6) in situ leaching and are, almost certainly, responsible for
the formation of worldwide economic accumulations of
Mathematical modelling by Lichtner and Biino (1992) supergene copper (Enders et al. 2006).
suggests that sulphate-reducing bacteria are involved
in the precipitation of pyrite, bornite and chalcocite in
the lower blanket of supergene enrichment zones. In a
THE ROLE OF MICROORGANISMS
related study, sulphur isotopes were used to demonstrate IN SUPERGENE URANIUM DEPOSITS
the involvement of sulphate-reducing bacteria in sulphide In roll-front uranium deposits, soluble uranyl complexes
enrichment blankets in the Mike gold deposit in the (e.g. rutherfordine and UO2CO3), along with other mobile
Carlin Trend (Nevada, USA) (Bawden et al. 2003). While metals, are transported away from a mineralised source via
sulphate-reducing bacteria occur naturally in weathering hydrological processes. Under aerobic conditions, microor-
profi les at Morenci, their populations are too small to have ganisms are capable of solubilising uranium through direct
produced significant enrichment (Enders et al. 2006). oxidation, thereby enabling mobilisation of uranium as

E LEMENTS 338 O C TOBER 2015

a soluble uranyl complex. Acid-generating reactions (e.g.
reactions 2 and 3) can also indirectly enhance uranium
solubilisation (reaction 7)

UO2(s) + ½O2 + 2H + → UO22+ + H2O (7)

By contrast, soluble uranyl complexes can be reduced under
anaerobic conditions by microorganisms (reaction 8) and
by microbially produced by-products (reaction 9)

CH3COOH + 4UO22+ + 2H2O → 2CO2 + 4UO2(s) + 8H+ (8)

UO22+ + FeS → UO2(s) + Fe2+ + S 0 (s) (9)
which leads to the immobilisation and enrichment of
uranium (Zammit et al. 2014; FIG. 3).
In roll-front deposits, uranium is mobilised from a nearby
source and transported until it meets reducing ground
waters where it is then deposited at the redox boundary.
When anaerobic microbial communities come into contact
with oxidising uranium-bearing groundwaters, they
metabolically reduce Fe3+ to Fe2+, reduce UO22+ to UO2(s)
(reaction 8), and reduce SO42− to H2S (reaction 5), leading to
the immobilisation and enrichment of uranium (Angiboust
et al. 2012; Zammit et al. 2014; FIG. 3). A study on uraninite
FIGURE 3 Back scattered electron, field emission scanning
and coffi nite from a sandstone-hosted roll-front deposit in
electron microscope image of a ‘biogenic’ uraninite
Xinjiang, northwest China, showed that these minerals are (Sierra Peña Blanca, Mexico) possessing structural and isotopic
indeed precipitated by microorganisms (Min et al. 2005). evidence of dissimilatory sulphate reduction (Angiboust et al. 2012).
Another study of coffi nite at the Beverly uranium deposit Biogenic pyrite (FeS2) is closely associated with uranophane (UO2).
in South Australia suggested that bacterial reduction may
have been the primary ore-forming process (Wülser et al. While mobility occurs under aerobic conditions, acido-
2011). Indirect uranium reduction via iron sulphide oxida- philic iron- and sulphur-oxidising bacteria can destabilise
tion also produces enrichments of uranium (reaction 9; Au(S2 O3 ) 2 3− complexes and so produce elemental gold
Angiboust et al. 2012; Ingham et al. 2014). (Southam and Saunders 2005). In the laboratory, the
resulting biomineralisation of gold under both oxidising
THE ROLE OF MICROORGANISMS and reducing conditions formed nanometre-size gold
IN SUPERGENE GOLD DEPOSITS colloid particles within bacterial cell envelopes and
The biogeochemical cycling of gold is well established in association with the secondary mineral precipitates
through studies on bacteria–gold interactions, which formed by the bacteria. Under aerobic conditions, ferric
highlight microbial contributions to gold weathering and iron (maintained through bioleaching; reaction 1) has
precipitation (Reith et al. 2007). Though gold is not readily been found to be a particularly important biogeochemical
maintained as a soluble complex, rapid gold dissolution– reactant contributing to the destabilisation of Au(S2O3) 23−
reprecipitation processes occur much faster than geological and to the subsequent reduction to Au0 (reactions 14, 15;
time scales. see Shuster et al. 2014). The substitution of biogenic jarosite
(acicular iron oxyhydroxide) minerals by colloidal gold
The exposure of electrum (naturally occurring gold alloys) links the biogeochemical cycling of iron to that of gold.
and gold-bearing metal–sulphide minerals to oxidising Specifically, iron reduction (see canga section, below)
conditions can release gold from the host mineral matrix. would release colloidal gold, which would thereby increase
This is thought to promote the oxidation of Au0 to Au +, gold mobility and potential reactivity. Under anaerobic
which results in the formation Au(S2 O3 ) 2 3− (reactions conditions, sulphate-reducing bacteria can substitute
10–12). Au(S2O3) 23− as an electron acceptor (reaction 16) promoting
the formation of gold sulphide (reaction 17) and elemental
2Au0 (s) + H2O2 + 2H + → 2Au + + 2H2O (10)
gold (reactions 18 and 19).
FeS2 + 6Fe3+ + 3H2O → 7Fe2+ + S2O32− + 6H + (11)
Au + + 2S2O32− → Au(S2O3) 23− (12) Au(S2O3) 23− + 16Fe3+ + 10H2O → 16Fe2+ + Au + +
(14)
4SO42− + 20H +
When considering gold complexation in the absence
of thiosulphate ligands, AuCl4 − complexes could form, Fe + Au + → Au0 (s) + Fe3+
2+ (15)
depending on the availability of chloride ions (reaction Au(S2O3) 23− + 2CH3COOH+ → Au + + 4HS − +
(16)
13) (Mann 1984; Gammons et al. 1997). 4CO2 + 2H2O
HS − + 2Au + → Au 2 S + H + (17)
3Au + + 6Cl− → 3AuCl2 − → AuCl4 − + 2Cl− + 2Au0 (13)
HS − + 2Au + → 2Au0 (s) + S 0 (s) + H + (18)
The biogeochemical conditions of surface to near-surface Biomass-CH3COOH + 8Au + + 2H2O → 2CO2 +
environments and the availability of anionic ligands are (19)
4Au0 (s) + 8H +
the primary factors that determine the formation of soluble
gold complexes (Mann 1984; Benedetti and Boulegue Gold(III) chloride is even less stable than gold(I) thiosul-
1991) and the mobility of gold. However, the mobility phate in the presence of bacteria. Heterotrophic soil
of Au(S2O3) 23− and AuCl4 − within hydrological systems is bacteria (e.g. Bacillus subtilis; Southam and Beveridge, 1994)
likely affected by an array of biogeochemical processes that or cyanobacteria (e.g. Plectonema boryanum) and dissimila-
could destabilise these gold complexes. tory sulphate-reducing bacteria directly reduce AuCl4 − to
Au0 even under halophilic conditions and possessing excess
chloride ions (Shuster et al. 2013). Like the biogeochemical
gold reactions in acidic and oxidised weathering environ-

E LEMENTS 339 O C TOBER 2015

ments, the presence of reduced iron and/or sulphur (as Fe2+
A
or FeS) can immobilise elemental gold from AuCl4 − (similar
to reactions 15 and 18).
When assessing the limited stability of inorganic gold
complexes in the presence of a wide range of bacteria, it
is essential to consider the importance of gold mobility
as complexes, as nanophases and as secondary gold parti-
cles (colloidal suspensions) within surface to near-surface
hydrological regimes. The overall result of weathering
(oxidation), complexation, and microbial ‘degradation’
of gold complexes that form nanometre-scale colloidal to
micrometre-scale octahedral gold (FIG. 4) is the movement
of gold downward in supergene systems (or laterally in
placers). The subsequent biological enrichment of gold
at the redox boundary (reactions 14–19; Lengke and
Southam 2007) can produce economic accumulations of
secondary gold.

THE ROLE OF MICROORGANISMS

IN CANGA-TYPE IRON DEPOSITS
B
High-grade iron-ore reserves contain more than 60% iron,
which generally occurs as iron (oxyhydr)oxides, such as
hematite, magnetite and goethite. Some of the world’s
largest iron-ore deposits are located in South America and
Australia and are the result of supergene lateritic weathering
acting on banded iron formations (BIFs). During supergene
lateritic weathering of BIFs, gangue minerals are leached,
resulting in a relative enrichment of iron; note that iron
oxide minerals also undergo multiple phases of dissolution
and precipitation (Ramanaidou and Morris 2010). This is
particularly evident in the ferruginous duricrust known
as canga, which caps supergene lateritic iron ores in wet
tropical conditions (FIGS. 5A, B).
Dorr (1964) was the first to propose that geomicrobiological
cycling of iron occurs in canga. Monteiro et al. (2014)
later described canga as ‘self-healing’ because recurrent
goethite dissolution and re-precipitation give it the capacity
to re-form. The only reasonable reducing agent capable
of ‘driving’ the frequent and repeated dissolution of iron
oxides in canga must come from the biosphere, either
FIGURE 4 (A) Back scattered electron, field emission scanning
indirectly from plants that exude organic acids around electron microscope image of a gold grain collected
their roots, or directly by microorganisms that are involved from West Coast Creek, Queensland, Australia. Location of photo
in iron reduction as part of their metabolism. In addition in B is indicated by arrow. (B) High magnification scanning electron
to the evidence for bacteriological iron reduction in canga, micrograph of one of the soil-covered, dark regions in (A), demon-
strating the presence of colloidal (spherical particles) and octahe-
electron microscopy has revealed that ferruginous strom- dral secondary gold crystals (arrow).
atolite-like textures (FIG. 5C) possess microfossils reminis-
cent of iron-oxidising bacteria (FIG. 5D). These observations
suggest that biological iron oxidation may also play a role
Fe3+ + 4H2O → Fe(OH) 3 · H2O (s) + 3H + (22)
in canga formation (see Monteiro et al. 2014).
Fe(OH) 3(s) → FeOOH (s) + H2O (23)
Biological iron reduction is an anaerobic process that is
important in iron-rich soils and sediments worldwide (e.g. In acidic aerobic environments or under near-surface
Lovley 1991). Biological iron reduction occurs when micro- low-oxygen conditions, microorganisms can oxidise ferrous
organisms use ferric iron as a terminal electron acceptor iron (reaction 21). Biological iron reduction and biolog-
during metabolic oxidation of either hydrogen or various ical iron oxidation both appear to occur in canga deposits
carbon compounds (e.g. goethite reduction with acetate; (Monteiro et al. 2014); therefore, either spatial or temporal
reaction 20). separation of environmental conditions suitable for both
microbial groups must be present. This means that anaer-
CH3COOH + 8FeOOH (s) + 16H + → 2CO2 + obic microenvironments co-exist alongside aerobic and
(20) microaerophilic environments within canga. Furthermore,
8Fe2+ + 14H2O
seasonal changes may be responsible for changes between
The ferrous iron produced by iron reduction is unstable in
aerobic and anaerobic conditions. During rainy periods,
the presence of oxygen and readily oxidises to ferric iron
subsurface environments receive an influx of organic
(reaction 21), or hydrolyses to form ferrihydrite (reaction
compounds, which contribute to the generation of anaer-
22), or can dehydrate to form goethite (reaction 23) abiot-
obic conditions. In dry months, evaporation will lead to
ically or biologically, indicating that these processes are
aerobic and microaerobic conditions. Understanding the
regenerative.
factors that control geomicrobiological iron cycling in
4Fe2+ + O2 + 4H + → 4Fe3+ + 2H2O (21) canga is important for a more complete understanding
of supergene lateritic iron-ore systems. Furthermore,

E LEMENTS 340 O C TOBER 2015

 FIGURE 5 (A) Google
map image A B
showing a kilometre-scale
canga deposit in Carajás,
Brazil (B) Field photograph
of ridge within (A),
highlighting the arid
landscape and the scrub
vegetation that grows on the
iron oxide. (C) Photograph
of stromatolite-like texture
observed along an ephem-
eral lake (see arrow in A). (D)
Back scattered electron, field
emission–scanning electron
microscope image of
polished canga. Arrows
indicate the bacteria-scale C D
microfossils (dark spots)
within the iron oxide matrix
(light grey) (see also,
Monteiro et al. 2014).

stimulating the natural geomicrobiological processes that microbe–gold interactions presents a range of new opportu-
occur in canga could be a useful strategy for rehabilitating nities in developing novel techniques for gold exploration,
iron-ore areas after mining activities have ceased. processing and mine remediation.
The role that microorganisms play in the oxidation and
THE FUTURE OF BIOTECHNOLOGY reduction of iron has served as the cornerstone to geomi-
IN MINING crobiological research. There is increasing evidence that
Bioleaching processes liberate a wide range of metals certain microorganisms play a critical role in the cycling of
under experimental conditions (Ehrlich and Newman iron and the formation of iron duricrusts within supergene
2008), suggesting that microorganisms could play an lateritic iron-ore systems. A thorough understanding of the
important role in the formation of supergene deposits. factors affecting microbial processes in these systems will
These processes are fundamentally interesting, but they be critical to artificially accelerating the re-formation of
also have commercial applications to the mining industry, canga and, therefore, for the remediation of post-mining
as well as offering potential routes for mine remediation. iron-ore sites.
Molecular biology is opening up a tremendous opportunity
In summary, understanding the role that microorganisms
for researching the role that microorganisms play in metal
play in the turnover of metals is fundamental to developing
mobility. For example, relatively little work has been done
new biotechnologies and will help shape the future of the
on the interaction between microorganisms and chalcopy-
minerals industry.
rite. Chalcopyrite accounts for approximately 70% of the
world’s copper reserves; however, copper from low-grade
chalcopyrite is not currently economically extractable ACKNOWLEDGMENTS
using traditional mining methods. Because biotechnology Electron microscopy was performed in the Nanofabrication
offers a potentially cost-effective alternative to traditional Laboratory at Western University (Canada) and in the
mining techniques, further research into the interactions Centre for Microscopy & Microanalysis at the University
between microorganisms and chalcopyrite could have of Queensland (Australia). Funding was provided through
enormous commercial value. a Natural Sciences and Engineering Research Council
(NSERC) of Canada Discovery and Accelerator Grants,
In the case of gold, the discovery of new, large, and easily
through ARC Discovery support, and by Vale Technology
accessible deposits is becoming increasingly rare, and
Institute, Vale SA. We would like to thank the reviewers
mining companies are pressured into locating economic
for their valuable suggestions and support.
deposits under increasingly deeper cover. Research into

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Mielke RE, Pace DL, Porter T, Southam G

(2003) A critical stage in the formation AHF analysentechnik AG :: Germany info@[Link] :: [Link]
of acid mine drainage: Colonization

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