Download Geomicrobiology of Iron in Extreme Environments

Geomicrobiology of Iron
in Extreme Environments
Alexis S. Templeton*
1811-5209/11/0007-0095$2.50 DOI: 10.2113/gselements.7.2.95
T
he rapid redox cycling of iron is one of the most pervasive geochemical
processes catalyzed by microbial organisms. Numerous microbial metabolisms rely on transferring electrons to and from iron, even in “extreme”
environments considered challenging for life due to high acidity, high alkalinity, high temperature, low organic content, or low water abundance. Recent
efforts to explore the iron biogeochemistry of extreme systems, such as
hydrothermal vents, seafloor basalts, serpentinizing systems, and acid mine
drainage, have significantly expanded our expectations regarding the distribution and activity of iron-dependent life on Earth, and potentially other
iron-rich silicate planets, such as Mars.
Keywords : iron oxidizing bacteria, chemosynthesis, acid mine drainage,
serpentinization, hydrothermal systems, oceanic crust
can also indirectly support microbial life: for example, the partial
oxidation of ferrous iron, Fe(II),
derived from olivine and pyroxene
minerals drives the evolution of H2
during the serpentinization of
ultramafic rocks (Fig. 1). This H 2
can be rapidly utilized by microbial organisms when it is released
at hydrothermal vents and terrestrial hot springs. In this article we
briefly explore the role of microbial organisms in the cycling of
iron in some of the “extreme environments” alluded to above.
INTRODUCTION
IRON IN SUBMARINE
ENVIRONMENTS
Microbial organisms are intimately involved in iron cycling
in diverse environments past and present (see Konhauser
et al. 2011 this issue). Some of the most “extreme” environments in which living systems depend on iron as an energy
source include systems rich in iron sulfide (e.g. pyrite) in
contact with an oxidizing atmosphere, as well as terrestrial
hot springs, ophiolites, submarine hydrothermal vents,
oceanic crust, and the deep subsurface. These geological
environments are considered extreme due to a lack of
organic carbon to sustain heterotrophic (see glossary in
Taylor and Konhauser 2011 this issue, for definition of this
and other technical terms) metabolisms and to an enormous variability in pH, temperature, pressure, and salinity,
all of which can significantly diminish cell viability.
Hydrothermal Systems
Modern hydrothermal vents at ocean seamounts and ridge
systems represent dynamic interfaces between highly
reduced fluids rich in metals and sulfide and seawater
containing abundant oxidants such as O2 , nitrate, and
sulfate (Bach and Früh-Green 2010). Chemosynthetic life
(i.e. organisms sustained by harnessing chemical energy)
is abundant in these environments. Megafauna, such as
tubeworms and bivalves, are dependent on symbiotic relationships with microbial communities conserving energy
from sulfide, hydrogen, and methane oxidation, but it has
been assumed that the oxidation of Fe(II) provides too little
biomass and too much mineral product to sustain similar
symbioses. However, the speciation of iron can strongly
affect the abundance and availability of the energy sources
available in hydrothermal fluids. For example, in Alvinella
pompejana tube worms on the East Pacific Rise, Fe(II) has
been shown to be critical for forming FeS (aq) clusters, which
affect the ecology of vent communities by detoxifying
H 2 S (aq) (Luther et al. 2001). In another example, fluids
extraordinarily enriched in Fe(II) have been measured at
the Rainbow hydrothermal vent field: in this case, thermodynamic calculations suggest that Fe(II) oxidation is
one of the most energetically feasible metabolisms, despite
the presence of abundant hydrogen and methane (Schmidt
et al. 2008). There is also speculation that Fe(II)-oxidizing
microbial organisms colonizing the branchial chambers of
vent shrimp play a role in symbiotic CO2 fixation and
biomass production.
Ferrous iron is one of the most abundant reductants on a
planet whose crust is dominantly composed of silicate
minerals. As the surface of the Earth has become progressively oxygenated, the increasing disequilibrium between
the deep crust and mantle compared to the Earth’s oceans
and atmosphere has created innumerable oxic–anoxic
interfaces where iron cycling is thermodynamically favorable. Microbial organisms exploit such disequilibria by
controlling the transfer of electrons from iron to strong
oxidants, typically oxygen and nitrate, under conditions
where the abiotic rates of reaction are suppressed (Emerson
et al. 2010). One classic example is acid mine drainage
(Fig. 1), where microbially catalyzed iron oxidation at high
Eh and low pH is several orders of magnitude faster than
the homogeneous oxidation of iron. Microbial organisms
can also exploit low-oxygen niches at the interface between
opposing fluxes of iron and oxygen at neutral pH. Geological
iron-oxidation processes under very low redox potential
Fe(II)-oxidizing bacteria and chemosynthetic communities
have rarely been identified in high-temperature hydrothermal fluids (e.g. >50 º C), where dissolved oxygen
concentrations are low. However, in lower-temperature,
diffuse venting environments along the flanks of ridges
and seamounts, the activity of iron-oxidizing bacteria has
* Department of Geological Sciences, UCB 399
University of Colorado, Boulder, CO 80309, USA
E-mail: [email protected]
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pp.
95–100
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commonly been invoked because of the presence of abundant iron oxide–encrusted sheaths and filaments, which
are aggregated together in gelatinous iron mats and rock
surface coatings. Fe(III)-rich microbial mats devoid of
megafauna were first discovered by Karl et al. (1988) at the
Loihi Seamount, where iron-rich hydrothermal fluids
contain abundant CO2 but are low in H2 S. Emerson and
Moyer (2002) have since documented extensive iron mats
with cellular abundances as high as 107–108 cells/ml associated with diffuse hydrothermal fluids precipitating mineral
flocs below 30 °C. Similar hydrothermal environments and
associated microbial mats have recently been observed at
Vailulu’u Seamount and the Kermadec arc (Staudigel et al.
2006; Hodges and Olson 2009) and may be ubiquitous at
active seamounts globally. Emerson et al. (2007) also
recently characterized a novel and ubiquitous class of
Fe(II)-oxidizing bacteria represented by Mariprofundus ferro­
oxydans of the Zetaproteobacteria. Mariprofundus excretes
an iron-encrusted stalk structure during continuous
growth and biomineralization, and closely related
Zetaproteobacteria are now being identified and attributed
to microbial iron oxidation in numerous submarine systems.
crust is an environment extremely poor in organic matter,
but abundant chemical energy is available where there is
high water–rock exchange between basalts, peridotites, and
oxygenated seawater. Several studies have suggested that
an extensive subseafloor biosphere is involved in basalt
dissolution, and morphological biosignatures of their
activities may be preserved in tubular and granular alteration features in volcanic glass, ranging in age from modern
to 3.5 billion years (Staudigel et al. 2008). For example,
basaltic glasses recovered from ocean drill cores commonly
exhibit elongated hollow and mineralized tubules that
propagate into fresh glass from cracks; these features are
interpreted as signs of microbial activity, although a direct
microbial role has not yet been demonstrated. Moreover,
the energy source for microbial growth within a hydrating
glass matrix is not known, but preliminary spectroscopic
data showing the partial oxidation of iron at the glass–
water interface suggest that iron transformations are a
critical component of the bioalteration process (Benzerara
et al. 2007; Staudigel et al. 2008).
Water–rock interaction along high permeability zones (e.g.
fractures) in the oceanic crust leads to a progressive oxidation of iron that may in part be microbially mediated (Bach
and Edwards 2003). Recently, Edwards et al. (2003) cultured
some of the first deep-sea microorganisms that would grow
using the Fe(II) in basalt, as well as pyrite and FeS, as their
sole source of energy in oxygenated seawater. Several
molecular studies have detected abundant and diverse
microbial biomass associated with seafloor basalts (see
Santelli et al. 2008), and so far it is assumed that chemolithoautotrophic iron oxidation during oxidative basalt
alteration provides the primary energy source.
Seafloor and Subseafloor Habitats
The oceanic crust is one of the most extensive potential
habitats for iron-dependent microorganisms due to the
abundance of reduced iron in mafic rocks. The oceanic
AMD
Microbial growth by iron oxidation is commonly hypothesized in many geological environments, but it has only
rarely been proven. Identifying iron-oxidizing microorganisms in culture-independent studies (e.g. by analysis of
DNA extracted from basalt and sulfides) is difficult, mostly
because the seafloor communities are surprisingly diverse.
Moreover, the phylogeny, physiology, and biochemistry of
iron-oxidizing bacteria remain poorly understood. The link
between iron oxidation and the activity of microorganisms
historically relied on the formation of unique structures
of biomineralized Fe(OH) 3 , such as iron-encrusted
Gallionella-like twisted stalks and Leptothrix-like tubular
sheaths. However, microbial organisms can also produce
copious amounts of structurally amorphous, high-surfacearea iron (oxyhydr)oxides that cannot be distinguished
from abiotic oxides. Also, microbial cell surfaces can
become entirely encrusted in metal-oxide minerals through
passive cell-surface interactions and adsorption processes
that do not rely on microbial catalysis and biomineralization processes at all (Fortin and Langley 2000). Therefore
it has become increasingly important to “catch microorganisms in the act” of catalyzing iron oxidation and demonstrate a direct link to growth, particularly the uptake and
fixation of carbon into cellular biomass and extracellular
polymers.
Fe3+(aq)
Eh (Volts)
Circumneutral
Fe-oxidation
Fe2+(aq)
Fe2O3 (s)
Serpentinization
Fe3O4 (s)
There is significant interest in understanding the relative
importance and the fluxes of iron released from hydrothermal activity as compared to basalt alteration in
sustaining seafloor biomes. Templeton et al. (2009) suggest
that seafloor biofilms on young basalt surfaces may often
be sustained by inputs of iron and organic carbon from
seawater and dispersed hydrothermal fluids, rather than
by basalt dissolution reactions alone. For example, these
workers showed that as biofilms are rapidly established on
seafloor-basalt surfaces, they catalyze the oxidation of
aqueous Fe(II) and Mn(II). This results in the formation
of highly reactive ferromanganese crusts capping rock
pH
Generalized Eh-pH diagram representing a few of the
chemical environments in which microbial life may be
sustained by reactions driven by the oxidation of Fe2+. AMD = acid
mine drainage, with pyrite shown as a key substrate for sulfuric acid
generation under oxidizing conditions. At circumneutral pH, a
weathered pillow basalt coated in ferric hydroxides is shown. At
alkaline pH, a partially serpentinized peridotite depicts the source
of H2 generated from Fe-oxidation reactions under highly reducing
conditions.
Figure 1
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surfaces, thereby creating a reactive sink for trace elements
in seawater. Yet intriguing work by Santelli et al. (2009)
and Mason et al. (2008), at the East Pacific Rise, Hawai‘i,
and the Juan de Fuca Ridge, indicates that the microbialcommunity composition must be directly linked to the
reaction history of the rocks. Apparently, as seafloor basalts
are progressively altered, iron cycling—the tight coupling
of microbial iron-oxidation and iron-reduction processes—
becomes increasingly important.
Hydration of Ultramafic Rocks
Seafloor microbial communities also thrive in low-temperature, H2 -rich, and CH4 -rich alkaline fluids issuing from
uplifted ultramafic massifs located off axis from global
ridge systems, such as the Lost City hydrothermal field
(Kelley et al. 2005). In these settings, thermophilic microbial organisms (i.e. microbes that can grow above 45 ºC)
are sustained through key metabolisms such as methanogenesis and methane oxidation, and the current focus is
on understanding the biological role in hydrogen, methane,
and sulfur cycling. From a geological perspective, the H2
and CH4 generation is directly attributed to the serpentinization of ultramafic rocks, such as peridotites occurring
deeper in the hydrothermal system. A commonly suggested
H2 -generating reaction representing the serpentinization
of olivine is shown in equation 1 (McCollom and Bach
2009):
Abundant, orange iron hydroxide mats forming in the
hot outflow channels of acid–sulfate–chloride springs
at Norris Geyser Basin in Yellowstone National Park, Idaho, USA
Figure 2
Acidianus, Sulfolobus, Acidimicrobium, Sulfobacillus, and
Metallosphaera spp. However, it has been difficult to demonstrate that thermophilic iron-oxidizing bacteria might be
environmentally relevant at more circumneutral springs.
Mg1.8Fe 0.2 SiO4 + 1.37H2O à 0.5Mg3Si2O5 (OH) 4 +
Olivine
Serpentine
0.3Mg(OH) 2 + 0.067Fe3O4 + 0.067H2 . Brucite
M agnetite
(1)
Acid Mine Drainage
In contrast, the role of microbial organisms in accelerating
the rate of acid generation from pyrite-rich host rocks and
mine tailings is well established. Sulfide minerals are not
stable at near-surface conditions on Earth in the presence
of water. One key concept in acid mine drainage (AMD)
chemistry is that Fe3+ (aq) is a labile species which oxidatively
attacks reduced sulfur minerals that can otherwise persist
out of thermodynamic equilibrium in oxygenated waters
(equation 2). As Fe2+ (aq) is released during the initially slow
weathering of pyrite, several genera of acidophilic bacteria
can rapidly catalyze the oxidation of Fe2+ (aq) to Fe3+ (aq) and
thereby control the overall rate of sulfide dissolution. This
will generate an autocatalytic cycle through the pervasive
regeneration of Fe3+ (aq) (equation 3).
Hydrogen is one of the most universal energy sources for
life, and it can be coupled to numerous oxidants, such as
CO2, sulfate, ferric hydroxides, nitrate, and O2, to conserve
energy for growth. The rate and extent of hydrogen generation is directly linked to changes in iron speciation as
olivine and pyroxene are converted to serpentine, magnetite, brucite, and talc, particularly at temperatures between
200 and 315 ºC (McCollom and Bach 2009). Therefore,
there may be an indirect link between iron released during
water–rock reactions and microbial growth, since Fe(II) is
the key to reducing H 2O to H 2 . Intriguingly, subsurface
microbial communities could potentially participate in and
directly harness the hydrogen-generating reactions occurring in ultramafic rocks, so long as the temperature limit
for life has not been exceeded. This possibility has not yet
been carefully explored and will likely require deep
drilling. For now, ongoing characterization of microbial
communities associated with alkaline vents at Lost City,
as well as with serpentine mud volcanoes along the Mariana
forearc (Mottl et al. 2003), will likely provide the initial
insights into what may be a ubiquitous extreme
environment.
Fe2+ + 0.25O2 + H + à Fe3+ + 0.5H2O .
(3)
The central questions regarding the generation and mitigation of acid mine drainage involve understanding the
molecular mechanisms of pyrite dissolution and the steps
that are directly or indirectly mediated by microorganisms.
Several studies have shown that direct cell attachment to
pyrite surfaces is not required for all organisms, since the
oxidative attack is often mediated by Fe3+ (aq), although
surface enzymes may be involved in electron transfer from
sulfide surfaces (Sand et al. 2001). Some of the best studied
acidophilic iron-oxidizing organisms include Acidithio­
bacillus ferrooxidans and Leptospirillum ferrooxidans, although
numerous other organisms participate in these reactions,
including Leptospirillum sp., Thiobacillus sp., some Firmicutes,
and Archaea such as Thermoplasmatales and Sulfolobus sp.,
to name only a few (Baker and Banfield 2003).
IRON IN “EXTREME” TERRESTRIAL
ENVIRONMENTS
Yellowstone National Park in the United States is one of
the best studied and most spectacular extreme environments on Earth, and many of its hot springs contain acidic
fluids rich in dissolved iron. Iron-rich microbial mats are
common adjacent to the outflow of acid–sulfate–chloride
springs (Fig. 2), and the hydrous ferric oxides commonly
incorporate toxic trace metals, such as arsenic, at high
molar ratios (Inskeep et al. 2004). However, the most
common chemosynthetic microbial metabolisms at
Yellowstone are dependent on H2, sulfur, and even arsenic.
The few iron-oxidizing thermophiles cultured from
Yellowstone solfataras include acidophiles within the
E lements
FeS2 + 14Fe3+ + 8H2O à 15Fe2+ + 2SO42- + 16H + . (2)
Increased understanding of the biological role in AMD
chemistry has led to great interest in harnessing the ability
of acidophilic, chemolithoautotrophic bacteria to enhance
the solubilization of low-grade metal sulfide ores containing
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minerals such as chalcopyrite (CuFeS2 ), chalcocite (Cu2 S),
molybdenite (MoS2 ), covellite (CuS), sphalerite (ZnS), and
galena (PbS). As with AMD, Acidithiobacillus ferrooxidans
(known for oxidizing Fe 2+ and reduced sulfur) and
Acidithiobacillus thiooxidans (known to oxidize elemental
sulfur) were initially the most studied organisms for
enhancing the rates of sulfuric acid production and metal
release (Bosecker 1997). However, numerous other organisms, such as Leptospirillum sp. (including Leptospirillum
ferrooxidans), Thiobacillus cuprinus, Sulfolobus sp.,
Sulfobacillus sp., Acidimicrobium sp., Ferromicrobium sp., and
even heterotrophic bacteria (e.g. Bacillus sp.), have been
studied for their ability to mobilize metals from sulfide
minerals under acidic conditions and across a range of
temperatures. The growth of the organisms must be favorable; in particular, the microorganisms must conserve
chemical energy from the oxidative reactions and exhibit
high levels of heavy metal tolerance to sustain growth and
continuous leaching activity.
Not surprisingly, there is growing interest in understanding
the coupled oxidation and reduction of iron in numerous
“extreme” environments as well. Ancient examples include
banded iron formations (see Konhauser et al. 2011), which
underwent significant diagenetic modification after the
initial deposition of (biogenic?) Fe(III) oxyhydroxides.
Recently increasing attention has been paid to the fluxes
of Fe(II) released from the downstream reaches of AMD
systems as an analog to banded iron formation biogeochemistry and to the resulting fractionation of δ56Fe that
might be preserved in the rock record (Tangalos et al. 2010).
There is also growing evidence that acidophilic microbial
Fe(II) oxidation and Fe(III) reduction may be tightly
coupled in sediments produced from coal mining (Blöthe
et al. 2008) and in acidic wetland (e.g. peat) environments
(Lüdecke et al. 2010). New insights into acidophilic iron
cycling have proved useful in efforts to remediate acid
mine drainage systems. For example, explicitly stimulating
dissimilatory iron reduction helps increase alkalinity and
the precipitation of metals in anaerobic wetlands that have
been constructed to receive AMD. The central concept is
that by adding high levels of organic carbon, such as
organic-rich sludges or compost materials, microbial organisms will reverse AMD-generating reactions, using the
carbon as a reductant for Fe(III) and sulfate, thus increasing
alkalinity and precipitating toxic metals as biogenic
sulfides.
What is astounding is the extremely low pH values and
high metal concentrations under which chemolithoautotrophic microbial communities can thrive in a positive
feedback loop with continued iron sulfide oxidation.
Seminal geochemical and microbiological studies have
been conducted at the Richmond Mine at Iron Mountain
in northern California, where Ag, Au, Cu, Fe, and Zn were
mined for over 100 years before the mine was ultimately
designated as an EPA Superfund Site to stop the release of
acid water to the Sacramento River (Nordstrom et al. 2000).
Low-diversity microbial biofilms can form at pH 0 to 1.5
and elevated temperatures (e.g. 40 ºC), and Edwards et al.
(2000) succeeded in cultivating the dominant organism
in this environment, Ferroplasma acidarmanus, enabling
further mechanistic studies. These workers also demonstrated that Acidithiobacillus ferrooxidans is more commonly
confined to biofilms peripheral to the ore body and is not
the key organism involved in primary acid generation
(Schrenk et al. 1998). Their work has since shifted towards
using cultivation-independent approaches to explore the
functional activity of the biofilm-forming populations,
which vary spatially and temporally. Several questions also
remain regarding how organisms can maintain a circumneutral intracellular pH and protein stability when challenged with such low external pH values.
To come full circle through the environments considered
in this article, it has been suggested that thermophilic iron
reduction may have dominated the earliest metabolisms
and biogeochemical processes in hydrothermal vent environments. Vargas et al. (1998) established that all the
extant hyperthermophilic Archaea and Bacteria they could
test were capable of reducing Fe(III), including isolated
organisms that are most closely related to the “last common
ancestor.” Since then, Kashefi et al. (2002) have demonstrated that novel Fe(III) -reducing bacteria, such as
Geothermobacter ferrireducens, can be cultured from extreme
environments, such as Yellowstone hot springs, by
providing H 2(aq) as an electron donor and Fe(III) as the
oxidant. Increasing efforts to cultivate Fe(III)-reducing
bacteria from submarine hydrothermal vents and microbial
mats have recently identified additional iron-reducing
bacteria closely related to Geothermobacter sp. The next step
in these studies is to determine whether Fe(III) reduction
is a major biogeochemical process in these mineral deposits,
or whether Fe(III) reduction may be limited due to paucity
of reductants, such as labile organic matter (Emerson et al.
2010).
A Glimpse at the Other Side of the Story:
Iron Reduction
As discussed in several of the companion papers (see Taylor
and Macquaker 2011 this issue), microbial iron reduction
is one of the most important biogeochemical processes for
the remineralization of organic carbon under anoxic conditions. Under acidic conditions, Fe(III) is highly soluble,
and numerous acidophilic heterotrophic bacteria can
reduce Fe(III) to Fe(II), even under microoxic conditions
(Johnson and McGinness 1991). However, pure cultures of
neutrophilic microorganisms that could respire solid-phase
Fe(III)- and Mn(IV)-oxide minerals, such as Shewanella sp.
MR-1 and Geobacter metallireducens GS-15, were not isolated
and characterized until the late 1980s (Nealson and Myers
1992). Since then, microbial Fe(III) reduction has become
one of the best studied geomicrobiological processes,
primarily due to interest from the U.S. Department of
Energy in understanding the stability and reactivity of
Fe(III) oxide minerals that can sequester or release heavy
metal contaminants and radionuclides into subsurface
aquifers. Global interest in the mechanisms controlling
the reductive dissolution of Fe oxides is also high due to
the interrelationship between iron and arsenic biogeochemistry in the aquifers of Bangladesh, Cambodia, and
Vietnam.
E lements
CONCLUDING REMARKS:
JUMPING FROM EXTREME ENVIRONMENTS
ON EARTH TO MARS
As our understanding of iron-dependent metabolisms on
Earth rapidly expands, so too does our interest in whether
chemolithoautotrophic microbial organisms may once
have been sustained through an active iron cycle on Mars.
Increasing evidence for a past hydrological cycle on Mars
has established the possibility of warmer, wetter environments, where the oxidative dissolution of iron-rich silicate
rocks under aqueous conditions might once have been
conducive to life. Moreover, the abundance of Fe(III)
minerals (e.g. oxides, hydroxides, sulfates, and clays)
suggests that Fe(III)-reducing metabolisms could have been
possible in microenvironments when strong reductants
such as H 2 were available. A key question is whether physical or chemical biosignatures of iron-cycling microorganisms have been preserved in the rock record. Initially a
significant amount of debate focused on whether single98
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A
B
Microbially produced organic sheaths and filaments
are commonly biomineralized with iron: will these
structures and morphologies be preserved in the rock record?
(A) A fresh microbial mat forming at Vailulu’u Seamount in Samoa,
where tubular sheaths are associated with incipient Fe oxyhydroxides.
(B) A basalt surface recovered from Loihi Seamount, Hawai‘i, where
morphologically similar Fe hydroxide–encrusted tubular sheaths
have been incorporated into the weathered rock surface. Note the
longitudinal and end views of the tubes visible throughout.
domain magnetite minerals preserved in the Martian meteorite ALH84001 could unequivocally be interpreted as a
sign of life activity (McKay et al. 1996). At the present time,
increasing attention is being paid to the potential preservation of biomineralized organic structures commonly
produced by iron-oxidizing microorganisms (Emerson et
al. 2010) (Fig. 3), as well as to the study of biological iron
isotope fractionations that could be preserved in Martian
sediments (e.g. Beard et al. 2003).
detrimental to life by breaking down organics, at low
temperatures microbial organisms can successfully
“breathe” perchlorate using numerous electron donors,
including Fe(II) (Coates and Achenbach 2004). Therefore,
pathways for the microbial oxidation of iron do not appear
to be a problem—the greater challenge lies in constraining
the activity of water. If there was sufficient water, not only
could life harness Fe(II)-oxidation reactions, serpentinization processes due to water–rock interaction in the ironrich mafic and ultramafic rocks of the Martian crust could
have sustained subsurface microbial communities, as is
proposed on Earth today.
Figure 3
Several of the “extreme” systems discussed so far, such as
iron-rich hydrothermal vents, submarine basalt “aquifers,”
acid mine drainage, and acid–sulfate systems in Yellowstone,
may provide an initial framework for considering past ironbased “habitats” on Mars. One outstanding question in
extrapolating any of these scenarios to Mars is determining
the source of oxidants, such as O2 and nitrate, that could
have been harnessed for microbial metabolisms based upon
iron oxidation. One of the most intriguing discoveries in
the past few years is the apparent abundance of the strong
oxidant perchlorate, which was detected in Martian soils
by NASA’s Phoenix lander (Hecht et al. 2009). Although
perchlorate may be such a strong oxidizer that it would be
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ACKNOWLEDGMENTS
We thank Kurt Konhauser, Andreas Kappler, and Danielle
Fortin for constructive feedback on this topic; David
Emerson for illuminating conversations about ironoxidizing bacteria; and the David and Lucille Packard
Foundation for financial support.
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