272 Northeastern Naturalist Vol. 16, Special Issue 5
Serpentinizing Fluids Craft Microbial Habitat
Dawn Cardace1,* and Tori M. Hoehler1
Abstract - Hydrogen produced by serpentinization has the potential to fuel subsurface
microbial metabolisms. In the serpentinizing subsurface, the solids comprise
ultramafic parent rocks derived from the Earth’s mantle, serpentine minerals, veins
of hydroxides, and accessory magnetite and/or other metal-rich grains. Fluid that occurs
with these solids is altered seawater and/or meteoric water and is predicted to be
reducing. Hydrogen, a powerful reducing agent, is generated when Fe2+ in Fe(OH)2 is
oxidized to magnetite, coupled to the reduction of water. Theoretical considerations
and experimental work suggest that serpentinization may generate fluid H2 concentrations
as high as ≈75 millimolar, and that related seeps on land should have ≈300
micromolar. Field observations have shown that submarine serpentinizing seeps
contain fluid H2 concentrations of 1 to 15 millimolar H2, subseafloor sediments have
≈7–100 nanomolar H2, and thermal springs have ≈13 nanomolar H2. Fluid H2 has the
potential to drive a variety of metabolic processes in oxygen- and organic carbondeprived
environments, such that considerable interest has developed in the potential
of serpentinizing systems as an abode of deep subsurface life. Based on empirical
parameters, we have modeled the free-energy change for an array of metabolic reactions
that may be associated with serpentinization, and find that metabolic niches do
exist for methanogenesis, ferric iron reduction, sulfate reduction, and nitrate reduction,
given environmentally realistic fluid chemistries.
Introduction
Microbial communities at work below the Earth’s surface occupy uncharted
territory. Considered solely in reference to life’s upper temperature
limit of approximately 130–150 ºC, the habitable subsurface may penetrate
the Earth’s crust to depths of 5–10 km, depending on regional heat flow. It
has been proposed that this deep subsurface habitat could accommodate up
to 2 x 1014 tons of biomass, an amount that, if concentrated, would blanket
the Earth’s surface to 1.5 m in thickness (Gold 1992). However, temperature
is not the sole limitation on biological activity. Organisms also require
liquid water, nutrients, and (perhaps most importantly for subsurface life) a
suitable energy source to build and sustain biomass. Lacking direct access
to sunlight or the abundant products of a photosynthetic surface biosphere
(O2 and organic matter), any microbial inhabitants of the deep subsurface
realm would have to be supported by the local (subsurface) geochemistry.
This fact requires that any would-be subsurface habitat provide a persistent
energy source of suitable type and magnitude. Serpentinizing systems may
provide such a source.
1NASA Ames Research Center, MS 239-4, Moffett Field, CA 94035-1000. *Corresponding
author - dawn.cardace-1@nasa.gov.
Soil and Biota of Serpentine: A World View
2009 Northeastern Naturalist 16(Special Issue 5):272–284
2009 D. Cardace and T.M. Hoehler 273
When upper mantle rocks, stable at 35–400 km depth, 227–1497 ºC, and
≈2–140 kbar pressure (Lodders and Fegley 1998), are exposed to conditions
characteristic of the planetary surface or near subsurface, their ultramafic
mineral constituents are no longer stable—that is, the minerals will spontaneously
react to form a new suite of stable minerals, with concomitant
release of energy. More specifically, exposure to water at these new pressure
and temperature conditions causes rapid weathering and rock alteration,
generating a new suite of daughter minerals, the most prominent of which
are serpentine group minerals (Fig. 1).
Hydrogen can be utilized as an energy source and electron donor for fixation
of CO2 into biomass by a diverse range of microorganisms (Schwarz
and Friedrich 2003) and is thus considered to have excellent life-supporting
potential in environments that lack light or organic matter as energy/electron
sources (Morita 2000). Many H2-dependent metabolisms deliver large
bioenergetic yields (Amend and Shock 2001), and several environments
on Earth are postulated to have food chains dependent on lithogenic H2
(Chapelle et al. 2002, Nealson et al. 2005). While these considerations (serpentinization
produces H2, and H2 is known to provide energy for microbes)
suggest, in a qualitative sense, that serpentinizing systems may be capable of
supporting subsurface communities, truly assessing this potential requires a
quantitative assessment of how much H2 is produced by serpentinization, and
at what rate, in comparison with the known requirements of microorganisms.
A key first step in such quantitative assessment is to determine whether H2
concentrations generated during serpentinization deliver useful free-energy
Figure 1. Diagram showing
that the interaction
of meteoric water (i.e.,
precipitation) or seawater
with ultramafic parent
rocks produces an
assemblage of serpentine
minerals, hydroxides
(aluminum, magnesium,
and iron), magnetite, and
hydrogen. Residual pyroxene
is also common.
274 Northeastern Naturalist Vol. 16, Special Issue 5
yields for microorganisms to capture. In general, it has been shown experimentally
that quantities of hydrogen sufficient to deliver useful free-energy
yields can be generated by serpentinization of diverse olivines ranging from
1 to 50 mol% iron (Oze and Sharma 2007). Whether this potential is met in
the environment, however, depends on a variety of environmental factors
and system-specific considerations.
The purpose of this paper is to examine the energy-yielding potential
of several H2-dependent metabolisms in fluid chemistries that are
environmentally realistic with respect to concentrations of H2 and other
physicochemical parameters. Four metabolisms are considered here: hydrogen
oxidation coupled with the reduction of (1) CO2 to CH4, (2) ferric
to ferrous iron, (3) nitrate to nitrogen, and (4) sulfate to sulfide. Published
geochemical data are used to determine whether there is a thermodynamic
drive for the selected metabolisms to occur.
The Geochemistry of Serpentinization
In the presence of water at temperatures and pressures characteristic of
the Earth’s surface or near-surface environments, ultramafic igneous rocks
composed of fayalite (iron-rich olivine), forsterite (magnesium-rich olivine),
and pyroxene alter to serpentine minerals (e.g., lizardite, chrysotile,
and antigorite) and hydroxides (Prichard 1979, Schulte et al. 2006), increasing
alkalinity, as shown in Reaction (1).
Fe2SiO4 + 5Mg2SiO4 + 9H2O→3Mg3Si2O5(OH)4
+ Mg(OH)2 + 2Fe(OH)2 (1)
Fayalite + forsterite + water → serpentine + brucite + iron hydroxide
Hydrogen, a powerful reducing agent, is generated when Fe2+ in Fe(OH)2
from (1) is oxidized to magnetite, coupled to the reduction of water.
3Fe(OH)2 → Fe3O4 + 2H2O + H2 (2)
Iron hydroxide → magnetite + water + hydrogen
Overall, this process can be expected to yield fluids that are highly alkaline
and enriched in H2, affirming early speculations that the reaction of water
with ferrous minerals could yield H2 (Ramdohr 1967). Because serpentine
minerals require more volume than precursor, parent minerals, they literally
take up more space, perhaps 33% more (Hostetler et al. 1966), causing fracturing
in the host rock. For this reason, unaltered parent rock is continually
accessed by fluids and experiencing serpentinization, over geologic time.
An excellent example of modern seafloor serpentinization is provided by
the venting fluids at Lost City Hydrothermal Field, located about 15 km west
of the Mid-Atlantic Ridge ocean spreading center. Here, seawater reacts with
uplifted peridotites (mantle rocks), generating high pH (10–11), H2- and
CH4-rich fluids (CH4(aq) at 2 millimolal and H2(aq) at 15 millimolal) that vent
at the rock-seawater interface. The H2 in these fluids is thought to sustain a
2009 D. Cardace and T.M. Hoehler 275
thriving, methane-cycling microbial community (Kelley et al. 2005). Even
in continental basalt aquifers, where the host rock is not as rich in reactive
iron as peridotite, lithoautotrophic microbial communities, involving methanogens,
acetogens, and sulfate reducers, have been observed (Stevens and
McKinley 1995, 2000; Stevens et al. 1993).
The major problem with scientific investigation of deep subsurface sites
is difficult access; deep drilling on continents and on the seafloor is expensive,
in terms of cost, equipment, time, and expertise, and investigating
windows into the subsurface (i.e., deep sea vents allowing escape of deeply
sourced fluids) is constrained by remotely operated vehicles (ROV) technology.
For this reason, the extent of the deep biosphere remains unknown.
Serpentinization can be studied near the Earth’s surface on land in
ultramafic parts of ophiolites, blocks of ocean crust, and associated sedimentary
rocks that have been tectonically emplaced on land. Ocean crust
forms at mid-ocean ridges, where seams in the tectonic plates that make up
the Earth’s crust allow mafic magma (i.e., molten rock rich in magnesium
and iron) to escape from magma chambers at depth to build ocean crust as
it solidifies. Ophiolites sample the vertical breadth of the ocean crust, ideally
comprising, from bottom to top: peridotite (mantle rock composed primarily
of olivine and pyroxene), layered gabbro (rock in which crystals are
layered, reflecting the settling of crystals in a subsurface magma chamber),
vertical dikes of basaltic rock (attesting to the vertical transport of magma
to the surface), pillow basalts (whose shape belies the sequential cooling of
lavas on the ocean floor), and marine sediments (as summarized in Juteau
2003). Because such sites have potential to expose zones of active serpentinization
at or near the land surface, they present an excellent opportunity
for detailed studies of fluid and rock chemistry, with the possibility for
repeated or long-term sampling. Studies of this type will be crucial for
investigating, in detail, the life-supporting potential of deep subsurface
serpentinizing systems.
At serpentinizing seeps on land, H2(aq) concentrations are predicted to
be on the order of 300 micromolar, based on thermodynamic modeling of
serpentinization reactions, whereas concentrations that are orders of magnitude
greater are possible where fluids are in equilibrium with serpentinite at
depth (Sleep et al. 2004). Since gas solubility depends on temperature and
pressure, fluids lose hydrogen as bubbles of free gas as the water approaches
the planetary surface. Fluid seeps associated with ophiolites have been characterized
in California and Oregon in the USA, New Caledonia, Oman, and
the former Yugoslavia (Barnes et al. 1967, 1978; Neal and Stanger 1983),
and western Newfoundland (Roberts and Deering 2005). Gas seeps also
occur, sourced in serpentinizing regions; good examples of H2 seepage at
40–70 vol% occur at Los Fuegos Eternos in the Zambales Ophiolite of the
Manila Trench forearc (Abrajano et al. 1988) and the Anita shear zone exposed
at Poison Bay on New Zealand’s South Island (Wood 1972). Typically,
276 Northeastern Naturalist Vol. 16, Special Issue 5
fluid from seeps exhibits high concentrations of Ca2+ (5–80 mg/L) and
OH- (6 to 70 mg/L), with pH ranging up to 12.1 (Barnes et al. 1967). Such
geochemically distinct fluids uniquely identify ongoing serpentinization in
the rock. Despite general similarities, however, a range of physicochemical
conditions may characterize serpentinizing systems. Contrasting parent rock
compositions, vein mineralogy, and aqueous geochemistry present a range
of conditions that may significantly influence the potential habitability of
a given serpentinizing system. Fluid chemistry defines which metabolisms
are possible, both by providing specific energy sources and by defining the
chemical environment in which an organism must function.
Modeling approach
Microbial metabolisms, as chemical reactions, are constrained by
thermodynamics. Determining the thermodynamic spontaneity of specific
reactions based on empirical data for subsurface, low temperature, alkaline
habitats serves as a starting point (as a necessary but not sufficient condition)
for evaluating habitability. Here, we used geochemical thermodynamic modeling
to calculate the energy yields for four reactions that represent potential
subsurface metabolisms. In brief, this calculation is done by evaluating the
Gibbs energy of reaction (ΔGr), which represents the chemical energy available
in a system to do useful work. ΔGr is the sum of the standard Gibbs
energy term (ΔGrº, which represents reaction energy at unit pressure and
with all product and reactant concentrations fixed at 1 molar) and a term (Qr,
the activity product) that reflects the chemical composition of the system (for
product and reactant concentrations that deviate from unit molarity). In the
latter term, the impact of different chemistries on ΔGr is taken into account;
if interstitial fluid chemistries incorporated in the Qr term differ, then ΔGr
also differs. Measured concentrations of interstitial fluids are transformed
into modeled activities (i.e., the effective concentrations of specified chemical
species), which are used directly in calculating ΔGr.
Once activities are known for all chemical constituents of a reaction, ΔGr
can be calculated at target conditions from the expression (3):
ΔGr = ΔGrº + RT lnQr (3),
where ΔGr is the Gibbs free energy of reaction, ΔGrº is the standard state
Gibbs free energy, R and T represent the gas constant and temperature in
kelvins, respectively, and Qr stands for the activity product, discussed below.
ΔGr
can be obtained for any temperature and pressure by calculating
the activity product as long as ΔGrº is known. ΔGrº can be determined at the
appropriate temperature and pressure for the aqueous species and minerals
using established equations of state (Helgeson et al. 1978, 1981; Shock and
Helgeson 1988, 1990; Shock et al. 1989, 1992; Tanger and Helgeson 1988),
or computed from data for ΔGrº and ΔGiº at temperatures up to 200 ºC at Psat,
available in Amend and Shock (2001).
2009 D. Cardace and T.M. Hoehler 277
The activity product, Qr , can be computed from environmental data as
shown in relation (4):
Qr = Πai
υi,r (4),
where ai represents the activity of the ith species, and υi,r represents the
stoichiometric reaction coefficient. Values of ai can be generated from concentration
data (Table 1) and activity coefficients, using the geochemical
speciation code EQ3 (Wolery 1992).
Results and Discussion
Four reactions were considered as potential serpentinization-supported
metabolisms. Hydrogen oxidation coupled with reduction of (i) CO2 to
Table 1. Data for seawater, observed serpentinizing seeps and predicted concentrations for
serpentinizing fluids, and the model inputs used in assessing the metabolic potential of these
waters. All concentrations are in ppm, except for pH and temperature (ºC). Computed reacted
meteoric water (Palandri and Reed 2004) values show the impact of water-rock ratio (w/r);
higher water to rock ratio lowers pH and major ions in the resulting seep water. Relevant citations
are presented in footnotes. Inputs (far right, modified from Barnes et al. 1967) served as
the basis for speciation and solubility geochemical modeling inputs for EQ3 (Wolery 1992),
with CH4(aq) concentration taken as 10μM and variable H2(aq). ND = not detected. - = no data.
Computed reacted
meteoric waterF John La
Day Cazadero Hahwalah Coulee log w/r log w/r Model
SeawaterA SpringB SpringC SpringD SpringE of 3 of 1 fluidG
pH ≈8.1 11.3 11.8 11.5 10.7 10.5 11.6 11.8
Temp. ≈15 31.0 18.0 25.0 23.0 25.0 25.0 16.0
Ca++ 415.0 35.0 53.0 60.0 10.8 4.7 78.6 48.0
Mg++ 1280.0 0.1 0.3 0.1 5.9 0.76 0.011 0.4
Na+ 10,781.0 33.0 50.0 230.0 26.1 3.8 12.7 40.0
K+ 399.0 2.3 1.2 8.0 3.3 0.2 1.1 1.1
Cl- 19,353.0 19.0 55.0 280.0 16.3 5.1 8.4 32.0
SO4
-- - - - 9.0 5.8 1 x10-26 1.8 x10-33 1.4
NO3
- - 0.4 1.0 - - - - 0.2
CO3
-- 71.0 - - - 20.0 0.8 0.4 1 x 10-7
SiO2(aq) 6.0 5.9 0.3 0.1 2.8 0.0016 0.032 5.2
Fe++ <0.001 0.0 0.0 ND ND 0.014 0.64 0.0
Al+++ <0.001 0.7 ND ND ND 2.6x10-8 2.0 0.4
Mn++ <0.001 0.0 ND ND ND 0.9 6.4 0.0
H2(aq) ND ND ND ND ND ND ND Variable
CH4(aq) ND ND ND ND ND ND ND 0.2
ALodders and Fegley 1998.
BGrant County, OR, USA; Barnes et al. 1967.
CSonoma County, CA, USA; Barnes et al. 1972.
DWadi Jizi, Oman; Barnes et al. 1978.
ENew Caledonia; Barnes et al. 1978.
FPalandri and Reed 2004.
GThis study.
278 Northeastern Naturalist Vol. 16, Special Issue 5
methane, (ii) ferric to ferrous iron, (iii) nitrate to nitrogen, and (iv) sulfate
to sulfide:
(i) CO2(aq) + 4H2(aq) = CH4(aq) + 2H2O(l),
(ii) H2(aq) + 2Fe3+ = 2Fe2+ + 2H+,
(iii) NO3
- + 2.5H2(aq) + H+ = 0.5N2(aq) + 3H2O(l), and
(iv) SO4
2- + 4H2(aq) + 2H+ = H2S(aq) + 4H2O(l).
Figure 2 shows, for the modeled fluid composition, the range of hydrogen
concentrations under which these four reactions are thermodynamically
favored (Gibbs Energy < 0) and spontaneous. The y axis on each plot shows
the calculated Gibbs Energy per mole of electrons transferred, noting that
more negative free-energy values correspond to more thermodynamically
favorable reactions. Spontaneity (Gibbs energy change less than zero) of
metabolic reactions is a condition for their successful exploitation as energy
sources by living organisms. The habitable niche, thusly defined, is where
the metabolic reaction is spontaneous within observed environmental conditions.
Reaction (i) is favored for a range of H2 activities, well into the range
of aH2(aq) expected based on theoretical calculations, and reactions (ii), (iii),
and (iv) are favored for the entire modeled range of aH2(aq). We examined
the Gibbs energy for these reactions over several orders of magnitude, from
log aH2 at -7 (≈100 nM H2) to -1 (≈100 mM H2). The lowest end of this hydrogen
range corresponds to the upper limit for subseafloor sediments and
thermal springs (<1–100 nM; Chapelle et al. 2002, D’Hondt et al. 2003,
Lovley and Goodwin 1988), and we expect that H2 supply should not be
limiting for resident microbes in this system, particularly if episodic serpentinization
events flush the system periodically with H2. Experimental results
for H2 in fluids in equilibrium with serpentinite land at the high end of this
range, where log aH2 approaches -1 (75 mM; Seyfried et al. 2007), while
theoretical predictions for surface seeps on land would fall near log aH2 =
-3.5 (≈300 micromolar; Sleep et al. 2004). Active serpentinizing seeps on
the seafloor have been observed around log aH2 = -3 to -1.8 (1 to 15 mM
H2; Kelley et al. 2005). If we assume that all the free hydrogen observed at
gas seeps from the Zambales ophiolite (40 vol% H2; Abrajano et al. 1988)
and the Anita Shear Zone at Poison Bay (70 vol% H2; Wood 1972) was
dissolved in water, the concentrations, based on a simple Henry’s Law calculation
with KH = 7.8 x 10-4 as in Sander (1999), would be on the order of
Figure 2 (opposite page). Four crossplots of log a(H2(aq)) vs. ΔGr illustrate where
the subsurface habitable niches exist, based on thermodynamic considerations.
Habitable niches are bounded above by ΔGr = 0 (i.e., equilibrium, no spontaneous
reaction), and to the right at log a(H2(aq)) = -1, the expected upper limit serpentinizing
systems (Sleep et al. 2004). The star indicates the approximate calculated value for
hydrogen dissolved in fluids associated with gas seeps at the Zambales Ophiolite and
the Anita Shear Zone; please see text for discussion. (i) the methanogenesis reaction
is favored for a range in log a(H2(aq) and is more favored at lower temperatures close
to equilibrium. The (ii) ferric iron reduction, (iii) nitrate, and (iv) sulfate reduction
reactions are favored across all H2(aq) activities considered.
2009 D. Cardace and T.M. Hoehler 279
340 to 540 micromolar H2(aq), or log aH2 between -3.5 and -3.3. These results
suggest that methanogenesis, ferric iron reduction, nitrate reduction, and
280 Northeastern Naturalist Vol. 16, Special Issue 5
sulfate reduction can, in principle, be supported by fluid chemistries associated
with serpentinizing systems.
Thermodynamic favorability of a metabolic reaction is a necessary
but not sufficient condition, if that reaction is to support living communities.
Biochemical and physicochemical environmental factors must also be
considered; in particular, the highly alkaline character of serpentized fluids
presents a challenge for biology. The potential metabolisms considered here
have all been documented in high pH environments. Microbially mediated
methane production from CO2 and H2 has been studied in the laboratory,
working with cultures of Methanoculleus sp. and Methanocalculus sp., collected
from briny Lonar Lake (India) water of pH 10 and cultured at pH 9
(Surakasi et al. 2007). Ferric iron reduction coupled to hydrogen oxidation
has been observed in cultures of Alkaliphilus metalliredigens Ye, Roh, Carroll,
Blair, Zhou, Shang, and Fields, from a saline leachate pond, at pH 9.5
(Roh et al. 2007). Nitrate reduction coupled to hydrogen oxidation in Paracoccus
denitrificans Beijerinck and Minkham and Pseudomonas stutzeri
Migula has also been monitored in the laboratory around pH of 8.2, maintained
via bicarbonate buffer (Strohm et al. 2007). In cultures from Kulunda
Steppe soda lakes in southeastern Siberia, pH ≈11, sulfate reducers have
been shown to use H2 as an electron donor (Foti et al. 2007). From these and
other studies, it is plain that known microbes carry out the reactions considered
here, in waters of similar pH.
For the metabolisms considered here, thermodynamic favorability under
environmentally realistic H2 concentrations and other physicochemical
conditions meets a first and critical requirement for the potential habitability
of serpentinizing systems. Energy must also be delivered at rates and levels
that meet the demands of biological energy conservation— a balance
in which both supply and demand are highly dependent on environmental
conditions (Hoehler 2004, 2007). If H2 is available in the system, it diffuses
freely across cell membranes and is accessible to biology; considering the
abundances of other necessary reactants and the rates of their delivery will
help constrain the true habitability of this environment. These modeling
results are the first step in characterizing the energy balance associated with
the potential habitability of these systems. Quantifying available H2 will be
necessary to ground-truth this work, and applying molecular techniques to
environmental DNA extracts from serpentinizing seep waters, to identify
whether these or similar microbes are present, is the next logical phase of
the project.
Concluding comments
Serpentinizing systems have extraordinary potential to sustain deep
subsurface life depending on chemical (rather than light) energy. Hydrogen-
utilizing organisms are theorized to live in the ultramafic subsurface,
deriving energy from hydrogen oxidation. On Earth, the lower crust and
upper mantle hold a large volume of ultramafic rock, variably serpentinized,
to tens of kilometers in depth. This proposed volume of habitable
2009 D. Cardace and T.M. Hoehler 281
space can host microbial biomass dependent on hydrogen production over
geologic time (Sleep and Zoback 2007). In addition, olivine-bearing mafic
rocks exist at or below the surface on Mars (Hoefen et al. 2003, McSween
et al. 2004, Yen et al. 2005) and are expected to be similar in composition
to mafics on Earth’s surface, providing close analogue environments to
terrestrial serpentinizing systems. On Europa, putative habitats include
submarine rocks (Lipps and Riebolt 2005), which may well have experienced
hydrothermal circulation and rock alteration reactions related to
serpentinization. Research into the subsurface habitability of terrestrial
serpentine terrains will ground-truth the search for life in ultramafic rock
complexes beyond Earth.
We infer from data and modeling results that the aqueous geochemistry
associated with serpentinizing seep waters are out of equilibrium with the
surface Earth and therefore offer energy, by virtue of chemical disequilibrium,
to a variety of H2-consuming metabolisms. Such fluids may therefore
be capable of supporting a variety of microbial populations with an energy
source that is decoupled from the surface photosynthetic biosphere. Model
results support the feasibility of all four metabolisms considered, and known
microbes do mediate these reactions at the alkaline pH values often associated
with serpentinized fluids. The serpentinizing subsurface thus holds
considerable promise as a large, untapped area of the deep biosphere on
Earth, and possibly beyond.
Acknowledgments
This work is funded by the NASA Postdoctoral Program, administered by Oak
Ridge Associated Universities, and a NASA Exobiology grant, “Quantifying the
habitability of low-temperature serpentinizing systems.”
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