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Serpentinizing Fluids Craft Microbial Habitat
Dawn Cardace and Tori M. Hoehler

Northeastern Naturalist, Volume 16, Special Issue 5 (2009): 272–284

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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. 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