Supply and Demand in Subseafloor Basalt Aquifers
Shock, E L
Subseafloor basalt aquifers contain 26 million cubic kilometers of water populated by unknown microbes that mediate the fluxes of elements between ridge flanks and seawater. The energy supporting this deep biosphere originates in the fundamental disequilibria between mid-ocean ridge basalts and seawater. Quantifying energy supplies depends in part on sampling and analysis of basalt aquifer fluids and in part on theoretical models of energy flow in complex natural systems. These approaches are joined through affinity diagrams that provide quantitative frameworks for testing models of the feedback between metabolism and weathering of oceanic crust. Fluid compositions can result from conductive cooling of hydrothermal fluids or mixing of hydrothermal fluids and seawater in regions proximal to the ridge, and conductive warming of seawater in basalt aquifers distal from the ridge. In all cases, temperature changes can be accompanied by diverse fluid-rock reactions. As a consequence, fluids can reach similar temperatures through multiple geochemical pathways, leading to diverse compositions. It is expected that these differences engender different habitats. Those influenced by deep hydrothermal fluids, such as post-eruptive fluids sampled at ridges and seamounts of the northeast Pacific, tend to be somewhat more acidic than habitats influenced by conductive heating of seawater. New results indicate that even at relatively low temperatures, these fluids provide ample energy for biosynthetic pathways including lipid and amino acid synthesis. For conductively heated habitats, preliminary results indicate that nitrate reduction must be coupled to oxidation of iron-bearing silicates for overall affinities to decrease in response to metabolism. In the extreme case of restricted fluids, in which water is the oxidant, hydrolytic oxidation of olivine provides sufficient hydrogen to reduce nicotineamide adenine dinucleotide at prevailing pH and silica activities. These are examples of how coupling biochemical demands with geochemical energy supplies defines habitats as alteration products and permits the integration of metabolism into assessments of elemental cycles.
A Geochemical Model for the Origin of Methane on Titan
Glein, C R, Shock, E L
The existence of methane in Titan's atmosphere has been a mystery for years [1]. The short photochemical lifetime of methane in the atmosphere suggests that methane is replenished from the interior. Observations by Cassini-Huygens have offered new insights into the origin of methane on Titan. These data have confirmed that Titan's methane is endogenic [2], consistent with geophysical models [3]. Today, an issue is the origin of methane on Titan in general. Why does Titan have methane in the first place? Here, we show that methane formation would have been unavoidable on early Titan. It is likely that Titan accreted materials similar to carbonaceous chondrites and comets, except for extreme volatiles in comets, such as carbon monoxide. Thus, we assume that Titan started with Fe-Ni metals and sulfides, silicates and oxides of the rock-forming elements, organic matter, carbon dioxide, methanol, and ammonia. After accretion, radiogenic heat would have melted ice, facilitating water-rock separation and interaction. Mineral dissolution and precipitation, along with acid-base reactions, would have been facile throughout differentiation, despite the low temperature. In contrast, most redox reactions, notably organic matter decomposition, would have been slow in cold aqueous solution. Eventually, the interior would have segregated into a muddy core, covered by a high-pressure ice layer, overlain by a salty ocean, capped by an ice shell [3]. The primordial muddy core would have been composed of phyllosilicates, organic matter, carbonates, sulfides, and presumably, metals. The early salty ocean would have been rich in sodium chloride and bicarbonate, in addition to methanol and ammonium salts. Methane would not have formed in hydrothermal systems at the ocean floor because the high-pressure ice layer would have inhibited hydrothermal circulation. Instead, we propose that methane is a byproduct of the thermal evolution of the core. Specifically, our core devolatilization hypothesis states that high temperatures driven by radioactive decay [4] changed the chemistry of the core via metamorphism. Preliminary calculations indicate that hydrous minerals recrystallize into anhydrous minerals by releasing water, which oxidizes Fe metal, producing dihydrogen (i.e., reducing conditions). In response, organic matter in the core is broken down into carbon-bearing solids, liquids, and gases, including methane. In time, methane can migrate into the ocean, where it can be trapped in clathrate hydrates and subsequently released into the atmosphere [3].
References:
[1] Owen T.C. (2000) P&SS 48, 747-752.
[2] Niemann H.B. et al. (2005) Nature 438, 779-784.
[3] Tobie G. et al. (2006) Nature 440, 61-64.
[4] Grasset O. et al. (2000) P&SS 48, 617-636.
Aerobic and Anaerobic Oxidation of Organic Acids in Yellowstone Hot Spring Ecosystems
Windman, T O, Zolotova, N, Shock, E
Thermodynamic analysis of energy supply based on samples collected from continental hot spring ecosystems at Yellowstone show that aerobic reactions yield the greatest energy. In terms of energy per mole of electrons transferred, aerobic oxidation of organic acids rivals or exceeds the energy supply from aerobic oxidation of hydrogen, CO, hydrogen sulfide, pyrite, sulfur or ammonia. This analysis is derived from samples collected where hot spring fluid are in contact with the atmosphere. It is likely that oxygen will be present at lower concentrations deeper in the system, which will place hard constraints on aerobic lifestyles. If so, which metabolisms could be supported deeper in the system? How will other oxidants be used to release energy? What characterizes the transition from aerobic to anaerobic oxidation? To answer these questions, pH, temperature, and alkalinity were measured in the field while measurements of dissolved oxygen and other redox-sensitive species (nitrate, ammonia, ferrous iron, and sulfide) were made with field-portable spectrophotometers and samples were taken for analysis of organic and inorganic ions by ion chromatography. Conditions in the subsurface can be predicted by starting from measured oxygen concentrations and calculating the effect of decreasing the concentration on the overall energetics of the system. Depending on hot spring composition, the amount of energy from aerobic oxidation of organic acid anions like succinate matches that from anaerobic oxidation (by nitrate or sulfate) once the log of the activity of dissolved oxygen drops to -6 to -8. These activities are 1 to 4 orders of magnitude lower that values determined for surface water in the hot springs. At lower oxygen activities aerobic oxidation gives way to anaerobic oxidation, and organic oxidation is more likely to involve nitrate and sulfate. Preliminary estimates indicate that these changes may occur at shallow depths in hot spring sediments (perhaps within the first centimeter), which suggests great differences between conditions inferred from fluids and those inferred from genomic data based on sediments or isolates from the same hot spring system.
Major Element Geochemistry of Biofilms in a Silica-Precipitating Hot Spring
Havig, J R ,Shock, E L, Moore, G
Hydrothermal biofilm communities represent one of the best present-day representations of early microbial communities, dating back to 2.5 Ga, and possibly 3.8 Ga in the geologic record. Silica-precipitating hydrothermal springs have been thought to have great potential for biosignature preservation. The interactions of hydrothermal water, biofilms, and precipitated siliceous sinter, however, remain poorly constrained. To this end, we collected water and biofilm, as well as contextual sinter and rock samples from various hot springs in Yellowstone National Park. Here we focus on one hot spring in Sentinel Meadow (Lower Geyser Basin), with temperature and pH that vary from the source (93 C, pH 7.4) to the farthest of five collection points down channel (56 C, pH 8.2). Elemental analysis reveals that the biofilms are made up of from <1 to ~11 % dry wt. carbon and ~0.1 to 1% dry wt. nitrogen. Major element analysis via electron microprobe and complimentary x-ray fluorescence show that (excluding C and N from the total) SiO2 constitutes 86 to 94 % dry weight mass, with the rest made up of Al2O3 (3 to 8%), Na2O (1.7 to 3.7%), K2O (0.6 to 1.5%), and minor amounts of FeO, CaO, MgO, and TiO2 (<1%). Local sinter is SiO2 (97.5% dry wt.), Na2O (1.5%), and <1% Al2O3, FeO, K2O, CaO, MgO, and TiO2. In addition, sinter contains measurable amounts of carbon (1.4%) and nitrogen (0.2%). Discrepancies between the biofilm and sinter values show that the geochemical compositions of biofilms are not captured by the precipitating silica. If biofilms accumulated elements strictly from the water, then it would take as much as 440 L of water to supply 1 gram (dry wt) of biofilm with the elements contained therein, assuming complete uptake. This seems especially unlikely in the case of Al, which is quite dilute (~500 ppb), poses very little benefit nutritionally, and increases in concentration down channel. Other major element components also exhibit at least one, if not all, of these traits. A potential source of the elements found in biofilms is aeolian-deposited dust. Area country rock is dominated by siliceous volcanism, represented locally by rhyolite samples collected from Sentinel Meadow. With an average value of ~10 wt % Al2O3 for the surrounding country rock, it would take approximately 0.6 grams of the ground up rock as dust to account for the Al found in one gram of biofilm. The low Al2O3 content of the sinter indicates that the Al is not entombed from the biofilms. A hypothesis for the above discrepancies in Al (as well as other elements) is that dust deposited in the water is captured on the biofilm surfaces, and the biofilm community then breaks down the dust, utilizing any nutritionally or metabolically important elements, and either precipitating (for Si) or releasing (for Al) unnecessary elements.
Biofilm function and variability in a hydrothermal ecosystem: insights from environmental genomes
Meyer-Dombard, D R, Raymond, J, Shock, E L
The ability to adapt to variable environmental conditions is key to survival for all organisms, but may be especially crucial to microorganisms in extreme environments such as hydrothermal systems. Streamer biofilm communities (SBCs) made up of thermophilic chemotrophic microorganisms are common in alkaline-chloride geothermal environments worldwide, but the in situ physiochemical growth parameters and requirements of SBCs are largely unknown [1]. Hot springs in Yellowstone National Park's alkaline geyser basins support SBC growth. However, despite the relative geochemical homogeneity of source pools and widespread ecosystem suitability in these regions (as indicated by energetic profiling [2]), SBCs are not ubiquitous in these ecosystems. The ability of hydrothermal systems to support the growth of SBCs, the relationship between these geochemically driven environments and the microbes that live there, and the function of individuals in these communities are aspects that are adressed here by applying environmental genomics. Analysis of 16S rRNA and total membrane lipid extracts have revealed that community composition of SBCs in "Bison Pool" varies as a function of changing environmental conditions along the outflow channel. In addition, a significant crenarchaeal component was discovered in the "Bison Pool" SBCs. In general, the SBC bacterial diversity triples while the archaeal component varies little (from 3 to 2 genera) in a 5-10°C gradient with distance from the source. While these SBCs are low in overall diversity, the majority of the taxa identified represent uncultured groups of Bacteria and Archaea. As a result, the community function of these taxa and their role in the formation of the biofilms is unknown. However, recent genomic analysis from environmental DNA affords insight into the roles of specific organisms within SBCs at "Bison Pool," and integration of these data with an extensive corresponding geochemical dataset may indicate shifting community function with geochemical variability. For example, calculations of energy availability and genomic data indicate a myriad of potential heterotrophic and autotrophic metabolic functions present at "Bison Pool" (genes for all known autotrophic C- fixation pathways, H2, CO, and formate oxidation, cellulose degredation, and Fe and As redox), as well as oxygenic and anoxygenic photosynthesis. These microbial communities and their environments are ideal for coordination of geochemical and genomic data, enabling informed analysis of SBC function and growth criteria.
[1] Jahnke, L. et al. (2001) AEM 67, 5179-5189
[2] Meyer-Dombard, D. et al. (2005) Geobiology 3, 211-227
Phototrophs vs. chemotrophs: surprising diversity at the intersection of hot springs communities
Raymond, J, Meyer-Dombard, D, Shock, E L
Access makes hot spring ecosystems ideal for combining geochemical data and thermodynamic models of energy supplies with cultivation-independent studies that shed light on biological diversity and function. We have recently undertaken combined 16S rRNA and metagenomic sampling of multiple communities found along a nearly 40 degree temperature gradient in a geochemically well-characterized alkaline hot spring in Yellowstone National Park (YNP). One unexpected result of this work comes at the so-called photosynthetic fringe, where "hot" chemotrophic metabolism gives way to "cool" phototrophy. This transition occurs between 55 and 73 degrees C in alkaline YNP springs for reasons that are poorly understood. While it is generally observed in other habitats that biodiversity increases as temperature decreases, 16S analysis reveals that diversity peaks at the fringe and tapers off at both higher and lower temperatures. Intriguingly, this increase is above and beyond what would be expected by merging the chemotrophic communities above the fringe with the photosynthetic communities below it, indicating that some facet of this unique intersection is supporting the potential for new niches to arise. Integrating metagenomic data with geochemical analyses offers molecular-level details for understanding how these niches develop and are sustained. The underlying interplay between geochemistry and genomics may well be driving the evolution and distribution of new metabolic capabilities including the presence of deeply branching RuBisCO and pyruvate:ferredoxin oxidoreductase homologs involved in autotrophic carbon fixation.