The metabolic rate of the biosphere and its components.

We assessed the relationship between rates of biological energy utilization and the biomass sustained by that energy utilization, at both the organism and biosphere level. We compiled a dataset comprising >10,000 basal, field, and maximum metabolic rate measurements made on >2,900 individual species, and, in parallel, we quantified rates of energy utilization, on a biomass-normalized basis, by the global biosphere and by its major marine and terrestrial components. The organism-level data, which are dominated by animal species, have a geometric mean among basal metabolic rates of 0.012 W (g C)-1 and an overall range of more than six orders of magnitude. The biosphere as a whole uses energy at an average rate of 0.005 W (g C)-1 but exhibits a five order of magnitude range among its components, from 0.00002 W (g C)-1 for global marine subsurface sediments to 2.3 W (g C)-1 for global marine primary producers. While the average is set primarily by plants and microorganisms, and by the impact of humanity upon those populations, the extremes reflect systems populated almost exclusively by microbes. Mass-normalized energy utilization rates correlate strongly with rates of biomass carbon turnover. Based on our estimates of energy utilization rates in the biosphere, this correlation predicts global mean biomass carbon turnover rates of ~2.3 y-1 for terrestrial soil biota, ~8.5 y-1 for marine water column biota, and ~1.0 y-1 and ~0.01 y-1 for marine sediment biota in the 0 to 0.1 m and >0.1 m depth intervals, respectively.

Relatively oxidized fluids fed Earth's earliest hydrothermal systems.

The properties of high-temperature lithospheric fluids within the early Earth are poorly known, yet many origin-of-life scenarios depend upon their characteristics. These fluids represent a key communication pathway between Earth's interior and hydrothermal pools. We use zircon chemistry, experiments, and modeling to infer the character of lithospheric fluids approaching 4 billion years. We constrain oxygen fugacity, chlorine content, and temperature, which allow us to model the solubility and transport of metals that are hypothesized to be crucial for the origin of life. We show that these fluids were more oxidized than the terrestrial mantle during this time and that they were interacting with near-surface aqueous systems, possibly subaerial hydrothermal pools, amplifying redox gradients in a location attractive for prebiotic molecular synthesis or sustained microbial activity.

The effect of pH on rates of reaction and hydrogen generation during serpentinization.

A series of three laboratory experiments were conducted to investigate how pH affects reaction pathways and rates during serpentinization. Two experiments were conducted under strongly alkaline conditions using olivine as reactant at 200 and 230°C, and the results were compared with previous studies performed using the same reactants and methods at more neutral pH. For both experiments, higher pH resulted in more rapid serpentinization of the olivine and generation of larger amounts of H2 for comparable reaction times. Proportionally greater amounts of Fe were partitioned into brucite and chrysotile and less into magnetite in the experiments conducted at higher pH. In a third experiment, alkaline fluids were injected into an ongoing experiment containing olivine and orthopyroxene to raise the pH from circumneutral to strongly alkaline conditions. Increasing the pH of the olivine-orthopyroxene experiment resulted in an immediate and steep increase in H2 production, and led to far more extensive reaction of the primary minerals compared to a similar experiment conducted under more neutral conditions. The results suggest that the development of strongly alkaline conditions in actively serpentinizing systems promotes increased rates of reaction and H2 production, enhancing the flux of H2 available to support biological activity in these environments. This article is part of a discussion meeting issue 'Serpentinite in the Earth System'.

Experimental Constraints on Abiotic Formation of Tubules and Other Proposed Biological Structures in Subsurface Volcanic Glass.

Formation of microtubules in volcanic glass from subsurface environments has been widely attributed to in situ activity of micro-organisms, but evidence directly linking those structures to biological processes remains lacking. Investigations into the alternative possibility of abiotic tubule formation have been limited. A laboratory experiment was conducted to examine whether moderate-temperature hydrothermal alteration of basaltic glass by seawater would produce structures similar to those ascribed to biological processes. Shards of glass were reacted with artificial seawater at 150°C for 48 days. Following reaction, the shards were uniformly covered with a brick-red alteration rind 10-30 µm thick composed primarily of phyllosilicates. Inspection of the margins of reacted shards with light microscopy did not reveal any tubule structures. However, the alteration products did include features containing micron-sized spheroidal structures that resemble granular alteration textures, which some investigators have attributed to biological activity. This result suggests that the granular textures may be at least partially abiotic, and that biological activity may make a smaller contribution to alteration of the oceanic crust than has been previously proposed. Also, while the experimental results do not exclude the possibility that tubules form abiotically, they do place limitations on the conditions under which this may occur.

Jarosite and Alunite in Ancient Terrestrial Sedimentary Rocks: Reinterpreting Martian Depositional and Diagenetic Environmental Conditions.

Members of the alunite group are precipitated at low pH (<1 to ~4) in oxidizing environments, are unstable in circumneutral conditions, and are widespread on Mars. At Mollies Nipple in Kane County, Utah, USA, jarosite and alunite are abundant as diagenetic cements in Jurassic sandstones. This research characterizes the jarosite and alunite cements with the goal of determining their origin, and tests the hypothesis that jarosite and alunite may be more stable than the current understanding indicates is possible. Previous studies have placed the jarosite- and alunite-bearing caprock at Mollies Nipple in the Navajo Sandstone, but the presence of water-lain deposits, volcanic ash, volcanic clasts, and peloids show that it is one of the overlying Middle Jurassic units that records sea level transgressions and regressions. A paragenetic timing, established from petrographic methods, shows that much of the cement was precipitated early in a marginal marine to coastal dune depositional environment with a fluctuating groundwater table that drove ferrolysis and evolved the groundwater to a low pH. Microbial interaction was likely a large contributor to the evolution of this acidity. Jarosite and alunite are clearly more stable in natural environments than is predicted by laboratory experiments, and therefore, the Martian environments that have been interpreted as largely acidic and/or dry over geologic time may have been more habitable than previously thought.

Methane Dynamics in a Tropical Serpentinizing Environment: The Santa Elena Ophiolite, Costa Rica.

Uplifted ultramafic rocks represent an important vector for the transfer of carbon and reducing power from the deep subsurface into the biosphere and potentially support microbial life through serpentinization. This process has a strong influence upon the production of hydrogen and methane, which can be subsequently consumed by microbial communities. The Santa Elena Ophiolite (SEO) on the northwestern Pacific coast of Costa Rica comprises ~250 km2 of ultramafic rocks and mafic associations. The climatic conditions, consisting of strongly contrasting wet and dry seasons, make the SEO a unique hydrogeological setting, where water-rock reactions are enhanced by large storm events (up to 200 mm in a single storm). Previous work on hyperalkaline spring fluids collected within the SEO has identified the presence of microorganisms potentially involved in hydrogen, methane, and methanol oxidation (such as Hydrogenophaga, Methylobacterium, and Methylibium spp., respectively), as well as the presence of methanogenic Archaea (such as Methanobacterium). Similar organisms have also been documented at other serpentinizing sites, however their functions have not been confirmed. SEO's hyperalkaline springs have elevated methane concentrations, ranging from 145 to 900 µM, in comparison to the background concentrations (<0.3 µM). The presence and potential activity of microorganisms involved in methane cycling in serpentinization-influenced fluids from different sites within the SEO were investigated using molecular, geochemical, and modeling approaches. These results were combined to elucidate the bioenergetically favorable methane production and/or oxidation reactions in this tropical serpentinizing environment. The hyperalkaline springs at SEO contain a greater proportion of Archaea and methanogens than has been detected in any terrestrial serpentinizing system. Archaea involved in methanogenesis and anaerobic methane oxidation accounted from 40 to 90% of total archaeal sequences. Genes involved in methanogenic metabolisms were detected from the metagenome of one of the alkaline springs. Methanogenic activities are likely to be facilitated by the movement of nutrients, including dissolved inorganic carbon (DIC), from surface water and their infiltration into serpentinizing groundwater. These data provide new insight into methane cycle in tropical serpentinizing environments.

Biosignature Preservation and Detection in Mars Analog Environments.

This review of material relevant to the Conference on Biosignature Preservation and Detection in Mars Analog Environments summarizes the meeting materials and discussions and is further expanded upon by detailed references to the published literature. From this diverse source material, there is a detailed discussion on the habitability and biosignature preservation potential of five primary analog environments: hydrothermal spring systems, subaqueous environments, subaerial environments, subsurface environments, and iron-rich systems. Within the context of exploring past habitable environments on Mars, challenges common to all of these key environments are laid out, followed by a focused discussion for each environment regarding challenges to orbital and ground-based observations and sample selection. This leads into a short section on how these challenges could influence our strategies and priorities for the astrobiological exploration of Mars. Finally, a listing of urgent needs and future research highlights key elements such as development of instrumentation as well as continued exploration into how Mars may have evolved differently from Earth and what that might mean for biosignature preservation and detection. Key Words: Biosignature preservation-Biosignature detection-Mars analog environments-Conference report-Astrobiological exploration. Astrobiology 17, 363-400.

Abiotic methane formation during experimental serpentinization of olivine.

Fluids circulating through actively serpentinizing systems are often highly enriched in methane (CH4). In many cases, the CH4 in these fluids is thought to derive from abiotic reduction of inorganic carbon, but the conditions under which this process can occur in natural systems remain unclear. In recent years, several studies have reported abiotic formation of CH4 during experimental serpentinization of olivine at temperatures at or below 200 °C. However, these results seem to contradict studies conducted at higher temperatures (300 °C to 400 °C), where substantial kinetic barriers to CH4 synthesis have been observed. Here, the potential for abiotic formation of CH4 from dissolved inorganic carbon during olivine serpentinization is reevaluated in a series of laboratory experiments conducted at 200 °C to 320 °C. A 13C-labeled inorganic carbon source was used to unambiguously determine the origin of CH4 generated in the experiments. Consistent with previous high-temperature studies, the results indicate that abiotic formation of CH4 from reduction of dissolved inorganic carbon during the experiments is extremely limited, with nearly all of the observed CH4 derived from background sources. The results indicate that the potential for abiotic synthesis of CH4 in low-temperature serpentinizing environments may be much more limited than some recent studies have suggested. However, more extensive production of CH4 was observed in one experiment performed under conditions that allowed an H2-rich vapor phase to form, suggesting that shallow serpentinization environments where a separate gas phase is present may be more favorable for abiotic synthesis of CH4.

Generation of Hydrogen and Methane during Experimental Low-Temperature Reaction of Ultramafic Rocks with Water.

UNLABELLED: Serpentinization of ultramafic rocks is widely recognized as a source of molecular hydrogen (H2) and methane (CH4) to support microbial activity, but the extent and rates of formation of these compounds in low-temperature, near-surface environments are poorly understood. Laboratory experiments were conducted to examine the production of H2 and CH4 during low-temperature reaction of water with ultramafic rocks and minerals. Experiments were performed by heating olivine or harzburgite with aqueous solutions at 90°C for up to 213 days in glass bottles sealed with butyl rubber stoppers. Although H2 and CH4 increased steadily throughout the experiments, the levels were very similar to those found in mineral-free controls, indicating that the rubber stoppers were the predominant source of these compounds. Levels of H2 above background were observed only during the first few days of reaction of harzburgite when CO2 was added to the headspace, with no detectable production of H2 or CH4 above background during further heating of the harzburgite or in experiments with other mineral reactants. Consequently, our results indicate that production of H2 and CH4 during low-temperature alteration of ultramafic rocks may be much more limited than some recent experimental studies have suggested. We also found no evidence to support a recent report suggesting that spinels in ultramafic rocks may stimulate H2 production. While secondary silicates were observed to precipitate during the experiments, formation of these deposits was dominated by Si released by dissolution of the glass bottles, and reaction of the primary silicate minerals appeared to be very limited. While use of glass bottles and rubber stoppers has become commonplace in experiments intended to study processes that occur during serpentinization of ultramafic rocks at low temperatures, the high levels of H2, CH4, and SiO2 released during heating indicate that these reactor materials are unsuitable for this purpose. KEY WORDS: Serpentinization-Hydrogen generation-Abiotic methane synthesis. Astrobiology 16, 389-406.

The energetics of organic synthesis inside and outside the cell.

Thermodynamic modelling of organic synthesis has largely been focused on deep-sea hydrothermal systems. When seawater mixes with hydrothermal fluids, redox gradients are established that serve as potential energy sources for the formation of organic compounds and biomolecules from inorganic starting materials. This energetic drive, which varies substantially depending on the type of host rock, is present and available both for abiotic (outside the cell) and biotic (inside the cell) processes. Here, we review and interpret a library of theoretical studies that target organic synthesis energetics. The biogeochemical scenarios evaluated include those in present-day hydrothermal systems and in putative early Earth environments. It is consistently and repeatedly shown in these studies that the formation of relatively simple organic compounds and biomolecules can be energy-yielding (exergonic) at conditions that occur in hydrothermal systems. Expanding on our ability to calculate biomass synthesis energetics, we also present here a new approach for estimating the energetics of polymerization reactions, specifically those associated with polypeptide formation from the requisite amino acids.

Geochemical constraints on sources of metabolic energy for chemolithoautotrophy in ultramafic-hosted deep-sea hydrothermal systems.

Numerical models are employed to investigate sources of chemical energy for autotrophic microbial metabolism that develop during mixing of oxidized seawater with strongly reduced fluids discharged from ultramafic-hosted hydrothermal systems on the seafloor. Hydrothermal fluids in these systems are highly enriched in H(2) and CH(4) as a result of alteration of ultramafic rocks (serpentinization) in the subsurface. Based on the availability of chemical energy sources, inferences are made about the likely metabolic diversity, relative abundance, and spatial distribution of microorganisms within ultramafic-hosted systems. Metabolic reactions involving H(2) and CH(4), particularly hydrogen oxidation, methanotrophy, sulfate reduction, and methanogenesis, represent the predominant sources of chemical energy during fluid mixing. Owing to chemical gradients that develop from fluid mixing, aerobic metabolisms are likely to predominate in low-temperature environments (<20-30 degrees C), while anaerobes will dominate higher-temperature environments. Overall, aerobic metabolic reactions can supply up to approximately 7 kJ of energy per kilogram of hydrothermal fluid, while anaerobic metabolic reactions can supply about 1 kJ, which is sufficient to support a maximum of approximately 120 mg (dry weight) of primary biomass production by aerobic organisms and approximately 20-30 mg biomass by anaerobes. The results indicate that ultramafic-hosted systems are capable of supplying about twice as much chemical energy as analogous deep-sea hydrothermal systems hosted in basaltic rocks.

Geochemistry: biosignatures and abiotic constraints on early life.

Ueno et al. contend that methane found in fluid inclusions within hydrothermally precipitated quartz in the Dresser Formation of western Australia (which is roughly 3.5 Gyr old) provides evidence for microbial methanogenesis in the early Archaean era. The authors discount alternative origins for this methane, suggesting that the range of delta(13)C(CH(4)) values that they record (-56 to -36 per thousand) is attributable to mixing between a primary microbial end-member with a delta(13)C(CH(4)) value of less than -56 per thousand and a mature thermogenic gas enriched in (13)C (about -36 per thousand). However, abiotic methane produced experimentally and in other Precambrian greenstone settings has (13)C-depleted delta(13)C(CH(4)) values, as well as Delta(13)C(CO(2)-CH(4)) relationships that encompass the range measured for the inclusions by Ueno et al. - which suggests that an alternative, abiotic origin for the methane is equally plausible. The conclusions of Ueno et al. about the timing of the onset of microbial methanogenesis might not therefore be justified.

A volcanic environment for bedrock diagenesis at Meridiani Planum on Mars.

Exposed bedrocks at Meridiani Planum on Mars display chemical and mineralogical evidence suggesting interaction with liquid water. On the basis of morphological observations as well as high abundances of haematite and sulphate minerals, the rocks have been interpreted as sediments that were deposited in a shallow body of briny water with subsequent evaporation leaving behind the sulphate minerals. The iron-sulphur mineralization at Meridiani has also been inferred to be analogous to that produced during oxidative weathering of metal sulphide minerals, such as occurs at acid mine drainage sites. Neither of these interpretations, however, is consistent with the chemical composition of the rocks. Here we propose an alternative model for diagenesis of Meridiani bedrock that involves deposition of volcanic ash followed by reaction with condensed sulphur dioxide- and water-bearing vapours emitted from fumaroles. This scenario does not require prolonged interaction with a standing body of surface water and may have occurred at high temperatures. Consequently, the model invokes an environment considerably less favourable for biological activity on Mars than previously proposed interpretations.

Geomicrobiology in oceanography: microbe-mineral interactions at and below the seafloor.

Oceanography is inherently interdisciplinary and, since its inception, has included the study of microbe-mineral interactions. From early studies of manganese nodules, to the discovery of hydrothermal vents, it has been recognized that microorganisms are involved at various levels in the transformation of rocks and minerals at and below the seafloor. Recent studies include mineral weathering at low temperatures and microbe-mineral interactions in the subseafloor "deep biosphere". A common characteristic of seafloor and subseafloor geomicrobiological processes that distinguishes them from terrestrial or near-surface processes is that they occur in the dark, one or more steps removed from the sunlight that fuels the near-surface biosphere on Earth. This review focuses on geomicrobiological studies and energy flow in dark, deep-ocean and subseafloor rock habitats.

Hydrogen and bioenergetics in the Yellowstone geothermal ecosystem.

The geochemical energy budgets for high-temperature microbial ecosystems such as occur at Yellowstone National Park have been unclear. To address the relative contributions of different geochemistries to the energy demands of these ecosystems, we draw together three lines of inference. We studied the phylogenetic compositions of high-temperature (>70 degrees C) communities in Yellowstone hot springs with distinct chemistries, conducted parallel chemical analyses, and carried out thermodynamic modeling. Results of extensive molecular analyses, taken with previous results, show that most microbial biomass in these systems, as reflected by rRNA gene abundance, is comprised of organisms of the kinds that derive energy for primary productivity from the oxidation of molecular hydrogen, H2. The apparent dominance by H2-metabolizing organisms indicates that H2 is the main source of energy for primary production in the Yellowstone high-temperature ecosystem. Hydrogen concentrations in the hot springs were measured and found to range up to >300 nM, consistent with this hypothesis. Thermodynamic modeling with environmental concentrations of potential energy sources also is consistent with the proposed microaerophilic, hydrogen-based energy economy for this geothermal ecosystem, even in the presence of high concentrations of sulfide.