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NASA NTRS2002

Energy Requirements of Hydrogen-Utilizing Microbes: Boundary Condition for Subsurface Life

For planetary bodies with surface conditions that are too harsh to permit continuous occupation by life, the deep subsurface offers a potentially stable and habitable niche. For organisms occupying this niche, the spectrum of possible metabolisms must be limited to those which do not include sunlight as an energy source or oxygen as a chemical reagent - generally, low-energy anaerobic oxidation-reduction processes. The quantity of energy released in such processes is critical, because currently understood mechanisms of biological energy conservation indicate that energy is only 'useful' to an organism when it is available at a certain minimum level - the 'biological energy quantum'. The mere existence of a BEQ implies that a significant fraction of the chemical energy present in the environment cannot be exploited by life; similarly, the absolute magnitude of the BEQ must be a key variable in determining the potential viability and distribution of subsurface microbial communities. Laboratory culture studies suggest that organisms require an energy of about -20 kJ/mol to grow. However, we find that hydrogen-utilizing microorganisms in an energy-limited natural ecosystem are active with energy yields as low as -10 kJ/mol. A lower BEQ would mean a significantly expanded range of energetically viable subsurface habitat for life.

Hoehler, Tori M.↗

NASA NTRS1998

Sources of Hydrogen as Food for Deep Microbial Communities

To survive in deep subsurface environments autolithotrophic microbial communities require a sustainable food supply. One possible source is H2 which forms when H2O reacts with ferrous iron at rock surfaces or mineral grain boundaries to produce H2 plus ferric iron. The amount of H2 that can be supplied in this way, however, is relatively small and may not last for more than a few hundred or thousand years. A much larger reservoir of H2 exists in the rocks, inside mineral grains, arising from an as yet little-known redox conversion that affects OH- in nominally anhydrous minerals. These OH- represent small amounts of "water" that become incorporated during crystallization in H2O-laden environments. A corollary of the H2 formation from OH- is the formation of peroxy, an oxidized form of oxygen. While the peroxy become part of the mineral structure, the H2 molecules are diffusively mobile and can escape from within the mineral grains, entering the intergranular space. Assuming cautiously realistic number densities of OH- undergoing the in situ redox conversion to H2 plus peroxy, a 10 km deep rock column is expected to contain enough H2 to allow for a constant degassing rate of 50-100 nmole H2 per day per sq cm over 30 million years.

Freund, Friedemann↗

NASA NTRS2002

Hydrogen in rocks: an energy source for deep microbial communities

To survive in deep subsurface environments, lithotrophic microbial communities require a sustainable energy source such as hydrogen. Though H2 can be produced when water reacts with fresh mineral surfaces and oxidizes ferrous iron, this reaction is unreliable since it depends upon the exposure of fresh rock surfaces via the episodic opening of cracks and fissures. A more reliable and potentially more voluminous H2 source exists in nominally anhydrous minerals of igneous and metamorphic rocks. Our experimental results indicate that H2 molecules can be derived from small amounts of H2O dissolved in minerals in the form of hydroxyl, OH- or O3Si-OH, whenever such minerals crystallized in an H2O-laden environment. Two types of experiments were conducted. Single crystal fracture experiments indicated that hydroxyl pairs undergo an in situ redox conversion to H2 molecules plus peroxy links, O3Si/OO\SiO3. While the peroxy links become part of the mineral structure, the H2 molecules diffused out of the freshly fractured mineral surfaces. If such a mechanism occurred in natural settings, the entire rock column would become a volume source of H2. Crushing experiments to facilitate the outdiffusion of H2 were conducted with common crustal igneous rocks such as granite, andesite, and labradorite. At least 70 nmol of H2/g diffused out of coarsely crushed andesite, equivalent at standard pressure and temperature to 5,000 cm3 of H2/m3 of rock. In the water-saturated, biologically relevant upper portion of the rock column, the diffusion of H2 out of the minerals will be buffered by H2 saturation of the intergranular water film.

Hydrogen/analysis↗

NASA NTRS2000

Understanding Microbial Contributions to Planetary Atmosphere

Should our search of distant, extrasolar planetary atmospheres encounter evidence of life, that evidence will most likely be the gaseous products of microorganisms. Our biosphere was exclusively microbial for over 80 percent of its history and, even today, microbes strongly influence atmospheric composition. Life's greatest environmental impact arises from its capacity for harvesting energy and creating organic matter. Microorganisms catalyze the equilibration of C, S and transition metal species at temperatures where such reactions can be very slow in the absence of life. Sunlight has been harvested through photosynthesis to create enormous energy reservoirs that exist in the form of coexisting reservoirs of reduced, organic C and S stored in Earth's crust, and highly oxidized species (oxygen, sulfate and ferric iron) stored in the crust, oceans and atmosphere. Our civilization taps that storehouse of energy by burning fossil fuels. As astrobiologists, we identify the chemical consequences of distant biospheres as expressed in the atmospheres of their planets. Our approach must recognize that planets, biospheres and atmospheres evolve and change. For example, a tectonically more active early Earth hosted a thermophilic, non-photosynthetic biosphere and a mildly reducing, carbon dioxide-rich and oxygen-poor atmosphere. Microorganisms acquired energy by consuming hydrogen and sulfide and producing a broad array of reduced C and S gases, most notably, methane. Later, diverse types of bacterial photosynthesis developed that enhanced productivity but were incapable of splitting water to produce oxygen. Later, but still prior to 2.6 billion years ago, oxygenic photosynthesis developed. We can expect to encounter distant biospheres that represent various stages of evolution and that coexist with atmospheres ranging from mildly reducing to oxidizing compositions. Accordinaly, we must be prepared to interpret a broad range of atmospheric compositions, all containing signatures of life. Remarkably little is known about the composition of our own earlier atmosphere, particularly prior to the rise of oxygen levels some 2.0 to 2.2 billion years ago. Thus, field and laboratory observations and theoretical simulations should be conducted to examine the relationships between the structure and function of microbial ecosystems and their gaseous products. Ecosystems that are analogs of our ancient biosphere (e.g., based upon chemosynthesis or non-oxygenic photosynthesis, thermophilic and subsurface communities, etc.) should be included. Because key environmental parameters such as temperature and levels of hydrogen, carbon dioxide and oxygen varied during planetary evolution, their consequences for microbial ecosystems should be explored.

DesMarais, David J.↗

NASA NTRS2002

Carbonate Platform Development and Stromatolite Morphogenesis: Constraints on Environmental and Biological Evolution

Work this past year has focused on the globally significant events of faunal turnover, tectonic reorganization, and biogeochemical change that closely coincided with the Precambrian-Cambrian boundary in the Sultanate oilman. Higher temporal and chronostratigraphic resolution are required in order to answer this question. Stratigraphic sections must contain fossils, volcanic rocks, and abundant carbonates with little or no diagenetic overprint. The Ara Group of the South Oman Salt Basin presents such a succession - with carbonate rocks tightly enclosed in a protective envelope of impermeable halite, these rocks have likely never exchanged with younger fluids. Our work has had two thrusts. The first pertains to the geochemistry of the Athel Formation, a deep water deposit formed at the Precambrian-Cambrian boundary which contains unique records of ocean anoxia for that time interval. This unit is important because it will enable tighter focus on the links which existed between global biogeochemical events and episodes of faunal extinction and radiation. The second direction involves a comparison of terminal Proterozoic thrombolites between Oman (subsurface) and Namibia (outcrop). These thrombolites are important not only as significant deposits of ancient microbial communities, but because they formed the key substrate for growth of the oldest calcified metazoans - Cloudina and Namacalathus.

Grotzinger, John P.↗

NASA NTRS1994

Subsurface Intertidal Microbes: A Cryptic Source Of Organic Carbon For Beach Ecosystems

Some freshwater, marine or hotspring beaches have no visible source of primary production, yet beneath the surface is an interstitial photosynthetic microbial community. To assess the significance of this source of organic carbon, we measured in situ carbon fixation rates in an intertidal marine beach through a diurnal cycle. Gross fixation for a transect (99 x 1 m) perpendicular to the shore was approx. 4041 mg C fixed/ day, or approx. 41 mg C fixed/ sq m day. In contrast, an adjacent well-established cyanobacterial (Lyngbya) mat was approx. 12 x as productive (approx. 490 mg C fixed/sq m day). Thus, subsurface sand mats may be an overlooked, yet important, endogenous source of organic carbon for intertidal ecosystems, as well as a sink in the global carbon cycle.

Rothschild, Lynn J.↗

NASA NTRS1992

On the possibility of chemosynthetic ecosystems in subsurface habitats on Mars

Recent discoveries of nonphotosynthetic microbial ecosystems on earth have prompted the present reexamination of the prospects for microbial life on Mars, where well-protected subsurface niches associated with hydrothermal activity could have furnished a refuge after surface conditions became inhospitable. It is noted that extensive geological features attest to widespread ground ice-volcanism interactions. Attention is given to the possibility of anaerobic systems employing CO2 as the primary source of carbon, and liquid water furnished by melted subsurface permafrost. Gases from deep volcanic activity could effect reduction, thereby establishing a chemolithoautotrophic basis for a methanogenic or acetogenic and sulfur-based ecology microbial community.

Boston, Penelope J.↗

NASA NTRS1991

Subsurface microbial habitats on Mars

We developed scenarios for shallow and deep subsurface cryptic niches for microbial life on Mars. Such habitats could have considerably prolonged the persistence of life on Mars as surface conditions became increasingly inhospitable. The scenarios rely on geothermal hot spots existing below the near or deep subsurface of Mars. Recent advances in the comparatively new field of deep subsurface microbiology have revealed previously unsuspected rich aerobic and anaerobic microbal communities far below the surface of the Earth. Such habitats, protected from the grim surface conditions on Mars, could receive warmth from below and maintain water in its liquid state. In addition, geothermally or volcanically reduced gases percolating from below through a microbiologically active zone could provide the reducing power needed for a closed or semi-closed microbial ecosystem to thrive.

Boston, P. J.↗

NASA NTRS1998

Mineralization of Bacteria in Terrestrial Basaltic Rocks: Comparison With Possible Biogenic Features in Martian Meteorite Allan Hills 84001

The identification of biogenic features altered by diagenesis or mineralization is important in determining whether specific features in terrestrial rocks and in meteorites may have a biogenic origin. Unfortunately, few studies have addressed the formation of biogenic features in igneous rocks, which may be important to these phenomena, including the controversy over possible biogenic features in basaltic martian meteorite ALH84001. To explore the presence of biogenic features in igneous rocks, we examined microcosms growing in basaltic small-scale experimental growth chambers or microcosms. Microbial communities were harvested from aquifers of the Columbia River Basalt (CRB) group and grown in a microcosm containing unweathered basalt chips and groundwater (technique described in. These microcosms simulated natural growth conditions in the deep subsurface of the CRB, which should be a good terrestrial analog for any putative martian subsurface ecosystem that may have once included ALH84001. Here we present new size measurements and photomicrographs comparing the putative martian fossils to biogenic material in the CRB microcosms. The range of size and shapes of the biogenic features on the CRB microcosm chips overlaps with and is similar to those on ALH84001 chips. Although this present work does not provide evidence for the biogenicity of ALH84001 features, we believe that, based on criteria of size, shape, and general morphology, a biogenic interpretation for the ALH84001 features remains plausible.

Thomas-Keprta, K. L.↗

NASA NTRS2002

Life Beneath Glacial Ice - Earth(!) Mars(?) Europa(?)

We are investigating a set of cold springs that deposit sulfur and carbonate minerals on the surface of a Canadian arctic glacier. The spring waters and mineral deposits contain microorganisms, as well as clear evidence that biological processes mediate subglacial chemistry, mineralogy, and isotope fractionation . The formation of native sulphur and associated deposits are related to bacterially mediated reduction and oxidation of sulphur below the glacier. A non-volcanic, topography driven geothermal system, harboring a microbiological community, operates in an extremely cold environment and discharges through solid ice. Microbial life can thus exist in isolated geothermal refuges despite long-term subfreezing surface conditions. Earth history includes several periods of essentially total glaciation. lee in the near subsurface of Mars may have discharged liquid water in the recent past Cracks in the ice crust of Europa have apparently allowed the release of water to the surface. Chemolithotrophic bacteria, such as those in the Canadian springs, could have survived beneath the ice of "Snowball Earth", and life forms with similar characteristics might exist beneath the ice of Mars or Europa. Discharges of water from such refuges may have brought to the surface living microbes, as well as longlasting chemical, mineralogical, and isotopic indications of subsurface life.

Allen, Carlton C.↗

NASA NTRS2013

Does Aspartic Acid Racemization Constrain the Depth Limit of the Subsurface Biosphere?

Previous studies of the subsurface biosphere have deduced average cellular doubling times of hundreds to thousands of years based upon geochemical models. We have directly constrained the in situ average cellular protein turnover or doubling times for metabolically active micro-organisms based on cellular amino acid abundances, D/L values of cellular aspartic acid, and the in vivo aspartic acid racemization rate. Application of this method to planktonic microbial communities collected from deep fractures in South Africa yielded maximum cellular amino acid turnover times of approximately 89 years for 1 km depth and 27 C and 1-2 years for 3 km depth and 54 C. The latter turnover times are much shorter than previously estimated cellular turnover times based upon geochemical arguments. The aspartic acid racemization rate at higher temperatures yields cellular protein doubling times that are consistent with the survival times of hyperthermophilic strains and predicts that at temperatures of 85 C, cells must replace proteins every couple of days to maintain enzymatic activity. Such a high maintenance requirement may be the principal limit on the abundance of living micro-organisms in the deep, hot subsurface biosphere, as well as a potential limit on their activity. The measurement of the D/L of aspartic acid in biological samples is a potentially powerful tool for deep, fractured continental and oceanic crustal settings where geochemical models of carbon turnover times are poorly constrained. Experimental observations on the racemization rates of aspartic acid in living thermophiles and hyperthermophiles could test this hypothesis. The development of corrections for cell wall peptides and spores will be required, however, to improve the accuracy of these estimates for environmental samples.

cellular↗

NASA NTRS1993

Microscale characterization of dissolved organic matter production and uptake in marine microbial mat communities

Intertidal marine microbial mats exhibited biologically mediated uptake of low molecular weight dissolved organic matter (DOM), including D-glucose, acetate, and an L-amino acid mixture at trace concentrations. Uptake of all compounds occurred in darkness, but was frequently enhanced under natural illumination. The photosystem 2 inhibitor, 3-(3,4-dichlorophenyl)-1,1-dimethyl urea (DCMU) generally failed to inhibit light-stimulated DOM uptake. Occasionally, light plus DCMU-amended treatments led to uptake rates higher than light-incubated samples, possibly due to phototrophic bacteria present in subsurface anoxic layers. Uptake was similar with either 3H- or 14C-labeled substrates, indicating that recycling of labeled CO2 via photosynthetic fixation was not interfering with measurements of light-stimulated DOM uptake. Microautoradiographs showed a variety of pigmented and nonpigmented bacteria and, to a lesser extent, cyanobacteria and eucaryotic microalgae involved in light-mediated DOM uptake. Light-stimulated DOM uptake was often observed in bacteria associated with sheaths and mucilage surrounding filamentous cyanobacteria, revealing a close association of organisms taking up DOM with photoautotrophic members of the mat community. The capacity for dark- and light-mediated heterotrophy, coupled to efficient retention of fixed carbon in the mat community, may help optimize net production and accretion of mats, even in oligotrophic waters.

NASA Discipline Exobiology↗

NASA NTRS2004

Searching for an Acidic Aquifer in the Rio Tinto Basin: First Geobiology Results of MARTE Project

Among the conceivable modern habitats to be explored for searching life on Mars are those potentially developed underground. Subsurface habitats are currently environments that, under certain physicochemical circumstances, have high thermal and hydrochemical stability [1, 2]. In planets like Mars lacking an atmospheric shield, such systems are obviously protected against radiation, which strongly alters the structure of biological macromolecules. Low porosity but fractured aquifers currently emplaced inside ancient volcano/sedimentary and hydrothermal systems act as excellent habitats [3] due to its thermal and geochemical properties. In these aquifers the temperature is controlled by a thermal balance between conduction and advection processes, which are driven by the rock composition, geological structure, water turnover of aquifers and heat generation from geothermal processes or chemical reactions [4]. Moreover, microbial communities based on chemolithotrophy can obtain energy by the oxidation of metallic ores that are currently associated to these environments. Such a community core may sustain a trophic web composed of non-autotrophic forms like heterotrophic bacteria, fungi and protozoa.

Fernandez-Remolar, D. C.↗

NASA NTRS1998

Deep Basalt Aquifers in Orcus Patera, Elysium Basin Mars: Perspectives for Exobiology Exploration

Direct indicators of shorelines, spillways, and terraces allowed to determine the extent of the Elysium Paleolake between the contour-lines 1000 and 500 m below the Martian datum. The Elysium Paleolake is bordered north by Orcus Patera (14N/181W), which lies west of the Tartarus Montes and Tartarus Colles. The Orcus Patera displays an ellipse-shaped collapsed caldera of 360-km long and 100-km wide. Viking topographic data show that the bottom of the caldera is located at 2500 below the Martian datum, and surrounded by a steep-walled ram art which crest is located at about 0 m elevation. Considering the localization of Orcus Patera in the Elysium paleolake, its altimetry, and the magmatic origin of this caldera, we propose the existence of a paleolake in Orcus Patera generated (a) by juvenile water from magma during the Noachian period, and (b) by intermittent influx of the Elysium Basin from Hesperian to Amazonian. Results are encouraging to consider this site as a potential high-energy source environment for microbial communities. are circumscribed by a 50-km wide lava field mapped as Noachian material. The structure of Orcus Patera represents the record of material erupted from a magmatic reservoir. The caldera is enclosed by steep inner walls (25% measured from topographic data), values which could be in agreement with the presence of a deep magmatic reservoir, as suggested by the typology of Crumpler et.al. The depth of the caldera might be due to the collapse of the magma reservoir, and the release of gases accompanying the magma thermal evolution. Origins of water for the paleolake(s): The water that generated a paleolake in Orcus Patera may have come from two origins: (1) Juvenile water: Plescia and Crips estimated a magma H20 content by weight between 0.5% and 1.5% using for the first value a comparison with terrestrial basalt, and for the second values from a Martian meteorite. The amount of H20 can be estimated by the volume of erupted lava, and the lava content of the caldera. In this study, we adopt a water content of 1%. The total volume of magma that has been contained in the caldera, and the volume of lava contained in the observed lava field is about 110 x 10(exp 6) cubic km, that gives a total volume of 1.10 x 10(exp 6) cubic km of water. The juvenile water expelled by the overpressure within the magma chamber charged with desolved water-vapor may have moved into the crust. The decrease in overburden pressure led to bubble formation. The ascent of these bubbles generated a pressurization of the magma, which was sufficient to fracture the overlaying magma layer, (2) Water from Elysium paleolake. During the Amazonian, the rise of the Elysium paleolake level generated an overspilling that supplied the caldera with water. The southern portion of the crest shows a deep gap 12-km wide at -1500 m elevation, locating the gap between 500 to 1000 in below the assumed water of Elysium paleolake, thus facilitating the influx of Elysium paleolake water into Orcus Patera. Bathymetric calculations give a floor area of 25,500 sq km at -2000 m elevation, and a water volume of 42,000 cubic km, with a lake-level at -1500 m. A substantial amount of water may have percolated through the fractured lava, and part of the volume may have overspilled the northern crest of Orcus Patera to debouch in the Tartarus Montes region. We envision the formation of a subsurface aqueous environment in basaltic rocks at the contact of the two water-source origins, possibly the percolating surface lake water, and more likely the juvenile water. Similarly to terrestrial calderas, Orcus Patera might be surrounded by ring-fractures caused by the collapse of the magma chamber that followed the release of gases. These ring-fractures may have been covered later by sedimentation in the caldera (lacustrine, aeolian, and volcanic), and by mass wasting. The detumescence of the magma in the caldera, and the vesiculation of the juvenile water may have operated simultaneously. Comparatively to terrestrial melts, Martian iron-rich melts are denser. This greater density implies greater effusion rates (eight-times terrestrial values), and larger fissuration widths (two-times terrestrial ones). With increasing vesiculation of magma, the bubbles interact with one-another because there are of similar pressure. They make a magma froth at the contact with the caldera surface, and on the walls of the fractures. In the saturated magma, froth, where the volume ratio of gases-to-liquid is about 4:1, the bubbles form a huge surface area of interconnected spaces. Bubbles near the caldera surface disrupt the magma, and fragmentation takes place, which moves downward through the magma column. On Earth, the bubbles are likely to grow between 1 and 50 mm in diameter due to the difference between the magma surface tension, and the bubble supersaturation pressure. The Martian low-pressure at surface level is likely to accelerate the expansion of the bubbles, and increase their final diameter and number, creating more voids in the magma. The strong magma froth with enclosed juvenile water bubbles interconnected with exsolved gas bubbles constitute a potential geothermal environment for geochemical energy production from basalt and water that does not require excessive temperatures. This process can start at +20C. Similar types of environments have been shown on Earth as potential energy sources for microbial metabolism, and could have provided deep aqueous basaltic niches for possible Martian microorganisms, even geologically recently. During the Amazonian, combination of volcanism and water activity still existed on Mars. Moreover, this type of potential niches open ways for investigation of possible oases of extinct or extant life, not only on paleolakes, and surface hydrothermalism spring areas, but also all large systems of fossae, which combine hydrologic and volcanic activities, and which provide an energy source, and an underground shelter to prevent surface UV bombardment. Additional information contained in the original.

Grin, E. A.↗

NASA NTRS2002

Distinguishing Indigenous from Contaminating Microorganisms in Rock Samples from a Deep Au Mine in South Africa

The concentration and distribution of microbial biomass within deep subsurface rock strata is not well known To date, most analyses are from water samples and a few cores. Hand samples, block samples and cores from an actively mined Carbon Leader ore zone at 3.2 kilometers depth were collected for microbial analyses. The Carbon Leader was comprised of quartz, S-bearing aromatic hydrocarbons, Fe(III) oxyhydroxides, sulfides, uraninite, Au and minor amounts of sulfate. The porosity of the ore was 1% and the maximum pore throat diameter was less than 0.1 microns; whereas, the porosity of the adjacent quartzite was .02 to .9% with a maximum pore throat diameter of 0.9 microns. Rhodamine dye, fluorescent microspheres, microbial enrichments, autoradiography, phospholipid fatty acid (PLEA) and 16S rDNA analyses were performed on these rock samples and the mining water. The date indicate that the levels of solute contamination less than 0.01% for pared rock samples. Despite this low level of contamination, PLEA, microbial enrichment, DNA and tracer analyses and calculations indicate that most of the viable microorganisms in the Carbon Leader represent gram negative aerobic heterotrophs and ammonia oxidizers that are phylogenetically identical or closely related to service water microorganisms. These microbial contaminants probably infiltrated the low permeability rock through mining-induced microfractures. Geochemical data also detected drilling water in a fault zone approx. 1 meter behind the rock face encountered during coring. The mining induced macrofractures that are common at these great depths act as pathways for the drilling water borne microorganisms into the lower temperature zone that extends several meters into rock strata from the rock face. Combined PLEA and T- RFLP analyses of the service water and Carbon Leader samples indicate that the concentration of indigenous microorganisms was less than 10(exp 2) cells/gram. Such a low concentrations result from the submicron pore throat diameters. PLFA. SO4-35 autoradiography and tracer analyses indicate that the bounding quartzite contains thermophilic sulfate reducing bacteria at 10(exp 3) cells/gram that are not attributable to drilling water contamination. The microorganisms may be surviving on sulfate generated by oxidation of sulfide by radiolytic reactions resulting from the high U concentration in the ore zone. The presence of up to 8,000 ppm of Fe(III) oxyhydroxides in the host rock will also act to recycle sulfide generated by the sulfate reducing bacteria into sulfate. The activity of these sulfate-reducing bacteria may be enhanced by mining induced fracturing which can propagate up to 40 meters into virgin rock where the temperatures are ca. 50 C, and decrepitate of sulfate rich fluid inclusions. In ultra deep mines, judicious application of tracers and multiple microbial characterization techniques can distinguish microbial contamination caused by the near field fracturing and drilling water migration from the indigenous microbial communities in rock strata. The importance of far field fracturing on indigenous microbial communities, however, remains unknown.

Onstott, T. C.↗