Some ecological mechanisms to generate habitability in planetary subsurface areas by chemolithotrophic communities: the Río Tinto subsurface ecosystem as a model system

Chemolithotrophic communities that colonize subsurface habitats have great relevance for the astrobiological exploration of our Solar System. We hypothesize that the chemical and thermal stabilization of an environment through microbial activity could make a given planetary region habitable. The MARTE project ground-truth drilling campaigns that sampled cryptic subsurface microbial communities in the basement of the Río Tinto headwaters have shown that acidic surficial habitats are the result of the microbial oxidation of pyritic ores. The oxidation process is exothermic and releases heat under both aerobic and anaerobic conditions. These microbial communities can maintain the subsurface habitat temperature through storage heat if the subsurface temperature does not exceed their maximum growth temperature. In the acidic solutions of the Río Tinto, ferric iron acts as an effective buffer for controlling water pH. Under anaerobic conditions, ferric iron is the oxidant used by microbes to decompose pyrite through the production of sulfate, ferrous iron, and protons. The integration between the physical and chemical processes mediated by microorganisms with those driven by the local geology and hydrology have led us to hypothesize that thermal and chemical regulation mechanisms exist in this environment and that these homeostatic mechanisms could play an essential role in creating habitable areas for other types of microorganisms. Therefore, searching for the physicochemical expression of extinct and extant homeostatic mechanisms through physical and chemical anomalies in the Mars crust (i.e., local thermal gradient or high concentration of unusual products such as ferric sulfates precipitated out from acidic solutions produced by hypothetical microbial communities) could be a first step in the search for biological traces of a putative extant or extinct Mars biosphere.     

Tírez lake as a terrestrial analog of Europa

Tírez Lake (La Mancha, central Spain) is proposed as a terrestrial analogue of Europa's ocean. The proposal is based on the comparison of the hydrogeochemistry of Tírez Lake with the geochemical features of the alteration mineralogy of meteoritic precursors and with Galileo's Near Infrared Mapping Spectrometer data on Europa's surface. To validate the astrobiological potential of Tírez Lake as an analog of Europa, different hydrogeochemical, mineral, and microbial analyses were performed. Experimental and theoretical modeling helped to understand the crystallization pathways that may occur in Europa's crust. Calculations about the oxidation state of the hypothetical Europan ocean were estimated to support the sulfate-rich neutral liquid model as the origin of Europa's observed hydrated minerals and to facilitate their comparison with Tírez's hydrogeochemistry. Hydrogeochemical and mineralogical analyses showed that Tírez waters corresponded to Mg-Na-SO(4)-Cl brines with epsomite, hexahydrite, and halite as end members. A preliminary microbial ecology characterization identified two different microbial domains: a photosynthetically sustained community represented by planktonic/benthonic forms and microbial mat communities, and a subsurficial anaerobic realm in which chemolithotrophy predominates. Fluorescence in situ hybridization has been used to characterize the prokaryotic diversity of the system. The subsurficial community seemed to be dominated by sulfate-reducing bacteria and methanogens. Frozen Tírez brines were analyzed by Fourier-transform infrared techniques providing spectra similar to those reported previously using pure components and to the Galileo spectral data. Calorimetric measurements of Tírez brines showed pathways and phase metastability for magnesium sulfate and sodium chloride crystallization that may aid in understanding the processes involved in the formation of Europa's icy crust. The use of fluorescence hybridization techniques for microbial detection and characterization in hypersaline environments makes this methodology strongly advisable for future Europa astrobiological missions.     

Magnetism, iron minerals, and life on Mars

A short critical review is provided on two questions linking magnetism and possible early life on Mars: (1) Did Mars have an Earth-like internal magnetic field, and, if so, during which period and was it a requisite for life? (2) Is there a connection between iron minerals in the martian regolith and life? We also discuss the possible astrobiological implications of magnetic measurements at the surface of Mars using two proposed instruments. A magnetic remanence device based on magnetic field measurements can be used to identify Noachian age rocks and lightning impacts. A contact magnetic susceptibility probe can be used to investigate weathering rinds on martian rocks and identify meteorites among the small regolith rocks. Both materials are considered possible specific niches for microorganisms and, thus, potential astrobiological targets. Experimental results on analogues are presented to support the suitability of such in situ measurements.     

Application of hyperspectral infrared analysis of hydrothermal alteration on Earth and Mars

An integrated analysis of both airborne and field short-wave infrared hyperspectral measurements was used in conjunction with conventional field mapping techniques to map hydrothermal alteration in the central portion of the Mount Painter Inlier in the Flinders Ranges, South Australia. The airborne hyperspectral data show the spatial distribution of spectrally distinct minerals occurring as primary minerals and as weathering and alteration products. Field spectral measurements, taken with a portable infrared mineral analyzer spectrometer and supported by thin-section analyses, were used to verify the mineral maps and enhance the level of information obtainable from the airborne data. Hydrothermal alteration zones were identified and mapped separately from the background weathering signals. A main zone of alteration, coinciding with the Paralana Fault zone, was recognized, and found to contain kaolinite, muscovite, biotite, and K-feldspar. A small spectral variation associated with a ring-like feature around Mount Painter was tentatively determined to be halloysite and interpreted to represent a separate hydrothermal fluid and fluid source, and probably a separate system. The older parts of the alteration system are tentatively dated as Permo-Carboniferous. The remote sensing of alteration at Mount Painter confirms that hyperspectral imaging techniques can produce accurate mineralogical maps with significant details that can be used to identify and map hydrothermal activity. Application of hyperspectral surveys such as that conducted at Mount Painter would be likely to provide similar detail about putative hydrothermal deposits on Mars.     

Porphyrin as an ideal biomarker in the search for extraterrestrial life

A key issue in astrobiological research is identifying target molecules that are unambiguously biological in origin and can be easily detected and recognized. We suggest porphyrin derivatives as an ideal target, because these chromophores are global in distribution and found in virtually all living organisms on Earth, including microorganisms that may approximate the early evolution of life on Earth. We discuss the inherent qualities that make porphyrin ideally suited for astrobiological research and discuss methods for detecting porphyrin molecules in terrestrial sedimentary environments. We present preliminary data to support the use of ToFSIMS as a powerful technique in the identification of porphyrins.     

Biosignature detection at an Arctic analog to Europa

The compelling evidence for an ocean beneath the ice shell of Europa makes it a high priority for astrobiological investigations. Future missions to the icy surface of this moon will query the plausibly sulfur-rich materials for potential indications of the presence of life carried to the surface by mobile ice or partial melt. However, the potential for generation and preservation of biosignatures under cold, sulfur-rich conditions has not previously been investigated, as there have not been suitable environments on Earth to study. Here, we describe the characterization of a range of biosignatures within potentially analogous sulfur deposits from the surface of an Arctic glacier at Borup Fiord Pass to evaluate whether evidence for microbial activities is produced and preserved within these deposits. Optical and electron microscopy revealed microorganisms and extracellular materials. Elemental sulfur (S?), the dominant mineralogy within field samples, is present as rhombic and needle-shaped mineral grains and spherical mineral aggregates, commonly observed in association with extracellular polymeric substances. Orthorhombic α-sulfur represents the stable form of S?, whereas the monoclinic (needle-shaped) γ-sulfur form rosickyite is metastable and has previously been associated with sulfide-oxidizing microbial communities. Scanning transmission electron microscopy showed mineral deposition on cellular and extracellular materials in the form of submicron-sized, needle-shaped crystals. X-ray diffraction measurements supply supporting evidence for the presence of a minor component of rosickyite. Infrared spectroscopy revealed parts-per-million level organics in the Borup sulfur deposits and organic functional groups diagnostic of biomolecules such as proteins and fatty acids. Organic components are below the detection limit for Raman spectra, which were dominated by sulfur peaks. These combined investigations indicate that sulfur mineral deposits may contain identifiable biosignatures that can be stabilized and preserved under low-temperature conditions. Borup Fiord Pass represents a useful testing ground for instruments and techniques relevant to future astrobiological exploration at Europa.     

Rock surfaces as life indicators: new ways to demonstrate life and traces of former life

Life and its former traces can only be detected from space when they are abundant and exposed to the planetary atmosphere at the moment of investigation by orbiters. Exposed rock surfaces present a multifractal labyrinth of niches for microbial life. Based upon our studies of highly stress-resistant microcolonial fungi of stone monument and desert rock surfaces, we propose that microbial biofilms that develop and become preserved on rock surfaces can be identified remotely by the following characteristics: (1) the existence of spectroscopically identifiable compounds that display unique adsorption, diffraction, and reflection patterns characteristic of biogenerated organic compounds (e.g., chlorophylls, carotenes, melanins, and possibly mycosporines), (2) demonstrably biogenic geomorphological features (e.g., biopitting, biochipping, and bioexfoliation), and (3) biominerals produced in association with biofilms that occupy rock surfaces (e.g., oxalates, forsterite, and special types of carbonates, sulfides, and silicates). Such traces or biosignatures of former life could provide macroscopically visible morphotypes and chemically identifiable products uniquely indicative of life.     

Recognition of fossil prokaryotes in Cretaceous methane seep carbonates: relevance to astrobiology

Recovery of prokaryotic body fossils from methane seep carbonates such as those of the Cretaceous Tepee Buttes of Colorado serves as a model for sampling in future astrobiological missions. The fossils, found primarily at the interface between paragenetic fabrics, suggest a sharp physicochemical gradient. Evidence of these microbial fossils occurs at a variety of scales. In the field, microbialite is found as meter-scale thrombolitic zones and centimeterscale stromatolitic crusts lining voids inferred to be the sites of ancient methane seepage. Petrographic fabrics suggestive of microbialite include indistinct peloids (0.1-1 mm in diameter) and crusts of authigenic micrite. Primary evidence obtained from scanning electron microscopy coupled with energy-dispersive x-ray spectroscopy analysis comprises pinnate bacteria (0.3 microm in diameter and 1-1.5 microm long), sheaths (2-4 microm in diameter), coccoids (0.5-1 microm in diameter, up to 40 per cluster), and the presence of framboidal pyrite (6-8 microm in diameter). These results are in agreement with studies of other ancient and modern seeps and suggest a morphological conservatism of microbial form that can be incorporated into studies of extraterrestrial environments where it is presumed that reduced gases drive the metabolic activity of prokaryote-like organisms. Target areas that could serve as conduits for reduced gas seeps include tectonic or impact-driven faulting, zones of cryosphere melting, or other disruptions in crustal coherence. Ancient seeps, preserved as localized anomalous evaporite deposits in the sedimentary cover, could be detected by remote sensing.     

Fluorescence microscopy as a tool for in situ life detection

The identification of extant and, in some cases, extinct bacterial life is most convincingly and efficiently performed with modern high-resolution microscopy. Epifluorescence microscopy of microbial autofluorescence or in conjunction with fluorescent dyes is among the most useful of these techniques. We explored fluorescent labeling and imaging of bacteria in rock and soil in the context of in situ life detection for planetary exploration. The goals were two-fold: to target non-Earth-centric biosignatures with the greatest possible sensitivity and to develop labeling procedures amenable to robotic implementation with technologies that are currently space qualified. A wide panel of commercially available dyes that target specific biosignature molecules was screened, and those with desirable properties (i.e., minimal binding to minerals, strong autofluorescence contrast, no need for wash steps) were identified. We also explored the potential of semiconductor quantum dots (QDs) as bacterial and space probes. A specific instrument for space implementation is suggested and discussed.     

Submicron magnetite grains and carbon compounds in Martian meteorite ALH84001: inorganic, abiotic formation by shock and thermal metamorphism

Purported biogenic features of the ALH84001 Martian meteorite (the carbonate globules, their submicron magnetite grains, and organic matter) have reasonable inorganic origins, and a comprehensive hypothesis is offered here. The carbonate globules were deposited from hydrothermal water, without biological mediation. Thereafter, ALH84001 was affected by an impact shock event, which raised its temperature nearly instantaneously to 500-700K, and induced iron-rich carbonate in the globules to decompose to magnetite and other minerals. The rapidity of the temperature increase caused magnetite grains to nucleate in abundance; hence individual crystals were very small. Nucleation and growth of magnetite crystals were fastest along edges and faces of the precursor carbonate grains, forcing the magnetite grains to be platy or elongated, including the "truncated hexa-octahedra" shape. ALH84001 had formed at some depth within Mars where the lithostatic pressure was significantly above that of Mars' surface. Also, because the rock was at depth, the impact heat dissipated slowly. During this interval, magnetite crystals approached chemical equilibria with surrounding minerals and gas. Their composition, nearly pure Fe(3)O(4), reflects those of equilibria; elements that substitute into magnetite are either absent from iron-rich carbonate (e.g., Ti, Al, Cr), or partitioned into other minerals during magnetite formation (Mg, Mn). Many microstructural imperfections in the magnetite grains would have annealed out as the rock cooled. In this post-shock thermal regime, carbon-bearing gas from the decomposition of iron carbonates reacted with water in the rock (or from its surroundings) to produce organic matter via Fischer-Tropschlike reactions. Formation of such organic compounds like polycyclic aromatic hydrocarbons would have been catalyzed by the magnetite (formation of graphite, the thermochemically stable phase, would be kinetically hindered).     

Serpentinization and its implications for life on the early Earth and Mars

Ophiolites, sections of ocean crust tectonically displaced onto land, offer significant potential to support chemolithoautotrophic life through the provision of energy and reducing power during aqueous alteration of their highly reduced mineralogies. There is substantial chemical disequilibrium between the primary olivine and pyroxene mineralogy of these ophiolites and the fluids circulating through them. This disequilibrium represents a potential source of chemical energy that could sustain life. Moreover, E (h)-pH conditions resulting from rock- water interactions in ultrabasic rocks are conducive to important abiotic processes antecedent to the origin of life. Serpentinization--the reaction of olivine- and pyroxene-rich rocks with water--produces magnetite, hydroxide, and serpentine minerals, and liberates molecular hydrogen, a source of energy and electrons that can be readily utilized by a broad array of chemosynthetic organisms. These systems are viewed as important analogs for potential early ecosystems on both Earth and Mars, where highly reducing mineralogy was likely widespread in an undifferentiated crust. Secondary phases precipitated during serpentinization have the capability to preserve organic or mineral biosignatures. We describe the petrology and mineral chemistry of an ophiolite-hosted cold spring in northern California and propose criteria to aid in the identification of serpentinizing terranes on Mars that have the potential to harbor chemosynthetic life.     

Location and sampling of aqueous and hydrothermal deposits in martian impact craters

Do large craters on Mars represent sites that contain aqueous and hydrothermal deposits that provide clues to astrobiological processes? Are these materials available for sampling in large craters? Several lines of evidence strongly support the exploration of large impact craters to study deposits important for astrobiology. The great depth of impact craters, up to several kilometers relative to the surrounding terrain, can allow the breaching of local aquifers, providing a source of water for lakes and hydrothermal systems. Craters can also be filled with water from outflow channels and valley networks to form large lakes with accompanying sedimentation. Impact melt and uplifted basement heat sources in craters > 50 km in diameter should be sufficient to drive substantial hydrothermal activity and keep crater lakes from freezing for thousands of years, even under cold climatic conditions. Fluid flow in hydrothermal systems is focused at the edges of large planar impact melt sheets, suggesting that the edge of the melt sheets will have experienced substantial hydrothermal alteration and mineral deposition. Hydrothermal deposits, fine-grained lacustrine sediments, and playa evaporite deposits may preserve evidence for biogeochemical processes that occurred in the aquifers and craters. Therefore, large craters may represent giant Petri dishes for culturing preexisting life on Mars and promoting biogeochemical processes. Landing sites must be identified in craters where access to the buried lacustrine sediments and impact melt deposits is provided by processes such as erosion from outflow channels, faulting, aeolian erosion, or excavation by later superimposed cratering events. Very recent gully formation and small impacts within craters may allow surface sampling of organic materials exposed only recently to the harsh oxidizing surface environment.     

A hydrothermal system associated with the Siljan impact structure, Sweden--implications for the search for fossil life on Mars

The Siljan ring structure (368 +/- 1.1 Ma) is the largest known impact structure in Europe. It isa 65-km-wide, eroded, complex impact structure, displaying several structural units, including a central uplifted region surrounded by a ring-shaped depression. Associated with the impact crater are traces of a post-impact hydrothermal system indicated by precipitated and altered hydrothermal mineral assemblages. Precipitated hydrothermal minerals include quartz veins and breccia fillings associated with granitic rocks at the outer margin of the central uplift, and calcite, fluorite, galena, and sphalerite veins associated with Paleozoic carbonate rocks located outside the central uplift. Two-phase water/gas and oil/gas inclusions in calcite and fluorite display homogenization temperatures between 75 degrees C and 137 degrees C. With an estimated erosional unloading of approximately 1 km, the formation temperatures were probably not more than 10-15 degrees C higher. Fluid inclusion ice-melting temperatures indicate a very low salt content, reducing the probability that the mineralization was precipitated during the Caledonian Orogeny. Our findings suggest that large impacts induce low-temperature hydrothermal systems that may be habitats for thermophilic organisms. Large impact structures on Mars may therefore be suitable targets in the search for fossil thermophilic organisms.     

Humans to Mars: a feasibility and cost-benefit analysis

Mars is a compelling astrobiological target, and a human mission would provide an opportunity to collect immense amounts of scientific data. Exploration alone, however, cannot justify the increased risk. Instead, three factors drive a human mission: economics, education, and exploration. A human mission has a unique potential to inspire the next generation of young people to enter critically needed science and engineering disciplines. A mission is economically feasible, and the research and development program put in place for a human mission would propel growth in related high-technology industries. The main hurdles are human physiological responses to 1–2 years of radiation and microgravity exposure. However, enabling technologies are sufficiently mature in these areas that they can be developed within a few decade timescale. Hence, the decision of whether or not to undertake a human mission to Mars is a political decision, and thus, educational and economic benefits are the crucial factors.     

Genesis and preservation of a uranium-rich paleozoic epithermal system with a surface expression (Northern Flinders Ranges, South Australia): radiogenic heat driving regional hydrothermal circulation over geological timescales

The surface expressions of hydrothermal systems are prime targets for astrobiological exploration, and fossil systems on Earth provide an analogue to guide this endeavor. The Paleozoic Mt. Gee-Mt. Painter system (MGPS) in the Northern Flinders Ranges of South Australia is exceptionally well preserved and displays both a subsurface quartz sinter (boiling horizon) and remnants of aerial sinter pools that lie in near-original position. The energy source for the MGPS is not related to volcanism but to radiogenic heat produced by U-Th-K-rich host rocks. This radiogenic heat source drove hydrothermal circulation over a long period of time (hundreds of millions of years, from Permian to present), with peaks in hydrothermal activity during periods of uplift and high water supply. This process is reflected by ongoing hot spring activity along a nearby fault. The exceptional preservation of the MGPS resulted from the lack of proximal volcanism, coupled with tectonics driven by an oscillating far-field stress that resulted in episodic basement uplift. Hydrothermal activity caused the remobilization of U and rare earth elements (REE) in host rocks into (sub)economic concentrations. Radiogenic-heat-driven systems are attractive analogues for environments that can sustain life over geological times; the MGPS preserves evidence of episodic fluid flow for the past ～300 million years. During periods of reduced hydrothermal activity (e.g., limited water supply, quiet tectonics), radiolytic H(2) production has the potential to support an ecosystem indefinitely. Remote exploration for deposits similar to those at the MGPS systems can be achieved by combining hyperspectral and gamma-ray spectroscopy.     

Entrapment of bacteria in fluid inclusions in laboratory-grown halite

Cells of the bacterium Pseudomonas aeruginosa, which were genetically modified to produce green fluorescent protein, were entrapped in fluid inclusions in laboratory-grown halite. The bacteria were used to inoculate NaCl-saturated aqueous solutions, which were allowed to evaporate and precipitate halite. The number, size, and distribution of fluid inclusions were highly variable, but did not appear to be affected by the presence of the bacteria. Many of the inclusions in crystals from inoculated solutions contained cells in populations ranging from two to 20. Microbial attachment to crystal surfaces was neither evident nor necessary for entrapment. Cells occurred exclusively within fluid inclusions and were not present in the crystal matrix. In both the inclusions and the hypersaline solution, the cells fluoresced and twitched, which indicates that the bacteria might have remained viable after entrapment. The fluorescence continued up to 13 months after entrapment, which indicates that little degradation of the bacteria occurred over that time interval. The entrapment, fluorescence, and preservation of cells were independent of the volume of hypersaline solution used or whether the solutions were completely evaporated prior to crystal extraction. The results of this study have a wide range of implications for the long-term survival of microorganisms in fluid inclusions and their detection through petrography. The results also demonstrate the preservation potential for microbes in hypersaline fluid inclusions, which could allow cells to survive harsh conditions of space, the deep geologic past, or burial in sedimentary basins.     

Sulfate content of Europa's ocean and shell: evolutionary considerations and some geological and astrobiological implications

Recent models for the origin of Jupiter indicate that the Galilean satellites were mostly derived from largely unprocessed solar nebula solids and planetesimals. In the jovian subnebula the solids that built Europa were first heated and then cooled, but the major effect was most likely partial or total devolatilization, and less likely to have been wholesale thermochemical reprocessing of rock + metal compositions (e.g., oxidation of Fe and hydration of silicates). Ocean formation and substantial alteration of interior rock by accreted water and ice would occur during and after accretion, but none of the formation models predicts or implies accretion of sulfates. Europa's primordial ocean was most likely sulfidic. After accretion and later radiogenic and tidal heating, the primordial ocean would have interacted hydrothermally with subjacent rock. It has been hypothesized that sulfides could be converted to sulfates if sufficient hydrogen was lost to space, but pressure effects and the impermeability of serpentinite imply that extraction of sulfate from thoroughly altered Europa-rock would have been inefficient (if indeed Mg sulfates formed at all). Permissive physical limits on the extent of alteration limit the sulfate concentration of Europa's evolved ocean to 10% by weight MgSO(4) or equivalent. Later oxidation of the deep interior of Europa may have also occurred because of water released by the breakdown of hydrated silicates, ultimately yielding S magma and/or SO(2) gas. Geological and astrobiological implications are considered.     

A call for proactive xenoarchaeological guidelines – Scientific, policy and socio-political considerations

As planetary exploration advances, the likelihood of encountering suspected artifacts of astrobiological activity increases, which, it is argued, should be investigated under the auspices of proto-scientific xenoarchaeology. Considering both the unfavorable conditions under which such an investigation may be undertaken (e.g., while observing international planetary protection protocols, utilizing remote sensing techniques in exotic pressure, temperature, chemical, and gravity environments, or adhering to stringent terrestrial biological quarantine and security measures) as well as the demonstrated propensity of the social mind to romanticize or mythologize even the most benign planetary landforms, it is clear that a reactive and poorly preconceived xenoarchaeological methodology will be plagued by inaccuracies, rushed judgments, unrealized bias, misinformation, and erroneous conclusions, along with the negative socio-political impacts that accompany them. Central principles for establishing a rigorous xenoarchaeological methodology are proposed, scientific and technical difficulties are discussed, pertinent international protocols and agreements are reviewed, and sociological and historical considerations are explored.     

Role of nutrition during long-term spaceflight

The authors discuss changes in macro- and micro-nutrients which occur in weightlessness and consider factors which help maintain appropriate nutrition during extended space flight. Basic energy requirements and metabolism are reviewed. The discussion of handling of foodstuffs includes protein, fats, carbohydrates, vitamins, folic acid, iron, and selenium. The discussion of fluids and minerals includes fluid intake, sodium, potassium, and calcium. Changes in gastrointestinal function are examined.     

Modern and ancient extremely acid saline deposits: terrestrial analogs for martian environments?

Extremely acid (pH <1) saline lakes and groundwaters existed in the mid-Permian of the mid-continent of North America. Modern counterparts have been found in acid saline lake systems throughout southern Australia. We compare and contrast the Permian Opeche Shale of North Dakota and Nippewalla Group of Kansas to modern Australian salt lakes in southern Western Australia and in northwest Victoria. With the exception of some minor variations in pH, evaporite mineralogy, and water geochemistry, the Permian and modern systems are similar and characterized by: (1) ephemeral saline continental playas hosted by red siliciclastic sediments, (2) evaporite minerals, including abundant sulfates, (3) Al-Fe-Si-rich waters with low pH values, (4) acidophilic microbes, and (5) paucity of carbonates. The composition of these terrestrial systems is strikingly similar to compositional data returned from the martian surface. Specifically, both Earth and martian systems have high amounts of iron oxides and sulfates, and little, if any, carbonates. We propose that the modern and ancient terrestrial acid saline environments may be good analogs for possible environments on Mars.