The potential for low-temperature abiotic hydrogen generation and a hydrogen-driven deep biosphere

The release and oxidation of ferrous iron during aqueous alteration of the mineral olivine is known to reduce aqueous solutions to such extent that molecular hydrogen, H2, forms. H2 is an efficient energy carrier and is considered basal to the deep subsurface biosphere. Knowledge of the potential for H2 generation is therefore vital to understanding the deep biosphere on Earth and on extraterrestrial bodies. Here, we provide a review of factors that may reduce the potential for H2 generation with a focus on systems in the core temperature region for thermophilic to hyperthermophilic microbial life. We show that aqueous sulfate may inhibit the formation of H2, whereas redox-sensitive compounds of carbon and nitrogen are unlikely to have significant effect at low temperatures. In addition, we suggest that the rate of H2 generation is proportional to the dissolution rate of olivine and, hence, limited by factors such as reactive surface areas and the access of water to fresh surfaces. We furthermore suggest that the availability of water and pore/fracture space are the most important factors that limit the generation of H2. Our study implies that, because of large heat flows, abundant olivine-bearing rocks, large thermodynamic gradients, and reduced atmospheres, young Earth and Mars probably offered abundant systems where microbial life could possibly have emerged.     

An extensive phase space for the potential martian biosphere

We present a comprehensive model of martian pressure-temperature (P-T) phase space and compare it with that of Earth. Martian P-T conditions compatible with liquid water extend to a depth of ～310?km. We use our phase space model of Mars and of terrestrial life to estimate the depths and extent of the water on Mars that is habitable for terrestrial life. We find an extensive overlap between inhabited terrestrial phase space and martian phase space. The lower martian surface temperatures and shallower martian geotherm suggest that, if there is a hot deep biosphere on Mars, it could extend 7 times deeper than the ～5?km depth of the hot deep terrestrial biosphere in the crust inhabited by hyperthermophilic chemolithotrophs. This corresponds to ～3.2% of the volume of present-day Mars being potentially habitable for terrestrial-like life.     

A microbial oasis in the hypersaline Atacama subsurface discovered by a life detector chip: implications for the search for life on Mars

The Atacama Desert has long been considered a good Mars analogue for testing instrumentation for planetary exploration, but very few data (if any) have been reported about the geomicrobiology of its salt-rich subsurface. We performed a Mars analogue drilling campaign next to the Salar Grande (Atacama, Chile) in July 2009, and several cores and powder samples from up to 5?m deep were analyzed in situ with LDChip300 (a Life Detector Chip containing 300 antibodies). Here, we show the discovery of a hypersaline subsurface microbial habitat associated with halite-, nitrate-, and perchlorate-containing salts at 2?m deep. LDChip300 detected bacteria, archaea, and other biological material (DNA, exopolysaccharides, some peptides) from the analysis of less than 0.5?g of ground core sample. The results were supported by oligonucleotide microarray hybridization in the field and finally confirmed by molecular phylogenetic analysis and direct visualization of microbial cells bound to halite crystals in the laboratory. Geochemical analyses revealed a habitat with abundant hygroscopic salts like halite (up to 260?g kg(-1)) and perchlorate (41.13?μg g(-1) maximum), which allow deliquescence events at low relative humidity. Thin liquid water films would permit microbes to proliferate by using detected organic acids like acetate (19.14?μg g(-1)) or formate (76.06?μg g(-1)) as electron donors, and sulfate (15875?μg g(-1)), nitrate (13490?μg g(-1)), or perchlorate as acceptors. Our results correlate with the discovery of similar hygroscopic salts and possible deliquescence processes on Mars, and open new search strategies for subsurface martian biota. The performance demonstrated by our LDChip300 validates this technology for planetary exploration, particularly for the search for life on Mars.     

Venus, Mars, and the ices on Mercury and the moon: astrobiological implications and proposed mission designs

Venus and Mars likely had liquid water bodies on their surface early in the Solar System history. The surfaces of Venus and Mars are presently not a suitable habitat for life, but reservoirs of liquid water remain in the atmosphere of Venus and the subsurface of Mars, and with it also the possibility of microbial life. Microbial organisms may have adapted to live in these ecological niches by the evolutionary force of directional selection. Missions to our neighboring planets should therefore be planned to explore these potentially life-containing refuges and return samples for analysis. Sample return missions should also include ice samples from Mercury and the Moon, which may contain information about the biogenic material that catalyzed the early evolution of life on Earth (or elsewhere). To obtain such information, science-driven exploration is necessary through varying degrees of mission operation autonomy. A hierarchical mission design is envisioned that includes spaceborne (orbital), atmosphere (airborne), surface (mobile such as rover and stationary such as lander or sensor), and subsurface (e.g., ground-penetrating radar, drilling, etc.) agents working in concert to allow for sufficient mission safety and redundancy, to perform extensive and challenging reconnaissance, and to lead to a thorough search for evidence of life and habitability.     

Subsurface filamentous fabrics: an evaluation of origins based on morphological and geochemical criteria, with implications for exopaleontology

The fossil record of the subsurface biosphere is sparse. Results obtained on subsurface filamentous fabrics (SFF) from >225 paleosubsurface sites in volcanics, oxidized ores, and paleokarst of subrecent to Proterozoic age are presented. SFF are mineral encrustations on filamentous or fibrous substrates that formed in subsurface environments. SFF occur in association with low-temperature aqueous mineral assemblages and consist of tubular, micron-thick (median 1.6 micron) filaments in high spatial density, which occur as irregular masses, matted fabrics, and vertically draped features that resemble stalactites. Micron-sized filamentous centers rule out a stalactitic origin. Morphometric analysis of SFF filamentous forms demonstrates that their shape more closely resembles microbial filaments than fibrous minerals. Abiogenic filament-like forms are considered unlikely precursors of most SFF, because abiogenic forms differ in the distribution of widths and have a lower degree of curvature and a lower number of direction changes. Elemental analyses of SFF show depletion in immobile elements (e.g., Al, Th) and a systematic enrichment in As and Sb, which demonstrates a relation to environments with high flows of water. Sulfur isotopic analyses are consistent with a biological origin of a SFF sample from a Mississippi Valley-Type deposit, which is consistent with data in the literature. Fe isotopes in SFF and active analogue systems, however, allow no discrimination between biogenic and abiogenic origins. The origin of most SFF is explained as permineralized remains of microbial filaments that possibly record rapid growth during phases of high water flow that released chemical energy. It is possible that some SFF formed due to encrustation of mineral fibers. SFF share similarities with Microcodium from soil environments. SFF are a logical target in the search for past life on Mars. The macroscopic nature of many SFF allows for their relatively easy in situ recognition and targeting for more detailed microstructural and geochemical analysis.     

Cave biosignature suites: microbes,minerals, and Mars

Earth's subsurface offers one of the best possible sites to search for microbial life and the characteristic lithologies that life leaves behind. The subterrain may be equally valuable for astrobiology. Where surface conditions are particularly hostile, like on Mars, the subsurface may offer the only habitat for extant lifeforms and access to recognizable biosignatures. We have identified numerous unequivocally biogenic macroscopic, microscopic, and chemical/geochemical cave biosignatures. However, to be especially useful for astrobiology, we are looking for suites of characteristics. Ideally, "biosignature suites" should be both macroscopically and microscopically detectable, independently verifiable by nonmorphological means, and as independent as possible of specific details of life chemistries--demanding (and sometimes conflicting) criteria. Working in fragile, legally protected environments, we developed noninvasive and minimal impact techniques for life and biosignature detection/characterization analogous to Planetary Protection Protocols. Our difficult field conditions have shared limitations common to extraterrestrial robotic and human missions. Thus, the cave/subsurface astrobiology model addresses the most important goals from both scientific and operational points of view. We present details of cave biosignature suites involving manganese and iron oxides, calcite, and sulfur minerals. Suites include morphological fossils, mineral-coated filaments, living microbial mats and preserved biofabrics, 13C and 34S values consistent with microbial metabolism, genetic data, unusual elemental abundances and ratios, and crystallographic mineral forms.     

Exploration and protection of Europa's biosphere: implications of permeable ice

Europa has become a high-priority objective for exploration because it may harbor life. Strategic planning for its exploration has been predicated on an extreme model in which the expected oceanic biosphere lies under a thick ice crust, buried too deep to be reached in the foreseeable future, which would beg the question of whether other active satellites might be more realistic objectives. However, Europa's ice may in fact be permeable, with very different implications for the possibilities for life and for mission planning. A biosphere may extend up to near the surface, making life far more readily accessible to exploration while at the same time making it vulnerable to contamination. The chances of finding life on Europa are substantially improved while the need for planetary protection becomes essential. The new National Research Council planetary protection study will need to go beyond its current mandate if meaningful standards are to be put in place.     

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.     

The physics,biology, and environmental ethics of making mars habitable

The considerable evidence that Mars once had a wetter, more clement, environment motivates the search for past or present life on that planet. This evidence also suggests the possibility of restoring habitable conditions on Mars. While the total amounts of the key molecules--carbon dioxide, water, and nitrogen--needed for creating a biosphere on Mars are unknown, estimates suggest that there may be enough in the subsurface. Super greenhouse gases, in particular, perfluorocarbons, are currently the most effective and practical way to warm Mars and thicken its atmosphere so that liquid water is stable on the surface. This process could take approximately 100 years. If enough carbon dioxide is frozen in the South Polar Cap and absorbed in the regolith, the resulting thick and warm carbon dioxide atmosphere could support many types of microorganisms, plants, and invertebrates. If a planet-wide martian biosphere converted carbon dioxide into oxygen with an average efficiency equal to that for Earth's biosphere, it would take > 100,000 years to create Earth-like oxygen levels. Ethical issues associated with bringing life to Mars center on the possibility of indigenous martian life and the relative value of a planet with or without a global biosphere.     

Life at the wedge: the activity and diversity of arctic ice wedge microbial communities

The discovery of polygonal terrain on Mars underlain by ice heightens interest in the possibility that this water-bearing habitat may be, or may have been, a suitable habitat for extant life. The possibility is supported by the recurring detection of terrestrial microorganisms in subsurface ice environments, such as ice wedges found beneath tundra polygon features. A characterization of the microbial community of ice wedges from the high Arctic was performed to determine whether this ice environment can sustain actively respiring microorganisms and to assess the ecology of this extreme niche. We found that ice wedge samples contained a relatively abundant number of culturable cells compared to other ice habitats (～10(5) CFU·mL(-1)). Respiration assays in which radio-labeled acetate and in situ measurement of CO(2) flux were used suggested low levels of microbial activity, though more sensitive techniques are required to confirm these findings. Based on 16S rRNA gene pyrosequencing, bacterial and archaeal ice wedge communities appeared to reflect surrounding soil communities. Two Pseudomonas sp. were the most abundant taxa in the ice wedge bacterial library (～50%), while taxa related to ammonia-oxidizing Thaumarchaeota occupied 90% of the archaeal library. The tolerance of a variety of isolates to salinity and temperature revealed characteristics of a psychrotolerant, halotolerant community. Our findings support the hypothesis that ice wedges are capable of sustaining a diverse, plausibly active microbial community. As such, ice wedges, compared to other forms of less habitable ground ice, could serve as a reservoir for life on permanently cold, water-scarce, ice-rich extraterrestrial bodies and are therefore of interest to astrobiologists and ecologists alike. .     

The cuatro ciénegas basin in coahuila, Mexico: an astrobiological precambrian park

Abstract The Cuatro Ciénegas Basin (CCB) is a rare oasis in the Chihuahuan Desert in the state of Coahuila, Mexico. It has a biological endemism similar to that of the Galapagos Islands, and its spring-fed ecosystems have very low nutrient content (nitrogen or phosphorous) and are dominated by diverse microbialites. Thus, it has proven to be a distinctive opportunity for the field of astrobiology, as the CCB can be seen as a proxy for an earlier time in Earth's history, in particular the late Precambrian, the biological frontier when prokaryotic life yielded at least partial dominance to eukaryotes and multicellular life. It is a kind of ecological time machine that provides abundant opportunities for collaborative investigations by geochemists, geologists, ecologists, and population biologists in the study of the evolutionary processes that structured Earth-based life, especially in the microbial realm. The CCB is an object of investigation for the identification of biosignatures of past and present biota that can be used in our search for extraterrestrial life. In this review, we summarize CCB research efforts that began with microbial ecology and population biology projects and have since been expanded into broader efforts that involve biogeochemistry, comparative genomics, and assessments of biosignatures. We also propose that, in the future, the CCB is sanctioned as a "Precambrian Park" for astrobiology. Key Words: Microbial mats-Stromatolites-Early Earth-Extremophilic microorganisms-Microbial ecology. Astrobiology 12, 641-647.     

Ionizing radiation and life

Ionizing radiation is a ubiquitous feature of the Cosmos, from exogenous cosmic rays (CR) to the intrinsic mineral radioactivity of a habitable world, and its influences on the emergence and persistence of life are wide-ranging and profound. Much attention has already been focused on the deleterious effects of ionizing radiation on organisms and the complex molecules of life, but ionizing radiation also performs many crucial functions in the generation of habitable planetary environments and the origins of life. This review surveys the role of CR and mineral radioactivity in star formation, generation of biogenic elements, and the synthesis of organic molecules and driving of prebiotic chemistry. Another major theme is the multiple layers of shielding of planetary surfaces from the flux of cosmic radiation and the various effects on a biosphere of violent but rare astrophysical events such as supernovae and gamma-ray bursts. The influences of CR can also be duplicitous, such as limiting the survival of surface life on Mars while potentially supporting a subsurface biosphere in the ocean of Europa. This review highlights the common thread that ionizing radiation forms between the disparate component disciplines of astrobiology.     

Hypersaline microbial systems of sabkhas: examples of life's survival in "extreme" conditions

Life and living systems need several important factors to establish themselves and to have a continued tradition. In this article the nature of the borderline situation for microbial life under heavy salt stress is analyzed and discussed using the example of biofilms and microbial mats of sabkha systems of the Red Sea. Important factors ruling such environments are described, and include the following: (1) Microbial life is better suited for survival in extremely changing and only sporadically water-supplied environments than are larger organisms (including humans). (2) Microbial life shows extremely poikilophilic adaptation patterns to conditions that deviate significantly from conditions normal for life processes on Earth today. (3) Microbial life adapts itself to such extremely changing and only ephemerally supportive conditions by the capacity of extreme changes (a) in morphology (pleomorphy), (b) in metabolic patterns (poikilotrophy), (c) in survival strategies (poikilophily), and (d) by trapping and enclosing all necessary sources of energy matter in an inwardly oriented diffusive cycle. All this is achieved without any serious attempt at escaping from the extreme and extremely changing conditions. Furthermore, these salt swamp systems are geophysiological generators of energy and material reservoirs recycled over a geological time scale. Neither energy nor material is wasted for propagation by spore formation. This capacity is summarized as poikilophilic and poikilotroph behavior of biofilm or microbial mat communities in salt and irradiationstressed environmental conditions of the sabkha or salt desert type. We use mainly cyanobacteria as an example, although other bacteria and even eukaryotic fungi may exhibit the same potential of living and surviving under conditions usually not suitable for life on Earth. It may, however, be postulated that such poikilophilic organisms are the true candidates for life support and survival under conditions never recorded on Planet Earth. Mars and some planets of other suns may be good candidates to search for life under conditions normally not thought to be favorable for the maintenance of life.     

Was there a late Archean biospheric explosion?

There is a growing body of evidence which suggests that the evolution of the planet drives the evolution of the biosphere. There have been 2 significant stages in Earth history when atmospheric oxygen levels rose rapidly, and both appear to be associated with supercontinent cycles. The earlier biospheric event, which extends across the Archean-Proterozoic boundary (ca. 3.0-2.2 Ga), has received little attention and is the focus of this study. Recent work on the Pilbara Craton of Western Australia has shown that concretion formed by microbial activity during the diagenesis of these sediments are absent from early Archean sediments but abundant in late Archean and early Paleoproterozoic successions of the Hamersley Basin, appearing abruptly in sedimentary rocks younger than 2.7 Ga. This study suggests that their internal architecture may have been defined by the diffusion of humic acids and the formation of polymer gels during diagenesis. The data imply that the biosphere expanded suddenly shortly after 3.0 Ga and may have begun to raise the oxygen levels of the oceanic water column earlier than thought-possibly as much as 300 my earlier.     

Microbial survival rates of Escherichia coli and Deinococcus radiodurans under low temperature, low pressure, and UV-Irradiation conditions, and their relevance to possible Martian life

Viability rates were determined for microbial populations of Escherichia coli and Deinococcus radiodurans under the environmental stresses of low temperature (-35 degrees C), low-pressure conditions (83.3 kPa), and ultraviolet (UV) irradiation (37 W/m(2)). During the stress tests the organisms were suspended in saltwater soil and freshwater soil media, at variable burial depths, and in seawater. Microbial populations of both organisms were most susceptible to dehydration stress associated with low-pressure conditions, and to UV irradiation. However, suspension in a liquid water medium and burial at larger depths (5 cm) improved survival rates markedly. Our results indicate that planetary surfaces that possess little to no atmosphere and have low water availability do not constitute a favorable environment for terrestrial microorganisms.     

Physical simulation for low-energy astrobiology environmental scenarios

Speculations about the extent of life of independent origin and the potential for sustaining Earth-based life in subsurface environments on both Europa and Mars are of current and relevant interest. Theoretical modeling based on chemical energetics has demonstrated potential options for viable biochemical metabolism (metabolic pathways) in these types of environments. Also, similar environments on Earth show microbial activity. However, actual physical simulation testing of specific environments is required to confidently determine the interplay of various physical and chemical parameters on the viability of relevant metabolic pathways. This testing is required to determine the potential to sustain life in these environments on a specific scenario by scenario basis. This study examines the justification, design, and fabrication of, as well as the culture selection and screening for, a psychrophilic/halophilic/anaerobic digester. This digester is specifically designed to conform to physical testing needs of research relating to potential extent physical environments on Europa and other planetary bodies in the Solar System. The study is a long-term effort and is currently in an early phase, with only screening-level data at this time. Full study results will likely take an additional 2 years. However, researchers in electromagnetic biosignature and in situ instrument development should be aware of the study at this time, as they are invited to participate in planning for future applications of the digester facility.     

Why implementing the space option is necessary for society

For several years, specialized agencies have been searching for "new programs" that could reinvigorate the support for space activities and stop their budgets' decline of. But the same time, they have been retrenching by focusing on collecting and distributing information, putting scientific research as their core projects. On a planet soon to host a 10-billion population that will impact the biosphere's workings as never before, at a time when many governments and organizations see the virtue in the management of scarcity, musing on the origins of life and of the solar system can hardly be expected to be invested with high priority. The space option arose from the analysis of the issues confronting humanity. In reviewing the material needs of the human population in the near future, the analysis finds that the impact on the biosphere will perforce be much larger than it usually seems to be acceptable to assume.     

An astrophysical view of Earth-based metabolic biosignature gases

Microbial life on Earth uses a wide range of chemical and energetic resources from diverse habitats. An outcome of this microbial diversity is an extensive and varied list of metabolic byproducts. We review key points of Earth-based microbial metabolism that are useful to the astrophysical search for biosignature gases on exoplanets, including a list of primary and secondary metabolism gas byproducts. Beyond the canonical, unique-to-life biosignature gases on Earth (O(2), O(3), and N(2)O), the list of metabolic byproducts includes gases that might be associated with biosignature gases in appropriate exoplanetary environments. This review aims to serve as a starting point for future astrophysical biosignature gas research.     

The possible origin and persistence of life on Enceladus and detection of biomarkers in the plume

The jets of icy particles and water vapor issuing from the south pole of Enceladus are evidence for activity driven by some geophysical energy source. The vapor has also been shown to contain simple organic compounds, and the south polar terrain is bathed in excess heat coming from below. The source of the ice and vapor, and the mechanisms that accelerate the material into space, remain obscure. However, it is possible that a liquid water environment exists beneath the south polar cap, which may be conducive to life. Several theories for the origin of life on Earth would apply to Enceladus. These are (1) origin in an organic-rich mixture, (2) origin in the redox gradient of a submarine vent, and (3) panspermia. There are three microbial ecosystems on Earth that do not rely on sunlight, oxygen, or organics produced at the surface and, thus, provide analogues for possible ecologies on Enceladus. Two of these ecosystems are found deep in volcanic rock, and the primary productivity is based on the consumption by methanogens of hydrogen produced by rock reactions with water. The third ecosystem is found deep below the surface in South Africa and is based on sulfur-reducing bacteria consuming hydrogen and sulfate, both of which are ultimately produced by radioactive decay. Methane has been detected in the plume of Enceladus and may be biological in origin. An indicator of biological origin may be the ratio of non-methane hydrocarbons to methane, which is very low (0.001) for biological sources but is higher (0.1-0.01) for nonbiological sources. Thus, Cassini's instruments may detect plausible evidence for life by analysis of hydrocarbons in the plume during close encounters.     

Biosignatures of early earths

A major goal of NASA's Origins Program is to find habitable planets around other stars and determine which might harbor life. Determining whether or not an extrasolar planet harbors life requires an understanding of what spectral features (i.e., biosignatures) might result from life's presence. Consideration of potential biosignatures has tended to focus on spectral features of gases in Earth's modern atmosphere, particularly ozone, the photolytic product of biogenically produced molecular oxygen. But life existed on Earth for about 1(1/2) billion years before the buildup of atmospheric oxygen. Inferred characteristics of Earth's earliest biosphere and studies of modern microbial ecosystems that share some of those characteristics suggest that organosulfur compounds, particularly methanethiol (CH(3)SH, the sulfur analog of methanol), may have been biogenic products on early Earth. Similar production could take place on extrasolar Earth-like planets whose biota share functional chemical characteristics with Earth life. Since methanethiol and related organosulfur compounds (as well as carbon dioxide) absorb at wavelengths near or overlapping the 9.6-microm band of ozone, there is potential ambiguity in interpreting a feature around this wavelength in an extrasolar planet spectrum.