Iron-magnesium silicate bioweathering on Earth (and Mars?)

We examined the common, iron-magnesium silicate minerals olivine and pyroxene in basalt and in mantle rocks to determine if they exhibit textures similar to bioweathering textures found in glass. Our results show that weathering in olivine may occur as long, narrow tunnels (1-3 microm in diameter and up to 100 microm long) and as larger irregular galleries, both of which have distinctive characteristics consistent with biological activity. These weathering textures are associated with clay mineral by-products and nucleic acids. We also examined olivine and pyroxene in martian meteorites, some of which experienced preterrestrial aqueous alteration. Some olivines and pyroxenes in the martian meteorite Nakhla were found to contain tunnels that are similar in size and shape to tunnels in terrestrial iron-magnesium silicates that contain nucleic acids. Though the tunnels found in Nakhla are similar to the biosignatures found in terrestrial minerals, their presence cannot be used to prove that the martian alteration features had a biogenic origin. The abundance and wide distribution of olivine and pyroxene on Earth and in the Solar System make bioweathering features in these minerals potentially important new biosignatures that may play a significant role in evaluating whether life ever existed on Mars.     

Volcano-ice interaction as a microbial habitat on Earth and Mars

Volcano-ice interaction has been a widespread geological process on Earth that continues to occur to the present day. The interaction between volcanic activity and ice can generate substantial quantities of liquid water, together with steep thermal and geochemical gradients typical of hydrothermal systems. Environments available for microbial colonization within glaciovolcanic systems are wide-ranging and include the basaltic lava edifice, subglacial caldera meltwater lakes, glacier caves, and subsurface hydrothermal systems. There is widespread evidence of putative volcano-ice interaction on Mars throughout its history and at a range of latitudes. Therefore, it is possible that life on Mars may have exploited these habitats, much in the same way as has been observed on Earth. The sedimentary and mineralogical deposits resulting from volcano-ice interaction have the potential to preserve evidence of any indigenous microbial populations. These include j?kulhlaup (subglacial outflow) sedimentary deposits, hydrothermal mineral deposits, basaltic lava flows, and subglacial lacustrine deposits. Here, we briefly review the evidence for volcano-ice interactions on Mars and discuss the geomicrobiology of volcano-ice habitats on Earth. In addition, we explore the potential for the detection of these environments on Mars and any biosignatures these deposits may contain.     

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.     

Morphological biosignatures and the search for life on Mars

This report provides a rationale for the advances in instrumentation and understanding needed to assess claims of ancient and extraterrestrial life made on the basis of morphological biosignatures. Morphological biosignatures consist of bona fide microbial fossils as well as microbially influenced sedimentary structures. To be recognized as evidence of life, microbial fossils must contain chemical and structural attributes uniquely indicative of microbial cells or cellular or extracellular processes. When combined with various research strategies, high-resolution instruments can reveal such attributes and elucidate how morphological fossils form and become altered, thereby improving the ability to recognize them in the geological record on Earth or other planets. Also, before fossilized microbially influenced sedimentary structures can provide evidence of life, criteria to distinguish their biogenic from non-biogenic attributes must be established. This topic can be advanced by developing process-based models. A database of images and spectroscopic data that distinguish the suite of bona fide morphological biosignatures from their abiotic mimics will avoid detection of false-positives for life. The use of high-resolution imaging and spectroscopic instruments, in conjunction with an improved knowledge base of the attributes that demonstrate life, will maximize our ability to recognize and assess the biogenicity of extraterrestrial and ancient terrestrial life.     

Olivine-respiring bacteria isolated from the rock-ice interface in a lava-tube cave, a Mars analog environment

The boundary between ice and basalt on Earth is an analogue for some near-surface environments of Mars. We investigated neutrophilic iron-oxidizing microorganisms from the basalt-ice interface in a lava tube from the Oregon Cascades with perennial ice. One of the isolates (Pseudomonas sp. HerB) can use ferrous iron Fe(II) from the igneous mineral olivine as an electron donor and O(2) as an electron acceptor. The optimum growth temperature is ～12-14°C, but growth also occurs at 5°C. Bicarbonate is a facultative source of carbon. Growth of Pseudomonas sp. HerB as a chemolithotrophic iron oxidizer with olivine as the source of energy is favored in low O(2) conditions (e.g., 1.6% O(2)). Most likely, microbial oxidation of olivine near pH 7 requires low O(2) to offset the abiotic oxidation of iron. The metabolic capabilities of this bacterium would allow it to live in near-surface, icy, volcanic environments of Mars in the present or recent geological past and make this type of physiology a prime candidate in the search for life on Mars.     

Preservation of martian organic and environmental records: final report of the Mars biosignature working group

The Mars Science Laboratory (MSL) has an instrument package capable of making measurements of past and present environmental conditions. The data generated may tell us if Mars is, or ever was, able to support life. However, the knowledge of Mars' past history and the geological processes most likely to preserve a record of that history remain sparse and, in some instances, ambiguous. Physical, chemical, and geological processes relevant to biosignature preservation on Earth, especially under conditions early in its history when microbial life predominated, are also imperfectly known. Here, we present the report of a working group chartered by the Co-Chairs of NASA's MSL Project Science Group, John P. Grotzinger and Michael A. Meyer, to review and evaluate potential for biosignature formation and preservation on Mars. Orbital images confirm that layered rocks achieved kilometer-scale thicknesses in some regions of ancient Mars. Clearly, interplays of sedimentation and erosional processes govern present-day exposures, and our understanding of these processes is incomplete. MSL can document and evaluate patterns of stratigraphic development as well as the sources of layered materials and their subsequent diagenesis. It can also document other potential biosignature repositories such as hydrothermal environments. These capabilities offer an unprecedented opportunity to decipher key aspects of the environmental evolution of Mars' early surface and aspects of the diagenetic processes that have operated since that time. Considering the MSL instrument payload package, we identified the following classes of biosignatures as within the MSL detection window: organism morphologies (cells, body fossils, casts), biofabrics (including microbial mats), diagnostic organic molecules, isotopic signatures, evidence of biomineralization and bioalteration, spatial patterns in chemistry, and biogenic gases. Of these, biogenic organic molecules and biogenic atmospheric gases are considered the most definitive and most readily detectable by MSL.     

Issues in planetary protection: policy, protocol and implementation

Planetary protection is NASA's term for the practice of protecting solar system bodies from Earth life while protecting Earth from life that may be brought back from other solar system bodies. Spacefaring nations will soon begin retrieving samples from Mars and other solar system bodies. For these samples, planetary protection is in order, and measures are already in place to prevent the forward contamination of Mars and other bodies by Earth microbes and the backward contamination of Earth by possible extraterrestrial life. A major goal of planetary protection controls on forward contamination is to preserve the planetary record of natural processes by preventing human-caused microbial introductions.     

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.     

Gypsum-permineralized microfossils and their relevance to the search for life on Mars

Abstract Orbital and in situ analyses establish that aerially extensive deposits of evaporitic sulfates, including gypsum, are present on the surface of Mars. Although comparable gypsiferous sediments on Earth have been largely ignored by paleontologists, we here report the finding of diverse fossil microscopic organisms permineralized in bottom-nucleated gypsums of seven deposits: two from the Permian (～260?Ma) of New Mexico, USA; one from the Miocene (～6?Ma) of Italy; and four from Recent lacustrine and saltern deposits of Australia, Mexico, and Peru. In addition to presenting the first report of the widespread occurrence of microscopic fossils in bottom-nucleated primary gypsum, we show the striking morphological similarity of the majority of the benthic filamentous fossils of these units to the microorganisms of a modern sulfuretum biocoenose. Based on such similarity, in morphology as well as habitat, these findings suggest that anaerobic sulfur-metabolizing microbial assemblages have changed relatively little over hundreds of millions of years. Their discovery as fossilized components of the seven gypsiferous units reported suggests that primary bottom-nucleated gypsum represents a promising target in the search for evidence of past life on Mars. Key Words: Confocal laser scanning microscopy-Gypsum fossils-Mars sample return missions-Raman spectroscopy-Sample Analysis at Mars (SAM) instrument-Sulfuretum. Astrobiology 12, 619-633.     

Can identification of a fourth domain of life be made from sequence data alone, and could it be done on Mars?

A central question in astrobiology is whether life exists elsewhere in the universe. If so, is it related to Earth life? Technologies exist that enable identification of DNA- or RNA-based microbial life directly from environmental samples here on Earth. Such technologies could, in principle, be applied to the search for life elsewhere; indeed, efforts are underway to initiate such a search. However, surveying for nucleic acid-based life on other planets, if attempted, must be carried out with caution, owing to the risk of contamination by Earth-based life. Here we argue that the null hypothesis must be that any DNA discovered and sequenced from samples taken elsewhere in the universe are Earth-based contaminants. Experience from studies of low-biomass ancient DNA demonstrates that some results, by their very nature, will not enable complete rejection of the null hypothesis. In terms of eliminating contamination as an explanation of the data, there may be value in identification of sequences that lie outside the known diversity of the three domains of life. We therefore have examined whether a fourth domain could be readily identified from environmental DNA sequence data alone. We concluded that, even on Earth, this would be far from trivial, and we illustrate this point by way of examples drawn from the literature. Overall, our conclusions do not bode well for planned PCR-based surveys for life on Mars, and we argue that other independent biosignatures will be essential in corroborating any claims for the presence of life based on nucleic acid sequences.     

Putative fossilized fungi from the lithified volcaniclastic apron of Gran Canaria, Spain

We report the discovery of fossilized filamentous structures in samples of the lithified, volcaniclastic apron of Gran Canaria, which were obtained during Leg 157 of the Ocean Drilling Program (ODP). These filamentous structures are 2-15 μm in diameter and several hundred micrometers in length and are composed of Si, Al, Fe, Ca, Mg, Na, Ti, and C. Chitin was detected in the filamentous structures by staining with wheat germ agglutinin dye conjugated with fluorescein isothiocyanate (WGA-FITC), which suggests that they are fossilized fungal hyphae. The further elucidation of typical filamentous fungal morphological features, such as septa, hyphal bridges, and anastomosis and their respective sizes, support this interpretation. Characteristic structures that we interpreted as fossilized spores were also observed in association with the putative hyphae. The fungal hyphae were found in pyroxene phenocrysts and in siderite pseudomorphs of a basalt breccia. The fungal colonization of the basalt clasts occurred after the brecciation but prior to the final emplacement and lithification of the sediment at ～16-14 Ma. The siderite appears to have been partially dissolved by the presence of fungal hyphae, and the fungi preferentially colonized Fe-rich carbonates over Fe-poor carbonates (aragonite). Our findings indicate that fungi may be an important geobiological agent in subseafloor environments and an important component of the deep subseafloor biosphere, and that hydrothermal environments associated with volcanism can support a diverse ecosystem, including eukaryotes.     

Mineralogical biosignatures and the search for life on Mars

If life ever existed, or still exists, on Mars, its record is likely to be found in minerals formed by, or in association with, microorganisms. An important concept regarding interpretation of the mineralogical record for evidence of life is that, broadly defined, life perturbs disequilibria that arise due to kinetic barriers and can impart unexpected structure to an abiotic system. Many features of minerals and mineral assemblages may serve as biosignatures even if life does not have a familiar terrestrial chemical basis. Biological impacts on minerals and mineral assemblages may be direct or indirect. Crystalline or amorphous biominerals, an important category of mineralogical biosignatures, precipitate under direct cellular control as part of the life cycle of the organism (shells, tests, phytoliths) or indirectly when cell surface layers provide sites for heterogeneous nucleation. Biominerals also form indirectly as by-products of metabolism due to changing mineral solubility. Mineralogical biosignatures include distinctive mineral surface structures or chemistry that arise when dissolution and/or crystal growth kinetics are influenced by metabolic by-products. Mineral assemblages themselves may be diagnostic of the prior activity of organisms where barriers to precipitation or dissolution of specific phases have been overcome. Critical to resolving the question of whether life exists, or existed, on Mars is knowing how to distinguish biologically induced structure and organization patterns from inorganic phenomena and inorganic self-organization. This task assumes special significance when it is acknowledged that the majority of, and perhaps the only, material to be returned from Mars will be mineralogical.     

Identification of morphological biosignatures in Martian analogue field specimens using in situ planetary instrumentation

We have investigated how morphological biosignatures (i.e., features related to life) might be identified with an array of viable instruments within the framework of robotic planetary surface operations at Mars. This is the first time such an integrated lab-based study has been conducted that incorporates space-qualified instrumentation designed for combined in situ imaging, analysis, and geotechnics (sampling). Specimens were selected on the basis of feature morphology, scale, and analogy to Mars rocks. Two types of morphological criteria were considered: potential signatures of extinct life (fossilized microbial filaments) and of extant life (crypto-chasmoendolithic microorganisms). The materials originated from a variety of topical martian analogue localities on Earth, including impact craters, high-latitude deserts, and hydrothermal deposits. Our in situ payload included a stereo camera, microscope, M?ssbauer spectrometer, and sampling device (all space-qualified units from Beagle 2), and an array of commercial instruments, including a multi-spectral imager, an X-ray spectrometer (calibrated to the Beagle 2 instrument), a micro-Raman spectrometer, and a bespoke (custom-designed) X-ray diffractometer. All experiments were conducted within the engineering constraints of in situ operations to generate realistic data and address the practical challenges of measurement. Our results demonstrate the importance of an integrated approach for this type of work. Each technique made a proportionate contribution to the overall effectiveness of our "pseudopayload" for biogenic assessment of samples yet highlighted a number of limitations of current space instrument technology for in situ astrobiology.     

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.     

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.     

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.     

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.     

Magnetotactic bacteria on Earth and on Mars

Continued interest in the possibility of evidence for life in the ALH84001 Martian meteorite has focused on the magnetite crystals. This review is structured around three related questions: is the magnetite in ALH84001 of biological or non-biological origin, or a mixture of both? does magnetite on Earth provide insight to the plausibility of biogenic magnetite on Mars? could magnetotaxis have developed on Mars? There are credible arguments for both the biological and non-biological origin of the magnetite in ALH84001, and we suggest that more studies of ALH84001, extensive laboratory simulations of non-biological magnetite formation, as well as further studies of magnetotactic bacteria on Earth will be required to further address this question. Magnetite grains produced by bacteria could provide one of the few inorganic traces of past bacterial life on Mars that could be recovered from surface soils and sediments. If there was biogenic magnetite on Mars in sufficient abundance to leave fossil remains in the volcanic rocks of ALH84001, then it is likely that better-preserved magnetite will be found in sedimentary deposits on Mars. Deposits in ancient lakebeds could contain well-preserved chains of magnetite clearly indicating a biogenic origin.     

Ultrastructural study of iron oxide precipitates: implications for the search for biosignatures in the Meridiani hematite concretions, Mars

Two terrestrial environments that have been proposed as analogs for the iron oxide precipitation in the Meridiani Planum region of Mars include the Rio Tinto precipitates and southern Utah marble concretions. Samples of two typical Utah iron oxide concretions and iron oxide precipitates in contact with biofilms from Rio Tinto have been studied to determine whether evidence could be found for biomediation in the precipitation process and to identify likely locations for fossil microorganisms. Scanning electron microscopy, energy dispersive X-ray, and gas chromatography-mass spectrometry (GC-MS) were used to search for biosignatures in the Utah marbles. The precipitation of iron oxides resembles known biosignatures, though organic compounds could not be confirmed with GC-MS analysis. In contrast, textural variations induced by biological activity are abundant in the modern Rio Tinto samples. Although no compelling evidence of direct or indirect biomediation was found in the Utah marbles, the ultrastructure of the iron oxide cement in the concretion suggests an inward growth during concretion precipitation from an initially spherical redox front. No indication for growth from a physical nucleus was found.     

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.