Petrographic carbon in ancient sediments constrains Proterozoic Era atmospheric oxygen levels.

Oxygen concentration defines the chemical structure of Earth's ecosystems while it also fuels the metabolism of aerobic organisms. As different aerobes have different oxygen requirements, the evolution of oxygen levels through time has likely impacted both environmental chemistry and the history of life. Understanding the relationship between atmospheric oxygen levels, the chemical environment, and life, however, is hampered by uncertainties in the history of oxygen levels. We report over 5,700 Raman analyses of organic matter from nine geological formations spanning in time from 742 to 1,729 Ma. We find that organic matter was effectively oxidized during weathering and little was recycled into marine sediments. Indeed, during this time interval, organic matter was as efficiently oxidized during weathering as it is now. From these observations, we constrain minimum atmospheric oxygen levels to between 2 to 24% of present levels from the late Paleoproterozoic Era into the Neoproterozoic Era. Indeed, our results reveal that eukaryote evolution, including early animal evolution, was not likely hindered by oxygen through this time interval. Our results also show that due to efficient organic recycling during weathering, carbon cycle dynamics can be assessed directly from the sediment carbon record.

Evaporative silicification in floating microbial mats: patterns of oxygen production and preservation potential in silica-undersaturated streams, El Tatio, Chile.

Microbial mats floating within multiple hydrothermally sourced streams in El Tatio, Chile, frequently exhibit brittle siliceous crusts (~1 mm thick) above the air-water interface. The partially silicified mats contain a diverse assemblage of microbial clades and metabolisms, including cyanobacteria performing oxygenic photosynthesis. Surficial crusts are composed of several amorphous silica layers containing well-preserved filaments (most likely cyanobacteria) and other cellular textures overlying EPS-rich unsilicified mats. Environmental logs, silica crust distribution, and microbial preservation patterns provide evidence for crust formation via repeated cycles of evaporation and silica precipitation. Within the mats, in situ microelectrode profiling reveals that daytime oxygen concentrations and pH values are diminished beneath silica crusts compared with adjacent unencrusted communities, indicating localized inhibition of oxygenic photosynthesis due to light attenuation. As a result, aqueous conditions under encrusted mats have a higher saturation state with regard to amorphous silica compared with adjacent, more active mats where high pH increases silica solubility, likely forming a modest feedback loop between diminished photosynthesis and crust precipitation. However, no fully lithified sinters are associated with floating encrusted mats in El Tatio streams, as both subaqueous and subaerial silica precipitation are limited by undersaturated, low-SiO2 (<150 ppm) stream waters. By contrast, well-cemented sinters can form by evaporation in silica-undersaturated solutions above 200 ppm SiO2 . Floating mats in El Tatio therefore represent a specific sinter preservation window, where evaporation in silica-undersaturated microbial mats produces crusts, which preserve cells and affect mat chemistry, but low-silica concentrations prevent the formation of lasting sinter deposits. Patterns of silica precipitation in El Tatio microbial communities show that the preservation potential of silicifying mats in the rock record is strongly dependent on aqueous silica concentrations.

Morphogenesis of digitate structures in hot spring silica sinters of the El Tatio geothermal field, Chile.

In silica-rich hot spring environments, internally laminated, digitate sinter deposits are often interpreted as bio-mediated structures. The organic components of microbial communities (cell surfaces, sheaths and extracellular polymeric substances) can act as templates for silica precipitation, therefore influencing digitate sinter morphogenesis. In addition to biologic surface-templating effects, various microenvironmental factors (hydrodynamics, local pH and fluctuating wind patterns) can also influence silica precipitation, and therefore the morphology of resulting digitate sinters. Digitate sinter morphology thus depends on the dynamic interplay between microenvironmentally driven silica precipitation and microbial growth, but the relative contributions of both factors are a topic of continuing research. Here we present a detailed study of digitate silica sinters in distal, low-temperature regimes of the El Tatio geothermal field, Chile. This high-altitude geothermal field is extremely arid and windy, and has one of the highest silica precipitation rates found in the world. We find that digitate silica sinters at El Tatio always accrete into the prevailing eastward wind direction and exhibit laminar growth patterns coinciding with day-night cycles of wind- and thermally driven evaporation and rewetting. Subaerial parts of digitate sinters lack preserved organics and sinter textures that would indicate past microbial colonization, while filamentous cyanobacteria with resistant, silicified sheaths only inhabit subaqueous cavities that crosscut the primary laminations. We conclude that, although fragile biofilms of extremophile micro-organisms may have initially been present and templated silica precipitation at the tips of these digitate sinters, the saltation of sand grains and precipitation of silica by recurrent wind- and thermally driven environmental forcing at El Tatio are important, if not dominant factors shaping the morphology of these digitate structures. Our study sheds light on the relative contributions of biogenic and abiogenic factors in sinter formation in geothermal systems, with geobiological implications for the cautious interpretation of stromatolite-like features in ancient silica deposits on Earth and Mars.

COSPAR Sample Safety Assessment Framework (SSAF).

The Committee on Space Research (COSPAR) Sample Safety Assessment Framework (SSAF) has been developed by a COSPAR appointed Working Group. The objective of the sample safety assessment would be to evaluate whether samples returned from Mars could be harmful for Earth's systems (e.g., environment, biosphere, geochemical cycles). During the Working Group's deliberations, it became clear that a comprehensive assessment to predict the effects of introducing life in new environments or ecologies is difficult and practically impossible, even for terrestrial life and certainly more so for unknown extraterrestrial life. To manage expectations, the scope of the SSAF was adjusted to evaluate only whether the presence of martian life can be excluded in samples returned from Mars. If the presence of martian life cannot be excluded, a Hold & Critical Review must be established to evaluate the risk management measures and decide on the next steps. The SSAF starts from a positive hypothesis (there is martian life in the samples), which is complementary to the null-hypothesis (there is no martian life in the samples) typically used for science. Testing the positive hypothesis includes four elements: (1) Bayesian statistics, (2) subsampling strategy, (3) test sequence, and (4) decision criteria. The test sequence capability covers self-replicating and non-self-replicating biology and biologically active molecules. Most of the investigations associated with the SSAF would need to be carried out within biological containment. The SSAF is described in sufficient detail to support planning activities for a Sample Receiving Facility (SRF) and for preparing science announcements, while at the same time acknowledging that further work is required before a detailed Sample Safety Assessment Protocol (SSAP) can be developed. The three major open issues to be addressed to optimize and implement the SSAF are (1) setting a value for the level of assurance to effectively exclude the presence of martian life in the samples, (2) carrying out an analogue test program, and (3) acquiring relevant contamination knowledge from all Mars Sample Return (MSR) flight and ground elements. Although the SSAF was developed specifically for assessing samples from Mars in the context of the currently planned NASA-ESA MSR Campaign, this framework and the basic safety approach are applicable to any other Mars sample return mission concept, with minor adjustments in the execution part related to the specific nature of the samples to be returned. The SSAF is also considered a sound basis for other COSPAR Planetary Protection Category V, restricted Earth return missions beyond Mars. It is anticipated that the SSAF will be subject to future review by the various MSR stakeholders.

An Alternative Approach for Assessing Biogenicity.

The search for signs of life in the ancient rock record, extreme terrestrial environments, and other planetary bodies requires a well-established, universal, and unambiguous test of biogenicity. This is notably true for cellular remnants of microbial life, since their relatively simple morphologies resemble various abiogenic microstructures that occur in nature. Although lists of qualitative biogenicity criteria have been devised, debates regarding the biogenicity of many ancient microfossils persist to this day. We propose here an alternative quantitative approach for assessing the biogenicity of putative microfossils. In this theoretical approach, different hypotheses-involving biology or not and depending on the geologic setting-are put forward to explain the observed objects. These hypotheses correspond to specific types of microstructures/systems. Using test samples, the morphology and/or chemistry of these systems are then characterized at the scale of populations. Morphologic parameters include, for example, circularity, aspect ratio, and solidity, while chemical parameters could include elementary ratios (e.g., N/C ratio), isotopic enrichments (e.g., δ13C), or chirality (e.g., molar proportion of stereoisomers), among others. Statistic trends distinguishing the different systems are then searched for empirically. The trends found are translated into "decision spaces" where the different systems are quantitatively discriminated and where the potential microfossil population can be located as a single point. This approach, which is formulated here on a theoretical level, will solve several problems associated with the classical qualitative criteria of biogenicity. Most importantly, it could be applied to reveal the existence of cellular life on other planets, for which characteristics of morphology and chemical composition are difficult to predict.

Structural and chemical heterogeneity of Proterozoic organic microfossils of the ca. 1 Ga old Angmaat Formation, Baffin Island, Canada.

Organic microfossils in Meso- and Neoproterozoic rocks are of key importance to track the emergence and evolution of eukaryotic life. An increasing number of studies combine Raman spectroscopy with synchrotron-based methods to characterize these microfossils. A recurring observation is that Raman spectra of organic microfossils show negligible variation on a sample scale and that variation between different samples can be explained by differences in thermal maturation or in the biologic origin of organic precursor material. There is a paucity of work, however, that explores the extent to which the petrographic framework and diagenetic processes might influence the chemical structure of organic materials. We present a detailed Raman spectroscopy-based study of a complex organic microfossil assemblage in the ca. 1 Ga old Angmaat Formation, Baffin Island, Canada. This formation contains abundant early diagenetic chert that preserves silicified microbial mats with numerous, readily identifiable organic microfossils. Individual chert beds show petrographic differences with discrete episodes of cementation and recrystallization. Raman spectroscopy reveals measurable variation of organic maturity between samples and between neighboring organic microfossils of the same taxonomy and taphonomic state. Scanning transmission X-ray microscopy performed on taphonomically similar coccoidal microfossils from the same thin section shows distinct chemical compositions, with varying ratios of aromatic compounds to ketones and phenols. Such observations imply that geochemical variation of organic matter is not necessarily coupled to thermal alteration or organic precursor material. Variation of the Raman signal across single samples is most likely linked to the diagenetic state of analyzed materials and implies an association between organic preservation and access to diagenetic fluids. Variation in the maturity of individual microfossils may be a natural outcome of local diagenetic processes and potentially exceeds differences derived from precursor organic material. These observations stress the importance of detailed in situ characterization by Raman spectroscopy to identify target specimens for further chemical analysis.

Mineral self-organization on a lifeless planet.

It has been experimentally demonstrated that, under alkaline conditions, silica is able to induce the formation of mineral self-assembled inorganic-inorganic composite materials similar in morphology, texture and nanostructure to the hybrid biomineral structures that, millions of years later, life was able to self-organize. These mineral self-organized structures (MISOS) have been also shown to work as effective catalysts for prebiotic chemical reactions and to easily create compartmentalization within the solutions where they form. We reason that, during the very earliest history of this planet, there was a geochemical scenario that inevitably led to the existence of a large-scale factory of simple and complex organic compounds, many of which were relevant to prebiotic chemistry. The factory was built on a silica-rich high-pH ocean and powered by two main factors: a) a quasi-infinite source of simple carbon molecules synthesized abiotically from reactions associated with serpentinization, or transported from meteorites and produced from their impact on that alkaline ocean, and b) the formation of self-organized silica-metal mineral composites that catalyze the condensation of simple molecules in a methane-rich reduced atmosphere. We discuss the plausibility of this geochemical scenario, review the details of the formation of MISOS and its catalytic properties and the transition towards a slightly alkaline to neutral ocean.

Identifying microbial life in rocks: Insights from population morphometry.

The identification of cellular life in the rock record is problematic, since microbial life forms, and particularly bacteria, lack sufficient morphologic complexity to be effectively distinguished from certain abiogenic features in rocks. Examples include organic pore-fillings, hydrocarbon-containing fluid inclusions, organic coatings on exfoliated crystals and biomimetic mineral aggregates (biomorphs). This has led to the interpretation and re-interpretation of individual microstructures in the rock record. The morphologic description of entire populations of microstructures, however, may provide support for distinguishing between preserved micro-organisms and abiogenic objects. Here, we present a statistical approach based on quantitative morphological description of populations of microstructures. Images of modern microbial populations were compared to images of two relevant types of abiogenic microstructures: interstitial spaces and silica-carbonate biomorphs. For the populations of these three systems, the size, circularity, and solidity of individual particles were calculated. Subsequently, the mean/SD, skewness, and kurtosis of the statistical distributions of these parameters were established. This allowed the qualitative and quantitative comparison of distributions in these three systems. In addition, the fractal dimension and lacunarity of the populations were determined. In total, 11 parameters, independent of absolute size or shape, were used to characterize each population of microstructures. Using discriminant analysis with parameter subsets, it was found that size and shape distributions are typically sufficient to discriminate populations of biologic and abiogenic microstructures. Analysis of ancient, yet unambiguously biologic, samples (1.0 Ga Angmaat Formation, Baffin Island, Canada) suggests that taphonomic effects can alter morphometric characteristics and complicate image analysis; therefore, a wider range of microfossil assemblages should be studied in the future before automated analyses can be developed. In general, however, it is clear from our results that there is great potential for morphometric descriptions of populations in the context of life recognition in rocks, either on Earth or on extraterrestrial bodies.

Formation and Preservation of Microbial Palisade Fabric in Silica Deposits from El Tatio, Chile.

Palisade fabric is a ubiquitous texture of silica sinter found in low temperature (<40°C) regimes of hot spring environments, and it is formed when populations of filamentous microorganisms act as templates for silica polymerization. Although it is known that postdepositional processes such as biological degradation and dewatering can strongly affect preservation of these fabrics, the impact of extreme aridity has so far not been studied in detail. Here, we report a detailed analysis of recently silicified palisade fabrics from a geyser in El Tatio, Chile, tracing the progressive degradation of microorganisms within the silica matrix. This is complemented by heating experiments of natural sinter samples to assess the role of diagenesis. Sheathed cyanobacteria, identified as Leptolyngbya sp., were found to be incorporated into silica sinter by irregular cycles of wetting, evaporation, and mineral precipitation. Transmission electron microscopy analyses revealed that nanometer-sized silica particles are filling the pore space within individual cyanobacterial sheaths, giving rise to their structural rigidity to sustain a palisade fabric framework. Diagenesis experiments further show that the sheaths of the filaments are preferentially preserved relative to the trichomes, and that the amount of water present within the sinter is an important factor for overall preservation during burial. This study confirms that palisade fabrics are efficiently generated in a highly evaporative geothermal field, and that these biosignatures can be most effectively preserved under dry diagenetic conditions.

In Situ Fe and S isotope analyses in pyrite from the 3.2 Ga Mendon Formation (Barberton Greenstone Belt, South Africa): Evidence for early microbial iron reduction.

On the basis of phylogenetic studies and laboratory cultures, it has been proposed that the ability of microbes to metabolize iron has emerged prior to the Archaea/Bacteria split. However, no unambiguous geochemical data supporting this claim have been put forward in rocks older than 2.7-2.5 giga years (Gyr). In the present work, we report in situ Fe and S isotope composition of pyrite from 3.28- to 3.26-Gyr-old cherts from the upper Mendon Formation, South Africa. We identified three populations of microscopic pyrites showing a wide range of Fe isotope compositions, which cluster around two δ56 Fe values of -1.8‰ and +1‰. These three pyrite groups can also be distinguished based on the pyrite crystallinity and the S isotope mass-independent signatures. One pyrite group displays poorly crystallized pyrite minerals with positive Δ33 S values > +3‰, while the other groups display more variable and closer to 0‰ Δ33 S values with recrystallized pyrite rims. It is worth to note that all the pyrite groups display positive Δ33 S values in the pyrite core and similar trace element compositions. We therefore suggest that two of the pyrite groups have experienced late fluid circulations that have led to partial recrystallization and dilution of S isotope mass-independent signature but not modification of the Fe isotope record. Considering the mineralogy and geochemistry of the pyrites and associated organic material, we conclude that this iron isotope systematic derives from microbial respiration of iron oxides during early diagenesis. Our data extend the geological record of dissimilatory iron reduction (DIR) back more than 560 million years (Myr) and confirm that micro-organisms closely related to the last common ancestor had the ability to reduce Fe(III).

Fungal colonization of an Ordovician impact-induced hydrothermal system.

Impacts are common geologic features on the terrestrial planets throughout the solar system, and on at least Earth and Mars impacts have induced hydrothermal convection. Impact-generated hydrothermal systems have been suggested to possess the same life supporting capability as hydrothermal systems associated with volcanic activity. However, evidence of fossil microbial colonization in impact-generated hydrothermal systems is scarce in the literature. Here we report of fossilized microorganisms in association with cavity-grown hydrothermal minerals from the 458 Ma Lockne impact structure, Sweden. Based on morphological characteristics the fossilized microorganisms are interpreted as fungi. We further infer the kerogenization of the microfossils, and thus the life span of the fungi, to be contemporaneous with the hydrothermal activity and migration of hydrocarbons in the system. Our results from the Lockne impact structure show that hydrothermal systems associated with impact structures can support colonization by microbial life.

Calibration of carbonate composition using micro-Raman analysis: application to planetary surface exploration.

Stromatolite structures in Early Archean carbonate deposits form an important clue for the existence of life in the earliest part of Earth's history. Since Mars is thought to have had similar environmental conditions early in its history, the question arises as to whether such stromatolite structures also evolved there. Here, we explore the capability of Raman spectroscopy to make semiquantitative estimates of solid solutions in the Ca-Mg-Fe(+Mn) carbonate system, and we assess its use as a rover-based technique for stromatolite characterization during future Mars missions. Raman microspectroscopy analysis was performed on a set of carbonate standards (calcite, ankerite, dolomite, siderite, and magnesite) of known composition. We show that Raman band shifts of siderite-magnesite and ankerite-dolomite solid solutions display a well-defined positive correlation (r(2) > 0.9) with the Mg# = 100 x Mg/(Mg + Fe + Mn + Ca) of the carbonate analyzed. Raman shifts calibrated as a function of Mg# were used in turn to evaluate the chemical composition of carbonates. Raman analysis of a suite of carbonates (siderite, sidero-magnesite, ankerite, and dolomite) of hydrothermal and sedimentary origin from the ca. 3.2 Ga old Barite Syncline, Barberton greenstone belt, South Africa, and from the ca. 3.5 Ga old Dresser Formation, Pilbara Craton, Western Australia, show good compositional agreement with electron microprobe analyses. These results indicate that Raman spectroscopy can provide direct information on the composition and structure of carbonates on planetary surfaces.

Early Archaean microorganisms preferred elemental sulfur, not sulfate.

Microscopic sulfides with low 34S/32S ratios in marine sulfate deposits from the 3490-million-year old Dresser Formation, Australia, have been interpreted as evidence for the presence of early sulfate-reducing organisms on Earth. We show that these microscopic sulfides have a mass-independently fractionated sulfur isotopic anomaly (Delta33S) that differs from that of their host sulfate (barite). These microscopic sulfides could not have been produced by sulfate-reducing microbes, nor by abiologic processes that involve reduction of sulfate. Instead, we interpret the combined negative delta34S and positive Delta33S signature of these microscopic sulfides as evidence for the early existence of organisms that disproportionate elemental sulfur.

Reassessing the evidence for the earliest traces of life.

The isotopic composition of graphite is commonly used as a biomarker in the oldest (>3.5 Gyr ago) highly metamorphosed terrestrial rocks. Earlier studies on isotopic characteristics of graphite occurring in rocks of the approximately 3.8-Gyr-old Isua supracrustal belt (ISB) in southern West Greenland have suggested the presence of a vast microbial ecosystem in the early Archean. This interpretation, however, has to be approached with extreme care. Here we show that graphite occurs abundantly in secondary carbonate veins in the ISB that are formed at depth in the crust by injection of hot fluids reacting with older crustal rocks (metasomatism). During these reactions, graphite forms from the disproportionation of Fe(II)-bearing carbonates at high temperature. These metasomatic rocks, which clearly lack biological relevance, were earlier thought to be of sedimentary origin and their graphite association provided the basis for inferences about early life. The new observations thus call for a reassessment of previously presented evidence for ancient traces of life in the highly metamorphosed Early Archaean rock record.

Clues from Fe isotope variations on the origin of early Archean BIFs from Greenland.

Archean rocks may provide a record of early Earth environments. However, such rocks have often been metamorphosed by high pressure and temperature, which can overprint the signatures of their original formation. Here, we show that the early Archean banded rocks from Isua, Akilia, and Innersuartuut, Greenland, are enriched in heavy iron isotopes by 0.1 to 0.5 per mil per atomic mass unit relative to igneous rocks worldwide. The observed enrichments are compatible with the transport, oxidation, and subsequent precipitation of ferrous iron emanating from hydrothermal vents and thus suggest that the original rocks were banded iron formations (BIFs). These variations therefore support a sedimentary origin for the Akilia banded rocks, which represent one of the oldest known occurrences of water-laid deposits on Earth.

Chromatographic separation and multicollection-ICPMS analysis of iron. Investigating mass-dependent and -independent isotope effects.

A procedure was developed that allows precise determination of Fe isotopic composition. Purification of Fe was achieved by ion chromatography on AG1-X8 strongly basic anion-exchange resin. No isotopic fractionation is associated with column chemistry within 0.02 per thousand /amu at 2sigma. The isotopic composition was measured with a Micromass IsoProbe multicollection inductively coupled plasma hexapole mass spectrometer. The Fe isotopic composition of the Orgueil CI1 carbonaceous chondrite, which best approximates the solar composition, is indistinguishable from that of IRMM-014 (-0.005 +/- 0.017 per thousand /amu). The IRMM-014 reference material is therefore used for normalization of the isotopic ratios. The protocol for analyzing mass-dependent variations is validated by measuring geostandards (IF-G, DTS-2, BCR-2, AGV-2) and heavily fractionated Fe left after vacuum evaporation of molten wüstite (FeO) and solar (MgO-Al(2)O(3)-SiO(2)-CaO-FeO in chondritic proportions) compositions. It is shown that the isotopic composition of Fe during evaporation of FeO follows a Rayleigh distillation with a fractionation factor alpha equal to (m(1)/m(2)()1/2), where m(1) and m(2) are the masses of the considered isotopes. This agrees with earlier measurements and theoretical expectations. The isotopic composition of Fe left after vacuum evaporation of solar composition also follows a Rayleigh distillation but with a fractionation factor (1.013 22 +/- 0.000 67 for the (56)Fe/(54)Fe ratio) that is lower than the square root of the masses (1.018 35). The protocol for analyzing mass-independent variations is validated by measuring terrestrial rocks that are not expected to show departure from mass-dependent fractionation. After internal normalization of the (57)Fe/(54)Fe ratio, the isotopic composition of Fe can be measured accurately with precisions of 0.2epsilon and 0.5epsilon at 2sigma for (56)Fe/(54)Fe and (58)Fe/(54)Fe ratios, respectively (epsilon refers to relative variations in parts per 10 000). For (58)Fe, this precision is an order of magnitude better than what had been achieved before. The method is applied to rocks that could potentially exhibit mass-independent effects, meteorites and Archaean terrestrial samples. The isotopic composition of a 3.8-Ga-old banded iron formation from Isua (IF-G, Greenland), and quartz-pyroxene rocks from Akilia and Innersuartuut (GR91-26 and SM/GR/171770, Greenland) are normal within uncertainties. Similarly, the Orgueil (CI1), Allende (CV3.2), Eagle Station (ESPAL), Brenham (MGPAL), and Old Woman (IIAB) meteorites do not show any mass-independent effect.