Thermochronologic perspectives on the deep-time evolution of the deep biosphere.

The Earth's deep biosphere hosts some of its most ancient chemolithotrophic lineages. The history of habitation in this environment is thus of interest for understanding the origin and evolution of life. The oldest rocks on Earth, formed about 4 billion years ago, are in continental cratons that have experienced complex histories due to burial and exhumation. Isolated fracture-hosted fluids in these cratons may have residence times older than a billion years, but understanding the history of their microbial communities requires assessing the evolution of habitable conditions. Here, we present a thermochronological perspective on the habitability of Precambrian cratons through time. We show that rocks now in the upper few kilometers of cratons have been uninhabitable (>∼122 °C) for most of their lifetime or have experienced high-temperature episodes, such that the longest record of habitability does not stretch much beyond a billion years. In several cratons, habitable conditions date back only 50 to 300 million years, in agreement with dated biosignatures. The thermochronologic approach outlined here provides context for prospecting and interpreting the little-explored geologic record of the deep biosphere of Earth's cratons, when and where microbial communities may have thrived, and candidate areas for the oldest records of chemolithotrophic microbes.

A Cryptic Alternative for the Evolution of Hyphae.

A growing awareness of a subsurface fossil record of mostly hyphal fungi organisms stretching back through the Phanerozoic to ≈400 megaannum (Ma) and possibly earlier, provides an alternative view on hyphal development. Parallel with the emergence of hyphal fungi during Ordovician-Devonian times when plants colonized the land, which is the traditional notion of hyphal evolution, hyphae-based fungi existed in the deep biosphere. New insights suggest that the fundamental functions of hyphae may have evolved in response to an ancient subsurface endolithic life style and might have been in place before the colonization of land. To address the gaps in the current understanding of hyphal evolution a strategy based on research prospects involving investigations of uncharted geological material, new diagnostics, and comparisons to live species is proposed.

A Combined X-ray Absorption and Mössbauer Spectroscopy Study on Fe Valence and Secondary Mineralogy in Granitoid Fracture Networks: Implications for Geological Disposal of Spent Nuclear Fuels.

Underground repository in crystalline bedrock is a widely accepted solution for long-term disposal of spent nuclear fuels. During future deglaciations, meltwater will intrude via bedrock fractures to the depths of future repositories where O2 left in the meltwater could corrode metal canisters and enhance the migration of redox-sensitive radionuclides. Since glacial meltwater is poor in reduced phases, the quantity and (bio)accessibility of minerogenic Fe(II) in bedrock fractures determine to what extent O2 in future meltwater can be consumed. Here, we determined Fe valence and mineralogy in secondary mineral assemblages sampled throughout the upper kilometer of fractured crystalline bedrock at two sites on the Baltic Shield, using X-ray absorption and Mössbauer spectroscopic techniques that were found to deliver matching results. The data point to extensive O2-consuming capacity of the bedrock fractures, because Fe(II)-rich phyllosilicates were abundant and secondary pyrite was dispersed deep into the bedrock with no overall increase in Fe(II) concentrations and Fe(II)/Fe(III) proportions with depth. The results imply that repeated Pleistocene deglaciations did not cause a measurable decrease in the Fe(II) pool. In surficial fractures, largely opened during glacial unloading, ferrihydrite and illite have formed abundantly via oxidative transformation of Fe(II)-rich phyllosilicates and recently exposed primary biotite/hornblende.

In situ Rb-Sr dating of slickenfibres in deep crystalline basement faults.

Establishing temporal constraints of faulting is of importance for tectonic and seismicity reconstructions and predictions. Conventional fault dating techniques commonly use bulk samples of syn-kinematic illite and other K-bearing minerals in fault gouges, which results in mixed ages of repeatedly reactivated faults as well as grain-size dependent age variations. Here we present a new approach to resolve fault reactivation histories by applying high-spatial resolution Rb-Sr dating to fine-grained mineral slickenfibres in faults occurring in Paleoproterozoic crystalline rocks. Slickenfibre illite and/or K-feldspar together with co-genetic calcite and/or albite were targeted with 50 µm laser ablation triple quadrupole inductively coupled plasma mass spectrometry analyses (LA-ICP-MS/MS). The ages obtained disclose slickenfibre growth at several occasions spanning over 1 billion years, from at least 1527 Ma to 349 ± 9 Ma. The timing of these growth phases and the associated structural orientation information of the kinematic indicators on the fracture surfaces are linked to far-field tectonic events, including the Caledonian orogeny. Our approach links faulting to individual regional deformation events by minimizing age mixing through micro-scale analysis of individual grains and narrow crystal zones in common fault mineral assemblages.

Timing and origin of natural gas accumulation in the Siljan impact structure, Sweden.

Fractured rocks of impact craters may be suitable hosts for deep microbial communities on Earth and potentially other terrestrial planets, yet direct evidence remains elusive. Here, we present a study of the largest crater of Europe, the Devonian Siljan structure, showing that impact structures can be important unexplored hosts for long-term deep microbial activity. Secondary carbonate minerals dated to 80 ± 5 to 22 ± 3 million years, and thus postdating the impact by more than 300 million years, have isotopic signatures revealing both microbial methanogenesis and anaerobic oxidation of methane in the bedrock. Hydrocarbons mobilized from matured shale source rocks were utilized by subsurface microorganisms, leading to accumulation of microbial methane mixed with a thermogenic and possibly a minor abiotic gas fraction beneath a sedimentary cap rock at the crater rim. These new insights into crater hosted gas accumulation and microbial activity have implications for understanding the astrobiological consequences of impacts.

Geochemical controls on dispersion of U and Th in Quaternary deposits, stream water, and aquatic plants in an area with a granite pluton.

The weathering of U and/or Th rich granite plutons, which occurs worldwide, may serve as a potentially important, but as yet poorly defined source for U and Th in (sub-)surface environments. Here, we assessed the impact of an outcrop of such granite (5 km in diameter) and its erosional products on the distribution of U and Th in four nemo-boreal catchments. The results showed that (i) the pluton was enriched in both U and Th; and (ii) secondary U and Th phases were accumulated by peat/gyttja and in other Quaternary deposits with high contents of organic matter. Movement of the ice sheet during the latest glaciation led to dispersal of U- and Th-rich materials eroded from the pluton, resulting in a progressive increase in dissolved U and Th concentrations, as well as U concentrations in aquatic plants with increasing proximity to the pluton. The accumulation of U in the aquatic plants growing upon the pluton (100-365 mg kg-1, dry ash weight) shows that this rock represents a long-term risk for adjacent ecosystems. Dissolved pools of U and Th were correlated with those of dissolved organic matter (DOM) and were predicted to largely occur as organic complexes. This demonstrates the importance of DOM in the transport of U and Th in the catchments. Large fractions of Ca2UO2(CO3)30(aq) were modeled to occur in the stream with highest pH and alkalinity and thus, explain the strongly elevated U concentrations and fluxes in this particular stream. In future climate scenarios, boreal catchments will experience intensified runoff and warmer temperature that favor the production of hydrologically accessible DOM and alkalinity. Therefore, the results obtained from this study have implications for predicting the distribution and transport of Th and U in boreal catchments, especially those associated with U and/or Th rich granite plutons.

Unprecedented 34 S-enrichment of pyrite formed following microbial sulfate reduction in fractured crystalline rocks.

In the deep biosphere, microbial sulfate reduction (MSR) is exploited for energy. Here, we show that, in fractured continental crystalline bedrock in three areas in Sweden, this process produced sulfide that reacted with iron to form pyrite extremely enriched in 34 S relative to 32 S. As documented by secondary ion mass spectrometry (SIMS) microanalyses, the δ34 Spyrite values are up to +132‰V-CDT and with a total range of 186‰. The lightest δ34 Spyrite values (-54‰) suggest very large fractionation during MSR from an initial sulfate with δ34 S values (δ34 Ssulfate,0 ) of +14 to +28‰. Fractionation of this magnitude requires a slow MSR rate, a feature we attribute to nutrient and electron donor shortage as well as initial sulfate abundance. The superheavy δ34 Spyrite values were produced by Rayleigh fractionation effects in a diminishing sulfate pool. Large volumes of pyrite with superheavy values (+120 ± 15‰) within single fracture intercepts in the boreholes, associated heavy average values up to +75‰ and heavy minimum δ34 Spyrite values, suggest isolation of significant amounts of isotopically light sulfide in other parts of the fracture system. Large fracture-specific δ34 Spyrite variability and overall average δ34 Spyrite values (+11 to +16‰) lower than the anticipated δ34 Ssulfate,0 support this hypothesis. The superheavy pyrite found locally in the borehole intercepts thus represents a late stage in a much larger fracture system undergoing Rayleigh fractionation. Microscale Rb-Sr dating and U/Th-He dating of cogenetic minerals reveal that most pyrite formed in the early Paleozoic era, but crystal overgrowths may be significantly younger. The δ13 C values in cogenetic calcite suggest that the superheavy δ34 Spyrite values are related to organotrophic MSR, in contrast to findings from marine sediments where superheavy pyrite has been proposed to be linked to anaerobic oxidation of methane. The findings provide new insights into MSR-related S-isotope systematics, particularly regarding formation of large fractions of 34 S-rich pyrite.

Fungi in Deep Subsurface Environments.

The igneous crust of the oceans and the continents represents the major part of Earth's lithosphere and has recently been recognized as a substantial, yet underexplored, microbial habitat. While prokaryotes have been the focus of most investigations, microeukaryotes have been surprisingly neglected. However, recent work acknowledges eukaryotes, and in particular fungi, as common inhabitants of the deep biosphere, including the deep igneous provinces. The fossil record of the subseafloor igneous crust, and to some extent the continental bedrock, establishes fungi or fungus-like organisms as inhabitants of deep rock since at least the Paleoproterozoic, which challenges the present notion of early fungal evolution. Additionally, deep fungi have been shown to play an important ecological role engaging in symbiosis-like relationships with prokaryotes, decomposing organic matter, and being responsible for mineral weathering and formation, thus mediating mobilization of biogeochemically important elements. In this review, we aim at covering the abundance and diversity of fungi in the various igneous rock provinces on Earth as well as describing the ecological impact of deep fungi. We further discuss what consequences recent findings might have for the understanding of the fungal distribution in extensive anoxic environments and for early fungal evolution.

Incorporation of Metals into Calcite in a Deep Anoxic Granite Aquifer.

Understanding metal scavenging by calcite in deep aquifers in granite is of importance for deciphering and modeling hydrochemical fluctuations and water-rock interaction in the upper crust and for retention mechanisms associated with underground repositories for toxic wastes. Metal scavenging into calcite has generally been established in the laboratory or in natural environments that cannot be unreservedly applied to conditions in deep crystalline rocks, an environment of broad interest for nuclear waste repositories. Here, we report a microanalytical study of calcite precipitated over a period of 17 years from anoxic, low-temperature (14 °C), neutral (pH: 7.4-7.7), and brackish (Cl: 1700-7100 mg/L) groundwater flowing in fractures at >400 m depth in granite rock. This enabled assessment of the trace metal uptake by calcite under these deep-seated conditions. Aquatic speciation modeling was carried out to assess influence of metal complexation on the partitioning into calcite. The resulting environment-specific partition coefficients were for several divalent ions in line with values obtained in controlled laboratory experiments, whereas for several other ions they differed substantially. High absolute uptake of rare earth elements and U(IV) suggests that coprecipitation into calcite can be an important sink for these metals and analogousactinides in the vicinity of geological repositories.

Anaerobic consortia of fungi and sulfate reducing bacteria in deep granite fractures.

The deep biosphere is one of the least understood ecosystems on Earth. Although most microbiological studies in this system have focused on prokaryotes and neglected microeukaryotes, recent discoveries have revealed existence of fossil and active fungi in marine sediments and sub-seafloor basalts, with proposed importance for the subsurface energy cycle. However, studies of fungi in deep continental crystalline rocks are surprisingly few. Consequently, the characteristics and processes of fungi and fungus-prokaryote interactions in this vast environment remain enigmatic. Here we report the first findings of partly organically preserved and partly mineralized fungi at great depth in fractured crystalline rock (-740 m). Based on environmental parameters and mineralogy the fungi are interpreted as anaerobic. Synchrotron-based techniques and stable isotope microanalysis confirm a coupling between the fungi and sulfate reducing bacteria. The cryptoendolithic fungi have significantly weathered neighboring zeolite crystals and thus have implications for storage of toxic wastes using zeolite barriers.Deep subsurface microorganisms play an important role in nutrient cycling, yet little is known about deep continental fungal communities. Here, the authors show organically preserved and partly mineralized fungi at 740 m depth, and find evidence of an anaerobic fungi and sulfate reducing bacteria consortium.

Fluoride abundance and controls in fresh groundwater in Quaternary deposits and bedrock fractures in an area with fluorine-rich granitoid rocks.

This study focuses on fluoride (F(-)) concentrations in groundwater in an area in northern Europe (Laxemar, southeast Sweden) where high F(-) concentrations have previously been found in surface waters such as streams and quarries. Fluoride concentrations were determined over time in groundwater in the Quaternary deposits ("regolith groundwater"), and with different sampling techniques from just beneath the ground surface to nearly -700m in the bedrock (fracture) groundwater. A number of potential controls of dissolved F(-) were studied, including geological variables, mineralogy, mineral chemistry and hydrology. In the regolith groundwater the F(-) concentrations (0.3-4.2mg/L) were relatively stable over time at each sampling site but varied widely among the sampling sites. In these groundwaters, the F(-) concentrations were uncorrelated with sample (filter) depth and the water table in meters above sea level (masl), with the thicknesses of the groundwater column and the regolith, and with the distribution of soil types at the sampling sites. Fluoride concentrations were, however, correlated with the anticipated spatial distribution of erosional material (till) derived from a F-rich circular granite intrusion. Abundant release of F(-) from such material is thus suggested, primarily via dissolution of fluorite and weathering of biotite. In the fresh fracture groundwater, the F(-) concentrations (1.2-7.4mg/L) were generally higher than in the regolith groundwater, and were uncorrelated with depth and with location relative to the granite intrusion. Two mechanisms explaining the overall high F(-) levels in the fracture groundwater were addressed. First, weathering/dissolution of fluorite, bastnäsite and apophyllite, which are secondary minerals formed in the fractures during past hydrothermal events, and biotite which is a primary mineral exposed on fracture walls. Second, long water-residence times, favoring water-rock interaction and build-up of high dissolved F(-) concentrations. The findings are relevant in contexts of extraction of groundwater for drinking-water purposes.

Extreme (13)C depletion of carbonates formed during oxidation of biogenic methane in fractured granite.

Precipitation of exceptionally 13C-depleted authigenic carbonate is a result of, and thus a tracer for, sulphate-dependent anaerobic methane oxidation, particularly in marine sediments. Although these carbonates typically are less depleted in 13C than in the source methane, because of incorporation of C also from other sources, they are far more depleted in 13C (δ13C as light as -69‰ V-PDB) than in carbonates formed where no methane is involved. Here we show that oxidation of biogenic methane in carbon-poor deep groundwater in fractured granitoid rocks has resulted in fracture-wall precipitation of the most extremely 13C-depleted carbonates ever reported, δ13C down to -125‰ V-PDB. A microbial consortium of sulphate reducers and methane oxidizers has been involved, as revealed by biomarker signatures in the carbonates and S-isotope compositions of co-genetic sulphide. Methane formed at shallow depths has been oxidized at several hundred metres depth at the transition to a deep-seated sulphate-rich saline water. This process is so far an unrecognized terrestrial sink of methane.