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At least 19 records

Lipid analysis of CO 2 -rich subsurface aquifers suggests an autotrophy-based deep biosphere with lysolipids enriched in CPR bacteria

Sediment-hosted CO 2 -rich aquifers deep below the Colorado Plateau (USA) contain a remarkable diversity of uncultivated microorganisms, including Candidate Phyla Radiation (CPR) bacteria that are putative symbionts unable to synthesize membrane lipids. The origin of organic carbon in these ecosystems is unknown and the source of CPR membrane lipids remains elusive. We collected cells from deep groundwater brought to the surface by eruptions of Crystal Geyser, sequenced the community, and analyzed the whole community lipidome over time. Characteristic stable carbon isotopic compositions of microbial lipids suggest that bacterial and archaeal CO 2 fixation ongoing in the deep subsurface provides organic carbon for the complex communities that reside there. Coupled lipidomic-metagenomic analysis indicates that CPR bacteria lack complete lipid biosynthesis pathways but still possess regular lipid membranes. These lipids may therefore originate from other community members, which also adapt to high in situ pressure by increasing fatty acid unsaturation. An unusually high abundance of lysolipids attributed to CPR bacteria may represent an adaptation to membrane curvature stress induced by their small cell sizes. Our findings provide new insights into the carbon cycle in the deep subsurface and suggest the redistribution of lipids into putative symbionts within this community.

59 BASIC BIOLOGICAL SCIENCES↗

Clays and Carbonates in a Groundwater-Fed 3.8 Ga Martian Lake: Insights to Subsurface Habitability on Mars

On Earth, the deep biosphere remains a largely unexplored, but clearly important carbon reservoir. Results from some uplifted central peaks in craters on Mars indicate that substantial carbon was also present at depth and might have helped sustain a deep biosphere. In fact, many factors relevant to deep biosphere habitability are more favorable on Mars than on Earth (e.g. porosity of the crust, geothermal gradient). Future exploration of Mars should include landing sites where materials have been exhumed from depth by meteor impact or basins where subsurface fluids have emerged, carrying clues to subsurface habitability. One of the most astrobiologically interesting sites on Mars McLaughlin Crater, a 93 km-diameter impact crater that formed approximately 4 b.y. ago. On the floor of the crater is a stratigraphic section of subhorizontal, layered sedimentary rocks with strong spectroscopic evidence for Fe-rich clay minerals and Mg-rich carbonates, which we interpret as ancient lacustrine deposits. The fluids that formed these materials likely originated in the subsurface, based on the paucity of channels leading into the crater basin and the fact that this is one of the deepest basins on Mars - a good candidate to have experienced upwelling of subsurface fluids. Therefore, the deposits within McLaughlin crater provide insight into subsurface processes on Mars. In this presentation, we will discuss the habitability of the martian subsurface as well as the geology of McLaughlin Crater and the possibility to detect biomarkers at that site with a future landed mission.

Michalski, Joseph↗

Novel candidate taxa contribute to key metabolic processes in Fennoscandian Shield deep groundwaters

The continental deep biosphere contains a vast reservoir of microorganisms, although a large proportion of its diversity remains both uncultured and undescribed. In this study, the metabolic potential (metagenomes) and activity (metatranscriptomes) of the microbial communities in Fennoscandian Shield deep subsurface groundwaters were characterized with a focus on novel taxa. DNA sequencing generated 1270 de-replicated metagenome-assembled genomes and single-amplified genomes, containing 7 novel classes, 34 orders, and 72 families. The majority of novel taxa were affiliated with Patescibacteria, whereas among novel archaea taxa, Thermoproteota and Nanoarchaeota representatives dominated. Metatranscriptomes revealed that 30 of the 112 novel taxa at the class, order, and family levels were active in at least one investigated groundwater sample, implying that novel taxa represent a partially active but hitherto uncharacterized deep biosphere component. The novel taxa genomes coded for carbon fixation predominantly via the Wood–Ljungdahl pathway, nitrogen fixation, sulfur plus hydrogen oxidation, and fermentative pathways, including acetogenesis. These metabolic processes contributed significantly to the total community’s capacity, with up to 9.9% of fermentation, 6.4% of the Wood–Ljungdahl pathway, 6.8% of sulfur plus 8.6% of hydrogen oxidation, and energy conservation via nitrate (4.4%) and sulfate (6.0%) reduction. Key novel taxa included the UBA9089 phylum, with representatives having a prominent role in carbon fixation, nitrate and sulfate reduction, and organic and inorganic electron donor oxidation. These data provided insights into deep biosphere microbial diversity and their contribution to nutrient and energy cycling in this ecosystem.

Candidatus↗

Life strategies for Aminicenantia in subseafloor oceanic crust

Abstract After decades studying the microbial “deep biosphere” in subseafloor oceanic crust, the growth and life strategies in this anoxic, low energy habitat remain poorly described. Using both single cell genomics and metagenomics, we reveal the life strategies of two distinct lineages of uncultivated Aminicenantia bacteria from the basaltic subseafloor oceanic crust of the eastern flank of the Juan de Fuca Ridge. Both lineages appear adapted to scavenge organic carbon, as each have genetic potential to catabolize amino acids and fatty acids, aligning with previous Aminicenantia reports. Given the organic carbon limitation in this habitat, seawater recharge and necromass may be important carbon sources for heterotrophic microorganisms inhabiting the ocean crust. Both lineages generate ATP via several mechanisms including substrate-level phosphorylation, anaerobic respiration, and electron bifurcation driving an Rnf ion translocation membrane complex. Genomic comparisons suggest these Aminicenantia transfer electrons extracellularly, perhaps to iron or sulfur oxides consistent with mineralogy of this site. One lineage, called JdFR-78, has small genomes that are basal to the Aminicenantia class and potentially use “primordial” siroheme biosynthetic intermediates for heme synthesis, suggesting this lineage retain characteristics of early evolved life. Lineage JdFR-78 contains CRISPR-Cas defenses to evade viruses, while other lineages contain prophage that may help prevent super-infection or no detectable viral defenses. Overall, genomic evidence points to Aminicenantia being well adapted to oceanic crust environments by taking advantage of simple organic molecules and extracellular electron transport.

Environmental Sciences & Ecology↗

Differential Expression of Core Metabolic Functions in Candidatus Altiarchaeum Inhabiting Distinct Subsurface Ecosystems

Candidatus Altiarchaea are widespread across aquatic subsurface ecosystems and possess a highly conserved core genome, yet adaptations of this core genome to different biotic and abiotic factors based on gene expression remain unknown. Here, we investigated the metatranscriptome of two Ca. Altiarchaeum populations that thrive in two substantially different subsurface ecosystems. In Crystal Geyser, a high-CO2 groundwater system in the USA, Ca. Altiarchaeum crystalense co-occurs with the symbiont Ca. Huberiarchaeum crystalense, while in the Muehlbacher sulfidic spring in Germany, an artesian spring high in sulfide concentration, Ca. A. hamiconexum is heavily infected with viruses. We here mapped metatranscriptome reads against their genomes to analyse the in situ expression profile of their core genomes. Out of 537 shared gene clusters, 331 were functionally annotated and 130 differed significantly in expression between the two sites. Main differences were related to genes involved in cell defence like CRISPR-Cas, virus defence, replication, transcription and energy and carbon metabolism. Our results demonstrate that altiarchaeal populations in the subsurface are likely adapted to their environment while influenced by other biological entities that tamper with their core metabolism. We consequently posit that viruses and symbiotic interactions can be major energy sinks for organisms in the deep biosphere.

archaea↗

Remote-Raman and Micro-Raman Studies of Solid CO2, CH4, Gas Hydrates and Ice

It is well known that on Mars CO2 is the principal constituent of the thin atmosphere and on a seasonal basis CO2 snow and frost coats the polar caps. Also over 25% of the Martian atmosphere freezes out and sublimes again each year. The Mars Odyssey Emission Imaging system (THEMIS) has discovered water ice exposed near the edge of Mars southern perennials cap. In recent years, it has been suggested that in Martian subsurface CO2 may exist as gas hydrate (8CO2 + 44 H2O) with melting temperature of 10C. Since the crust of Mars has been stable for enough time there is also a possibility that methane formed by magmatic processes and/or as a byproduct of anaerobic deep biosphere activity to have raised toward the planet s surface. This methane would have been captured and stored as methane hydrate, which concentrates methane and water. Determination of abundance and distribution of these ices on the surface and in the near surface are of fundamental importance for understanding Martian atmosphere, and for future exploration of Mars. In this work, we have evaluated feasibility of using remote Raman and micro-Raman spectroscopy as potential nondestructive and non-contact techniques for detecting solid CO2, CH4 gas, and gas hydrates as well as water-ice on planetary surfaces.

Sharma, S. K.↗

Mud Volcanoes - A New Class of Sites for Geological and Astrobiological Exploration of Mars

Mud volcanoes provide a unique low-temperature window into the Earth s subsurface - including the deep biosphere - and may prove to be significant sources of atmospheric methane. The identification of analogous features on Mars would provide an important new class of sites for geological and astrobiological exploration. We report new work suggesting that features in Acidalia Planitia are most consistent with their being mud volcanoes.

Allen, C.C.↗

Methanogenesis, Mesospheric Clouds, and Global Habitability

Hyperthermophilic methanogens can exist in a deep hot biosphere up to 110 C, or 10 km deep. Methane (CH4) itself is thermodynamically stable to depths of 300 km. Geologic (microbial plus abiogenic thermal) methane is transported upward, attested to by its association with helium, to form petroleum pools. Near or at the surface, geologic CH4 mixes with other natural and with anthropogenic CH4 yielding annual emissions into the atmosphere of 500 Tg, of which 200 Tg are natural and 300 Tg are man-made. The atmospheric lifetime of CH4, a greenhouse gas 20 times more effective than CO2 in raising global temperatures, is approximately 10 years. It is removed from the atmosphere mainly by reactions with hydroxyl radical (OH) to form CO2, but also by dry soil and by conversion to H2O in the stratosphere and middle atmosphere. A sudden rise in atmospheric temperatures by 9-12 C some 55 million years ago has been explained by the release in a few thousand years of three trillion tons of CH4 out of 15 trillion tons that had formed beneath the sea floor. What prevented this CH4-induced greenhouse effect from running away? An analog to the CH4-burp of 55 million years ago is the CH4-doubling over the past century which resulted in a increase in upper level H2O from 4.3 ppmv to 6 ppmv. This 30% increase in H2O vapor yielded a tenfold increase in brightness of polar mesospheric clouds because of a strong dependence of the ice particle nucleation rate on the water saturation ratios. Models show that at a given temperature the optical depth of mesospheric clouds scales as [H2O]beta with beta varying between 4 and 8. Radiative transfer tools applied to mesospheric particles suggest that an optical depth of approximately one, or 1000 times the current mesospheric cloud optical depth, would result in tropospheric cooling of about 10 K. Assuming beta=6, a thousandfold increase in optical thickness would require a three-fold increase of H2O, or a 20-fold increase of CH4. At the current rate of anthropogenic emissions this is expected to occur within the next 1000 years. This timescale is also commensurate with what has been assumed for the CH4- burp 55 million years ago.

Pueschel, Rudolf F.↗

The fate of organic carbon in marine sediments - New insights from recent data and analysis

Organic carbon in marine sediments is a critical component of the global carbon cycle, and its degradation influences a wide range of phenomena, including the magnitude of carbon sequestration over geologic timescales, the recycling of inorganic carbon and nutrients, the dissolution and precipitation of carbonates, the production of methane and the nature of the seafloor biosphere. Although much has been learned about the factors that promote and hinder rates of organic carbon degradation in natural systems, the controls on the distribution of organic carbon in modern and ancient sediments are still not fully understood. In this review, we summarize how recent findings are changing entrenched perspectives on organic matter degradation in marine sediments: a shift from a structurally-based chemical reactivity viewpoint towards an emerging acceptance of the role of the ecosystem in organic matter degradation rates. That is, organic carbon has a range of reactivities determined by not only the nature of the organic compounds, but by the biological, geochemical, and physical attributes of its environment. This shift in mindset has gradually come about due to a greater diversity of sample sites, the molecular revolution in biology, discoveries concerning the extent and limits of life, advances in quantitative modeling, investigations of ocean carbon cycling under a variety of extreme paleo-conditions (e.g. greenhouse environments, euxinic/anoxic oceans), the application of novel analytical techniques and interdisciplinary efforts. Adopting this view across scientific disciplines will enable additional progress in understanding how marine sediments influence the global carbon cycle.

Organic carbon↗

Subsurface microbial communities as a tool for characterizing regional-scale groundwater flow

Subsurface microbial community distribution patterns are influenced by biogeochemical and groundwater fluxes and may inform hydraulic connections along groundwater-flow paths. This study examined the regional-scale microbial community of the Death Valley Regional Flow System and evaluated whether subsurface communities can be used to identify groundwater-flow paths between recharge and discharge areas. Samples were collected from 36 sites in three groundwater basins: Pahute Mesa–Oasis Valley (PMOV), Ash Meadows (AM), and Alkali Flat–Furnace Creek Ranch (AFFCR). Microbial diversity within and between communities varied by location, and communities were separated into two overall groups that affiliated with the AM and PMOV/AFFCR basins. Network analysis revealed patterns between clusters of common microbes that represented groundwaters with similar geochemical conditions and largely corroborated hydraulic connections between recharge and discharge areas. Null model analyses identified deterministic and stochastic ecological processes contributing to microbial community assemblages. Most communities were more different than expected and governed by dispersal limitation, geochemical differences, or undominating processes. However, certain communities from sites located within or near the Nevada National Security Site were more similar than expected and dominated by homogeneous dispersal or selection. Overall, the (dis)similarities between the microbial communities of DVRFS recharge and discharge areas supported previously documented hydraulic connections between: (1) Spring Mountains and Ash Meadows; (2) Frenchman and Yucca Flat and Amargosa Desert; and (3) Amargosa Desert and Death Valley. However, only a portion of the flow path between Pahute Mesa and Oasis Valley could be supported by microbial community analyses, likely due to well-associated artifacts in samples from the two Oasis Valley sites. This study demonstrates the utility of combining microbial data with hydrologic, geologic, and water-chemistry information to comprehensively characterize groundwater systems, highlighting both strengths and limitations of this approach.

54 ENVIRONMENTAL SCIENCES↗

Transportability of exogenous microbial community correlates with interwell connectivity in deep aquifers

Subsurface resource engineering operations often utilize continuous injection of externally-sourced water into geological reservoirs for formation pressure maintenance, resource recovery or energy/waste storage. Such injected water generally contains naturally occurring microbes. Little is known, however, about how the injectate microbes transport through geological media as a community, how such transportability is affected by injector-producer connectivity, and whether such knowledge can be utilized for flowpath characterization. In this study, we analyzed daily-to-weekly timeseries microbial community data from the injected- and produced-fluids of a ten-month flow test at a deep, well-characterized engineered aquifer. We found that the injectate microbial community was distinct from the indigenous community at the amplicon sequence variant (ASV) level, and that the transportability of injectate community towards a given producer, quantified by an “nASV-Overlap” metric we propose, had strong and significant positive correlation with known injector-producer connectivities at our site. This suggests that the better the connectivity, the higher the probability for more injectate species to flow through the interwell region and arrive at a producer. Because interwell connectivity is an important yet usually unknown parameter in subsurface resource engineering, such correlation in turn points to nASV-Overlap as a useful indicator of interwell connectivity for aquifer characterization and long-term monitoring. Based on our findings, an nASV-Overlap-based microbial tracing approach was developed for characterizing and monitoring the relative connectivities across multiple producers with a given injector. A side-by-side comparison between the new nASV-Overlap approach and traditional artificial tracer methods is presented, and their respective strengths and limitations are discussed.

Deep biosphere↗

Genomic comparisons of a bacterial lineage that inhabits both marine and terrestrial deep subsurface systems

It is generally accepted that diverse, poorly characterized microorganisms reside deep within Earth’s crust. One such lineage of deep subsurface-dwelling Bacteria is an uncultivated member of the Firmicutes phylum that can dominate molecular surveys from both marine and continental rock fracture fluids, sometimes forming the sole member of a single-species microbiome. Here, we reconstructed a genome from basalt-hosted fluids of the deep subseafloor along the eastern Juan de Fuca Ridge flank and used a phylogenomic analysis to show that, despite vast differences in geographic origin and habitat, it forms a monophyletic clade with the terrestrial deep subsurface genome of “ Candidatus Desulforudis audaxviator” MP104C. While a limited number of differences were observed between the marine genome of “ Candidatus Desulfopertinax cowenii” modA32 and its terrestrial relative that may be of potential adaptive importance, here it is revealed that the two are remarkably similar thermophiles possessing the genetic capacity for motility, sporulation, hydrogenotrophy, chemoorganotrophy, dissimilatory sulfate reduction, and the ability to fix inorganic carbon via the Wood-Ljungdahl pathway for chemoautotrophic growth. Our results provide insights into the genetic repertoire within marine and terrestrial members of a bacterial lineage that is widespread in the global deep subsurface biosphere, and provides a natural means to investigate adaptations specific to these two environments.

Jungbluth, Sean P.↗

Energy Requirements of Hydrogen-utilizing Microbes: A Boundary Condition for Subsurface Life

Microbial ecosystems based on the energy supplied by water-rock chemistry carry particular significance in the context of geo- and astrobiology. With no direct dependence on solar energy, lithotrophic microbes could conceivably penetrate a planetary crust to a depth limited only by temperature or pressure constraints (several kilometers or more). The deep lithospheric habitat is thereby potentially much greater in volume than its surface counterpart, and in addition offers a stable refuge against inhospitable surface conditions related to climatic or atmospheric evolution (e.g., Mars) or even high-energy impacts (e.g., early in Earth's history). The possibilities for a deep microbial biosphere are, however, greatly constrained by life s need to obtain energy at a certain minimum rate (the maintenance energy requirement) and of a certain minimum magnitude (the energy quantum requirement). The mere existence of these requirements implies that a significant fraction of the chemical free energy available in the subsurface environment cannot be exploited by life. Similar limits may also apply to the usefulness of light energy at very low intensities or long wavelengths. Quantification of these minimum energy requirements in terrestrial microbial ecosystems will help to establish a criterion of energetic habitability that can significantly constrain the prospects for life in Earth's subsurface, or on other bodies in the solar system. Our early work has focused on quantifying the biological energy quantum requirement for methanogenic archaea, as representatives of a plausible subsurface metabolism, in anoxic sediments (where energy availability is among the most limiting factors in microbial population growth). In both field and laboratory experiments utilizing these sediments, methanogens retain a remarkably consistent free energy intake, in the face of fluctuating environmental conditions that affect energy availability. The energy yields apparently required by methanogens in these sediment systems for sustained metabolism are about half that previously thought necessary. Lowered energy requirements would imply that a correspondingly greater proportion of the planetary subsurface could represent viable habitat for microorganisms.

Hoehler, Tori M.↗

Does Aspartic Acid Racemization Constrain the Depth Limit of the Subsurface Biosphere?

Previous studies of the subsurface biosphere have deduced average cellular doubling times of hundreds to thousands of years based upon geochemical models. We have directly constrained the in situ average cellular protein turnover or doubling times for metabolically active micro-organisms based on cellular amino acid abundances, D/L values of cellular aspartic acid, and the in vivo aspartic acid racemization rate. Application of this method to planktonic microbial communities collected from deep fractures in South Africa yielded maximum cellular amino acid turnover times of approximately 89 years for 1 km depth and 27 C and 1-2 years for 3 km depth and 54 C. The latter turnover times are much shorter than previously estimated cellular turnover times based upon geochemical arguments. The aspartic acid racemization rate at higher temperatures yields cellular protein doubling times that are consistent with the survival times of hyperthermophilic strains and predicts that at temperatures of 85 C, cells must replace proteins every couple of days to maintain enzymatic activity. Such a high maintenance requirement may be the principal limit on the abundance of living micro-organisms in the deep, hot subsurface biosphere, as well as a potential limit on their activity. The measurement of the D/L of aspartic acid in biological samples is a potentially powerful tool for deep, fractured continental and oceanic crustal settings where geochemical models of carbon turnover times are poorly constrained. Experimental observations on the racemization rates of aspartic acid in living thermophiles and hyperthermophiles could test this hypothesis. The development of corrections for cell wall peptides and spores will be required, however, to improve the accuracy of these estimates for environmental samples.

cellular↗

The Evolution and Disruption of Planetary Systems

Planetary systems that encounter passing stars can experience severe orbital disruption, and the efficiency of this process is greatly enhanced when the impinging systems are binary pairs rather than single stars. Using a Monte Carlo approach, we have performed nearly half a million numerical experiments to examine the long term ramifications of planetary scattering on planetary systems. We have concluded that systems which form in dense environments such as Orion's Trapezium cluster have roughly a ten percent chance of being seriously disrupted. We have also used our programs to explore the long-term prospects for our own Solar system. Given the current interstellar environment, we have computed the odds that Earth will find its orbit seriously disrupted prior to the emergence of a runaway greenhouse effect driven by the Sun's increasing luminosity. This estimate includes both direct disruption events and scattering processes that seriously alter the orbits of the Jovian planets, which then force severe changes upon the Earth's orbit. We then explore the consequences of the Earth being thrown into deep space. The surface biosphere would rapidly shut down under conditions of zero insolation, but the Earth's radioactive heat is capable of maintaining life deep underground, and perhaps in hydrothermal vent communities, for some time to come. Although unlikely for the Earth, this scenario may be common throughout the universe, since many environments where liquid water could exist (e.g., Europa and Callisto) must derive their energy from internal (rather than external) heating.

Laughlin, Gregory↗