Search

Subglacial Antarctic aquatic environments are important targets for scientific exploration due to the unique ecosystems they support and their sediments containing palaeoenvironmental records. Directly accessing these environments while preventing forward contamination and demonstrating that it has not been introduced is logistically challenging. The Whillans Ice Stream Subglacial Access Research Drilling (WISSARD) project designed, tested and implemented a microbiologically and chemically clean method of hot-water drilling that was subsequently used to access subglacial aquatic environments. We report microbiological and biogeochemical data collected from the drilling system and underlying water columns during sub-ice explorations beneath the McMurdo and Ross ice shelves and Whillans Ice Stream. Our method reduced microbial concentrations in the drill water to values three orders of magnitude lower than those observed in Whillans Subglacial Lake. Furthermore, the water chemistry and composition of microorganisms in the drill water were distinct from those in the subglacial water cavities. The submicron filtration and ultraviolet irradiation of the water provided drilling conditions that satisfied environmental recommendations made for such activities by national and international committees. Our approach to minimizing forward chemical and microbiological contamination serves as a prototype for future efforts to access subglacial aquatic environments beneath glaciers and ice sheets.

Subglacial Lake Whillans lies below around 800m of Antarctic ice and is isolated from fresh sources of photosynthetic organic matter to sustain life. The diverse microbial ecosystems within the lake and underlying sediments are therefore dependent on a combination of relict, overridden, marine-derived organic matter and mineral-derived energy. Here, we conduct experiments to replicate subglacial erosion involving both gentle and high-energy crushing of Subglacial Lake Whillans sediments and the subsequent addition of anoxic water. We find that substantial quantities of reduced species, including hydrogen, methane, acetate and ammonium and oxidised species such as hydrogen peroxide, sulfate and carbon dioxide are released. We propose that the concomitant presence of both hydrogen and hydrogen peroxide, alongside high concentrations of mineral surface radicals, suggests that the splitting of water on freshly abraded mineral surfaces increases the concentrations of redox pairs from rock-water reactions and could provide a mechanism to augment the energy available to microbial ecosystems. The crushing and wetting of rocks by erosion under glaciers produces chemical compounds that could fuel microbial activity, as demonstrated by experiments on material collected from Subglacial Lake Whillans in Antarctica

Wet-based regions of glaciers and ice sheets are now recognized to host unique and diverse microbial communities capable of influencing global biogeochemical cycles. However, the isolated nature of subglacial environments poses limitations upon the supply of protons for chemical weathering and energy sources (electron donors/acceptors) to support in situ microbial communities. A less well recognized source of these substrates is the release of gases from mineral structures, pore spaces or fluid inclusions and the generation of gases from the breakage of mineral bonds during the mechanical breakdown of rocks by moving ice. Here, we investigate the potential release of H2, CO2, CO, and short chain hydrocarbons, particularly CH4, by glacial erosion at rates relevant to chemical weathering and microbial activity beneath glaciers. A wide range of magmatic, metamorphic, and sedimentary rocks, and subglacial sediments from glaciated catchments in Greenland, Norway and Canada were ground in the laboratory to varying grain sizes and the release of gases was measured. The volume of gas released increased as the grain size of the ground sediments decreased. The results of these laboratory experiments were used to estimate rates of catchment-scale gas release based upon estimates of long term abrasion rates at each glacier. H2 generation was calculated to be sufficient to potentially support previously estimated rates of methanogenesis in the upper centimeters of subglacial sediment at a gneissic catchment in Greenland and a sedimentary catchment in Canada. Sufficient CO2 could be released by grinding to drive as much as 20% of subglacial chemical weathering at a metamorphic catchment in Svalbard, with potential implications for the inferred quantity of CO2 drawn-down from the atmosphere by glacial weathering. Rates of CH4 generation from grinding bedrock has the potential to be greater than subglacial microbial generation in a sedimentary catchment in Canada with carbon rich bedrock, suggesting a potentially important source of CH4 for methanotrophic microorganisms. We conclude that mechanical erosion beneath a range of glaciers generates significant quantities of gases which have the potential to enhance chemical weathering and/or support subglacial microbial communities in the deep icy biosphere.

Rock glaciers are periglacial alpine landforms that are found in many locations worldwide. Whereas well-developed models of deformation are established for traditional alpine glaciers, rock glacier deformation is poorly understood. Geophysical data from Lone Peak Rock Glacier (LPRG), southwest Montana, USA, are paired with lidar bare-earth 1 m digital elevation model (DEM) analysis to explore potential genetic relationships between internal composition, structure and regularly spaced arcuate transverse ridges expressed at the rock glacier surface. The internal composition of LPRG is heterogeneous, with frozen debris and clean ice overlain by an unconsolidated talus mantle. Upslope-dipping, clearly distinguished reflectors in the ground-penetrating radar (GPR) longitudinal survey at LPRG correspond to transverse ridges. The spacing and slope of individual features at the surface and in the subsurface were measured and compared and are found to be similar. The structures observed at LPRG and other rock glaciers are similar to structures detected in glaciotectonically altered sediment, ice-cored moraines and other rock glacier settings. This finding suggests that transverse ridges on rock glaciers may be used as geomorphic indicators of internal deformation. This study contributes to the body of research on the application of GPR to rock glaciers, and is the first to directly pair and analyze individual surface topographic features with internal structures.

Two ∼4 m vertical sequences of basal ice were collected from tunnels dug into the northern lateral margin of Taylor Glacier, McMurdo Dry Valleys, Antarctica. In both cases the basal sequences exhibit two contrasting ice facies groups; clean (debris-free) and banded dispersed (debris-rich). Debris-rich ices exhibit elevated CO2 and depleted O2 concentrations compared to the clean facies. Bacterial cell numbers, respiration rates, and nutrient concentrations are highest in debris-rich layers. Together, our geochemical and biological data indicate that microbial heterotrophic respiration is likely occurring in situ within the basal ice matrix at ambient temperatures near −15°C. This implies that the basal ice zone of polar glaciers and larger ice sheets is a viable subglacial microbial habitat and active biome of significant volume that has not previously been considered.

Measurement of gases entrapped in clean ice from basal portions of the Taylor Glacier, Antarctica, revealed that CO2 ranged from 229 to 328 ppmv and O2 was near 20% of the gas volume. In contrast, vertically adjacent sections of the sediment laden basal ice contained much higher concentrations of CO2 (60,000 to 325,000 ppmv), whereas O2 represented 4 to 18% of the total gas volume. The deviation in gas composition from atmospheric values occurred concurrently with increased microbial cell concentrations in the basal ice profile, suggesting that in situ microbial processes (i.e., aerobic respiration) may have altered the entrapped gas composition. Molecular characterization of 16S rRNA genes amplified from samples of the basal ice indicated a low diversity of bacteria, and most of the sequences characterized (87%) were affiliated with the phylum, Firmicutes. The most abundant phylotypes in libraries from ice horizons with elevated CO2 and depleted O2 concentrations were related to the genus Paenisporosarcina, and 28 isolates from this genus were obtained by enrichment culturing. Metabolic experiments with Paenisporosarcina sp. TG14 revealed its capacity to conduct macromolecular synthesis when frozen in water derived from melted basal ice samples and incubated at −15 °C. The results support the hypothesis that the basal ice of glaciers and ice sheets are cryospheric habitats harboring bacteria with the physiological capacity to remain metabolically active and biogeochemically cycle elements within the subglacial environment.

The abundance of water at the base of glaciers and polar ice sheets forms lacustrine features and habitats in the saturated sediments of subglacial hydrological systems. Nutrients and energy sources may be made available through mineralization of stored organic matter or through glacial processes (e.g., bedrock comminution) that provide redox couples for microbial life. The logistical challenges of accessing subglacial environments has limited direct observations to a small number of locations, but microorganisms and associated microbial activities have been found in all subglacial environments examined to date (i.e., basal ice and sediment cores, subglacial lakes, and subglacial outflows at glacial margins). Molecular and biogeochemical data imply that the microbial clades common in subglacial environments are utilizing reduced iron, sulfur, and nitrogen compounds as energy sources to fuel primary production at the glacial bed. Here, we review the latest information on the diversity of subglacial environments and discuss how interactions between physical and biogeochemical processes affect microbial ecosystems and processes at the glacier bed.

Summary The habitability of icy environments may be limited by low temperature, low nutrient concentrations, high solute concentrations and the physical ice matrix. The basal ice of ice sheets and glaciers contains sediments that may be a source of nutrients for microbial activity. Here we quantify microbial respiration and active cell populations of Antarctic glacial isolates Paenisporosarcina sp. B5 and Chryseobacterium sp. V3519-10 in laboratory ices with abundant nutrients at temperatures from −4°C to −33°C. At all temperatures, initial high rates of metabolism were followed by lower rates suggestive of a non-reproductive metabolic state such as maintenance or dormancy. Metabolism was sustained by viable cells as quantified via culturability, CTC reduction and LIVE/DEAD staining. Respiration rates based on active cell populations did not correspond to rates representative of reproductive growth from the literature, but suggested lower levels of metabolism. Our data demonstrated that bacteria actively respired acetate in polycrystalline ice with abundant nutrients despite low temperatures and the physical ice matrix. Our results suggest that the debris-rich basal ice that exists at temperatures just below the freezing point and underlies portions of both the Greenland and Antarctic ice sheets represents a significant potential habitat for metabolically active microbial communities.

Summary Metabolic activity, but not growth, has been observed in ice at temperatures from −5°C to −32°C. To improve understanding of metabolism in ice, we simultaneously examined various aspects of metabolism (14C-acetate utilization, macromolecule syntheses and viability via reduction of CTC) of the glacial isolates Sporosarcina sp. B5 and Chryseobacterium sp. V3519-10 during incubation in nutrient-rich ice and brine at −5°C for 50 days. Measured rates of acetate utilization and macromolecule syntheses were high in the first 20 days suggesting adjustment to the lower temperatures and higher salt concentrations of both the liquid vein network in the ice and the brine. Following this adjustment, reproductive growth of both organisms was evident in brine, and suggested for Sporosarcina sp. B5 in ice by increases in cell numbers and biomass. Chryseobacterium sp. V3519-10 cells incubated in ice remained active. These data indicate that neither low temperature nor high salt concentrations prohibit growth in ice, but some other aspect of living within ice slows growth to within the detection limits of current methodologies. These results imply that microbial growth is plausible in natural ice systems with comparable temperatures and sufficient nutrients, such as debris-rich basal ices of glaciers and ice masses.

Microbes live under glaciers that have persisted for millions of years, without a clear energy supply. Analyses of crushed rocks suggest that interactions of glaciers with the rocks beneath can produce enough H2 to support methanogenic bacteria. Substantial parts of the beds of glaciers, ice sheets and ice caps are at the pressure melting point1. The resulting water harbours diverse subglacial microbial ecosystems2,3 capable of affecting global biogeochemical cycles4,5. Such subglacial habitats may have acted as refugia during Neoproterozoic glaciations6. However, it is unclear how life in subglacial environments could be supported during glaciations lasting millions of years because energy from overridden organic carbon would become increasingly depleted7,8. Here we investigate the potential for abiogenic H2 produced during rock comminution to provide a continual source of energy to support subglacial life. We collected a range of silicate rocks representative of subglacial environments in Greenland, Canada, Norway and Antarctica and crushed them with a sledgehammer and ball mill to varying surface areas. Under an inert atmosphere in the laboratory, we added water, and measured H2 production with time. H2 was produced at 0 °C in all silicate–water experiments, probably through the reaction of water with mineral surface silica radicals formed during rock comminution. H2 production increased with increasing temperature or decreasing silicate rock grain size. Sufficient H2 was produced to support previously measured rates of methanogenesis under a Greenland glacier. We conclude that abiogenic H2 generation from glacial bedrock comminution could have supported life and biodiversity in subglacial refugia during past extended global glaciations.

This paper describes the physical and chemical properties of the snow- pack on John Evans Glacier, Ellesmere Island, Canadian Arctic Archipelago, and investigates the controls on snowpack solute concentrations and atmospheric deposition. The snowpack contains three layers that are traceable across the whole glacier. These represent fall accumulation that has been metamorphosed to depth hoar, winter accumulation mixed with snow reworked by wind from the underlying depth hoar, and spring accumulation mixed with wind-reworked snow. The seasonal cycle in snow chemistry closely reflects changes in the composition of the atmospheric aerosol at Alert, with some modification of NO3− concentrations by post-depositional processes. Mean water-weighted solute concentrations in the snowpack are largely independent of accumulation, while atmospheric deposition tends to increase with accumulation. This suggests that, for most species, wet deposition is the dominant depositional process throughout the year. However, concentrations of Ca2+ and K+ increase with both accumulation and elevation, implying an enhanced input from dry deposition of soil dust above 800 m elevation. Concentrations of SO42− are inversely related to accumulation, especially in the winter layer, suggesting a significant input from non-precipitating events, such as dry deposition or riming, during this period of very limited snowfall.

The debris-rich basal ice layers of a high Arctic glacier were shown to contain metabolically diverse microbes that could be cultured oligotrophically at low temperatures (0.3 to 4°C). These organisms included aerobic chemoheterotrophs and anaerobic nitrate reducers, sulfate reducers, and methanogens. Colonies purified from subglacial samples at 4°C appeared to be predominantly psychrophilic. Aerobic chemoheterotrophs were metabolically active in unfrozen basal sediments when they were cultured at 0.3°C in the dark (to simulate nearly in situ conditions), producing 14 CO 2 from radiolabeled sodium acetate with minimal organic amendment (≥38 μM C). In contrast, no activity was observed when samples were cultured at subfreezing temperatures (≤−1.8°C) for 66 days. Electron microscopy of thawed basal ice samples revealed various cell morphologies, including dividing cells. This suggests that the subglacial environment beneath a polythermal glacier provides a viable habitat for life and that microbes may be widespread where the basal ice is temperate and water is present at the base of the glacier and where organic carbon from glacially overridden soils is present. Our observations raise the possibility that in situ microbial production of CO 2 and CH 4 beneath ice masses (e.g., the Northern Hemisphere ice sheets) is an important factor in carbon cycling during glacial periods. Moreover, this terrestrial environment may provide a model for viable habitats for life on Mars, since similar conditions may exist or may have existed in the basal sediments beneath the Martian north polar ice cap.

Measurements made at John Evans Glacier, eastern Ellesmere Island, Nunavut, Canada in 1994 and 1996 provide new insight into the internal hydrology of polythermal glaciers. During the early part of each melt season, supraglacial waters enter the glacier via a crevasse field about 4 km from the terminus and are stored in a subglacial reservoir. Release of the water from the reservoir occurs initially via an artesian fountain on the glacier surface and by upwelling of waters through subglacial sediments at the terminus (event1). Channelization of the subglacial waters then occurs and water is discharged as an outburst flood (event 2), which releases a considerably larger volume of water than event 1. Thus, drainage of the subglacial reservoir follows a cyclical pattern in which discharge oscillations increase in amplitude over time. The cycle may end with complete reservoir drainage. The total volume of water released was much greater in 1994 than in 1996, primarily because the 1994 melt season was longer and warmer than the 1996 season. Interannual differences in the form of the outflow hydrographs, and in the extent and timing of connections between the subglacial reservoir and marginal melt streams, are linked to variations in the size and rate of growth of the subglacial reservoir. This hydrological behaviour may have important implications for the dynamics of polythermal glaciers.

Liquid water has been known to occur beneath the Antarctic ice sheet for more than 40 years, but only recently have these subglacial aqueous environments been recognized as microbial ecosystems that may influence biogeochemical transformations on a global scale. Here we present the first geomicrobiological description of water and surficial sediments obtained from direct sampling of a subglacial Antarctic lake. Subglacial Lake Whillans (SLW) lies beneath approximately 800 m of ice on the lower portion of the Whillans Ice Stream (WIS) in West Antarctica and is part of an extensive and evolving subglacial drainage network. The water column of SLW contained metabolically active microorganisms and was derived primarily from glacial ice melt with solute sources from lithogenic weathering and a minor seawater component. Heterotrophic and autotrophic production data together with small subunit ribosomal RNA gene sequencing and biogeochemical data indicate that SLW is a chemosynthetically driven ecosystem inhabited by a diverse assemblage of bacteria and archaea. Our results confirm that aquatic environments beneath the Antarctic ice sheet support viable microbial ecosystems, corroborating previous reports suggesting that they contain globally relevant pools of carbon and microbes that can mobilize elements from the lithosphere and influence Southern Ocean geochemical and biological systems.

Geologic, chemical and isotopic evidence indicate that Earth has experienced numerous intervals of widespread glaciation throughout its history, with roughly 11% of present day Earth’s land surface covered in ice. Despite the pervasive nature of glacial ice both today and in Earth’s past and the potential contribution of these systems to global biogeochemical cycles, the composition and phylogenetic structure of an active microbial community in subglacial systems has yet to be described. Here, using RNA-based approaches, we demonstrate the presence of active and endogenous archaeal, bacterial and eukaryal assemblages in cold (0–1 °C) subglacial sediments sampled from Robertson Glacier, Alberta, Canada. Patterns in the phylogenetic structure and composition of subglacial sediment small subunit (SSU) ribosomal RNA (rRNA) assemblages indicate greater diversity and evenness than in glacial surface environments, possibly due to facilitative or competitive interactions among populations in the subglacial environment. The combination of phylogenetically more even and more diverse assemblages in the subglacial environment suggests minimal niche overlap and optimization to capture a wider spectrum of the limited nutrients and chemical energy made available from weathering of bedrock minerals. The prevalence of SSU rRNA affiliated with lithoautotrophic bacteria, autotrophic methane producing archaea and heterotrophic eukarya in the subglacial environment is consistent with this hypothesis and suggests an active contribution to the global carbon cycle. Collectively, our findings demonstrate that subglacial environments harbor endogenous active ecosystems that have the potential to impact global biogeochemical cycles over extended periods of time.

Polycrystalline ice, as found in glaciers and the ice sheets of Antarctica, is a low porosity porous media consisting of a complicated and dynamic pore structure of liquid-filled intercrystalline veins within a solid ice matrix. In this work, Nuclear Magnetic Resonance measurements of relaxation rates and molecular diffusion, useful for probing pore structure and transport dynamics in porous systems, were used to physically characterize the unfrozen vein network structure in ice and its response to the presence of metabolic products produced by V3519-10, a cold tolerant microorganism isolated from the Vostok ice core. Recent research has found microorganisms that can remain viable and even metabolically active within icy environments at sub-zero temperatures. One potential mechanism of survival for V3519-10 is secretion of an extracellular ice binding protein that binds to the prism face of ice crystals and inhibits ice recrystallization, a coarsening process resulting in crystal growth with ice aging. Understanding the impact of ice binding activity on the bulk vein network structure in ice is important to modeling of frozen geophysical systems and in development of ice interacting proteins for biotechnology applications, such as cryopreservation of cell lines, and manufacturing processes in food sciences. Here, we present the first observations of recrystallization inhibition in low porosity ice containing V3519-10 extracellular protein extract as measured with Nuclear Magnetic Resonance and Magnetic Resonance Imaging.

Cryopreservation of microorganisms in ancient glacial ice is possible if lethal levels of macromolecular damage are not incurred and cellular integrity is not compromised via intracellular ice formation or recrystallization. Previously, a bacterium (isolate 3519-10) recovered from a depth of 3,519 m below the surface in the Vostok ice core was shown to secrete an ice-binding protein (IBP) that inhibits the recrystallization of ice. To explore the advantage that IBPs confer to ice-entrapped cells, experiments were designed to examine the expression of 3519-10's IBP gene and protein at different temperatures, assess the effect of the IBP on bacterial viability in ice, and determine how the IBP influences the physical structure of the ice. Total RNA isolated from cultures grown between 4 and 25°C and analyzed by reverse transcription-PCR indicated constitutive expression of the IBP gene. Sodium dodecyl sulfate-polyacrylamide gel electrophoretic analysis of 3519-10's extracellular proteins revealed a polypeptide of the predicted size of the 54-kDa IBP at all temperatures tested. In the presence of 100 μg mL(-1) of extracellular protein from 3519-10, the survival of Escherichia coli was increased by greater than 100-fold after 5 freeze-thaw cycles. Microscopic analysis of ice formed in the presence of the IBP indicated that per square millimeter field of view, there were ~5 times as many crystals as in ice formed in the presence of washed 3519-10 cells and non-IBP producing bacteria, and ~10 times as many crystals as in filtered deionized water. Presumably, the effect that the IBP has on bacterial viability and ice crystal structure is due to its activity as an inhibitor of ice recrystallization. A myriad of molecular adaptations are likely to play a role in bacterial persistence under frozen conditions, but the ability of 3519-10's IBP to control ice crystal structure, and thus the liquid vein network within the ice, may provide one explanation for its successful survival deep within the Antarctic ice sheet for thousands of years.

[1] The basal regions of continental ice sheets are gaps in our current understanding of the Earth’s biosphere and biogeochemical cycles. We draw on existing and new chemical data sets for subglacial meltwaters to provide the first comprehensive assessment of sub‐ice sheet biogeochemical weathering. We show that size of the ice mass is a critical control on the balance of chemical weathering processes and that microbial activity is ubiquitous in driving dissolution. Carbonate dissolution fueled by sulfide oxidation and microbial CO2 dominate beneath small valley glaciers. Prolonged meltwater residence times and greater isolation characteristic of ice sheets lead to the development of anoxia and enhanced silicate dissolution due to calcite saturation. We show that sub‐ice sheet environments are highly geochemically reactive and should be considered in regional and global solute budgets. For example, calculated solute fluxes from Antarctica (72–130 t yr −1 ) are the same order of magnitude as those from some of the world’s largest rivers and rates of chemical weathering (10–17 t km −2 yr −1 ) are high for the annual specific discharge (2.3–4.1 × 10 −3 m). Our model of chemical weathering dynamics provides important information on subglacial biodiversity and global biogeochemical cycles and may be used to design strategies for the first sampling of Antarctic Subglacial Lakes and other sub‐ice sheet environments for the next decade.

[1] Glacial meltwaters draining shield bedrock under the Greenland Ice Sheet (GIS) contain

Viable microbes have been detected beneath several geographically distant glaciers underlain by different lithologies, but comparisons of their microbial communities have not previously been made. This study compared the microbial community compositions of samples from two glaciers overlying differing bedrock. Bulk meltwater chemistry indicates that sulfide oxidation and carbonate dissolution account for 90% of the solute flux from Bench Glacier, Alaska, whereas gypsum/anhydrite and carbonate dissolution accounts for the majority of the flux from John Evans Glacier, Ellesmere Island, Nunavut, Canada. The microbial communities were examined using two techniques: clone libraries and dot blot hybridization of 16S rRNA genes. Two hundred twenty-seven clones containing amplified 16S rRNA genes were prepared from subglacial samples, and the gene sequences were analyzed phylogenetically. Although some phylogenetic groups, including the Betaproteobacteria , were abundant in clone libraries from both glaciers, other well-represented groups were found at only one glacier. Group-specific oligonucleotide probes were developed for two phylogenetic clusters that were of particular interest because of their abundance or inferred biochemical capabilities. These probes were used in quantitative dot blot hybridization assays with a range of samples from the two glaciers. In addition to shared phyla at both glaciers, each glacier also harbored a subglacial microbial population that correlated with the observed aqueous geochemistry. These results are consistent with the hypothesis that microbial activity is an important contributor to the solute flux from glaciers.

We describe a viable microbial community in a subglacial lake within the Grímsvötn volcanic caldera, Iceland. We used a hot water drill to penetrate the 300-m ice shelf and retrieved lake water and volcanic tephra sediments. We also acquired samples of borehole water before and after penetration to the lake, overlying glacial ice and snow, and water from a nearby subaerial geothermal lake for comparative analyses. Lake water is at the freezing point and fresh (total dissolved solids = 260 mg L(-1)). Detectable numbers of cells were found in samples of the lake water column and tephra sediments: 2 x 10(4) ml(-1) and 4 x 10(7) g(-1), respectively. Plate counts document abundant cold-adapted cultivable organisms in the lake water, but not in the borehole (before penetration) or glacial ice. Denaturing gradient gel electrophoresis (DGGE) of 16S rRNA gene fragments amplified from genomic DNA extracted from Grímsvötn samples indicates that the lake community is distinct from the assemblages of organisms in borehole water (before penetration) and the overlying ice and snow. Sequencing of selected DGGE bands revealed that many sequences are highly similar to known psychrophilic organisms or cloned DNA from other cold environments. Significant uptake of 14C-labeled bicarbonate occurred in dark, low-temperature incubations of lake water samples, indicating the presence of autotrophs. Acetylene reduction assays under similar incubation conditions showed no significant nitrogen fixation potential by lake water samples. This may be a consequence of the inhibition of diazotrophy by nitrogen in the lake.