Microbial assemblages and associated biogeochemical processes in Lake Bonney, a permanently ice-covered lake in the McMurdo Dry Valleys, Antarctica.

BACKGROUND: Lake Bonney, which is divided into a west lobe (WLB) and an east lobe (ELB), is a perennially ice-covered lake located in the McMurdo Dry Valleys of Antarctica. Despite previous reports on the microbial community dynamics of ice-covered lakes in this region, there is a paucity of information on the relationship between microbial genomic diversity and associated nutrient cycling. Here, we applied gene- and genome-centric approaches to investigate the microbial ecology and reconstruct microbial metabolic potential along the depth gradient in Lake Bonney. RESULTS: Lake Bonney is strongly chemically stratified with three distinct redox zones, yielding different microbial niches. Our genome enabled approach revealed that in the sunlit and relatively freshwater epilimnion, oxygenic photosynthetic production by the cyanobacterium Pseudanabaena and a diversity of protists and microalgae may provide new organic carbon to the environment. CO-oxidizing bacteria, such as Acidimicrobiales, Nanopelagicales, and Burkholderiaceae were also prominent in the epilimnion and their ability to oxidize carbon monoxide to carbon dioxide may serve as a supplementary energy conservation strategy. In the more saline metalimnion of ELB, an accumulation of inorganic nitrogen and phosphorus supports photosynthesis despite relatively low light levels. Conversely, in WLB the release of organic rich subglacial discharge from Taylor Glacier into WLB would be implicated in the possible high abundance of heterotrophs supported by increased potential for glycolysis, beta-oxidation, and glycoside hydrolase and may contribute to the growth of iron reducers in the dark and extremely saline hypolimnion of WLB. The suboxic and subzero temperature zones beneath the metalimnia in both lobes supported microorganisms capable of utilizing reduced nitrogens and sulfurs as electron donors. Heterotrophs, including nitrate reducing sulfur oxidizing bacteria, such as Acidimicrobiales (MAG72) and Salinisphaeraceae (MAG109), and denitrifying bacteria, such as Gracilimonas (MAG7), Acidimicrobiales (MAG72) and Salinisphaeraceae (MAG109), dominated the hypolimnion of WLB, whereas the environmental harshness of the hypolimnion of ELB was supported by the relatively low in metabolic potential, as well as the abundance of halophile Halomonas and endospore-forming Virgibacillus. CONCLUSIONS: The vertical distribution of microbially driven C, N and S cycling genes/pathways in Lake Bonney reveals the importance of geochemical gradients to microbial diversity and biogeochemical cycles with the vertical water column.

Trace element, rare earth element and trace carbon compounds in Subglacial Lake Whillans, West Antarctica.

Whillans Subglacial Lake (SLW) lies beneath 801 m of ice in the lower portion of the Whillans Ice Stream (WIS) in West Antarctica and is part of an extensive and active subglacial drainage network. Here, the geochemical characterization of SLW rare earth elements (REE), trace elements (TE), free amino acids (FAA), and phenolic compounds (PC) measured in lakewater and sediment porewater are reported. The results show, on average, higher values of REEs in the lakewater than in the porewater, and clear changes in all REE concentrations and select redox sensitive trace element concentrations in porewaters at a depth of ~15 cm in the 38 cm lake sediment core. This is consistent with prior results on the lake sediment redox conditions based on gas chemistry and microbiological data. Low concentrations of vanillyl phenols were measured in the SLW water column with higher concentrations in porewater samples and their concentration profiles in the sediments may also reflect changing redox conditions in the sediments. Vanillin concentrations increased with depth in the sediments as oxygenation decreases, while the concentrations of vanillic acid, the more oxidized component, were higher in the more oxygenated surface sediments. Collectively these results indicate redox changes occurring with the upper 38 cm of sediment in SLW and provide support for the existence of a seawater source, already hypothesized, in the sediments below the lowest measured depth, and of a complex and dynamic geochemical system beneath the West Antarctic Ice Sheet. Our results are the first to detail geochemical properties from an Antarctic subglacial environment using direct sampling technology. Due to their isolation from the wider environment, subglacial lakes represent one of our planets last pristine environments that provide habitats for microbial life and natural biogeochemical cycles but also impact the basal hydrology and can cause ice flow variations.

Postglacial adaptations enabled colonization and quasi-clonal dispersal of ammonia-oxidizing archaea in modern European large lakes.

Ammonia-oxidizing archaea (AOA) play a key role in the aquatic nitrogen cycle. Their genetic diversity is viewed as the outcome of evolutionary processes that shaped ancestral transition from terrestrial to marine habitats. However, current genome-wide insights into AOA evolution rarely consider brackish and freshwater representatives or provide their divergence timeline in lacustrine systems. An unbiased global assessment of lacustrine AOA diversity is critical for understanding their origins, dispersal mechanisms, and ecosystem roles. Here, we leveraged continental-scale metagenomics to document that AOA species diversity in freshwater systems is remarkably low compared to marine environments. We show that the uncultured freshwater AOA, "Candidatus Nitrosopumilus limneticus," is ubiquitous and genotypically static in various large European lakes where it evolved 13 million years ago. We find that extensive proteome remodeling was a key innovation for freshwater colonization of AOA. These findings reveal the genetic diversity and adaptive mechanisms of a keystone species that has survived clonally in lakes for millennia.

Biogeochemical and historical drivers of microbial community composition and structure in sediments from Mercer Subglacial Lake, West Antarctica.

Ice streams that flow into Ross Ice Shelf are underlain by water-saturated sediments, a dynamic hydrological system, and subglacial lakes that intermittently discharge water downstream across grounding zones of West Antarctic Ice Sheet (WAIS). A 2.06 m composite sediment profile was recently recovered from Mercer Subglacial Lake, a 15 m deep water cavity beneath a 1087 m thick portion of the Mercer Ice Stream. We examined microbial abundances, used 16S rRNA gene amplicon sequencing to assess community structures, and characterized extracellular polymeric substances (EPS) associated with distinct lithologic units in the sediments. Bacterial and archaeal communities in the surficial sediments are more abundant and diverse, with significantly different compositions from those found deeper in the sediment column. The most abundant taxa are related to chemolithoautotrophs capable of oxidizing reduced nitrogen, sulfur, and iron compounds with oxygen, nitrate, or iron. Concentrations of dissolved methane and total organic carbon together with water content in the sediments are the strongest predictors of taxon and community composition. δ¹³C values for EPS (-25 to -30‰) are consistent with the primary source of carbon for biosynthesis originating from legacy marine organic matter. Comparison of communities to those in lake sediments under an adjacent ice stream (Whillans Subglacial Lake) and near its grounding zone provide seminal evidence for a subglacial metacommunity that is biogeochemically and evolutionarily linked through ice sheet dynamics and the transport of microbes, water, and sediments beneath WAIS.

Antarctic lake phytoplankton and bacteria from near-surface waters exhibit high sensitivity to climate-driven disturbance.

The McMurdo Dry Valleys (MDVs), Antarctica, represent a cold, desert ecosystem poised on the threshold of melting and freezing water. The MDVs have experienced dramatic signs of climatic change, most notably a warm austral summer in 2001-2002 that caused widespread flooding, partial ice cover loss and lake level rise. To understand the impact of these climatic disturbances on lake microbial communities, we simulated lake level rise and ice-cover loss by transplanting dialysis-bagged communities from selected depths to other locations in the water column or to an open water perimeter moat. Bacteria and eukaryote communities residing in the surface waters (5 m) exhibited shifts in community composition when exposed to either disturbance, while microbial communities from below the surface were largely unaffected by the transplant. We also observed an accumulation of labile dissolved organic carbon in the transplanted surface communities. In addition, there were taxa-specific sensitivities: cryptophytes and Actinobacteria were highly sensitive particularly to the moat transplant, while chlorophytes and several bacterial taxa increased in relative abundance or were unaffected. Our results reveal that future climate-driven disturbances will likely undermine the stability and productivity of MDV lake phytoplankton and bacterial communities in the surface waters of this extreme environment.

Organic matter distribution in the icy environments of Taylor Valley, Antarctica.

Glaciers can accumulate and release organic matter affecting the structure and function of associated terrestrial and aquatic ecosystems. We analyzed 18 ice cores collected from six locations in Taylor Valley (McMurdo Dry Valleys), Antarctica to determine the spatial abundance and quality of organic matter, and the spatial distribution of bacterial density and community structure from the terminus of the Taylor Glacier to the coast (McMurdo Sound). Our results showed that dissolved and particulate organic carbon (DOC and POC) concentrations in the ice core samples increased from the Taylor Glacier to McMurdo Sound, a pattern also shown by bacterial cell density. Fluorescence Excitation Emission Matrices Spectroscopy (EEMs) and multivariate parallel factor (PARAFAC) modeling identified one humic-like (C1) and one protein-like (C2) component in ice cores whose fluorescent intensities all increased from the Polar Plateau to the coast. The fluorescence index showed that the bioavailability of dissolved organic matter (DOM) also decreased from the Polar Plateau to the coast. Partial least squares path modeling analysis revealed that bacterial abundance was the main positive biotic factor influencing both the quantity and quality of organic matter. Marine aerosol influenced the spatial distribution of DOC more than katabatic winds in the ice cores. Certain bacterial taxa showed significant correlations with DOC and POC concentrations. Collectively, our results show the tight connectivity among organic matter spatial distribution, bacterial abundance and meteorology in the McMurdo Dry Valley ecosystem.

A Perspective of the Cumulative Risks from Climate Change on Mt. Everest: Findings from the 2019 Expedition.

In 2019, the National Geographic and Rolex Perpetual Planet Everest expedition successfully retrieved the greatest diversity of scientific data ever from the mountain. The confluence of geologic, hydrologic, chemical and microbial hazards emergent as climate change increases glacier melt is significant. We review the findings of increased opportunity for landslides, water pollution, human waste contamination and earthquake events. Further monitoring and policy are needed to ensure the safety of residents, future climbers, and trekkers in the Mt. Everest watershed.

Enhanced trace element mobilization by Earth's ice sheets.

Trace elements sustain biological productivity, yet the significance of trace element mobilization and export in subglacial runoff from ice sheets is poorly constrained at present. Here, we present size-fractionated (0.02, 0.22, and 0.45 µm) concentrations of trace elements in subglacial waters from the Greenland Ice Sheet (GrIS) and the Antarctic Ice Sheet (AIS). Concentrations of immobile trace elements (e.g., Al, Fe, Ti) far exceed global riverine and open ocean mean values and highlight the importance of subglacial aluminosilicate mineral weathering and lack of retention of these species in sediments. Concentrations are higher from the AIS than the GrIS, highlighting the geochemical consequences of prolonged water residence times and hydrological isolation that characterize the former. The enrichment of trace elements (e.g., Co, Fe, Mn, and Zn) in subglacial meltwaters compared with seawater and typical riverine systems, together with the likely sensitivity to future ice sheet melting, suggests that their export in glacial runoff is likely to be important for biological productivity. For example, our dissolved Fe concentration (20,900 nM) and associated flux values (1.4 Gmol y-1) from AIS to the Fe-deplete Southern Ocean exceed most previous estimates by an order of magnitude. The ultimate fate of these micronutrients will depend on the reactivity of the dominant colloidal size fraction (likely controlled by nanoparticulate Al and Fe oxyhydroxide minerals) and estuarine processing. We contend that ice sheets create highly geochemically reactive particulates in subglacial environments, which play a key role in trace elemental cycles, with potentially important consequences for global carbon cycling.

Subsurface In Situ Detection of Microbes and Diverse Organic Matter Hotspots in the Greenland Ice Sheet.

We used a deep-ultraviolet fluorescence mapping spectrometer, coupled to a drill system, to scan from the surface to 105 m depth into the Greenland ice sheet. The scan included firn and glacial ice and demonstrated that the instrument is able to determine small (mm) and large (cm) scale regions of organic matter concentration and discriminate spectral types of organic matter at high resolution. Both a linear point cloud scanning mode and a raster mapping mode were used to detect and localize microbial and organic matter "hotspots" embedded in the ice. Our instrument revealed diverse spectral signatures. Most hotspots were <20 mm in diameter, clearly isolated from other hotspots, and distributed stochastically; there was no evidence of layering in the ice at the fine scales examined (100 µm per pixel). The spectral signatures were consistent with organic matter fluorescence from microbes, lignins, fused-ring aromatic molecules, including polycyclic aromatic hydrocarbons, and biologically derived materials such as fulvic acids. In situ detection of organic matter hotspots in ice prevents loss of spatial information and signal dilution when compared with traditional bulk analysis of ice core meltwaters. Our methodology could be useful for detecting microbial and organic hotspots in terrestrial icy environments and on future missions to the Ocean Worlds of our Solar System.

WATSON: In Situ Organic Detection in Subsurface Ice Using Deep-UV Fluorescence Spectroscopy.

Terrestrial icy environments have been found to preserve organic material and contain habitable niches for microbial life. The cryosphere of other planetary bodies may therefore also serve as an accessible location to search for signs of life. The Wireline Analysis Tool for the Subsurface Observation of Northern ice sheets (WATSON) is a compact deep-UV fluorescence spectrometer for nondestructive ice borehole analysis and spatial mapping of organics and microbes, intended to address the heterogeneity and low bulk densities of organics and microbial cells in ice. WATSON can be either operated standalone or integrated into a wireline drilling system. We present an overview of the WATSON instrument and results from laboratory experiments intended to determine (i) the sensitivity of WATSON to organic material in a water ice matrix and (ii) the ability to detect organic material under various thicknesses of ice. The results of these experiments show that in bubbled ice the instrument has a depth of penetration of 10 mm and a detection limit of fewer than 300 cells. WATSON incorporates a scanning system that can map the distribution of organics and microbes over a 75 by 25 mm area. WATSON demonstrates a sensitive fluorescence mapping technique for organic and microbial detection in icy environments including terrestrial glaciers and ice sheets, and planetary surfaces including Europa, Enceladus, or the martian polar caps.

The Antarctic psychrophiles Chlamydomonas spp. UWO241 and ICE-MDV exhibit differential restructuring of photosystem I in response to iron.

Chlamydomonas sp. UWO241 is a psychrophilic alga isolated from the deep photic zone of a perennially ice-covered Antarctic lake (east lobe Lake Bonney, ELB). Past studies have shown that C. sp. UWO241 exhibits constitutive downregulation of photosystem I (PSI) and high rates of PSI-associated cyclic electron flow (CEF). Iron levels in ELB are in the nanomolar range leading us to hypothesize that the unusual PSI phenotype of C. sp. UWO241 could be a response to chronic Fe-deficiency. We studied the impact of Fe availability in C. sp. UWO241, a mesophile, C. reinhardtii SAG11-32c, as well as a psychrophile isolated from the shallow photic zone of ELB, Chlamydomonas sp. ICE-MDV. Under Fe-deficiency, PsaA abundance and levels of photooxidizable P700 (ΔA820/A820) were reduced in both psychrophiles relative to the mesophile. Upon increasing Fe, C. sp. ICE-MDV and C. reinhardtii exhibited restoration of PSI function, while C. sp. UWO241 exhibited only moderate changes in PSI activity and lacked almost all LHCI proteins. Relative to Fe-excess conditions (200 µM Fe2+), C. sp. UWO241 grown in 18 µM Fe2+ exhibited downregulation of light harvesting and photosystem core proteins, as well as upregulation of a bestrophin-like anion channel protein and two CEF-associated proteins (NdsS, PGL1). Key enzymes of starch synthesis and shikimate biosynthesis were also upregulated. We conclude that in response to variable Fe availability, the psychrophile C. sp. UWO241 exhibits physiological plasticity which includes restructuring of the photochemical apparatus, increased PSI-associated CEF, and shifts in downstream carbon metabolism toward storage carbon and secondary stress metabolites.

Distinct Microbial Assemblage Structure and Archaeal Diversity in Sediments of Arctic Thermokarst Lakes Differing in Methane Sources.

Developing a microbial ecological understanding of Arctic thermokarst lake sediments in a geochemical context is an essential first step toward comprehending the contributions of these systems to greenhouse gas emissions, and understanding how they may shift as a result of long term changes in climate. In light of this, we set out to study microbial diversity and structure in sediments from four shallow thermokarst lakes in the Arctic Coastal Plain of Alaska. Sediments from one of these lakes (Sukok) emit methane (CH4) of thermogenic origin, as expected for an area with natural gas reserves. However, sediments from a lake 10 km to the North West (Siqlukaq) produce CH4 of biogenic origin. Sukok and Siqlukaq were chosen among the four lakes surveyed to test the hypothesis that active CH4-producing organisms (methanogens) would reflect the distribution of CH4 gas levels in the sediments. We first examined the structure of the little known microbial community inhabiting the thaw bulb of arctic thermokarst lakes near Barrow, AK. Molecular approaches (PCR-DGGE and iTag sequencing) targeting the SSU rRNA gene and rRNA molecule were used to profile diversity, assemblage structure, and identify potentially active members of the microbial assemblages. Overall, the potentially active (rRNA dominant) fraction included taxa that have also been detected in other permafrost environments (e.g., Bacteroidetes, Actinobacteria, Nitrospirae, Chloroflexi, and others). In addition, Siqlukaq sediments were unique compared to the other sites, in that they harbored CH4-cycling organisms (i.e., methanogenic Archaea and methanotrophic Bacteria), as well as bacteria potentially involved in N cycling (e.g., Nitrospirae) whereas Sukok sediments were dominated by taxa typically involved in photosynthesis and biogeochemical sulfur (S) transformations. This study revealed a high degree of archaeal phylogenetic diversity in addition to CH4-producing archaea, which spanned nearly the phylogenetic extent of currently recognized Archaea phyla (e.g., Euryarchaeota, Bathyarchaeota, Thaumarchaeota, Woesearchaeota, Pacearchaeota, and others). Together these results shed light on expansive bacterial and archaeal diversity in Arctic thermokarst lakes and suggest important differences in biogeochemical potential in contrasting Arctic thermokarst lake sediment ecosystems.

Prokaryotes in the WAIS Divide ice core reflect source and transport changes between Last Glacial Maximum and the early Holocene.

We present the first long-term, highly resolved prokaryotic cell concentration record obtained from a polar ice core. This record, obtained from the West Antarctic Ice Sheet (WAIS) Divide (WD) ice core, spanned from the Last Glacial Maximum (LGM) to the early Holocene (EH) and showed distinct fluctuations in prokaryotic cell concentration coincident with major climatic states. The time series also revealed a ~1,500-year periodicity with greater amplitude during the Last Deglaciation (LDG). Higher prokaryotic cell concentration and lower variability occurred during the LGM and EH than during the LDG. A sevenfold decrease in prokaryotic cell concentration coincided with the LGM/LDG transition and the global 19 ka meltwater pulse. Statistical models revealed significant relationships between the prokaryotic cell record and tracers of both marine (sea-salt sodium [ssNa]) and burning emissions (black carbon [BC]). Collectively, these models, together with visual observations and methanosulfidic acid (MSA) measurements, indicated that the temporal variability in concentration of airborne prokaryotic cells reflected changes in marine/sea-ice regional environments of the WAIS. Our data revealed that variations in source and transport were the most likely processes producing the significant temporal variations in WD prokaryotic cell concentrations. This record provided strong evidence that airborne prokaryotic cell deposition differed during the LGM, LDG, and EH, and that these changes in cell densities could be explained by different environmental conditions during each of these climatic periods. Our observations provide the first ice-core time series evidence for a prokaryotic response to long-term climatic and environmental processes.

Early diverging lineages within Cryptomycota and Chytridiomycota dominate the fungal communities in ice-covered lakes of the McMurdo Dry Valleys, Antarctica.

Antarctic ice-covered lakes are exceptional sites for studying the ecology of aquatic fungi under conditions of minimal human disturbance. In this study, we explored the diversity and community composition of fungi in five permanently covered lake basins located in the Taylor and Miers Valleys of Antarctica. Based on analysis of the 18S rRNA sequences, we showed that fungal taxa represented between 0.93% and 60.32% of the eukaryotic sequences. Cryptomycota and Chytridiomycota dominated the fungal communities in all lakes; however, members of Ascomycota, Basidiomycota, Zygomycota, and Blastocladiomycota were also present. Of the 1313 fungal OTUs identified, the two most abundant, belonging to LKM11 and Chytridiaceae, comprised 74% of the sequences. Significant differences in the community structure were determined among lakes, water depths, habitat features (i.e., brackish vs. freshwaters), and nucleic acids (DNA vs. RNA), suggesting niche differentiation. Network analysis suggested the existence of strong relationships among specific fungal phylotypes as well as between fungi and other eukaryotes. This study sheds light on the biology and ecology of basal fungi in aquatic systems. To our knowledge, this is the first report showing the predominance of early diverging lineages of fungi in pristine limnetic ecosystems, particularly of the enigmatic phylum Cryptomycota.

Decadal ecosystem response to an anomalous melt season in a polar desert in Antarctica.

Amplified climate change in polar regions is significantly altering regional ecosystems, yet there are few long-term records documenting these responses. The McMurdo Dry Valleys (MDV) cold desert ecosystem is the largest ice-free area of Antarctica, comprising soils, glaciers, meltwater streams and permanently ice-covered lakes. Multi-decadal records indicate that the MDV exhibited a distinct ecosystem response to an uncharacteristic austral summer and ensuing climatic shift. A decadal summer cooling phase ended in 2002 with intense glacial melt ('flood year')-a step-change in water availability triggering distinct changes in the ecosystem. Before 2002, the ecosystem exhibited synchronous behaviour: declining stream flow, decreasing lake levels, thickening lake ice cover, decreasing primary production in lakes and streams, and diminishing soil secondary production. Since 2002, summer air temperatures and solar flux have been relatively consistent, leading to lake level rise, lake ice thinning and elevated stream flow. Biological responses varied; one stream cyanobacterial mat type immediately increased production, but another stream mat type, soil invertebrates and lake primary productivity responded asynchronously a few years after 2002. This ecosystem response to a climatic anomaly demonstrates differential biological community responses to substantial perturbations, and the mediation of biological responses to climate change by changes in physical ecosystem properties.

Biogeography of cryoconite bacterial communities on glaciers of the Tibetan Plateau.

Cryoconite holes, water-filled pockets containing biological and mineralogical deposits that form on glacier surfaces, play important roles in glacier mass balance, glacial geochemistry and carbon cycling. The presence of cryoconite material decreases surface albedo and accelerates glacier mass loss, a problem of particular importance in the rapidly melting Tibetan Plateau. No studies have addressed the microbial community composition of cryoconite holes and their associated ecosystem processes on Tibetan glaciers. To further enhance our understanding of these glacial ecosystems on the Tibetan Plateau and to examine their role in carbon cycling as the glaciers respond to climate change, we explored the bacterial communities within cryoconite holes associated with three climatically distinct Tibetan Plateau glaciers using Illumina sequencing of the V4 region of the 16S rRNA gene. Cryoconite bacterial communities were dominated by Cyanobacteria, Chloroflexi, Betaproteobacteria, Bacteroidetes and Actinobacteria. Cryoconite bacterial community composition varied according to their geographical locations, exhibiting significant differences among glaciers studied. Regional beta diversity was driven by the interaction between geographic distance and environmental variables; the latter contributed more than geographic distance to the variation in cryoconite microbial communities. Our study is the first to describe the regional-scale spatial variability and to identify the factors that drive regional variability of cryoconite bacterial communities on the Tibetan Plateau.

Diversity and Distribution of Freshwater Aerobic Anoxygenic Phototrophic Bacteria across a Wide Latitudinal Gradient.

Aerobic anoxygenic phototrophs (AAPs) have been shown to exist in numerous marine and brackish environments where they are hypothesized to play important ecological roles. Despite their potential significance, the study of freshwater AAPs is in its infancy and limited to local investigations. Here, we explore the occurrence, diversity and distribution of AAPs in lakes covering a wide latitudinal gradient: Mongolian and German lakes located in temperate regions of Eurasia, tropical Great East African lakes, and polar permanently ice-covered Antarctic lakes. Our results show a widespread distribution of AAPs in lakes with contrasting environmental conditions and confirm that this group is composed of different members of the Alpha- and Betaproteobacteria. While latitude does not seem to strongly influence AAP abundance, clear patterns of community structure and composition along geographic regions were observed as indicated by a strong macro-geographical signal in the taxonomical composition of AAPs. Overall, our results suggest that the distribution patterns of freshwater AAPs are likely driven by a combination of small-scale environmental conditions (specific of each lake and region) and large-scale geographic factors (climatic regions across a latitudinal gradient).

Niche specialization of bacteria in permanently ice-covered lakes of the McMurdo Dry Valleys, Antarctica.

Perennially ice-covered lakes in the McMurdo Dry Valleys, Antarctica, are chemically stratified with depth and have distinct biological gradients. Despite long-term research on these unique environments, data on the structure of the microbial communities in the water columns of these lakes are scarce. Here, we examined bacterial diversity in five ice-covered Antarctic lakes by 16S rRNA gene-based pyrosequencing. Distinct communities were present in each lake, reflecting the unique biogeochemical characteristics of these environments. Further, certain bacterial lineages were confined exclusively to specific depths within each lake. For example, candidate division WM88 occurred solely at a depth of 15 m in Lake Fryxell, whereas unknown lineages of Chlorobi were found only at a depth of 18 m in Lake Miers, and two distinct classes of Firmicutes inhabited East and West Lobe Bonney at depths of 30 m. Redundancy analysis revealed that community variation of bacterioplankton could be explained by the distinct conditions of each lake and depth; in particular, assemblages from layers beneath the chemocline had biogeochemical associations that differed from those in the upper layers. These patterns of community composition may represent bacterial adaptations to the extreme and unique biogeochemical gradients of ice-covered lakes in the McMurdo Dry Valleys.

Physiological Ecology of Microorganisms in Subglacial Lake Whillans.

Subglacial microbial habitats are widespread in glaciated regions of our planet. Some of these environments have been isolated from the atmosphere and from sunlight for many thousands of years. Consequently, ecosystem processes must rely on energy gained from the oxidation of inorganic substrates or detrital organic matter. Subglacial Lake Whillans (SLW) is one of more than 400 subglacial lakes known to exist under the Antarctic ice sheet; however, little is known about microbial physiology and energetics in these systems. When it was sampled through its 800 m thick ice cover in 2013, the SLW water column was shallow (~2 m deep), oxygenated, and possessed sufficient concentrations of C, N, and P substrates to support microbial growth. Here, we use a combination of physiological assays and models to assess the energetics of microbial life in SLW. In general, SLW microorganisms grew slowly in this energy-limited environment. Heterotrophic cellular carbon turnover times, calculated from 3H-thymidine and 3H-leucine incorporation rates, were long (60 to 500 days) while cellular doubling times averaged 196 days. Inferred growth rates (average ~0.006 d-1) obtained from the same incubations were at least an order of magnitude lower than those measured in Antarctic surface lakes and oligotrophic areas of the ocean. Low growth efficiency (8%) indicated that heterotrophic populations in SLW partition a majority of their carbon demand to cellular maintenance rather than growth. Chemoautotrophic CO2-fixation exceeded heterotrophic organic C-demand by a factor of ~1.5. Aerobic respiratory activity associated with heterotrophic and chemoautotrophic metabolism surpassed the estimated supply of oxygen to SLW, implying that microbial activity could deplete the oxygenated waters, resulting in anoxia. We used thermodynamic calculations to examine the biogeochemical and energetic consequences of environmentally imposed switching between aerobic and anaerobic metabolisms in the SLW water column. Heterotrophic metabolisms utilizing acetate and formate as electron donors yielded less energy than chemolithotrophic metabolisms when calculated in terms of energy density, which supports experimental results that showed chemoautotrophic activity in excess of heterotrophic activity. The microbial communities of subglacial lake ecosystems provide important natural laboratories to study the physiological and biogeochemical behavior of microorganisms inhabiting cold, dark environments.

Microbial Community Structure of Subglacial Lake Whillans, West Antarctica.

Subglacial Lake Whillans (SLW) is located beneath ∼800 m of ice on the Whillans Ice Stream in West Antarctica and was sampled in January of 2013, providing the first opportunity to directly examine water and sediments from an Antarctic subglacial lake. To minimize the introduction of surface contaminants to SLW during its exploration, an access borehole was created using a microbiologically clean hot water drill designed to reduce the number and viability of microorganisms in the drilling water. Analysis of 16S rRNA genes (rDNA) amplified from samples of the drilling and borehole water allowed an evaluation of the efficacy of this approach and enabled a confident assessment of the SLW ecosystem inhabitants. Based on an analysis of 16S rDNA and rRNA (i.e., reverse-transcribed rRNA molecules) data, the SLW community was found to be bacterially dominated and compositionally distinct from the assemblages identified in the drill system. The abundance of bacteria (e.g., Candidatus Nitrotoga, Sideroxydans, Thiobacillus, and Albidiferax) and archaea (Candidatus Nitrosoarchaeum) related to chemolithoautotrophs was consistent with the oxidation of reduced iron, sulfur, and nitrogen compounds having important roles as pathways for primary production in this permanently dark ecosystem. Further, the prevalence of Methylobacter in surficial lake sediments combined with the detection of methanogenic taxa in the deepest sediment horizons analyzed (34-36 cm) supported the hypothesis that methane cycling occurs beneath the West Antarctic Ice Sheet. Large ratios of rRNA to rDNA were observed for several operational taxonomic units abundant in the water column and sediments (e.g., Albidiferax, Methylobacter, Candidatus Nitrotoga, Sideroxydans, and Smithella), suggesting a potentially active role for these taxa in the SLW ecosystem. Our findings are consistent with chemosynthetic microorganisms serving as the ecological foundation in this dark subsurface environment, providing new organic matter that sustains a microbial ecosystem beneath the West Antarctic Ice Sheet.