Microbiota within the perennial ice cover of Lake Vida, Antarctica

Lake Vida, located in the McMurdo Dry Valleys, Antarctica, is an 'ice-sealed' lake with approximately 19 m of ice covering a highly saline water column (approximately 245 ppt). The lower portions of the ice cover and the lake beneath have been isolated from the atmosphere and land for circa 2800 years. Analysis of microbial assemblages within the perennial ice cover of the lake revealed a diverse array of bacteria and eukarya. Bacterial and eukaryal denaturing gradient gel electrophoresis phylotype profile similarities were low (<59%) between all of the depths compared (five depths spanning 11 m of the ice cover), with the greatest differences occurring between surface and deep ice. The majority of bacterial 16S rRNA gene sequences in the surface ice were related to Actinobacteria (42%) while Gammaproteobacteria (52%) dominated the deep ice community. Comparisons of assemblage composition suggest differences in ice habitability and organismal origin in the upper and lower portions of ice cover. Specifically, the upper ice cover microbiota likely reflect the modern day transport and colonization of biota from the terrestrial landscape, whereas assemblages in the deeper ice are more likely to be persistent remnant biota that originated from the ancient liquid water column of the lake that froze.     

In situ monitoring of microclimate and metabolic activity in lichens from Antarctic extremes: a comparison between South Shetland Islands and the McMurdo Dry Valleys

Lichens are the dominant organisms in terrestrial Antarctic ecosystems and show a decline in species number, coverage, and growth rate from the maritime Antarctic (62°S) to the McMurdo Dry Valleys (78°S). While Livingston Island (maritime Antarctica) is a hot spot for lichen biodiversity, the McMurdo Dry Valleys (continental Antarctica) are known as one of the most extreme environments for life. Previous studies suggest the biodiversity gradient to be linked to water availability acting through length of active period, but no activity data are available for the Dry Valleys. The work presented here compares metabolic activity of lichens at Livingston Island and the Dry Valleys for 4½ months from continuous monitoring that involves concurrent measurements of chlorophyll fluorescence and microclimate. The latitudinal comparison involves two contrasting habitats for plant physiological activity and microclimate. Two species of the foliose genus Umbilicaria were monitored in both regions plus one sample of the crustose Caloplaca in the Dry Valleys. The results showed a very large difference in the duration of activity over the monitoring period, and this supports the different coverage, species abundance, and growth rates already reported for lichens between both regions. Despite this large difference in activity, and in habitat conditions, analysis of the activity behaviour of the two Umbilicaria species shows interesting common features, while the crustose Caloplaca had additional strategies to improve hydration. This offers one explanation for the abundance of crustose lichens inside the Valleys, indicating better adaptation strategies to a polar desert.     

Persistent effects of a discrete warming event on a polar desert ecosystem

A discrete warming event (December 21, 2001–January 12, 2002) in the McMurdo Dry Valleys, Antarctica, enhanced glacier melt, stream flow, and melting of permafrost. Effects of this warming included a rapid rise in lake levels and widespread increases in soil water availability resulting from melting of subsurface ice. These increases in liquid water offset hydrologic responses to a cooling trend experienced over the previous decade and altered ecosystem properties in both aquatic and terrestrial ecosystems. Here, we present hydrological and meteorological data from the McMurdo Dry Valleys Long Term Ecological Research project to examine the influence of a discrete climate event (warming of >2 °C) on terrestrial environments and soil biotic communities. Increases in soil moisture following this event stimulated populations of a subordinate soil invertebrate species (Eudorylaimus antarcticus, Nematoda). The pulse of melt-water had significant influences on Taylor Valley ecosystems that persisted for several years, and illustrates that the importance of discrete climate events, long recognized in hot deserts, are also significant drivers of soil and aquatic ecosystems in polar deserts. Thus, predictions of Antarctic ecosystem responses to climate change which focus on linear temperature trends may miss the potentially significant influence of infrequent climate events on hydrology and linked ecological processes.     

Terrestrial mesofauna in above- and below-ground habitats: Taylor Valley,Antarctica

In the McMurdo Dry Valleys region of Antarctica, above-ground production is often limited to mosses and algae that occur near seasonally available liquid water such as ephemeral streams and ice-covered lakes. Compared to surrounding dry soils these critical transition zones are highly productive and harbor a more diverse assemblage of soil animals, including rotifers, tardigrades, nematodes and microarthropods. Current cooling trends punctuated by warming events, and predicted future climate warming are expected to affect the hydrology of this region and thereby biodiversity and ecosystem functioning. Above-ground communities are exposed to more variable temperature, relative humidity and greater UV radiation, and may be more vulnerable to climate change than sediments beneath, which are buffered from short-term changes. In this study, we compared above- and below-ground communities associated with either moss or cyanobacterial mats along glacial-fed streams and lakes differing in biological complexity (diversity, productivity and habitat suitability). All groups of soil fauna were more abundant in the above-ground material compared to the sediment beneath. Common indicators of habitat suitability (chlorophyll a, soil pH, soil salinity, and soil nitrogen) did not differ between vegetation types but were significantly different among sites. Variables most correlated with invertebrate abundances were sediment salinity, chlorophyll a content and nitrogen concentration. The McMurdo Dry Valleys are expected to become warmer and wetter as a result of climate change. This will likely increase the area of suitable habitat for most soil animals as areas of liquid water potentially increase and become available for longer periods of time.     

Hypolithic microbial communities of quartz rocks from Miers Valley, McMurdo Dry Valleys, Antarctica

The McMurdo Dry Valleys region of eastern Antarctica is a cold desert that presents extreme challenges to life. Hypolithic microbial colonisation of the subsoil surfaces of translucent quartz rocks represent a significant source of terrestrial biomass and productivity in this region. Previous studies have described hypoliths as dominated by cyanobacteria. However, hypoliths that occur in the lower Dry Valleys such as the Miers, Garwood and Marshall Valleys are unusual as they are not necessarily cyanobacteria-dominated. These hypoliths support significant eukaryal colonisation by fungi and mosses in addition to cyanobacteria-dominated bacterial assemblages and so have considerable ecological value in this barren landscape. Here, we characterise these novel hypoliths by analysis of environmental rRNA gene sequences. The hypolithic community was demonstrated to be distinct from the surrounding soil and non-translucent rocks. Hypoliths supported cyanobacterial signatures from the Oscillatoriales and Nostocales. Other heterotrophic bacterial signatures were also recovered, and these were phylogenetically diverse and spanned 8 other bacterial phyla. Archaeal phylotypes recovered were phylogenetically affiliated with the large group of unclassified, uncultured Crenarcheota. Eukaryal phylotypes indicated that free-living ascomycetous fungi, chlorophytes and mosses (Bryum sp.) were all supported by these hypoliths, and these are thought to be responsible for the extensive eukaryotic biomass that develops around quartz rocks.     

Microbial Phototrophic, Heterotrophic, and Diazotrophic Activities Associated with Aggregates in the Permanent Ice Cover of Lake Bonney, Antarctica

Abstract The McMurdo Dry Valley lakes, Antarctica, one of the Earth's southernmost ecosystems containing liquid water, harbor some of the most environmentally extreme (cold, nutrient-deprived) conditions on the planet. Lake Bonney has a permanent ice cover that supports a unique microbial habitat, provided by soil particles blown onto the lake surface from the surrounding, ice-free valley floor. During continuous sunlight summers (Nov.-Feb.), the dark soil particles are heated by solar radiation and melt their way into the ice matrix. Layers and patches of aggregates and liquid water are formed. Aggregates contain a complex cyanobacterial-bacterial community, concurrently conducting photosynthesis (CO2 fixation), nitrogen (N2) fixation, decomposition, and biogeochemical zonation needed to complete essential nutrient cycles. Aggregate-associated CO2- and N2-fixation rates were low and confined to liquid water (i.e., no detectable activities in the ice phase). CO2 fixation was mediated by cyanobacteria; both cyanobacteria and eubacteria appeared responsible for N2 fixation. CO2 fixation was stimulated primarily by nitrogen (NO3-), but also by phosphorus (PO43-). PO43- and iron (FeCl3 + EDTA) enrichment stimulated of N2 fixation. Microautoradiographic and physiological studies indicate a morphologically and metabolically diverse microbial community, exhibiting different cell-specific photosynthetic and heterotrophic activities. The microbial community is involved in physical (particle aggregation) and chemical (establishing redox gradients) modification of a nutrient- and organic matter-enriched microbial "oasis," embedded in the desertlike (i.e., nutrient depleted) lake ice cover. Aggregate-associated production and nutrient cycling represent microbial self-sustenance in a microenvironment supporting "life at the edge," as it is known on Earth.     

Growth of elaborate microbial pinnacles in Lake Vanda,Antarctica

Microbial pinnacles in ice‐covered Lake Vanda, McMurdo Dry Valleys, Antarctica, extend from the base of the ice to more than 50 m water depth. The distribution of microbial communities, their photosynthetic potential, and pinnacle morphology affects the local accumulation of biomass, which in turn shapes pinnacle morphology. This feedback, plus environmental stability, promotes the growth of elaborate microbial structures. In Lake Vanda, all mats sampled from greater than 10 m water depth contained pinnacles with a gradation in size from <1‐mm‐tall tufts to pinnacles that were centimeters tall. Small pinnacles were cuspate, whereas larger ones had variable morphology. The largest pinnacles were up to ~30 cm tall and had cylindrical bases and cuspate tops. Pinnacle biomass was dominated by cyanobacteria from the morphological and genomic groups Leptolyngbya, Phormidium, and Tychonema. The photosynthetic potential of these cyanobacterial communities was high to depths of several millimeters into the mat based on PAM fluorometry, and sufficient light for photosynthesis penetrated ~5 mm into pinnacles. The distribution of photosynthetic potential and its correlation to pinnacle morphology suggests a working model for pinnacle growth. First, small tufts initiate from random irregularities in prostrate mat. Some tufts grow into pinnacles over the course of ~3 years. As pinnacles increase in size and age, their interiors become colonized by a more diverse community of cyanobacteria with high photosynthetic potential. Biomass accumulation within this subsurface community causes pinnacles to swell, expanding laminae thickness and creating distinctive cylindrical bases and cuspate tops. This change in shape suggests that pinnacle morphology emerges from a specific distribution of biomass accumulation that depends on multiple microbial communities fixing carbon in different parts of pinnacles. Similarly, complex patterns of biomass accumulation may be reflected in the morphology of elaborate ancient stromatolites.     

Draft Genome Sequence of Paenisporosarcina sp. Strain TG-14, a Psychrophilic Bacterium Isolated from Sediment-Laden Stratified Basal Ice from Taylor Glacier,McMurdo Dry Valleys,Antarctica

The psychrophilic bacterium Paenisporosarcina sp. TG-14 was isolated from sediment-laden stratified basal ice from Taylor Glacier, McMurdo Dry Valleys, Antarctica. Here we report the draft genome sequence of this strain, which may provide useful information on the cold adaptation mechanism in extremely variable environments.     

Debris-Rich Basal Ice as a Microbial Habitat,Taylor Glacier,Antarctica

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.     

Origin and Phylogeny of Microbes Living in Permanent Antarctic Lake Ice

Abstract The phylogenetic diversity of bacteria and cyanobacteria colonizing sediment particles in the permanent ice cover of an Antarctic lake was characterized by analyses of 16S rRNA genes amplified from environmental DNA. Samples of mineral particles were collected from a depth of 2.5 m in the 4-m-thick ice cover of Lake Bonney, McMurdo Dry Valleys, Antarctica. A rRNA gene clone library of 198 clones was made and characterized by sequencing and oligonucleotide probe hybridization. The library was dominated by representatives of the cyanobacteria, proteobacteria, and Planctomycetales, but also contained diverse clones representing many other microbial groups, including the Acidobacterium/Holophaga division, the Green Non-Sulfur division, and the Actinobacteria. Six oligonucleotide probes were made for the most abundant clades recovered in the library. To determine whether the ice microbial community might originate from wind dispersal of the algal mats found elsewhere in Taylor Valley, the probes were hybridized to 16S rDNAs amplified from three samples of terrestrial cyanobacterial mats collected at nearby sites, as well as to bacterial 16S rDNAs from the lake ice community. The results demonstrate the presence of a diverse microbial community dominated by cyanobacteria in the lake ice, and also show that the dominant members of the lake ice microbial community are found in terrestrial mats elsewhere in the area. The lake ice microbial community appears to be dominated by organisms that are not uniquely adapted to the lake ice ecosystem, but instead are species that originate elsewhere in the surrounding region and opportunistically colonize the unusual habitat provided by the sediments suspended in lake ice. Received: 16 August 1999; Accepted: 28 December 1999; Online Publication: 28 April 2000     

Low-diversity fungal assemblage in an Antarctic Dry Valleys soil

The McMurdo Dry Valleys of Antarctica present extreme environmental challenges. Life is restricted to patchy occurrence of lichens, mosses and invertebrates, plus soil microbial communities. Fungi have been described in lichen symbioses but relatively little is known about the occurrence of free-living soil fungi in the Dry Valleys. A challenge in estimating fungal species richness has been the extent to which estimates based on either cultivation or environmental DNA reflect the active assemblage in cold-arid soils. Here, we describe analysis for inland Dry Valleys soil of environmental DNA and RNA (cDNA) to infer total and putative metabolically active assemblages, respectively, plus cultivation approaches using a variety of laboratory growth conditions. Environmental sequences indicated a highly restricted assemblage of just seven phylotypes that affiliated phylogenetically within two known genera, Helicodendron and Zalerion, plus previously unidentified fungal phylotypes. None of the commonly encountered molds and mitosporic genera recorded from maritime Antarctic locations were encountered. A striking difference was observed in the frequency of recovery for phylotypes between libraries. This suggests that both species richness and beta diversity estimates based on DNA libraries have the potential to misinform putatively active assemblages. Cultivation yielded a cold-tolerant Zalerion strain that affiliated with DNA and RNA library clones, and a psychrotrophic yeast (Debaryomyces hansenii), which was not detected using either culture-independent approach.     

The ecological role of moss in a polar desert: implications for aboveground–belowground and terrestrial–aquatic linkages

The McMurdo Dry Valleys of Antarctica is one of the coldest and driest habitats on the planet. As vascular plants are absent in this region, moss is the main form of aboveground primary production with a potentially important contribution to biogeochemical cycling, yet little is known about their ecological role. To determine the relationship between moss and soil properties relevant to biogeochemistry, we sampled both from a variety of locations in the Dry Valleys. Moss presence was compared to soil properties, and we measured the plasticity of moss stoichiometry (C:N:P) across gradients in nutrient availability. Results demonstrate that many soil properties significantly differed with moss presence, particularly conductivity and pH, but there is no strong evidence that this is caused by the moss presence and not the conditions inherent to the microsites where moss was found. There is great variability in moss stoichiometry, with some significant differences between sites, but generally variability within sites is larger than variation among sites. Results suggest that the main source of moss nutrients is from the soil, rather than water, but correlations with any one nutrient source are weak, suggesting a great deal of plasticity in moss stoichiometry and nutrient uptake.     

Wind dispersal of soil invertebrates in the McMurdo Dry Valleys, Antarctica

Dispersal of soil organisms is crucial for their spatial distribution and adaptation to the prevailing conditions of the Antarctic Dry Valleys. This study investigated the possibility of wind dispersal of soil invertebrates within the dry valleys. Soil invertebrates were evaluated in (1) pockets of transported sediments to lake ice and glacier surfaces, (2) wind-transported dust particles in collection pans (Bundt pans) 100 cm above the soil surface, and (3) sediments transported closer to the surface (<50 cm) and collected in open top chambers (OTCs). Invertebrates were extracted and identified. Nematodes were identified to species and classified according to life stage and sex. Three species of nematodes were recovered and Scottnema lindsayae was the most dominant. There were more juveniles (∼71%) in the transported sediments than adults (29%). Tardigrades and rotifers were more abundant in sediments on lake and glacier surfaces while nematodes were more abundant in the dry sediment collections of Bundt pans and OTCs. The abundance of immobile (dead) nematodes in the Bundt pans and OTCs was three times greater than active (live) nematodes. Anhydrobiosis constitutes a survival mechanism that allows wind dispersal of nematodes in the McMurdo Dry Valleys. Our results show that soil invertebrates are dispersed by wind in the Dry Valleys and are viable in ice communities on lake surfaces and glaciers.     

The Extremophile Endolithella mcmurdoensis gen. et sp. nov. (Trebouxiophyceae,Chlorellaceae), A New Chlorella-like Endolithic Alga From Antarctica

The McMurdo Dry Valleys constitute the largest ice-free region of Antarctica and one of the most extreme deserts on Earth. Despite the low temperatures, dry and poor soils and katabatic winds, some microbes are able to take advantage of endolithic microenvironments, inhabiting the pore spaces of soil and constituting photosynthesis-based communities. We isolated a green microalga, Endolithella mcmurdoensis gen. et sp. nov, from an endolithic sandstone sample collected in the McMurdo Dry Valleys (Victoria Land, East Antarctica) during the K020 expedition, in January 2013. The single non-axenic isolate (E. mcmurdoensis LEGE Z-009) exhibits cup-shaped chloroplasts, electron-dense bodies, and polyphosphate granules but our analysis did not reveal any diagnostic morphological characters. On the basis of phylogenetic analysis of the 18S rRNA (SSU) gene, the isolate was found to represent a new genus within the family Chlorellaceae.     

Review: the Antarctic Chlamydomonas raudensis: an emerging model for cold adaptation of photosynthesis

Permanently cold habitats dominate our planet and psychrophilic microorganisms thrive in cold environments. Environmental adaptations unique to psychrophilic microorganisms have been thoroughly described; however, the vast majority of studies to date have focused on cold-adapted bacteria. The combination of low temperatures in the presence of light is one of the most damaging environmental stresses for a photosynthetic organism: in order to survive, photopsychrophiles (i.e. photosynthetic organisms adapted to low temperatures) balance temperature-independent reactions of light energy capture/transduction with downstream temperature-dependent metabolic processes such as carbon fixation. Here, we review research on photopsychrophiles with a focus on an emerging model organism, Chlamydomonas raudensis UWO241 (UWO241). UWO241 is a psychrophilic green algal species and is a member of the photosynthetic microbial eukaryote community that provides the majority of fixed carbon for ice-covered lake ecosystems located in the McMurdo Dry Valleys, Antarctica. The water column exerts a range of environmental stressors on the phytoplankton community that inhabits this aquatic ecosystem, including low temperatures, extreme shade of an unusual spectral range (blue-green), high salinity, nutrient deprivation and extremes in seasonal photoperiod. More than two decades of work on UWO241 have produced one of our most comprehensive views of environmental adaptation in a cold-adapted, photosynthetic microbial eukaryote.     

Distribution patterns of benthic microalgal standing stock at McMurdo Sound,Antarctica

Summary During the austral summer of 1975–76 and winter of 1977 benthic and water column chlorophyll a and phaeopigments were measured at several sites along the east and west sides of McMurdo Sound, Antarctica. Estimates of in situ primary productivity were made at some McMurdo Sound locations. Additionally, water column samples were collected at 5 stations in the Ross Sea during January, 1976. Standing stock data are analyzed to identify seasonal and spatial patterns. Variability in algal standing stock was related to ambient light levels and appeared to be mediated by ice and snow cover whereby the highest algal standing stock was present under high light conditions (low ice and snow cover, shallow water, summer). Differences in published benthic invertebrate densities appear to be closely allied to differences in benthic primary production, and less so to in situ planktonic ice microalgal production.     

Stratification and dynamics of microbial loop communities in Lake Fryxell, Antarctica

1. Lake Fryxell, situated in the McMurdo Dry Valleys, Antarctica, offers the opportunity to study microbial loop processes in the absence of crustacean zooplankton and other higher organisms. This is the first study of Lake Fryxell to provide detailed temporal and vertical variations of microbial loop organisms.
2. Protozoan communities are concentrated around the chemocline (9–10 m) in Lake Fryxell. Phototrophic nanoflagellates (PNAN), heterotrophic nanoflagellates (HNAN) and ciliates formed deep maxima of 14 580, 694 and 58 cells mL−1 respectively. Although abundance and biomass at the chemocline was high, diversity of protozoa was low, Plagiocampa accounting for> 80% of the total ciliate biomass.
3. In the mixolimnion (4.5–8 m), protozoa were less abundant, but more diverse, with 24 ciliate morphotypes being identified within this region of the water column. Inter-annual variability of protozoan biomass and abundance was greater in the mixolimnion than at the chemocline due to more variable nutrient and prey concentrations.
4. Physicochemical gradients in Lake Fryxell were very stable because the perennial ice cover reduced wind driven currents. As a consequence, ciliate species occurred in distinct depth strata, Monodinium being most abundant directly beneath the ice cover, Askenasia having maximum abundance at 8 m and Plagiocampa dominating ciliate biomass at the chemocline. The lack of vertical mixing reduced seasonal successions of PNAN and ciliate species. Three cryptophyte species dominated the PNAN community at all times (>79% of total biomass).     

Cold-active halophilic bacteria from the ice-sealed Lake Vida,Antarctica

Lake Vida is a large, permanently ice-covered lake in the Victoria Valley of the McMurdo Dry Valleys, Antarctica and is unique among Dry Valley lakes because it is ice-sealed, with an ice-cover of nearly 19 m. Enrichment cultures of melt-water from Lake Vida 15.9 m ice yielded five pure cultures of aerobic, heterotrophic bacteria. Of these, one strain grew at −8°C and the four others at −4°C. All isolates were either halotolerant or halophilic, with two strains capable of growth at 15% NaCl. Phylogenetic analysis revealed the Lake Vida isolates to be Gammaproteobacteria, related to species of Psychrobacter and Marinobacter. This is the first report of pure cultures of bacteria from Lake Vida, and the isolates displayed a phenotype consistent with life in a cold hypersaline environment.     

Dilution-to-Extinction Culturing of Psychrotolerant Planktonic Bacteria from Permanently Ice-covered Lakes in the McMurdo Dry Valleys,Antarctica

Lakes in the McMurdo Dry Valleys of Antarctica are characterized by a permanent ice cover and little or no anthropogenic influence. Although bacterial cultures have been obtained from these habitats, recent culture-independent studies indicate that the most abundant microbes in these systems are not yet cultivated. By using dilution-to-extinction cultivation methods with sterilized and nutrient-amended lake water as media, we isolated 148 chemotrophic psychrotolerant bacterial cultures from fresh surface water of Lake Fryxell and the east lobe of Lake Bonney and the hypersaline, suboxic bottom water from the west lobes of Lake Bonney. Screening of the 16S ribosomal ribonucleic acid (rRNA) genes of the cultures by restriction fragment length polymorphism (RFLP) yielded 57 putatively pure psychrotolerant, slow growing cultures grouped into 18 clusters. The sequencing of 16S rRNA genes of randomly selected representatives of each RFLP cluster revealed that the corresponding isolates belong to the Alphaproteobacteria (six RFLP patterns), Betaproteobacteria (six RFLP patterns), Bacteroidetes (four RFLP patterns), and Actinobacteria (two RFLP patterns). Phylogenetic analysis of the sequences showed that the vast majority of the isolates were not closely related to previously described species. Thirteen of 18 RFLP patterns shared a 16S ribosomal deoxyribonucleic acid sequence similarity of 97% or less with the closest described species, and four isolates had a sequence similarity of 93% or less with the nearest described species. Phylogenetic analysis showed that these sequences were representatives of deeply branching organisms in the respective phylum. A comparison of the isolates with 16S rRNA clone libraries prepared from the same environments showed substantial overlap, indicating that dilution-to-extinction culturing in natural lake water media can help isolate some of the most abundant organisms in these perennially ice-covered lakes.