Microbial Mats of the McMurdo Dry Valleys, Antarctica: Oases of Biological Activity in a Very Cold Desert.

Cyanobacterial mats in the Antarctic Dry Valleys are photosynthetic microbial ecosystems living at the extreme of conditions on Earth with respect to temperature, light, water and nutrient availability. They are metabolically active for about 8 weeks during the austral summer when temperatures briefly rise above freezing and glacial and lake melt waters are available. There is much to learn about the biogeochemical impact of mats in these environments and the microbial communities associated with them. Our data demonstrate that these mats attain surprisingly high rates of carbon (CO2) and dinitrogen (N2) fixation when liquid water is available, in some cases comparable to rates in warmer temperate or tropical environments. C and N2 fixation in Dry Valley mats in turn substantially elevate dissolved organic C and inorganic N pools and thereby promote enhanced microbial secondary production. Moreover, the microbial community fingerprint of these mats is unique compared with the more ubiquitous dry soils that do not contain mats. Components of the heterotrophic microbiota may also contribute substantially to N inputs through N2 fixation.

The distribution and relative ecological roles of autotrophic and heterotrophic diazotrophs in the McMurdo Dry Valleys, Antarctica.

The McMurdo Dry Valleys (MDV) in Antarctica harbor a diverse assemblage of mat-forming diazotrophic cyanobacteria that play a key role in nitrogen cycling. Prior research showed that heterotrophic diazotrophs also make a substantial contribution to nitrogen fixation in MDV. The goals of this study were to survey autotrophic and heterotrophic diazotrophs across the MDV to investigate factors that regulate the distribution and relative ecological roles of each group. Results indicated that diazotrophs were present only in samples with mats, suggesting a metabolic coupling between autotrophic and heterotrophic diazotrophs. Analysis of 16S rRNA and nifH gene sequences also showed that diazotrophs were significantly correlated to the broader bacterial community, while co-occurrence network analysis revealed potential interspecific interactions. Consistent with previous studies, heterotrophic diazotrophs in MDV were diverse, but largely limited to lakes and their outlet streams, or other environments protected from desiccation. Despite the limited distribution, heterotrophic diazotrophs may make a substantial contribution to the nitrogen budget of MDV due to larger surface area and longer residence times of lakes. This work contributes to our understanding of key drivers of bacterial community structure in polar deserts and informs future efforts to investigate the contribution of nitrogen fixation to MDV ecosystems.

Rapid Microbial Dynamics in Response to an Induced Wetting Event in Antarctic Dry Valley Soils.

The cold deserts of the McMurdo Dry Valleys (MDV), Antarctica, host a high level of microbial diversity. Microbial composition and biomass in arid vs. ephemerally wetted regions are distinctly different, with wetted communities representing hot spots of microbial activity that are important zones for biogeochemical cycling. While climatic change is likely to cause wetting in areas not historically subject to wetting events, the responses of microorganisms inhabiting arid soils to water addition is unknown. The purpose of this study was to observe how an associated, yet non-wetted microbial community responds to an extended addition of water. Water from a stream was diverted to an adjacent area of arid soil with changes in microbial composition and activities monitored via molecular and biochemical methods over 7 weeks. The frequency of genetic signatures related to both prokaryotic and eukaryotic organisms adapted to MDV aquatic conditions increased during the limited 7 week period, indicating that the soil community was transitioning into a typical "high-productivity" MDV community. This work is consistent with current predictions that MDV microbial communities in arid regions are highly sensitive to climate change, and further supports the notion that changes in community structure and associated biogeochemical cycling may occur much more rapidly than predicted.

Carbon-Fixation Rates and Associated Microbial Communities Residing in Arid and Ephemerally Wet Antarctic Dry Valley Soils.

Carbon-fixation is a critical process in severely oligotrophic Antarctic Dry Valley (DV) soils and may represent the major source of carbon in these arid environments. However, rates of C-fixation in DVs are currently unknown and the microorganisms responsible for these activities unidentified. In this study, C-fixation rates measured in the bulk arid soils (<5% moisture) ranged from below detection limits to ∼12 nmol C/cc/h. Rates in ephemerally wet soils ranged from ∼20 to 750 nmol C/cc/h, equating to turnover rates of ∼7-140 days, with lower rates in stream-associated soils as compared to lake-associated soils. Sequencing of the large subunit of RuBisCO (cbbL) in these soils identified green-type sequences dominated by the 1B cyanobacterial phylotype in both arid and wet soils including the RNA fraction of the wet soil. Red-type cbbL genes were dominated by 1C actinobacterial phylotypes in arid soils, with wetted soils containing nearly equal proportions of 1C (actinobacterial and proteobacterial signatures) and 1D (algal) phylotypes. Complementary 16S rRNA and 18S rRNA gene sequencing also revealed distinct differences in community structure between biotopes. This study is the first of its kind to examine C-fixation rates in DV soils and the microorganisms potentially responsible for these activities.

Microbial community composition of transiently wetted Antarctic Dry Valley soils.

During the summer months, wet (hyporheic) soils associated with ephemeral streams and lake edges in the Antarctic Dry Valleys (DVs) become hotspots of biological activity and are hypothesized to be an important source of carbon and nitrogen for arid DV soils. Recent research in the DV has focused on the geochemistry and microbial ecology of lakes and arid soils, with substantially less information being available on hyporheic soils. Here, we determined the unique properties of hyporheic microbial communities, resolved their relationship to environmental parameters and compared them to archetypal arid DV soils. Generally, pH increased and chlorophyll a concentrations decreased along transects from wet to arid soils (9.0 to ~7.0 for pH and ~0.8 to ~5 µg/cm(3) for chlorophyll a, respectively). Soil water content decreased to below ~3% in the arid soils. Community fingerprinting-based principle component analyses revealed that bacterial communities formed distinct clusters specific to arid and wet soils; however, eukaryotic communities that clustered together did not have similar soil moisture content nor did they group together based on sampling location. Collectively, rRNA pyrosequencing indicated a considerably higher abundance of Cyanobacteria in wet soils and a higher abundance of Acidobacterial, Actinobacterial, Deinococcus/Thermus, Bacteroidetes, Firmicutes, Gemmatimonadetes, Nitrospira, and Planctomycetes in arid soils. The two most significant differences at the genus level were Gillisia signatures present in arid soils and chloroplast signatures related to Streptophyta that were common in wet soils. Fungal dominance was observed in arid soils and Viridiplantae were more common in wet soils. This research represents an in-depth characterization of microbial communities inhabiting wet DV soils. Results indicate that the repeated wetting of hyporheic zones has a profound impact on the bacterial and eukaryotic communities inhabiting in these areas.

Diverse and highly active diazotrophic assemblages inhabit ephemerally wetted soils of the Antarctic Dry Valleys.

Eolian transport of biomass from ephemerally wetted soils, associated with summer glacial meltwater runoffs and lake edges, to low-productivity areas of the Antarctic Dry Valleys (DV) has been postulated to be an important source of organic matter (fixed nitrogen and fixed carbon) to the entire DV ecosystem. However, descriptions and identification of the microbial members responsible for N(2) fixation within these wetted sites are limited. In this study, N(2) fixers from wetted soils were identified by direct nifH gene sequencing and their in situ N(2) fixation activities documented via acetylene reduction and RNA-based quantitative PCR assays. Shannon-index nifH diversity levels ranged between 1.8 and 2.6 and included the expected cyanobacterial signatures and a large number of phylotypes related to the gamma-, beta-, alpha-, and delta-proteobacteria. N(2) fixation rates ranged between approximately 0.5 and 6 nmol N cm(-3) h(-1) with measurements indicating that approximately 50% of this activity was linked with sulfate reduction at some sites. Comparisons with proximal dry soils also suggested that these communities are not ubiquitously distributed, and conditions unrelated to moisture content may define the composition, diversity, or habitat suitability of the microbial communities within wetted soils of the DVs.

Fixation and fate of C and N in the cyanobacterium Trichodesmium using nanometer-scale secondary ion mass spectrometry.

The marine cyanobacterium Trichodesmium is ubiquitous in tropical and subtropical seas and is an important contributor to global N and C cycling. We sought to characterize metabolic uptake patterns in individual Trichodesmium IMS-101 cells by quantitatively imaging (13)C and (15)N uptake with high-resolution secondary ion mass spectrometry (NanoSIMS). Trichodesmium fix both CO(2) and N(2) concurrently during the day and are, thus, faced with a balancing act: the O(2) evolved during photosynthesis inhibits nitrogenase, the key enzyme in N(2) fixation. After performing correlated transmission electron microscopy (TEM) and NanoSIMS analysis on trichome thin-sections, we observed transient inclusion of (15)N and (13)C into discrete subcellular bodies identified as cyanophycin granules. We speculate that Trichodesmium uses these dynamic storage bodies to uncouple CO(2) and N(2) fixation from overall growth dynamics. We also directly quantified both CO(2) and N(2) fixation at the single cell level using NanoSIMS imaging of whole cells in multiple trichomes. Our results indicate maximal CO(2) fixation rates in the morning, compared with maximal N(2) fixation rates in the afternoon, bolstering the argument that segregation of CO(2) and N(2) fixation in Trichodesmium is regulated in part by temporal factors. Spatial separation of N(2) and CO(2) fixation may also have a role in metabolic segregation in Trichodesmium. Our approach in combining stable isotope labeling with NanoSIMS and TEM imaging can be extended to other physiologically relevant elements and processes in other important microbial systems.