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Studies of microbial biogeography are often convoluted by extremely high diversity and differences in microenvironmental factors such as pH and nutrient availability. Desert endolithic (inside rock) communities are exceptionally simple ecosystems that can serve as a tractable model for investigating long-range biogeographic effects on microbial communities. We conducted a comprehensive survey of endolithic sandstones using high-throughput marker gene sequencing to characterize global patterns of diversity in endolithic microbial communities. We also tested a range of abiotic variables in order to investigate the factors that drive community assembly at various trophic levels. Macroclimate was found to be the primary driver of endolithic community composition, with the most striking difference witnessed between hot and polar deserts. This difference was largely attributable to the specialization of prokaryotic and eukaryotic primary producers to different climate conditions. On a regional scale, microclimate and properties of the rock substrate were found to influence community assembly, although to a lesser degree than global hot versus polar conditions. We found new evidence that the factors driving endolithic community assembly differ between trophic levels. While phototrophic taxa were rigorously selected for among different sites, heterotrophic taxa were more cosmopolitan, suggesting that stochasticity plays a larger role in heterotroph assembly. This study is the first to uncover the global drivers of desert endolithic diversity using high-throughput sequencing. We demonstrate that phototrophs and heterotrophs in the endolithic community assemble under different stochastic and deterministic influences, emphasizing the need for studies of microorganisms in context of their functional niche in the community.

It is surprising to encounter active saline spring activity at a constant 6°C temperature year-round not far away from the North Pole, at latitude 79°24′N, where the permafrost is ca. 600 m thick and average annual temperature is -15°C. These perennial springs in Expedition Fiord, Queen Elizabeth Islands, Canadian Arctic Archipelago, had previously been explained as a recent, periglacial process. However, the discovery near White Glacier (79°26.66′N; 90°42.20′W; 350 m.a.s.l.) of a network of veins of hydrothermal origin with a similar mineralogy to travertine precipitates formed by the springs suggests that their fluids have much deeper circulation and are related to evaporite structures (salt diapirs) that underlie the area. The relatively high minimum trapping temperature of the fluid inclusions (avg. ~200 ± 45°C, 1σ) in carbonate and quartz in the vein array, and in quartz veins west of the site, explains a local thermal anomaly detected through low-temperature thermochronology. This paper reviews and updates descriptive features of the perennial springs in Expedition Fiord and compares their mineralogy, geochemistry, and geology to the vein array by White Glacier, which is interpreted as a hydrothermal predecessor of the springs. The perennial springs in Axel Heiberg Island are known for half a century and have been extensively described in the literature. Discharging spring waters are hypersaline (1-4 molal NaCl; ~5 to 19 wt% NaCl) and precipitate Fe-sulfides, sulfates, carbonates, and halides with acicular and banded textures representing discharge pulsations. At several sites, waters and sediments by spring outlets host microbial communities that are supported by carbon- and energy-rich reduced substrates including sulfur and methane. They have been studied as possible analogs for life-supporting environments in Mars. The vein array at White Glacier consists of steep to subhorizontal veins, mineralized fractures, and breccias within a gossan area of ca. 350 × 50 m. The host rock is altered diabase and a chaotic matrix-supported breccia composed of limestone, sandstone, and anhydrite-gypsum. Mineralization consists of brown calcite (pseudomorph after aragonite) in radial aggregates as linings of fractures and cavities, with transparent, sparry calcite and quartz at the centre of larger cavities. Abundant sulfides pyrite and marcasite and minor chalcopyrite, sphalerite, and galena occur in masses and veins, much like in base metal deposits known as Mississippi Valley Type; their weathering is responsible for brown Fe oxides forming a gossan. Epidote and chlorite rim veins where the host rock is Fe- and Mg-rich diabase. The banded carbonate textures with organic matter and sulfides are reminiscent of textures observed in mineral precipitates forming in the active springs at Colour Peak Diapir. Very small fluid inclusions (5-10 μm) in two generations of vein calcite (hexagonal, early brown calcite we denominate “cal1” lining vein walls; white-orange sparry calcite “cal2” infilling veins) have bulk salinities that transition between an early, high-salinity end-member brine (up to ~20 wt% NaCl equivalent) to a later, low-salinity end-member fluid (nearly pure water) and show large fluctuations in salinity with time. Inclusions that occupy secondary planes and also growth zones in the later calcite infilling (deemed primary) have Th ranging from 100°C to 300°C (n=120, average~200°C; independent of salinity), 2 orders of magnitude higher than average discharging water temperatures of 6°C at Colour Peak Diapir. Carbon isotope composition (δ13CVPDB) of the White Glacier vein array carbonates ranges from approximately -20 to -30‰, like carbonates formed by the degradation of petroleum, whereas carbonates at Colour Peak Diapir springs have a value of -10‰. Oxygen isotope composition (δ18OVSMOW) of vein carbonates ranges from -0.3‰ to +3.5‰, compatible with a coeval fluid at 250°C with a composition from -3.5‰ to -7.0‰. These data are consistent with carbonates having precipitated from mixtures of heated formational waters and high-latitude meteoric waters. In contrast, the δ18OVSMOW value for carbonates at Colour Peak Diapir springs is +10‰, derived from high-latitude meteoric waters at 6°C. The sulfur isotope (δ34SVCDT) composition of Fe-sulfides at the perennial springs is +19.2‰, similar to the δ34SVCDT of Carboniferous-age sulfate of the diapirs and consistent with low-temperature microbial reduction of finite (closed-system) sulfate. The δ34SVCDT values of Fe-sulfides in the vein array range from -2.7‰ to +16.4‰, possibly reflecting higher formation temperatures involving reduction of sulfate by organics. We suggest that the similar setting, mineralogical compositions, and textures between the hydrothermal vein array and the active Colour Peak Diapir springs imply a kinship. We suggest that overpressured basinal fluids expelled from the sedimentary package and deforming salt bodies at depth during regional compressional tectonic deformation ca. 50 million years ago (Eocene) during what is known as the Eurekan Orogeny created (by hydrofracturing) the vein array at White Glacier (and probably other similar ones), and the network of conduits created continued to be a pathway around salt bodies for deeply circulating fluids to this day. Fluid inclusion data suggest that the ancient conduit system was at one point too hot to support life but may have been since colonized by microorganisms as the system cooled. Thermochronology data suggest that the hydrologic system cooled to temperatures possibly sustaining life about 10 million years ago, making it since then a viable analogue environment for the establishment of microbial life in similar situations on other planets.

In a previous paper (Shtober-Zisu et al., 2012) we described millimeter to centime-sized fluid-free holes within the interiors of stalagmites of widely varying origin. We present here further observations of this phenomenon, using X-ray tomography, macroscopic and microscopic observation of sections of twenty-six stalagmites from various sites in North America and the Caribbean region. We can distinguish three types of cavities in speleothems: primary µm-sized fluid inclusions; mm to cm sized holes, aligned along the stalagmite growth axis which are clearly syngenetic; and µm to cm-sized holes away from the growth axis (“off-axis holes or OAHs”) deeply buried inside their host stalagmites, and cutting primary growth layers. Neither axial nor off axis holes contain fluid today. Off-axis holes appear to have been formed by internal corrosion of the calcite host, possibly enhanced by the action of bacteria which were sustained by permeation of through the body of the stalagmite of water containing dissolved organic species. A modern stalagmite from Israel is shown to contain bacteria associated with active hole formation.

Plants have the potential to accumulate toxic amounts of cadmium (Cd), and understanding how and where Cd is stored in plants is important for ensuring food safety. Previous experiments have determined that a greater amount of Cd is translocated into the leaves of lettuce (Lactuca sativa) as compared to barley leaves (Hordeum vulgare). Preferential retention of Cd in root of barley would explain this difference. Hence, the purpose of this study was to determine the localization and coordination environment of Cd (i.e., the ligands to which Cd was bound) in the different root tissues of lettuce and barley using histochemical staining, electron microscopy and micro X-ray spectroscopy. Retention of Cd in barley roots could be explained by accumulation of Cd at the endodermis, comparatively higher amounts of Cd sequestered in the symplast of cortical cells and binding to xylem cell walls. Increased translocation of Cd to lettuce shoots seemed to be due to a less effective barrier at the endodermis and less sequestration of Cd in the cortex. Regardless of the tissue type, most of the Cd2+ was bound to S ligands in the roots of barley, possibly reflecting accumulation of Cd–phytochelatin and Cd–S molecules in the vacuoles. In lettuce roots, Cd was more evenly distributed among ligands containing S, O and NO3 groups, which is indicative of proportionately more Cd binding to the cell walls, relative to barley. These results will be useful in uncovering the mechanisms of differential Cd-tolerance and sequestration in lettuce and barley.

Microbialite-forming communities interact with the environment and influence the precipitation of calcium carbonate through their metabolic activity. The functional genes associated with these metabolic processes and their environmental interactions are therefore critical to microbialite formation. The microbiomes associated with microbialite-forming ecosystems are just now being elucidated and the extent of shared pathways and taxa across different environments is not fully known. In this study, we profiled the microbiome of microbial communities associated with lacustrine thrombolites located in Lake Clifton, Western Australia using metagenomic sequencing and compared it to the non-lithifying mats associated with surrounding sediments to determine whether differences in the mat microbiomes, particularly with respect to metabolic pathways and environmental interactions, may potentially contribute to thrombolite formation. Additionally, we used stable isotope biosignatures to delineate the dominant metabolism associated with calcium carbonate precipitation in the thrombolite build-ups. Results indicated that the microbial community associated with the Lake Clifton thrombolites was predominantly bacterial (98.4%) with Proteobacteria, Cyanobacteria, Bacteroidetes, and Actinobacteria comprising the majority of annotated reads. Thrombolite-associated mats were enriched in photoautotrophic taxa and functional genes associated with photosynthesis. Observed δ(13)C values of thrombolite CaCO3 were enriched by at least 3.5‰ compared to theoretical values in equilibrium with lake water DIC, which is consistent with the occurrence of photoautotrophic activity in thrombolite-associated microbial mats. In contrast, the microbiomes of microbial communities found on the sandy non-lithifying sediments of Lake Clifton represented distinct microbial communities that varied in taxa and functional capability and were enriched in heterotrophic taxa compared to the thrombolite-associated mats. This study provides new insight into the taxa and functional capabilities that differentiate potentially lithifying mats from other non-lithifying types and suggests that thrombolites are actively accreting and growing in limited areas of Lake Clifton.

Cryptoendolithic habitats in the Canadian high Arctic are associated with a variety of microbial community assemblages, including cyanobacteria, algae, and fungi. These habitats were analyzed for the presence of metal ions by sequential extraction and evaluated for relationships between these and the various microorganisms found at each site using multivariate statistical methods. Cyanobacteria-dominated communities exist under higher pH conditions with elevated concentrations of calcium and magnesium, whereas communities dominated by fungi and algae are characterized by lower pH conditions and higher concentrations of iron, aluminum, and silicon in the overlying surfaces. These results suggest that the activity of the dominant microorganisms controls the pH of the surrounding environment, which in turn dictates rates of weathering or the possibility for surface crust formation, both ultimately deciding the structure of microbial diversity for each cryptoendolithic habitat.

When CO2 is sequestered into the deep subsurface, changes to the subsurface microbial community will occur. Capnophiles, microorganisms that grow in CO2-rich environments, are some organisms that may be selected for under the new environmental conditions. To determine whether capnophiles comprise an important part of CO2-rich environments, an isolate from Crystal Geyser, Utah, U.S.A., a CO2- rich spring considered a carbon sequestration analogue, was characterized. The isolate was cultured under varying CO2, pH, salinity, and temperature, as well as different carbon substrates and terminal electron acceptors (TEAs) to elucidate growth conditions and metabolic activity. Designated CG-1, the isolate is related (99%) to Lactobacillus casei in 16S rRNA gene identity, growing at PCO2 between 0 to 1.0 MPa. Growth is inhibited at 2.5 MPa, but stationary phase cultures exposed to this pressure survive beyond 5 days. At 5.0 MPa, survival is at least 24 hours. CG-1 grows in neutral pH, 0.25 M NaCl, and between 25° to 45°C andconsumes glucose, lactose, sucrose, or crude oil, likely performing lactic acid fermentation. Fatty acid profiles between 0.1 MPa to 1.0 MPa suggests decreases in cell size and increases in membrane rigidity. Transmission electron microscopy reveals rod shaped bacteria at 0.1 MPa. At 1.0 MPa, cells are smaller, amorphous, and produce abundant capsular material. Its ability to grow in environments regardless of the presence of CO2 suggests we have isolated an organism that is more capnotolerant than capnophilic. Results also show that microorganisms are capable of surviving the stressful conditions created by the introduction of CO2 for sequestration. Furthermore, our ability to culture an environmental isolate indicates that organisms found in CO2 environments from previous genomic and metagenomics studies are viable, metabolizing, and potentially affecting the surrounding environment.

Methane (CH4) emission by carbon-rich cryosols at the high latitudes in Northern Hemisphere has been studied extensively. In contrast, data on the CH4 emission potential of carbon-poor cryosols is limited, despite their spatial predominance. This work employs CH4 flux measurements in the field and under laboratory conditions to show that the mineral cryosols at Axel Heiberg Island in the Canadian high Arctic consistently consume atmospheric CH4. Omics analyses present the first molecular evidence of active atmospheric CH4-oxidizing bacteria (atmMOB) in permafrost-affected cryosols, with the prevalent atmMOB genotype in our acidic mineral cryosols being closely related to Upland Soil Cluster α. The atmospheric (atm) CH4 uptake at the study site increases with ground temperature between 0 °C and 18 °C. Consequently, the atm CH4 sink strength is predicted to increase by a factor of 5–30 as the Arctic warms by 5–15 °C over a century. We demonstrate that acidic mineral cryosols are a previously unrecognized potential of CH4 sink that requires further investigation to determine its potential impact on larger scales. This study also calls attention to the poleward distribution of atmMOB, as well as to the potential influence of microbial atm CH4 oxidation, in the context of regional CH4 flux models and global warming.

Planococcus halocryophilus strain Or1, isolated from high Arctic permafrost, grows and divides at -15 °C, the lowest temperature demonstrated to date, and is metabolically active at -25 °C in frozen permafrost microcosms. To understand how P. halocryophilus Or1 remains active under the subzero and osmotically dynamic conditions that characterize its native permafrost habitat, we investigated the genome, cell physiology and transcriptomes of growth at -15 °C and 18% NaCl compared with optimal (25 °C) temperatures. Subzero growth coincides with unusual cell envelope features of encrustations surrounding cells, while the cytoplasmic membrane is significantly remodeled favouring a higher ratio of saturated to branched fatty acids. Analyses of the 3.4 Mbp genome revealed that a suite of cold and osmotic-specific adaptive mechanisms are present as well as an amino acid distribution favouring increased flexibility of proteins. Genomic redundancy within 17% of the genome could enable P. halocryophilus Or1 to exploit isozyme exchange to maintain growth under stress, including multiple copies of osmolyte uptake genes (Opu and Pro genes). Isozyme exchange was observed between the transcriptome data sets, with selective upregulation of multi-copy genes involved in cell division, fatty acid synthesis, solute binding, oxidative stress response and transcriptional regulation. The combination of protein flexibility, resource efficiency, genomic plasticity and synergistic adaptation likely compensate against osmotic and cold stresses. These results suggest that non-spore forming P. halocryophilus Or1 is specifically suited for active growth in its Arctic permafrost habitat (ambient temp. ~ -16 °C), indicating that such cryoenvironments harbor a more active microbial ecosystem than previously thought. © 2013 International Society for Microbial Ecology.

Correction to: The ISME Journal (2015) 9, 1880–1891; doi:10.1038/ismej.2015.13; published online 14 April 2015 Since the publication of this article, the authors have identified an error in the reported values for CH4 oxidation rates calculated from the microcosm experiment (Table 1), which also affected the reported Q10 values (on page 7 and Figure 3)

We examined the environmental stresses experienced by cyanobacteria living in endolithic gneissic habitats in the Haughton impact structure, Devon Island, Canadian High Arctic (75° N) and compared them with the endolithic habitat at the opposite latitude in the Dry Valleys of Antarctica (76° S). In the Arctic during the summer, there is a period for growth of approximately 2.5 months when temperatures rise above freezing. During this period, freeze–thaw can occur during the diurnal cycle, but freeze–thaw excursions are rare within higher-frequency temperature changes on the scale of minutes, in contrast with the Antarctic Dry Valleys. In the Arctic location rainfall of approximately 3 mm can occur in a single day and provides moisture for endolithic organisms for several days afterwards. This rainfall is an order of magnitude higher than that received in the Dry Valleys over 1 year. In the Dry Valleys, endolithic communities may potentially receive higher levels of ultraviolet radiation than the Arctic location because ozone depletion is more extreme. The less extreme environmental stresses experienced in the Arctic are confirmed by the presence of substantial epilithic growth, in contrast to the Dry Valleys. Despite the more extreme conditions experienced in the Antarctic location, the diversity of organisms within the endolithic habitat, which includes lichen and eukaryotic algal components, is higher than observed at the Arctic location, where genera of cyanobacteria dominate. The lower biodiversity in the Arctic may reflect the higher water flow through the rocks caused by precipitation and the more heterogeneous physical structure of the substrate. The data illustrate an instance in which extreme climate is anti-correlated with microbial biological diversity.