Persistent microbial communities in hyperarid subsurface habitats of the Atacama Desert: Insights from intracellular DNA analysis.

Desert environments constitute one of the largest and yet most fragile ecosystems on Earth. Under the absence of regular precipitation, microorganisms are the main ecological component mediating nutrient fluxes by using soil components, like minerals and salts, and atmospheric gases as a source for energy and water. While most of the previous studies on microbial ecology of desert environments have focused on surface environments, little is known about microbial life in deeper sediment layers. Our study is extending the limited knowledge about microbial communities within the deeper subsurface of the hyperarid core of the Atacama Desert. By employing intracellular DNA extraction and subsequent 16S rRNA sequencing of samples collected from a soil pit in the Yungay region of the Atacama Desert, we unveiled a potentially viable microbial subsurface community residing at depths down to 4.20 m. In the upper 80 cm of the playa sediments, microbial communities were dominated by Firmicutes taxa showing a depth-related decrease in biomass correlating with increasing amounts of soluble salts. High salt concentrations are possibly causing microbial colonization to cease in the lower part of the playa sediments between 80 and 200 cm depth. In the underlying alluvial fan deposits, microbial communities reemerge, possibly due to gypsum providing an alternative water source. The discovery of this deeper subsurface community is reshaping our understanding of desert soils, emphasizing the need to consider subsurface environments in future explorations of arid ecosystems.

Eolian erosion of polygons in the Atacama Desert as a proxy for hyper-arid environments on Earth and beyond.

Polygonal networks occur on various terrestrial and extraterrestrial surfaces holding valuable information on the pedological and climatological conditions under which they develop. However, unlike periglacial polygons that are commonly used as an environmental proxy, the information that polygons in the hyper-arid Atacama Desert can provide is little understood. To promote their use as a proxy, we investigated a polygonal network within an inactive channel that exhibits uncommonly diverse surface morphologies and mineral compositions, using geochemical and remote sensing techniques. Our findings show that the polygons belong to a continuous network of the same genetic origin. Their differences result from post-formational differential eolian erosion up to 50 cm depth, exposing indurated subsurface horizons rich in sulfate or nitrate and chloride. Their location in an ancient channel could lead to the misinterpretation of fluvial polygon erosion, however, we find no such signs but evidence for aqueous resurfacing of microtopography by fog and minimal rainwater infiltration. Our findings extend the use of polygons as proxies in the Atacama Desert, indicating saline soils and hyper-arid conditions. We conclude that this example of polygon erosion can guide future polygon research, especially regarding the use of erosional surfaces on Earth and beyond to gain valuable subsurface insights.

Leave no stone unturned: individually adapted xerotolerant Thaumarchaeota sheltered below the boulders of the Atacama Desert hyperarid core.

BACKGROUND: The hyperarid core of the Atacama Desert is an extremely harsh environment thought to be colonized by only a few heterotrophic bacterial species. Current concepts for understanding this extreme ecosystem are mainly based on the diversity of these few species, yet a substantial area of the Atacama Desert hyperarid topsoil is covered by expansive boulder accumulations, whose underlying microbiomes have not been investigated so far. With the hypothesis that these sheltered soils harbor uniquely adapted microbiomes, we compared metagenomes and geochemistry between soils below and beside boulders across three distantly located boulder accumulations in the Atacama Desert hyperarid core. RESULTS: Genome-resolved metagenomics of eleven samples revealed substantially different microbial communities in soils below and beside boulders, despite the presence of shared species. Archaea were found in significantly higher relative abundance below the boulders across all samples within distances of up to 205 km. These key taxa belong to a novel genus of ammonia-oxidizing Thaumarchaeota, Candidatus Nitrosodeserticola. We resolved eight mid-to-high quality genomes of this genus and used comparative genomics to analyze its pangenome and site-specific adaptations. Ca. Nitrosodeserticola genomes contain genes for ammonia oxidation, the 3-hydroxypropionate/4-hydroxybutyrate carbon fixation pathway, and acetate utilization indicating a chemolithoautotrophic and mixotrophic lifestyle. They also possess the capacity for tolerating extreme environmental conditions as highlighted by the presence of genes against oxidative stress and DNA damage. Site-specific adaptations of the genomes included the presence of additional genes for heavy metal transporters, multiple types of ATP synthases, and divergent genes for aquaporins. CONCLUSION: We provide the first genomic characterization of hyperarid soil microbiomes below the boulders in the Atacama Desert, and report abundant and highly adapted Thaumarchaeaota with ammonia oxidation and carbon fixation potential. Ca. Nitrosodeserticola genomes provide the first metabolic and physiological insight into a thaumarchaeal lineage found in globally distributed terrestrial habitats characterized by various environmental stresses. We consequently expand not only the known genetic repertoire of Thaumarchaeota but also the diversity and microbiome functioning in hyperarid ecosystems. Video Abstract.

Microbial Hotspots in Lithic Microhabitats Inferred from DNA Fractionation and Metagenomics in the Atacama Desert.

The existence of microbial activity hotspots in temperate regions of Earth is driven by soil heterogeneities, especially the temporal and spatial availability of nutrients. Here we investigate whether microbial activity hotspots also exist in lithic microhabitats in one of the most arid regions of the world, the Atacama Desert in Chile. While previous studies evaluated the total DNA fraction to elucidate the microbial communities, we here for the first time use a DNA separation approach on lithic microhabitats, together with metagenomics and other analysis methods (i.e., ATP, PLFA, and metabolite analysis) to specifically gain insights on the living and potentially active microbial community. Our results show that hypolith colonized rocks are microbial hotspots in the desert environment. In contrast, our data do not support such a conclusion for gypsum crust and salt rock environments, because only limited microbial activity could be observed. The hypolith community is dominated by phototrophs, mostly Cyanobacteria and Chloroflexi, at both study sites. The gypsum crusts are dominated by methylotrophs and heterotrophic phototrophs, mostly Chloroflexi, and the salt rocks (halite nodules) by phototrophic and halotolerant endoliths, mostly Cyanobacteria and Archaea. The major environmental constraints in the organic-poor arid and hyperarid Atacama Desert are water availability and UV irradiation, allowing phototrophs and other extremophiles to play a key role in desert ecology.

Transitory microbial habitat in the hyperarid Atacama Desert.

Traces of life are nearly ubiquitous on Earth. However, a central unresolved question is whether these traces always indicate an active microbial community or whether, in extreme environments, such as hyperarid deserts, they instead reflect just dormant or dead cells. Although microbial biomass and diversity decrease with increasing aridity in the Atacama Desert, we provide multiple lines of evidence for the presence of an at times metabolically active, microbial community in one of the driest places on Earth. We base this observation on four major lines of evidence: (i) a physico-chemical characterization of the soil habitability after an exceptional rain event, (ii) identified biomolecules indicative of potentially active cells [e.g., presence of ATP, phospholipid fatty acids (PLFAs), metabolites, and enzymatic activity], (iii) measurements of in situ replication rates of genomes of uncultivated bacteria reconstructed from selected samples, and (iv) microbial community patterns specific to soil parameters and depths. We infer that the microbial populations have undergone selection and adaptation in response to their specific soil microenvironment and in particular to the degree of aridity. Collectively, our results highlight that even the hyperarid Atacama Desert can provide a habitable environment for microorganisms that allows them to become metabolically active following an episodic increase in moisture and that once it decreases, so does the activity of the microbiota. These results have implications for the prospect of life on other planets such as Mars, which has transitioned from an earlier wetter environment to today's extreme hyperaridity.