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.

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The Atacama Desert is the oldest and driest non-polar desert on Earth. Millions of years of hyperaridity enabled salt accumulations through atmospheric deposition. These salts can serve as proxies to decipher the interaction between water and soil as well as to understand the habitability with changing environmental settings. Therefore, we investigated four soil profiles regarding their mineralogy, salt abundance, and sulfate stable isotopic composition. The profiles were located along an elevation transect in the hyperarid region southeast of Antofagasta, Chile. The two lower sites situated on the distal parts of inactive alluvial fan deposits were subject to occasional fog occurrences. The upper steeper-sloped sites experienced no fog but are subject to minimal erosion. In all soil profiles, sulfates are the dominant salts showing a downward transition from gypsum to anhydrite that is accompanied by an increase of highly soluble salts and a decrease of sulfate δ 34 S and δ 18 O values. These trends are consistent with downward directed water infiltration during rare rain events causing salt dissolution followed by precipitation within the deeper soil column. This conclusion is also w supported by our Rayleigh fractionation model. We attribute the presence of anhydrite at > 40 cm depth to the cooccurrence of nitrate and chloride salts, which decreases water activity during sulfate precipitation and therefore drives anhydrite formation. Along the elevation transect, the total salt inventories of each profile show a trend for nitrates and chlorides concentration decreasing with elevation. This observation together with the sulfate stable isotopes indicates a fog-independent source and suggests remobilization of soluble salts through enhanced washout from hillslopes to alluvial fans. These findings are essential for assessing the longterm regional habitability of hyperarid environments and have also relevance for Mars.

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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.