Abstract
Over the past 150 million years, the hyperarid core of the Atacama Desert has been transformed by geologic and atmospheric conditions into one of the most unique and inhospitable landscapes on the planet. This makes it an ideal Mars analog that has been explored for decades as preliminary studies on the space life discovery. However, two heavy rainfalls that occurred in the Atacama in 2015 and 2017 provide a unique opportunity to study the response of resident extremophiles to rapid environmental change associated with excessive water and salt shock. Here we combine geochemical analyses with molecular biology to study the variations in salts and microbial communities along an aridity gradient, and to examine the reshuffling of hyperarid microbiomes before and after the two rainfall events. Analysis of microbial community composition revealed that soils within the southern desert were consistently dominated by Actinobacteria, Proteobacteria, Acidobacteria, Planctomycetes, Chloroflexi, Bacteroidetes, Gemmatimonadetes, and Verrucomicrobia; soils within the hyperarid sites were dominated by Aquificae and Deinococcus-Thermus before heavy rainfalls, while these organisms almost totally diminished after rainfall, and the hyperarid microbial consortia and metabolisms transformed to a more southern desert pattern along with increased biodiversity. Salts at the shallow subsurface were dissolved and leached down to a deeper layer, both benefitting and challenging indigenous microorganisms with the excessive input of water and ions. Microbial viability was found to change with aridity and rainfall events but correlated with elevation, pH, conductivity, chloride, nitrate, sulfate, and soil organic matters (SOM). Metagenomic functional pathways related to stressor responses also increased in post-rainfall hyperarid soils. Our findings contribute to the primary goal of Atacama Mars analog research for understanding the microbial community structure and adaptations: this study sheds light on the structure of xerophilic, halophilic, and radioresistant microbiomes in hyperarid environments, and their response to changes in water availability.