Spatial and Temporal Variability of Microbial Communities and Salt Distributions Across an Aridity Gradient Before and After Heavy Rains in the Atacama Desert

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.

Phospholipid biomarkers in Mars-analogous soils of the Atacama Desert

“…Similarly, in consistence with taxonomic analysis, the proportion of Proteobacteria did not change much between sites: 11–13% Proteobacteria as observed in identified taxa (Shen et al ., 2020 a ) and 5.8–7.7% Proteobacteria-derived monounsaturated fatty acids as found in this study.…”

“…3a) as in other Earth ecosystems (Moss et al ., 1997). The two terminally branched saturated fatty acids ( a -C15:0 and i -C16:0) were only detectable in TZ-5, indicating more Firmicutes there (Dong et al ., 2006), which was consistent with DNA taxonomic analysis, 34.9% of Firmicutes in TZ-5 compared to 0.0–5.7% in other sites (Ben-David et al ., 2011; Shen et al ., 2020 a ). Similarly, in consistence with taxonomic analysis, the proportion of Proteobacteria did not change much between sites: 11–13% Proteobacteria as observed in identified taxa (Shen et al ., 2020 a ) and 5.8–7.7% Proteobacteria-derived monounsaturated fatty acids as found in this study. 3-OH C14:0 was only detectable in TZ-6, indicating a higher diversity but not necessarily higher abundance in hydroxy fatty acid (Table 2 and Fig.…”

“…The two terminally branched saturated fatty acids ( a -C15:0 and i -C16:0) were only detectable in TZ-5, indicating more Firmicutes there (Dong et al ., 2006), which was consistent with DNA taxonomic analysis, 34.9% of Firmicutes in TZ-5 compared to 0.0–5.7% in other sites (Ben-David et al ., 2011; Shen et al ., 2020 a ).…”