Life at the extreme: Plant-driven hotspots of soil nutrient cycling in the hyper-arid core of the Atacama Desert

The hyperarid core of the Atacama Desert represents one of the most intense environments on Earth, often being used as an analog for Mars regolith. The area is characterized by extremes in climate (e.g., temperature, humidity, UV irradiation) and edaphic factors (e.g., hyper-salinity, high pH, compaction, high perchlorates, and low moisture, phosphorus and organic matter). However, the halophytic C4 plant Distichlis spicata appears to be one of the few species on the planet that can thrive in this environment. Within this habitat it captures windblown sand leading to the formation of unique structures and the generation of above-ground phyllosphere soil. Using a combination of approaches (e.g., X-ray Computed Tomography, TXRF, δ13C/δ15N isotope profiling, microbial PLFAs, 14C turnover, phosphate sorption isotherms) we examined the factors regulating the biogeochemical cycling of nitrogen (N), phosphorus (P) and carbon (C) in both vegetated and unvegetated areas. Our results showed that D. spicata rhizomes with large aerenchyma were able to break through the highly cemented topsoil layer leading to root proliferation in the underlying soil. The presence of roots increased soil water content, P availability and induced a change in microbial community structure and promoted microbial growth and activity. In contrast, soil in the phyllosphere exhibited almost no biological activity. Organic C stocks and recent C4 plant derived input increased as follows: phyllosphere (1941 g C m−2; 85% recent) > soils under plants (575–748 g C m−2; 55–60%) > bare soils (491–642 g C m−2; 9–17%). Due to the high levels of nitrate in soil (>2 t ha−1) and high rates of P sorption/precipitation, our data suggest that the microbial activity is both C and P, but not N limited. Root-mediated salt uptake combined with foliar excretion and dispersal of NaCl into the surrounding area indicated that D. spicata was responsible for actively removing ca. 55% of the salt from the rhizosphere. We also demonstrate that NH3 emissions may represent a major N loss pathway from these soil ecosystems during the processing of organic N. We attribute this to NH3 volatilization to the high pH of the soil and slow rates of nitrification. In conclusion, we demonstrate that the extremophile D. spicata physically, chemically and biologically reengineers the soil to create a highly bioactive hotspot within the climate-extreme of the Atacama Desert.