Metabolic versatility of soil microbial communities below the rocks of the hyperarid Dalangtan Playa

Abstract

ABSTRACT Microbial assemblages inhabiting soils sheltered by rocks are widespread in the hyperarid and hypersaline Dalangtan Playa, which could contribute significantly to the ecological processes in this desert ecosystem. Here, we performed geochemical and metagenomic analyses of soils below and beside rocks in the Dalangtan Playa. Fourier transform infrared (FTIR) spectra show more evident signals of organic aromatic molecules in soils below rocks than in nearby bare soils. Soils below rocks harbor distinct microbial communities and much higher biomass and Cyanobacteria abundance in comparison to soils beside rocks. High-quality genomes recovered by hybrid short- and long-read assembly reveal the previously underappreciated contribution of Actinobacteriota in sheltered soils to the primary production of desert ecosystems. In contrast to bare soil communities, the metabolic versatility of sheltered soil communities indicates their critical roles in carbon, nitrogen, and sulfur cycling in the Dalangtan Playa. Trace gases (CO and H 2 ) could be significant energy sources for the respiration and sometimes carbon fixation of both bare and sheltered soil microorganisms in nutrient-deprived environments. The presence of multiple stress response genes against DNA damage, oxidative stress, and osmotic stress, as well as pathways for the biosynthesis and uptake of compatible solutes in genomes across all samples, reveals their capacity for tolerating polyextreme conditions. IMPORTANCE The hyperarid Dalangtan Playa in the western Qaidam Basin, northwestern China, is a unique terrestrial analog of Mars. Despite the polyextreme environments of this area, habitats below translucent rocks capable of environmental buffering could serve as refuges for microbial life. In this study, the hybrid assembly of Illumina short reads and Nanopore long reads recovered high-quality and high-continuity genomes, allowing for high-accuracy analysis and a deeper understanding of extremophiles in the sheltered soils of the Dalangtan Playa. Our findings reveal self-supporting and metabolically versatile sheltered soil communities adapted to a hyperarid and hypersaline playa, which provides implications for the search for life signals on Mars.