Metabolic transitions along a moisture gradient in a poly-extreme high-altitude desert ecosystem within the Atacama Desert

Abstract Background The Barrancas Blancas (BB) plain, situated in the high-altitude Atacama region, is a cryogenic, hyper-arid, poly-extreme environment. The seasonal formation of a temporary freshwater lake under these harsh conditions provides a unique opportunity to examine how liquid water influences the metabolic responses of desert microbial communities. Using a metatranscriptomic approach, we characterised microbial community responses along a 70-meter natural moisture gradient. Results Along the gradient, the most active sites (8–23 m from the lake) exhibited high RNA recovery and diverse metabolic functions. Bacillariophyta (diatoms) drove oxygenic phototrophy, while Pseudomonadota contributed to anoxygenic phototrophy and nitrogen fixation. Additionally, Pseudomonadota, Actinomycetota, and Bacteroidota expressed genes for the oxidation of nitrate, sulfide, thiosulfate, and trace gases (H₂, CO). The energy derived from these processes was reflected in the high capacity for carbon fixation by these taxa. Moreover, network analysis revealed that these primary producers co-occurred with a diverse range of heterotrophic prokaryotic and eukaryotic groups. In contrast, at the driest site, hydrogen oxidation was the primary energy-conserving process, predominantly associated with Actinomycetota, which also contributed to hydrogenotrophic carbon fixation. Notably, even at this site, heterotrophic eukaryotes co-occurred with these chemolithotrophic primary producers. Conclusions This study presents the first transcriptomic analysis from the high-altitude Atacama Desert, facilitated by the favourable moisture conditions. Furthermore, these findings highlight a moisture-driven transition in microbial energy acquisition strategies and emphasise the ecological significance of both photoautotrophy and chemolithotrophy, which likely vary depending on the dynamics of temporary lakes. The BB plain and its lake thus offer a robust model for understanding microbial resilience, functional plasticity, community assembly, and trophic interactions in extreme environments, providing novel insights into life at the edge of habitability. Graphical abstract