Discovering microbial communities within the deep biosphere of arid and humid ecosystems.

The deep biosphere is one of the most extensive and enduring habitats, comprising a significant fraction of Earth"s total biomass. Microbes inhabiting the pore space of sedimentary and igneous rocks in the subsurface encounter various challenges, including anoxic, xeric, and oligotrophic conditions. The initially organic-free igneous systems are nutrient-limited. Thus, they depend on biomass input from the surface through fluid transport along tectonic fractures. Little is known about processes in the deep subsurface of arid landscapes, where surface water input is extremely limited.

Our study provides insights into the deep biosphere of arid (Pan de Azúcar) and humid (Nahuelbuta) ecosystems along the coast of Chile. We analyzed microbial communities from up to 55 m deep subsurface granite rocks using 16S rRNA gene amplicon and shotgun metagenomics sequencing. By integrating DNA-based taxonomic and fluorescein diacetate hydrolytic activity (FDA) data, we identified a diverse deep biosphere microbial community beneath both the humid and arid surface conditions showing a potentially higher activity level compared to shallow desert soil communities. This community was characterised mainly by ubiquitous heterotrophic bacteria assigned to Pseudarthrobacter, Janthinobacterium, and Pseudomonas, regardless of surface climate. However, rare taxa affiliated with common chemolithoautotrophs, e.g., Thiobacillus, Sulfuriverula, and Sulfuricurvum, were only observed in the arid subsurface of Pan de Azúcar. This indicates an increased adaption to nutrient-limiting conditions in the arid desert deep biosphere. Functional analyses revealed sulfur and carbon monoxide as the most likely alternative electron donors, while no potential evidence for hydrogenotrophy or iron cycling was detected in both climates.

We discovered a diverse and potentially active deep biosphere inhabiting granitic rocks, a system partially influenced by climate conditions on Earth's surface. This contributes to the knowledge about energy acquisition in deep biosphere ecosystems and its interconnection with surface conditions.